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Part I - Understanding within-host processes

Published online by Cambridge University Press:  28 October 2019

Edited by
Kenneth Wilson ,
Andy Fenton  and
Dan Tompkins
Kenneth Wilson
Affiliation:
Lancaster University
Andy Fenton
Affiliation:
University of Liverpool
Dan Tompkins
Affiliation:
Predator Free 2050 Ltd
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Keywords

Parasite diversitylong-term prevalencebumblebeetrypanosomeCrithidiagenotypesgeographic variation.asexual reproductioncoevolutionepidemiologygenetic diversityhost–parasite interactionsMicrophallusPotamopyrgus antipodarumsexual reproductionCoinfectionwithin-host parasite interactionsmicroparasitemacroparasiteepidemiological modelshelminthsparasite community ecologyinterspecific interactionsmiceSIR modelslife historytrade-offsresistancetoleranceStrongylesTeladorsagia circumcinctaantibodiespopulation dynamicsdisease(mal)nutritionintegral projection modelsenvironmentSyncerus cafferparasite interactionsmacroparasitemicroparasitebovine tuberculosishelminthsrift valley fevertick-borne infectionsresistanceevolutionchildhood diseasejuvenile susceptibilitycost of resistancelifespanage structuresterilisingplant–pathogenanther-smut diseaseectoparasiteladybirdmating systemphenologyseasonal epidemicssexually transmitted infectionSTI
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Wildlife Disease Ecology
Linking Theory to Data and Application
 , pp. 1 - 222
Publisher: Cambridge University Press
Print publication year: 2019

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References

References

Abbott, K.R. (2006) Bumblebees avoid flowers containing evidence of past predation events. Canadian Journal of Zoology, 84, 1240–1247.CrossRefGoogle Scholar
Akopyants, N.S., Kimbllin, N., Secundino, N., et al. (2009) Demonstration of genetic exchange during cyclical development of Leishmania in the sand fly vector. Science, 324, 265–268.Google Scholar
Anderson, R.M. & May, R.M. (1978) Regulation and stability of host–parasite population interactions. I. Regulatory processes. Journal of Animal Ecology, 47, 219–247.Google Scholar
Anderson, R.M. & May, R.M. (1982) Coevolution of hosts and parasites. Parasitology, 85, 411–426.Google Scholar
Antúnez, K., Martín-Hernández, R., Prieto, L., et al. (2009) Immune suppression in the honey bee (Apis mellifera) following infection by Nosema ceranae (Microsporidia). Environmental Microbiology, 11, 2284–2290.Google Scholar
Baer, B. & Schmid-Hempel, P. (1999) Experimental variation in polyandry affects parasite loads and fitness in a bumble-bee. Nature, 397, 151–154.Google Scholar
Baer, B. & Schmid-Hempel, P. (2003) Bumblebee workers from different sire groups vary in susceptibility to parasite infection. Ecology Letters, 6, 106–110.CrossRefGoogle Scholar
Barribeau, S.M., Sadd, B., du Plessis, L., et al. (2015) A depauperate immune repertoire precedes evolution of sociality in bees. Genome Biology, 16, 83.Google Scholar
Barribeau, S.M., Sadd, B.M., du Plessis, L. & Schmid-Hempel, P. (2014) Gene expression differences underlying genotype-by-genotype specificity in a host–parasite system. Proceedings of the National Academy of Sciences of the United States of America, 111, 3496–3501.CrossRefGoogle Scholar
Barribeau, S.M. & Schmid-Hempel, P. (2013) Qualitatively different immune response of the bumblebee host, Bombus terrestris, to infection by different genotypes of the trypanosome gut parasite, Crithidia bombi. Infection, Genetics and Evolution, 20, 249–256.Google Scholar
Barribeau, S.M., Schmid-Hempel, P. & Sadd, B. M. (2016) Royal decree: gene expression in transgenerationally immune primed bumblebee workers mimics a primary immune response. PLoS ONE, 11, e0159635.Google Scholar
Barry, J.D. & McCulloch, R. (2001) Antigenic variation in trypanosomes: enhanced phenotypic variation in a eukaryotic parasite. Advances in Parasitology, 49, 1–70.Google Scholar
Biesmeijer, J.C., Roberts, S.P.M., Reemer, M., et al. (2006) Parallel declines on pollinators and insect-pollinated plants in Britain and the Netherlands. Science, 313, 351–354.Google Scholar
Blanford, S., Thomas, M.B., Pugh, C. & Pell, J.K. (2003) Temperature checks the Red Queen? Resistance and virulence in a fluctuating environment. Ecology Letters, 6, 2–5.Google Scholar
Brown, M.J.F., Loosli, R. & Schmid-Hempel, P. (2000) Condition-dependent expression of virulence in a trypanosome infecting bumblebees. Oikos, 91, 421–427.CrossRefGoogle Scholar
Brown, M.J.F., Moret, Y. & Schmid-Hempel, P. (2003a) Activation of host constitutive immune defence by an intestinal trypanosome parasite of bumble bees. Parasitology, 126, 253–260.Google Scholar
Brown, M.J.F., Schmid-Hempel, R. & Schmid-Hempel, P. (2003b) Strong context-dependent virulence in a host–parasite system: reconciling genetic evidence with theory. Journal of Animal Ecology, 72, 994–1002.Google Scholar
Brunner, F.S., Schmid-Hempel, P. & Barribeau, S.M. (2013) Immune gene expression in Bombus terrestris: signatures of infection despite strong variation among populations, colonies, and sister workers. PLoS ONE, 8, e68181.Google Scholar
Cameron, S.A., Lozier, J.D., Strange, J.P., et al. (2011) Patterns of widespread decline in North American bumble bees. Proceedings of the National Academy of Sciences of the United States of America, 108, 662–667.Google Scholar
Carius, H.J., Little, T.J. & Ebert, D. (2001) Genetic variation in a host–parasite association: potential for coevolution and frequency-dependent selection. Evolution, 55, 1136–1145.Google Scholar
Cariveau, D.P., Powell, J.E., Koch, H., Winfree, R. & Moran, N.A. (2014) Variation in gut microbial communities and its association with pathogen infection in wild bumble bees (Bombus). The ISME Journal, 8, 2369–2379.Google Scholar
Cisarovsky, G. & Schmid-Hempel, P. (2014a) Combining laboratory and field approaches to investigate the importance of flower nectar in the horizontal transmission of a bumblebee parasite. Entomologia Experimentalis et Applicata, 1–7, 1–7.Google Scholar
Cisarovsky, G. & Schmid-Hempel, P. (2014b) Few colonies of the host Bombus terrestris disproportionately affect the genetic diversity of its parasite, Crithidia bombi. Infection, Genetics and Evolution, 21, 192–197.Google Scholar
Cotter, S.C., Kruuk, L.E.B. & Wilson, K. (2004) Costs of resistance: genetic correlations and potential trade-offs in an insect immune system. Journal of Evolutionary Biology, 17, 421–429.Google Scholar
Cremer, S., Armitage, S.A.O. & Schmid-Hempel, P. (2007) Social immunity. Current Biology, 17, R693–R702.Google Scholar
Dawkins, R. (1982) The Extended Phenotype. Oxford: W.H. Freeman.Google Scholar
de Meeus, T., McCoy, K.D., Prugnolle, F., et al. (2006) Population genetics and molecular ecology or how to “debusquer la bête”. Infection, Genetics and Evolution, 7, 308–332.Google Scholar
Deshwal, S. & Mallon, E.B. (2014) Antimicrobial peptides play a functional role in bumblebee anti-trypanosome defense. Developmental & Comparative Immunology, 42, 240–243.Google Scholar
Dias, F.d.A., Vasconcellos, L.R.d.C., Romeiro, A., et al. (2014) Transovum transmission of trypanosomatid cysts in the milkweed bug, Oncopeltus fasciatus.PLoS ONE, 9, e108746.Google Scholar
Durrer, S. (1996) Parasite load and assemblages of bumblebee species. PhD thesis. Department of Environmental Sciences, ETH Zurich, Zürich: Verlag Studentenschaft.Google Scholar
Durrer, S. & Schmid-Hempel, P. (1994) Shared use of flowers leads to horizontal pathogen transmission. Proceedings of the Royal Society of London B, 258, 299–302.Google Scholar
Durrer, S. & Schmid-Hempel, P. (1995) Parasites and the regional distribution of bumble bee species. Ecography, 18, 114–122.Google Scholar
Dussaubat, C., Brunet, J.-L., Higes, M., et al. (2012) Gut pathology and responses to the microsporidium Nosema ceranae in the honey bee, Apis mellifera. PLoS ONE, 7, e37017.Google Scholar
Ebert, D., Duneau, D., Hall, M.D., et al. (2016) A population biology perspective on the stepwise infection process of the bacterial pathogen Pasteuria ramosa in Daphnia. Advances in Parasitology, 91, 265–310.Google Scholar
Engel, P., Martinson, V.G. & Moran, N.A. (2012) Functional diversity within the simple gut microbiota of the honey bee. Proceedings of the National Academy of Sciences of the United States of America, 109, 11,002–11,007.Google Scholar
Engel, P. & Moran, N.A. (2013a) Functional and evolutionary insights into the simple yet specific gut microbiota of the honey bee from metagenomic analysis. Gut Microbes, 4, 60–65.Google Scholar
Engel, P. & Moran, N.A. (2013b) The gut microbiota of insects – diversity in structure and function. FEMS Microbiological Reviews, 37, 699–735.Google Scholar
Erler, S., Popp, M., Wolf, S. & Lattorff, H.M.G. (2012) Sex, horizontal transmission, and multiple hosts prevent local adaptation of Crithidia bombi, a parasite of bumblebees (Bombus spp.). Ecology and Evolution, 2, 930–940.Google Scholar
Estoup, A., Solignac, M., Cornuet, J.M., Goudet, J. & Scholl, A. (1996) Genetic differentiation of continental and island populations of Bombus terrestris (Hymenoptera: Apidae) in Europe. Molecular Ecology, 5, 19–31.Google Scholar
Ewald, P.W. (1980) Evolutionary biology and the treatment of signs and symptoms of infectious disease. Journal of Theoretical Biology, 86, 169–176.Google Scholar
Ewald, P.W. (1983) Host–parasite relations, vectors, and the evolution of disease severity. Annual Review of Ecology and Systematics, 14, 465–485.Google Scholar
Fenton, A., Antonovics, J. & Brockhurst, M.A. (2009) Inverse gene-for-gene infection genetics and coevolutionary dynamics. The American Naturalist, 174, E230–E242.Google Scholar
Fitzpatrick, U., Murray, T.E., Paxton, R.J., et al. (2007) Rarity and decline in bumblebees – a test of causes and correlates in the Irish fauna. Biological Conservation, 136, 185–194.Google Scholar
Flegontov, P., Butenko, A., Firsov, S., et al. (2015). Genome of Leptomonas pyrrhocoris: a high-quality reference for monoxenous trypanosomatids and new insights into evolution of Leishmania. Scientific Reports, 6, 23704.Google Scholar
Folly, A.J., Koch, H., Stevenson, P.C. & Brown, M.J.F. (2017) Larvae act as a transient transmission hub for the prevalent bumblebee parasite Crithidia bombi. Journal of Invertebrate Pathology, 148, 81–85.Google Scholar
Fouks, B. & Lattorff, H.M.G. (2011) Recognition and avoidance of contaminated flowers by foraging bumblebees (Bombus terrestris). PLoS ONE, 6, e26328.Google Scholar
Frank, S.A. (1994) Coevolutionary genetics of hosts and parasites with quantitative inheritance. Evolutionary Ecology, 8, 74–94.Google Scholar
Frank, S.A. & Schmid-Hempel, P. (2008) Mechanisms of pathogenesis and the evolution of parasite virulence. Journal of Evolutionary Biology, 21, 396–404.Google Scholar
Fürst, M.A., McMahon, D.P., Osborne, J.L., Paxton, R.J. & Brown, M.J.F. (2014) Disease associations between honeybees and bumblebees as a threat to wild pollinators. Nature, 506, 364–366.Google Scholar
Gallot-Lavallée, M., Schmid-Hempel, R., Vandamme, R., Vergara, C.H. & Schmid-Hempel, P. (2016) Large scale patterns of abundance and distribution of parasites in Mexican bumblebees. Journal of Invertebrate Pathology, 133, 73–83.Google Scholar
Gandon, S. & Michalakis, Y. (2002) Local adaptation, evolutionary potential and host–parasite coevolution: interactions between migration, mutation, population size and generation time. Journal of Evolutionary Biology, 15, 451–462.Google Scholar
Gaunt, M.W., Yeo, M., Frame, I.A., et al. (2003) Mechanism of genetic exchange in American trypanosomes. Nature, 421, 936–939.Google Scholar
Gegear, R.J., Otterstatter, M.C. & Thomson, J.D. (2006) Bumble-bee foragers infected by a gut parasite have an impaired ability to utilize floral information. Proceedings of the Royal Society of London B, 273, 1073–1078.Google Scholar
Gibson, W. & Stevens, J. (1999) Genetic exchange in the Trypanosomatidae. Advances in Parasitology, 43, 1–46.Google Scholar
Gillespie, S.D. & Adler, L.S. (2013) Indirect effects on mutualisms: parasitism of bumble bees and pollination service to plants. Ecology, 94, 454–464.Google Scholar
Gillespie, S.D., Carrero, K. & Adler, L.S. (2015) Relationships between parasitism, bumblebee foraging behaviour, and pollination service to Trifolium pratense flowers. Ecological Entomology, 40, 650–653.Google Scholar
Goulson, D. (2003a) Bumblebees – Their Behaviour and Ecology. New York, NY: Oxford University Press.Google Scholar
Goulson, D. (2003b) Conserving wild bees for crop pollination. Food, Agriculture & Environment, 1, 142–144.Google Scholar
Goulson, D., Lye, G.C. & Darvill, B. (2008) Decline and conservation of bumble bees. Annual Review of Ecology and Systematics, 53, 191–208.Google Scholar
Graystock, P., Goulson, D. & Hughes, W.O.H. (2015) Parasites in bloom: flowers aid dispersal and transmission of pollinator parasites within and between bee species. Proceedings of the Royal Society of London B, 282.Google Scholar
Hamilton, W.D. (1980) Sex versus non-sex versus parasite. Oikos, 35, 282–290.Google Scholar
Hamilton, W.D., Axelrod, A. & Tanese, R. (1990) Sexual reproduction as an adaptation to resist parasites (a review). Proceedings of the National Academy of Sciences of the United States of America, 87, 3566–3573.Google Scholar
Hamilton, W.D. & Zuk, M. (1982) Heritable true fitness and bright birds: a role for parasites? Science, 218, 384–387.Google Scholar
Howard, R.S. & Lively, C.M. (2002) The Ratchet and the Red Queen: the maintenance of sex in parasites. Journal of Evolutionary Biology, 15, 648–656.Google Scholar
Imhoof, B. & Schmid-Hempel, P. (1999) Colony success of the bumble bee, Bombus terrestris, in relation to infections by two protozoan parasites, Crithidia bombi and Nosema bombi. Insectes Sociaux, 46, 233–238.Google Scholar
Inoue, M.N., Yokoyama, J. & Tsuchida, K. (2010) Colony growth and reproductive ability of feral nests of the introduced bumblebee Bombus terrestris in northern Japan. Insectes Sociaux, 57, 29–38.Google Scholar
Ishemgulova, A., Butenko, A., Kortisiova, L., et al. (2017) Molecular mechanisms of thermal resistance of the insect trypanosomatid Crithidia thermophila. PLoS ONE, 12, e0174165.Google Scholar
Koch, H., Abrol, D.P., Li, J. & Schmid-Hempel, P. (2013) Diversity and possible evolutionary patterns of bacterial gut associates of corbiculate bees. Molecular Ecology, 22, 2028–2044.Google Scholar
Koch, H. & Schmid-Hempel, P. (2011a) Bacterial communities in Central European bumblebees: low diversity and high specificity. Microbial Ecology, 62, 121–133.Google Scholar
Koch, H. & Schmid-Hempel, P. (2011b) Socially transmitted gut microbiota protect bumble bees against an intestinal parasite. Proceedings of the National Academy of Sciences of the United States of America, 108, 19,288–19,292.Google Scholar
Koch, H. & Schmid-Hempel, P. (2012) Gut microbiota instead of host genotype drive the specificity in the interaction of a natural host–parasite system. Ecology Letters, 15, 1095–1103.Google Scholar
König, C. & Schmid-Hempel, P. (1995) Foraging activity and immunocompetence in workers of the bumble bee, Bombus terrestris L. Proceedings of the Royal Society of London B, 260, 225–227.Google Scholar
Korner, P. & Schmid-Hempel, P. (2004) In vivo dynamics of an immune response in the bumble bee Bombus terrestris. Journal of Invertebrate Pathology, 87, 59–66.Google Scholar
Kwong, W.K., Engel, P., Koch, H. & Moran, N.A. (2014) Genomics and host specialization of honey bee and bumble bee gut symbionts. Proceedings of the National Academy of Sciences of the United States of America, 111, 11,509–11,514.Google Scholar
Leggett, H.C., Cornwallis, C.K. & West, S.A. (2012) Mechanisms of pathogenesis, infective dose and virulence in human parasites. PLoS Pathogens, 8, e1002512.Google Scholar
Lemaitre, B. (2012) The drosophila gut: a new paradigm for epithelial immune response. Cytokine, 59, 494.Google Scholar
Ley, R.E., Lozupone, C.A., Hamady, M., Knight, R. & Gordon, J.I. (2008) Worlds within worlds: evolution of the vertebrate gut microbiota. Nature Reviews Microbiology, 6, 776–788.Google Scholar
Li, J., Chen, W., Wu, J., et al. (2012) Diversity of Nosema associated with bumblebees (Bombus spp.) from China. International Journal of Parasitology, 42, 49–61.Google Scholar
Little, T.J. & Kraaijeveld, A.R. (2004) Ecological and evolutionary implications of immunological priming in invertebrates. Trends in Ecology and Evolution, 19, 58–60.Google Scholar
Luijckx, P., Fienberg, H., Duneau, D. & Ebert, D. (2013) A matching-allele model explains host resistance to parasites. Current Biology, 23, 1–4.Google Scholar
MacLeod, A., Tweedie, A., McLellan, S., et al. (2005) Allelic segregation and independent assortment in Trypanosoma brucei crosses: proof that the genetic system is Mendelian and involves meiosis. Molecular and Biochemical Parasitology, 143, 12–19.Google Scholar
Maharramov, J., Meeus, I., Maebe, K., et al. (2013) Genetic variability of the Neogregarine Apicystis bombi, an etiological agent of an emergent bumblebee disease. PLoS ONE, 8, e81475.Google Scholar
Manley, R., Boots, M. & Bayer-Wilfert, L. (2017) Condition-dependent virulence of Slow Bee Paralysis Virus in Bombus terrestris: are the impacts of honeybee viruses in wild pollinators underestimated? Oecologia, 184, 305–315.Google Scholar
Martinez-Calvillo, S., Vizuet-de-Rueda, J.C., Florencio-Martinez, L.E., Manning-Cela, R.G. & Figuera-Angulo, E.E. (2010) Gene expression in trypanosomatid parasites. Journal of Biomedicine and Biotechnology, 2010, 525241.Google Scholar
Martinson, V.G., Danforth, B.N., Minckley, R.L., et al. (2011) A simple and distinctive microbiota associated with honey bees and bumble bees. Molecular Ecology, 20, 619–628.Google Scholar
Marxer, M., Barribeau, S.M. & Schmid-Hempel, P. (2016a) Experimental evolution of a trypanosome parasite of bumblebees and its implications for infection success and host immune response. Evolutionary Biology, 43, 160–170.Google Scholar
Marxer, M., Vollenweider, V. & Schmid-Hempel, P. (2016b) Insect antimicrobial peptides act synergistically to inhibit a trypanosome parasite. Philosophical Transactions of the Royal Society B, 371, 20150302.Google Scholar
McArt, S.H., Koch, H., Irwin, R.E. & Adler, L.S. (2014) Arranging the bouquet of disease: floral traits and the transmission of plant and animal pathogens. Ecology Letters, 17, 624–636.Google Scholar
McMahon, D., Fürst, M., Caspar, J., et al. (2015) A sting in the spit: widespread cross-infection of multiple RNA viruses across wild and managed bees. Journal of Animal Ecology, 84, 615–624.Google Scholar
Mikaelyan, A., Thompson, C.L., Hofer, M.J. & Brune, A. (2015) Deterministic assembly of complex bacterial communities in guts of germ-free cockroaches. Applied and Environmental Microbiology, 82, 1256–1263.Google Scholar
Mikkola, K. (1984) Migration of wasp and bumble bee queens across the Gulf of Finland (Hymenoptera: Vespidae and Apidae). Notulae Entomologica, 64, 125–128.Google Scholar
Moore, J. (1984) Parasites and altered host behavior. Scientific American, 250, 108–115.Google Scholar
Moran, N.A., Hansen, A.K., Powell, J.E. & Sabree, Z.L. (2012) Distinctive gut microbiota of honey bees assessed using deep sampling from individual worker bees. PLoS ONE, 7, e36393.Google Scholar
Moret, Y. & Schmid-Hempel, P. (2000) Survival for immunity: the price of immune system activation for bumblebee workers. Science, 290, 1166–1168.Google Scholar
Müller, C.B. & Schmid-Hempel, P. (1993) Correlates of reproductive success among field colonies of Bombus lucorum L.: the importance of growth and parasites. Ecological Entomology, 17, 343–353.Google Scholar
Näpflin, K. & Schmid-Hempel, P. (2018) Host effects on microbiota community assembly. Journal of Animal Ecology, 87, 331–340.Google Scholar
Näpflin, K. & Schmid-Hempel, P. (2018) High gut microbiota diversity provides lower resistance against infection by an intestinal parasite. American Naturalist, 192, 131–141.Google Scholar
Otterstatter, M.C., Gegear, R.J., Colla, S. & Thomson, J.D. (2005) Effects of parasitic mites and protozoa on the flower constancy and foraging rate of bumble bees. Behavioural Ecology and Scoiobiology, 58, 383–389.Google Scholar
Peters, A.D. & Lively, C.M. (1999) The Red Queen and fluctuating epistasis: a population genetic analysis of antagonistic coevolution. The American Naturalist, 154, 393–405.Google Scholar
Råberg, L., Sim, D. & Read, A.F. (2007) Disentangling genetic variation for resistance and tolerance to infectious diseases in animals. Science, 318, 812–814.Google Scholar
Rahnamaeian, M., Cytryńska, M., Zdybicka-Barabas, A., et al. (2015) Insect antimicrobial peptides show potentiating functional interactions against Gram-negative bacteria. Proceedings of the Royal Society of London B, 282, 20150293.Google Scholar
Ravoet, J., Schwarz, R.S., Descamps, T., et al. (2015) Differential diagnosis of the honey bee trypanosomatids Crithidia mellificae and Lotmaria passim. Journal of Invertebrate Pathology, 130, 21–27.Google Scholar
Rheins, L.A. & Karp, R.D. (1986) Effect of gender on the inducible humoral immune response to honeybee venom in the American cockroach (Periplaneta americana). Developmental and Comparative Immunology, 9, 41–49.Google Scholar
Richardson, L.L., Adler, L.S., Leonard, A.S., et al. (2015) Secondary metabolites in floral nectar reduce parasite infections in bumblebees. Proceedings of the Royal Society of London B, 282, 20142471.Google Scholar
Richardson, L.L., Bowers, M.D. & Irwin, R.E. (2016) Nectar chemistry mediates the behavior of parasitized bees: consequences for plant fitness. Ecology, 97, 325–337.Google Scholar
Riddell, C., Adams, S., Schmid-Hempel, P., Mallon, E.B. & Rankin, D.J. (2009). Differential expression of immune defences is associated with specific host–parasite interactions in insects. PLoS ONE, 4, e7621.Google Scholar
Riddell, C.E., Lobaton Garces, J.D., Adams, S., et al. (2014) Differential gene expression and alternative splicing in insect immune specificity. BMC Genomics, 15, 1031.Google Scholar
Riddell, C.E., Sumner, S., Adams, S. & Mallon, E.B. (2011) Pathways to immunity: temporal dynamics of the bumblebee (Bombus terrestris) immune response against a trypanosome gut parasite. Insect Molecular Biology, 20, 529–540.Google Scholar
Routtu, J. & Ebert, D. (2015) Genetic architecture of resistance in Daphnia hosts against two species of host-specific parasites. Heredity, 114, 241–248.Google Scholar
Ruiz-Gonzalez, M.X., Bryden, J., Moret, Y., et al. (2012) Dynamic transmission, host quality and population structure in a multi-host parasite of bumble bees. Evolution, 66, 3052–3066.Google Scholar
Sadd, B., Kleinlogel, Y., Schmid-Hempel, R. & Schmid-Hempel, P. (2005) Trans-generational immune priming in a social insect. Biology Letters, 1, 386–388.Google Scholar
Sadd, B. & Schmid-Hempel, P. (2006) Insect immunity shows specificity in protection upon secondary pathogen exposure. Current Biology, 16, 1206–1210.Google Scholar
Sadd, B. & Schmid-Hempel, P. (2007) Facultative but persistent trans-generational immunity via the mother’s eggs in bumblebees. Current Biology, 17, R1046–R1047.Google Scholar
Sadd, B. & Schmid-Hempel, P. (2009) A distinct infection cost associated with trans-generational immune priming of antibacterial immunity in bumble-bees. Biology Letters, 5, 798–801.Google Scholar
Sadd, B.M., Barribeau, S.M., Bloch, G., et al. (2015) The genomes of two key bumblebee species with primitive eusocial organization. Genome Biology, 16, 76.Google Scholar
Salathé, M., Kouyos, R.D. & Bonhoeffer, S. (2008) The state of affairs in the kingdom of the Red Queen. Trends in Ecology and Evolution, 23, 439–445.Google Scholar
Salathé, R. & Schmid-Hempel, P. (2011) Genotypic structure of a multi-host bumblebee parasite suggests a major role for ecological niche overlap. PLoS ONE, 6, e22054.Google Scholar
Salathé, R. & Schmid-Hempel, P. (2012) Probing mixed-genotype infections I: extraction and cloning of infections from hosts of the trypanosomatid Crithidia bombi. PLoS ONE, 7, e49046.Google Scholar
Sasaki, A. (2000) Host–parasite coevolution in a multilocus gene-for-gene system. Proceedings of the Royal Society of London B, 267, 2183–2188.Google Scholar
Sauter, A., Brown, M.J.F., Baer, B. & Schmid-Hempel, P. (2001) Males of social insects can prevent queens from multiple mating. Proceedings of the Royal Society of London B, 268, 1449–1454.Google Scholar
Schaub, G.A. (1992) The effects of trypanosomatids on insects. Advances in Parasitology, 31, 255–319.Google Scholar
Schlüns, H., Sadd, B.M., Schmid-Hempel, P. & Crozier, R.H. (2010). Infection with the trypanosome Crithidia bombi and expression of immune-related genes in the bumblebee Bombus terrestris. Developmental and Comparative Immunology, 34, 705–709.Google Scholar
Schmid-Hempel, P. (1998) Parasites in Social Insects. Princeton, NJ: Princeton University Press.Google Scholar
Schmid-Hempel, P. (2001) On the evolutionary ecology of host–parasite interactions – addressing the questions with bumblebees and their parasites. Naturwissenschaften, 88, 147–158.Google Scholar
Schmid-Hempel, P. (2003) Variation in immune defence as a question of evolutionary ecology. Proceedings of the Royal Society of London B, 270, 357–366.Google Scholar
Schmid-Hempel, P. (2005) Natural insect host–parasite systems show immune priming and specificity – puzzles to be solved. BioEssays, 27, 1026–1034.Google Scholar
Schmid-Hempel, P. (2011) Evolutionary Parasitology – The Integrated Study of Infections, Immunology, Ecology, and Genetics. Oxford: Oxford University Press.Google Scholar
Schmid-Hempel, P. (2017) Parasites and their social hosts. Trends in Parasitology, 33, 453–462.Google Scholar
Schmid-Hempel, P., Aebi, M., Barribeau, S., et al. (2018) The genomes of Crithidia bombi and C. expoeki, common parasites of bumblebees. PLoS ONE, 13(1), e0189738.Google Scholar
Schmid-Hempel, P. & Frank, S.A. (2007) Pathogenesis, virulence, and infective dose. PLoS Pathogens, 3, 1372–1373.Google Scholar
Schmid-Hempel, P., Puhr, K., Kruger, N., Reber, C. & Schmid-Hempel, R. (1999) Dynamic and genetic consequences of variation in horizontal transmission for a microparasitic infection. Evolution, 53, 426–434.Google Scholar
Schmid-Hempel, P. & Reber Funk, C. (2004) The distribution of genotypes of the trypanosome parasite, Crithidia bombi, in populations of its host, Bombus terrestris.Parasitology, 129, 147–158.Google Scholar
Schmid-Hempel, P. & Schmid-Hempel, R. (1993) Transmission of a pathogen in Bombus terrestris, with a note on division of labour in social insects. Behavioural Ecology and Sociobiology, 33, 319–327.Google Scholar
Schmid-Hempel, P. & Stauffer, H.P. (1998). Parasites and flower choice of bumblebees. Animal Behaviour, 55, 819–825.Google Scholar
Schmid-Hempel, R., Eckhardt, M., Goulson, D., et al. (2013) The invasion of southern South America by imported bumblebees and associated parasites. Journal of Animal Ecology, 83, 823–837.Google Scholar
Schmid-Hempel, R. & Schmid-Hempel, P. (2000) Female mating frequencies in social insects: Bombus spp. from Central Europe. Insectes Sociaux, 47, 36–41.Google Scholar
Schmid-Hempel, R. & Tognazzo, M. (2010) Molecular divergence defines two distinct lineages of Crithidia bombi (Trypanosomatidae), parasites of bumblebees. Journal of Eukaryotic Microbiology, 57, 337–345.Google Scholar
Schmid-Hempel, R., Tognazzo, M., Salathé, R. & Schmid-Hempel, P. (2011) Genetic exchange and emergence of novel strains in directly transmitted trypanosomatids. Infection, Genetics, and Evolution, 11, 564–571.Google Scholar
Schwarz, R.S., Bauchan, G., Murphy, C., et al. (2015) Characterization of two species of Trypanosomatidae from the honey bee Apis mellifera: Crithidia mellificae Langridge and McGhee, 1967 and Lotmaria passim n. gen., n. sp. Journal of Eukaryotic Microbiology, 62, 567–583.Google Scholar
Schwarz, R.S. & Evans, J.D. (2013) Single and mixed-species trypanosome and microsporidia infections elicit distinct, ephemeral cellular and humoral immune responses in honey bees. Developmental & Comparative Immunology, 40, 300–310.Google Scholar
Shykoff, J.A. & Schmid-Hempel, P. (1991) Parasites delay worker reproduction in bumblebees: consequences for eusociality. Behavioral Ecology, 2, 242–248.CrossRefGoogle Scholar
Simpson, A., Stevens, J. & Lukes, J. (2006) The evolution and diversity of kinetoplastid flagellates. Trends in Parasitology, 22, 168–174.Google Scholar
Stout, J.C. & Goulson, D. (2001) The use of conspecific and interspecific scent marks by foraging bumblebees and honeybees. Animal Behaviour, 62, 183–189.Google Scholar
Tait, A., Morrison, L.J., Duffy, C.W., et al. (2011). Trypanosome genetics: populations, phenotypes and diversity. Veterinary Parasitology, 181, 61–68.Google Scholar
Tibayrenc, M. & Ayala, F.J. (2002) The clonal theory of parasitic protozoa: 12 years on. Trends in Parasitology, 18, 405–410.Google Scholar
Tibayrenc, M. & Ayala, F.J. (2013) How clonal are Trypanosoma and Leishmania? Trends in Parasitology, 29, 264–269.Google Scholar
Tognazzo, M., Schmid-Hempel, R. & Schmid-Hempel, P. (2012) Probing mixed-genotype infections II: high multiplicity in natural infections of the trypanosomatid, Crithidia bombi, in its host, Bombus spp. PLoS ONE, 7, e49137.Google Scholar
Ulrich, Y., Sadd, B. & Schmid-Hempel, P. (2011) Strain filtering and transmission of a mixed infection in a social insect. Journal of Evolutionary Biology, 24, 354–362.Google Scholar
Ulrich, Y. & Schmid-Hempel, P. (2012) Host modulation of parasite competition in multiple infections. Proceedings of the Royal Society of London B, 279, 2982–2989.Google Scholar
Ulrich, Y. & Schmid-Hempel, P. (2015) The distribution of parasite strains among hosts affects disease spread in a social insect. Infection, Genetics, Evolution, 32, 348–353.CrossRefGoogle Scholar
Van Boven, M. & Weissing, F.J. (2004) The evolutionary economics of immunity. The American Naturalist, 163, 277–294.Google Scholar
Velthuis, H.H.W. & van Doorn, A. (2006) A century of advances in bumblebee domestication and the economic and environmental aspects of its commercialization for pollination. Apidologie, 37, 421–451.Google Scholar
Widmer, A. & Schmid-Hempel, P. (1999) The population genetic structure of a large temperate pollinator species, Bombus pascuorum (Scopoli) (Hymenoptera, Apidae). Molecular Ecology, 8, 387–398.Google Scholar
Widmer, A., Schmid-Hempel, P., Estoup, A. & Scholl, A. (1998) Population genetic structure and colonization history of Bombus terrestris s.l. (Hymenoptera: Apidae) from the Canary Islands and Madeira. Heredity, 81, 563–572.Google Scholar
Wilfert, L., Gadau, J., Baer, B. & Schmid-Hempel, P. (2007) Natural variation in the genetic architecture of a host–parasite interaction in the bumblebee, Bombus terrestris.Molecular Ecology, 16, 1327–1339.Google Scholar
Williams, P.H., Brown, M.J.F., Carolan, J.C., et al. (2012) Assessing cryptic species of the bumblebee subgenus Bombus s. str. world-wide with COI barcodes (Hymenoptera: Apidae). Systematics and Biodiversity, 10, 21–56.Google Scholar
Williams, P.H., Cameron, S.A., Hines, H.M., Cederbergc, B. & Rasmont, P. (2008) A simplified subgeneric classification of the bumblebees (genus Bombus). Apidologie, 39, 1–29.Google Scholar
Wilson, K., Thomas, M.B., Blanford, S., et al. (2002) Coping with crowds: density-dependent disease resistance in desert locusts. Proceedings of the National Academy of Sciences of the United States of America, 99, 5471–5475.Google Scholar
Yourth, C.P. (2004) Virulence and transmission of Crithidia bombi in bumble bees. PhD thesis, ETH Zurich. Zurich: ETH Zurich.Google Scholar
Yourth, C.P. & Schmid-Hempel, P. (2006) Serial passage of the parasite Crithidia bombi within a colony of its host, Bombus terrestris, reduces success in unrelated hosts. Proceedings of the Royal Society of London B, 273, 655–659.Google Scholar
Zasloff, M. (2013) Antimicrobial Peptides. New York, NY: John Wiley & Son.Google Scholar
Zuk, M.& Stoehr, A.M. (2002) Immune defence and host life history. American Naturalist, 160, S9–S22.Google Scholar

References

Agrawal, A. & Lively, C.M. (2002) Infection genetics: gene-for-gene versus matching-alleles models and all points in between. Evolution Ecology Research, 4, 79–90.Google Scholar
Agrawal, A. & Lively, C.M. (2003) Modelling infection as a two-step process combining gene-for- gene and matching-allele genetics. Proceedings of the Royal Society of London B: Biological Sciences, 270, 323–334.Google Scholar
Engelstädter, J. & Bonhoeffer, S. (2009) Red Queen dynamics with non-standard fitness interactions. PLoS Computational Biology, 5, e1000469.Google Scholar
Fenton, A., Antonovics, J. & Brockhurst, M.A. (2012) Two-step infection processes can lead to coevolution between functionally independent infection and resistance pathways. Evolution, 66, 2030–2041.Google Scholar
Flor, H.H. (1956) The complementary genetic system in flax and flax rust. Advances in Genetics, 8, 29–54.Google Scholar
Frank, S.A. (1992) Models of plant–pathogen coevolution. Trends in Genetics, 8, 213–219.Google Scholar
Frank, S.A. (1993) Specificity versus detectable polymorphism in host–parasite genetics. Proceedings of the Royal Society of London B, 254, 191–197.Google Scholar
Frank, S.A. (1994) Recognition and polymorphism in host–parasite genetics. Philosophical Transactions of the Royal Society of London B, 346, 283–293.Google Scholar
Frank, S.A. (1996) Statistical properties of polymorphism in host–parasite genetics. Evolutionary Ecology, 10, 307–317.CrossRefGoogle Scholar
Grosberg, R. & Hart, M. (2000) Mate selection and the evolution of highly polymorphic self/nonself recognition genes. Science, 289, 2111–2114.Google Scholar
King, K. & Lively, C. (2012) Does genetic diversity limit disease spread in natural host populations? Heredity, 109, 199–203.Google Scholar
Lively, C.M. (2010) The effect of host genetic diversity on disease spread. American Naturalist, 175, E149–E152.Google Scholar
Lively, C.M. (2016) Coevolutionary epidemiology: disease spread, local adaptation, and sex. American Naturalist, 187, E77–E82.Google Scholar

References

Adams, M.W., Ellingboe, A.H. & Rossman, E.C. (1971) Biological uniformity and disease epidemics. BioScience, 21, 1067–1070.Google Scholar
Altermatt, F. & Ebert, D. (2008) Genetic diversity of Daphnia magna populations enhances resistance to parasites. Ecology Letters, 11, 918–928.Google Scholar
Augspurger, C.K. & Kelly, C.K. (1984) Pathogen mortality of tropical tree seedlings: experimental studies of the effects of dispersal distance, seedling density, and light conditions. Oecologia, 61, 211–217.Google Scholar
Bell, T., Freckleton, R.P. & Lewis, O.T. (2006) Plant pathogens drive density-dependent seedling mortality in a tropical tree. Ecology Letters, 9, 569–574.Google Scholar
Bento, G., Routtu, J., Fields, P.D., et al. (2017) The genetic basis of resistance and matching-allele interactions of a host–parasite system: the Daphnia magna–Pasteuria ramosa model. PLoS Genetics, 13, e1006596.Google Scholar
Biggs, B. & Malthus, T. (1982) Macroinvertebrates associated with various aquatic macrophytes in the backwaters and lakes of the upper Clutha Valley, New Zealand. New Zealand Journal of Marine and Freshwater Research, 16, 81–88.Google Scholar
Browning, J.A. & Frey, K.J. (1969) Multiline cultivars as a means of disease control. Annual Review of Phytopathology, 7, 355–382.Google Scholar
Carius, H.J., Little, T.J. & Ebert, D. (2001) Genetic variation in a host–parasite association: potential for coevolution and frequency-dependent selection. Evolution, 55, 1136–1145.Google Scholar
Collier, K., Ilcock, R. & Meredith, A. (1997) Influence of substrate type and physico-chemical conditions on macroinvertebrate faunas and biotic indices of some lowland Waikato, New Zealand, streams. New Zealand Journal of Marine and Freshwater Research, 32, 1–19.Google Scholar
Decaestecker, E., Gaba, S., Raeymaekers, J.A.M., et al. (2007) Host–parasite ‘Red Queen’ dynamics archived in pond sediment. Nature, 450, 870–873.Google Scholar
Duffy, M.A. & Sivars-Becker, L. (2007) Rapid evolution and ecological host–parasite dynamics. Ecology Letters, 10, 44–53.Google Scholar
Duneau, D., Luijckx, P., Ben-Ami, F., Laforsch, C. & Ebert, D. (2011) Resolving the infection process reveals striking differences in the contribution of environment, genetics and phylogeny to host–parasite interactions. BMC Biology, 9, 11.Google Scholar
Dybdahl, M.F., Jokela, J., Delph, L.F., Koskella, B. & Lively, C.M. (2008) Hybrid fitness in a locally adapted parasite. American Naturalist, 172, 772–782.Google Scholar
Dybdahl, M.F. & Krist, A.C. (2004) Genotypic vs. condition effects on parasite-driven rare advantage. Journal of Evolutionary Biology, 17, 967–973.Google Scholar
Dybdahl, M.F. & Lively, C.M. (1995) Diverse endemic and polyphyletic clones in mixed populations of the freshwater snail, Potamopyrgus antipodarum. Journal of Evolutionary Biology, 8, 385–398.Google Scholar
Dybdahl, M.F. & Lively, C.M. (1996) The geography of coevolution: comparative population structures for a snail and its trematode parasite. Evolution, 50, 2264–2275.Google Scholar
Dybdahl, M.F. & Lively, C.M. (1998) Host–parasite coevolution: evidence for rare advantage and time-lagged selection in a natural population. Evolution, 52, 1057–1066.Google Scholar
Fontcuberta Garcia-Cuenca, A., Dumas, Z. & Schwander, T. (2016) Extreme genetic diversity in asexual grass thrips populations. Journal of Evolutionary Biology, 29, 887–899.Google Scholar
Forsyth, D. & McCallum, I. (1981) Benthic macroinvertebrates of Lake Taupo. New Zealand Journal of Marine and Freshwater Research, 15, 41–46.Google Scholar
Fox, J., Dybdahl, M.F., Jokela, J. & Lively, C.M. (1996) Genetic structure of coexisting sexual and clonal subpopulations in a freshwater snail (Potamopyrgus antipodarum). Evolution, 50, 1541–1548.Google Scholar
Gandon, S. (2002) Local adaptation and the geometry of host–parasite coevolution. Ecology Letters, 5, 246–256.Google Scholar
Gandon, S., Capowiez, Y., Dubois, Y., Michalakis, Y. & Olivieri, I. (1996) Local adaptation and gene-for-gene coevolution in a metapopulation model. Proceedings of the Royal Society of London B, 263, 1003–1009.Google Scholar
Gandon, S. & Michalakis, Y. (2002) Local adaptation, evolutionary potential and host–parasite coevolution: interactions between migration, mutation, population size and generation time. Journal of Evolutionary Biology, 15, 451–462.Google Scholar
Gandon, S. & Nuismer, S.L. (2009) Interactions between genetic drift, gene flow, and selection mosaics drive parasite local adaptation. American Naturalist, 173, 212–224.Google Scholar
Ganz, H.H. & Ebert, D. (2010) Benefits of host genetic diversity for resistance to infection depend on parasite diversity. Ecology, 91, 1263–1268.Google Scholar
Garrett, K.A. & Mundt, C.C. (1999) Epidemiology in mixed host populations. Phytopathology, 89, 984–990.Google Scholar
Gibson, A.K., Jokela, J. & Lively, C.M. (2016) Fine-scale spatial covariation between infection prevalence and susceptibility in a natural population. American Naturalist, 188, 1–14.Google Scholar
Gibson, A.K., Xu, J.Y. & Lively, C.M. (2016) Within-population covariation between sexual reproduction and susceptibility to local parasites. Evolution, 70, 2049–2060.Google Scholar
Gibson, A.K., Delph, L.F. & Lively, C.M. (2017) The two-fold cost of sex: experimental evidence from a natural system. Evolution Letters, 1, 6–15.Google Scholar
Gibson, A.K., Vergara, D., Delph, L.F. & Lively, C.M. (2018) Periodic parasite-mediated selection for and against sex. American Naturalist, 192, 537–551.Google Scholar
Hamilton, W.D. (1980) Sex versus non-sex versus parasite. Oikos, 35, 282–290.Google Scholar
Hamilton, W.D., Axelrod, R. & Tanese, R. (1990) Sexual reproduction as an adaptation to resist parasites (a review). Proceedings of the National Academy of Sciences of the United States of America, 87, 3566–3573.Google Scholar
Hechinger, R.F. (2012) Faunal survey and identification key for the trematodes (Platyhelminthes: Digenea) infecting Potamopyrgus antipodarum (Gastropoda: Hydrobiidae) as first intermediate host. Zootaxa, 3418, 1–27.Google Scholar
Howard, R.S. & Lively, C.M. (1994) Parasitism, mutation accumulation and the maintenance of sex. Nature, 367, 554–557.Google Scholar
Howard, R.S. & Lively, C.M. (1998) The maintenance of sex by parasitism and mutation accumulation under epistatic fitness functions. Evolution, 52, 604–610.Google Scholar
Jensen, N.F. (1952) Intra-varietal diversification in oat breeding. Agronomy Journal, 44, 30–34.Google Scholar
Jokela, J., Dybdahl, M.F. & Lively, C.M. (2009) The maintenance of sex, clonal dynamics, and host–parasite coevolution in a mixed population of sexual and asexual snails. American Naturalist, 174, S43–S53.Google Scholar
Jokela, J., Lively, C.M., Dybdahl, M.F. & Fox, J. (2003) Genetic variation in sexual and clonal lineages of a freshwater snail. Biological Journal of the Linnean Society, 79, 165–181.Google Scholar
King, K.C., Delph, L.F., Jokela, J. & Lively, C.M. (2009) The geographic mosaic of sex and the Red Queen. Current Biology, 19, 1438–1441.Google Scholar
King, K.C., Delph, L.F., Jokela, J. & Lively, C.M. (2011) Coevolutionary hotspots and coldspots for host sex and parasite local adaptation in a snail–trematode interaction. Oikos, 120, 1335–1340.Google Scholar
King, K.C. & Lively, C.M. (2012) Does genetic diversity limit disease spread in natural host populations? Heredity, 109, 199–203.Google Scholar
Koskella, B. & Lively, C.M. (2007) Advice of the rose: experimental coevolution of a trematode parasite and its snail host. Evolution, 61, 152–159.Google Scholar
Koskella, B. & Lively, C.M. (2009) Evidence for negative frequency-dependent selection during experimental coevolution of a freshwater snail and a sterilizing trematode. Evolution, 63, 2213–2221.Google Scholar
Koskella, B., Vergara, D. & Lively, C.M. (2011) Experimental evolution of sexual host populations in response to sterilizing parasites. Evolutionary Ecology Research, 13, 315–322.Google Scholar
Laine, A.L., Burdon, J.J., Dodds, P.N. & Thrall, P.H. (2011) Spatial variation in disease resistance: from molecules to metapopulations. Journal of Ecology, 99, 96–112.Google Scholar
Lively, C.M. (1987) Evidence from a New Zealand snail for the maintenance of sex by parasitism. Nature, 328, 519–521.Google Scholar
Lively, C.M. (1989) Adaptation by a parasitic trematode to local populations of its snail host. Evolution, 43, 1663–1671.Google Scholar
Lively, C.M. (1992) Parthenogenesis in a freshwater snail: reproductive assurance versus parasitic release. Evolution, 46, 907–913.Google Scholar
Lively, C.M. (1999) Migration, virulence, and the geographic mosaic of adaptation by parasites. American Naturalist, 153, S34–S47.Google Scholar
Lively, C.M. (2009) The maintenance of sex: host–parasite coevolution with density-dependent virulence. Journal of Evolutionary Biology, 22, 2086–2093.Google Scholar
Lively, C.M. (2010a) Antagonistic coevolution and sex. Evolution: Education and Outreach, 3, 19–25.Google Scholar
Lively, C.M. (2010b) The effect of host genetic diversity on disease spread. American Naturalist, 175, E149–E152.Google Scholar
Lively, C.M. (2010c) An epidemiological model of host–parasite coevolution and sex. Journal of Evolutionary Biology, 23, 1490–1497.Google Scholar
Lively, C.M. (2016) Coevolutionary epidemiology: disease spread, local adaptation, and sex. American Naturalist, 187, E77–E82.Google Scholar
Lively, C.M. & Dybdahl, M.F. (2000) Parasite adaptation to locally common host genotypes. Nature, 405, 679–681.Google Scholar
Lively, C.M., Dybdahl, M.F., Jokela, J., Osnas, E.E. & Delph, L.F. (2004) Host sex and local adaptation by parasites in a snail–trematode interaction. American Naturalist, 164, S6–S18.Google Scholar
Lively, C.M., Johnson, S.G., Delph, L.F. & Clay, K. (1995) Thinning reduces the effect of rust infection on jewelweed (Impatiens capensis). Ecology, 76, 1859–1862.Google Scholar
Lively, C.M. & Jokela, J. (2002) Temporal and spatial distributions of parasites and sex in a freshwater snail. Evolutionary Ecology Research, 4, 219–226.Google Scholar
Luijckx, P., Ben-Ami, F., Mouton, L., Du Pasquier, L. & Ebert, D. (2011) Cloning of the unculturable parasite Pasteuria ramosa and its Daphnia host reveals extreme genotype–genotype interactions. Ecology Letters, 14, 125–131.Google Scholar
Luijckx, P., Fienberg, H., Duneau, D. & Ebert, D. (2012) Resistance to a bacterial parasite in the crustacean Daphnia magna shows Mendelian segregation with dominance. Heredity, 108, 547–551.Google Scholar
Luijckx, P., Fienberg, H., Duneau, D. & Ebert, D. (2013) A matching-allele model explains host resistance to parasites. Current Biology, 23, 1085–1088.Google Scholar
May, R.M. & Anderson, R.M. (1983) Epidemiology and genetics in the coevolution of parasites and hosts. Proceedings of the Royal Society of London B, 219, 281–313.Google Scholar
Maynard Smith, J. (1971) The origin and maintenance of sex. In: Williams, G.C. (ed.), Group Selection (pp. 163–175). Chicago, IL: Aldine Atherton.Google Scholar
McKone, M., Gibson, A.K., Cook, D., et al. (2016) Fine-scale association between parasites and sex in Potamopyrgus antipodarum within a New Zealand lake. New Zealand Journal of Ecology, 40, 1.Google Scholar
Meagher, S. (1999) Genetic diversity and Capillaria hepatica (Nematoda) prevalence in Michigan deer mouse populations. Evolution, 53, 1318–1324.Google Scholar
Metzger, C.M.J.A., Luijckx, P., Bento, G., Mariadassou, M. & Ebert, D. (2016) The Red Queen lives: epistasis between linked resistance loci. Evolution, 70, 480–487.Google Scholar
Mundt, C. (2002) Use of multiline cultivars and cultivar mixtures for disease management. Annual Review of Phytopathology, 40, 381–410.Google Scholar
Neiman, M., Jokela, J. & Lively, C.M. (2005) Variation in asexual lineage age in Potamopyrgus antipodarum, a New Zealand snail. Evolution, 59, 1945–1952.Google Scholar
Newton, W.L. (1953) The inheritance of susceptibility to infection with Schistosoma mansoni in Australorbis glabratus. Experimental Parasitology, 2, 242–257.Google Scholar
Osnas, E.E. & Lively, C.M. (2004) Parasite dose, prevalence of infection and local adaptation in a host–parasite system. Parasitology, 128, 223–228.Google Scholar
Osnas, E.E. & Lively, C.M. (2005) Immune response to sympatric and allopatric parasites in a snail–trematode interaction. Frontiers in Zoology, 2, 8.Google Scholar
Osnas, E.E. & Lively, C.M. (2006) Host ploidy, parasitism and immune defence in a coevolutionary snail–trematode system. Journal of Evolutionary Biology, 19, 42–48.Google Scholar
Otto, S.P. & Nuismer, S.L. (2004) Species interactions and the evolution of sex. Science, 304, 1018–1020.Google Scholar
Paczesniak, D., Adolfsson, S., Liljeroos, K., et al. (2014) Faster clonal turnover in high-infection habitats provides evidence for parasite-mediated selection. Journal of Evolutionary Biology, 27, 417–428.Google Scholar
Parker, M.A. (1985) Local population differentiation for compatibility in an annual legume and its host-specific fungal pathogen. Evolution, 39, 713–723.Google Scholar
Pielou, E.C. (1969) An Introduction to Mathematical Ecology. New York, NY: John Wiley & Sons.Google Scholar
Pilet, F., Chacon, G., Forbes, G.A. & Andrivon, D. (2006) Protection of susceptible potato cultivars against late blight in mixtures increases with decreasing disease pressure. Phytopathology, 96, 777–783.Google Scholar
Richards, C.S. (1975) Genetic factors in susceptibility of Biomphalaria glabrata for different strains of Schistosoma mansoni. Parasitology, 70, 231–241.Google Scholar
Richards, C.S. & Merritt, J.W. (1972) Genetic factors in the susceptibility of juvenile Biomphalaria glabrata to Schistosoma mansoni infection. American Journal of Tropical Medicine and Hygiene, 21, 425–434.Google Scholar
Schmid, B. (1994) Effects of genetic diversity in experimental stands of Solidago altissima: evidence for the potential role of pathogens as selective agents in plant populations. Journal of Ecology, 82, 165–175.Google Scholar
Talbot, J. & Ward, J. (1987) Macroinvertebrates associated with aquatic macrophyties in Lake Alexandrina, New Zealand. New Zealand Journal of Marine and Freshwater Research, 21, 199–213.Google Scholar
Thrall, P.H. & Burdon, J.J. (2000) Effect of resistance variation in a natural plant host–pathogen metapopulation on disease dynamics. Plant Pathology, 49, 767–773.Google Scholar
Thrall, P.H., Burdon, J.J. & Young, A. (2001) Variation in resistance and virulence among demes of a plant host–pathogen metapopulation. Journal of Ecology, 89, 736–748.Google Scholar
Tseng, M. (2004) Sex–specific response of a mosquito to parasites and crowding. Proceedings of the Royal Society of London B, 271, S186–S188.Google Scholar
Vergara, D., Jokela, J. & Lively, C.M. (2014) Infection dynamics in coexisting sexual and asexual host populations: support for the Red Queen Hypothesis. American Naturalist, 184, S22–S30.CrossRefGoogle ScholarPubMed
Vergara, D., Lively, C.M., King, K.C. & Jokela, J. (2013) The geographic mosaic of sex and infection in lake populations of a New Zealand snail at multiple spatial scales. American Naturalist, 182, 484–493.Google Scholar
Wallace, C. (1992) Parthenogenesis, sex and chromosomes in Potamopyrgus antipodarum. Journal of Molluscan Studies, 58, 93–107.Google Scholar
Webster, J., Shrivastava, J., Johnson, P. & Blair, L. (2007) Is host–schistosome coevolution going anywhere? BMC Evolutionary Biology, 7, 91.Google Scholar
Webster, J. & Woolhouse, M. (1998) Selection and strain specificity of compatibility between snail intermediate hosts and their parasitic schistosomes. Evolution, 52, 1627–1634.Google Scholar
Webster, J.P. & Davies, C.M. (2001) Coevolution and compatibility in the snail–schistosome system. Parasitology, 123, 41–56.Google Scholar
Webster, J.P., Gower, C.M. & Blair, L. (2004) Do hosts and parasites coevolve? Empirical support from the Schistosoma system. American Naturalist, 164, S33–S51.Google Scholar
Winterbourn, M. (1970) Population studies on the New Zealand freshwater gastropod, Potamopyrgus antipodarum. Proceedings of the Malacological Society of London, 39, 139–149.Google Scholar
Wolfe, M. (1985) The current status and prospects of multiline cultivars and variety mixtures for disease resistance. Annual Review of Phytopathology, 23, 251–273.Google Scholar
Zhu, Y., Chen, H., Fan, J., et al. (2000) Genetic diversity and disease control in rice. Nature, 406, 718–722.Google Scholar

References

Abu-Madi, M.A., Behnke, J.M., Lewis, J.W. & Gilbert, F.S. (1998) Descriptive epidemiology of Heligmosomoides polygyrus in Apodemus sylvaticus from three contrasting habitats in southeast England. Journal of Helminthology, 72, 93–100.Google Scholar
Abu-Madi, M.A., Behnke, J.M., Lewis, J.W. & Gilbert, F.S. (2000) Seasonal and site specific variation in the component community structure of intestinal helminths in Apodemus sylvaticus from three contrasting habitats in south-east England. Journal of Helminthology, 74, 7–15.Google Scholar
Anderson, R.M. & May, R.M. (1978) Regulation and stability of host–parasite population interactions. I. Regulatory processes. Journal of Animal Ecology, 47, 219–247.Google Scholar
Anderson, R.M. & May, R.M. (1981) The population dynamics of microparasites and their invertebrate hosts. Philosophical Transactions of the Royal Society of London B, 291, 451–524.Google Scholar
Anderson, R.M. & May, R.M. (1992) Infectious Diseases of Humans: Dynamics and Control. Oxford: Oxford University Press.Google Scholar
Basáñez, M.-G., French, M.D., Walker, M. & Churcher, T.S. (2012) Paradigm lost: how parasite control may alter pattern and process in human helminthiases. Trends in Parasitology, 28, 161–171.Google Scholar
Behnke, J. & Harris, P.D. (2010) Heligmosomoides bakeri: a new name for an old worm? Trends in Parasitology, 26, 524–529.Google Scholar
Behnke, J.M., Bajer, A., Sinski, E. & Wakelin, D. (2001) Interactions involving intestinal nematodes of rodents: experimental and field studies. Parasitology, 122, S39–S49.Google Scholar
Behnke, J.M., Gilbert, F.S., Abu-Madi, M.A. & Lewis, J.W. (2005) Do the helminth parasites of wood mice interact? Journal of Animal Ecology, 74, 982–993.Google Scholar
Bentwich, Z., Kalinkovich, A., Weisman, Z., et al. (1999) Can eradication of helminthic infections change the face of AIDS and tuberculosis? Immunology Today, 20, 485–487.Google Scholar
Blackwell, A.D., Martin, M., Kaplan, H. & Gurven, M. (2013) Antagonism between two intestinal parasites in humans: the importance of co-infection for infection risk and recovery dynamics. Proceedings of The Royal Society of London B, 280, 20131671.Google Scholar
Bordes, F., Guegan, J.F. & Morand, S. (2011) Microparasite species richness in rodents is higher at lower latitudes and is associated with reduced litter size. Oikos, 120, 1889–1896.Google Scholar
Bordes, F. & Morand, S. (2009) Coevolution between multiple helminth infestations and basal immune investment in mammals: cumulative effects of polyparasitism? Parasitology Research, 106, 33–37.Google Scholar
Bottomley, C., Isham, V. & Basanez, M.G. (2005) Population biology of multispecies helminth infection: interspecific interactions and parasite distribution. Parasitology, 131, 417–433.Google Scholar
Bottomley, C., Isham, V. & Basanez, M.G. (2007) Population biology of multispecies helminth infection: competition and coexistence. Journal of Theoretical Biology, 244, 81–95.Google Scholar
Bush, A.O. & Holmes, J.C. (1986) Intestinal helminths of lesser scaup ducks: an interactive community. Canadian Journal of Zoology – Revue Canadienne de Zoologie, 64, 142–152.Google Scholar
Costa, F., Porter, F.H., Rodrigues, G., et al. (2014) Infections by Leptospira interrogans, Seoul Virus, and Bartonella spp. among Norway rats (Rattus norvegicus) from the urban slum environment in Brazil. Vector-borne and Zoonotic Diseases, 14(1), 33–40. DOI:10.1089/vbz.2013.1378.Google Scholar
Cox, F.E.G. (2001) Concomitant infections, parasites and immune responses. Parasitology, 122, S23–S38.Google Scholar
de Bellocq, J.G., Sara, M., Casanova, J.C., Feliu, C. & Morand, S. (2003) A comparison of the structure of helminth communities in the woodmouse, Apodemus sylvaticus, on islands of the western Mediterranean and continental Europe. Parasitology Research, 90, 64–70.Google Scholar
Dobson, A.P. (1985) The population dynamics of competition between parasites. Parasitology, 91, 317–347.Google Scholar
Dobson, A.P. (1988) The population biology of parasite-induced changes in host behavior. Quarterly Review of Biology, 63, 139–165.Google Scholar
Druilhe, P., Tall, A. & Sokhna, C. (2005) Worms can worsen malaria: towards a new means to roll back malaria? Trends in Parasitology, 21, 359–362.Google Scholar
Elton, C., Ford, E.B. & Baker, J.R. (1931) The health and parasites of a wild mouse population. Proceedings of the Royal Society of London B, 101, 657–721.Google Scholar
Ezenwa, V.O., Etienne, R.S., Luikart, G., Beja-Pereira, A. & Jolles, A.E. (2010) Hidden consequences of living in a wormy world: nematode-induced immune suppression facilitates tuberculosis invasion in African buffalo. American Naturalist, 176, 613–624.Google Scholar
Ezenwa, V.O. & Jolles, A.E. (2015) Opposite effects of anthelmintic treatment on microbial infection at individual versus population scales. Science, 347, 175–177.Google Scholar
Fenton, A. (2008) Worms and germs: the population dynamic consequences of microparasite–macroparasite co-infection. Parasitology, 135, 1545–1560.Google Scholar
Fenton, A. (2013) Dances with worms: the ecological and evolutionary impacts of deworming on coinfecting pathogens. Parasitology, 140, 1119–1132.Google Scholar
Fenton, A., Knowles, S.C.L., Petchey, O.L. & Pedersen, A.B. (2014) The reliability of observational approaches for detecting interspecific parasite interactions: comparison with experimental results. International Journal for Parasitology, 44, 437–445.Google Scholar
Fenton, A. & Perkins, S.E. (2010) Applying predator–prey theory to modelling immune-mediated, within-host interspecific parasite interactions. Parasitology, 137, 1027–1038.Google Scholar
Fenton, A., Viney, M.E. & Lello, J. (2010) Detecting interspecific macroparasite interactions from ecological data: patterns and process. Ecology Letters, 13, 606–615.Google Scholar
Ferrari, N., Cattadori, I.M., Rizzoli, A. & Hudson, P.J. (2009) Heligmosomoides polygyrus reduces infestation of Ixodes ricinus in free-living yellow-necked mice, Apodemus flavicollis. Parasitology, 136, 305–316.Google Scholar
Forbes, K.M., Henttonen, H., Hirvela-Koski, V., et al. (2015) Food provisioning alters infection dynamics in populations of a wild rodent. Proceedings of the Royal Society of London B, 282, 20151939.Google Scholar
Gatto, M. & De Leo, G.A. (1998) Interspecific competition among macroparasites in a density-dependent host population. Journal of Mathematical Biology, 37, 467–490.Google Scholar
Gause, G.E. (1934) The Struggle for Existence. Baltimore, MD: Williams & Wilkins.Google Scholar
Graham, A.L. (2008) Ecological rules governing helminth–microparasite coinfection. Proceedings of the National Academy of Sciences of the United States of America, 105, 566–570.Google Scholar
Griffiths, E.C., Pedersen, A.B., Fenton, A. & Petchey, O.L. (2011) The nature and consequences of coinfection in humans. Journal of Infection, 63, 200–206.Google Scholar
Griffiths, E.C., Pedersen, A.B., Fenton, A. & Petchey, O.L. (2014) Analysis of a summary network of co-infection in humans reveals that parasites interact most via shared resources. Proceedings of the Royal Society of London B, 281, 20132286.Google Scholar
Gupta, S., Maiden, M.C.J., Feavers, I.M., et al. (1996) The maintenance of strain structure in populations of recombining infectious agents. Nature Medicine, 2, 437–442.Google Scholar
Gupta, S., Swinton, J. & Anderson, R.M. (1994) Theoretical studies of the effects of heterogeneity in the parasite population on the transmission dynamics of malaria. Proceedings of the Royal Society of London B, 256, 231–238.Google Scholar
Gutiérrez, R., Morick, D., Cohen, C., Hawlena, H. & Harrus, S. (2014) The effect of ecological and temporal factors on the composition of Bartonella infection in rodents and their fleas. ISME Journal, 8, 1598–1608.Google Scholar
Harms, G. & Feldmeier, H. (2002) HIV infection and tropical parasitic diseases – deleterious interactions in both directions? Tropical Medicine and International Health, 7, 479–488.Google Scholar
Harris, J.B., Podolsky, M.J., Bhuiyan, T.R., et al. (2009) Immunologic responses to Vibrio cholerae in patients co-infected with intestinal parasites in Bangladesh. PLoS Neglected Tropical Diseases, 3, e403.Google Scholar
Hastings, A. (1987) Can competition be detected using species co-occurrrence data? Ecology, 68, 117–123.Google Scholar
Haukisalmi, V. & Henttonen, H. (1993a) Coexistence in helminths of the bank vole Clethrionomys glareolus. 1. Patterns of co-occurrence. Journal of Animal Ecology, 62, 221–229.Google Scholar
Haukisalmi, V. & Henttonen, H. (1993b) Coexistence in helminths of the bank vole Clethrionomys glareolus. 2. Intestinal distribution and interspecific interactions. Journal of Animal Ecology, 62, 230–238.Google Scholar
Haukisalmi, V. & Henttonen, H. (1998) Analysing interspecific associations in parasites: alternative methods and effects of sampling heterogeneity. Oecologia, 116, 565–574.Google Scholar
Hayes, K.S., Bancroft, A.J., Goldrick, M., et al. (2010) Exploitation of the intestinal microflora by the parasitic nematode Trichuris muris. Science, 328, 1391–1394.Google Scholar
Holmes, J.C. (1961) Effects of concurrent infections on Hymenolepis diminuta (Cestoda) and Moniliformis dubius (Acanthocephala). 1. General effects and comparison with crowding. Journal of Parasitology, 47, 209–216.Google Scholar
Holmes, J.C. (1962) Effects of concurrent infections on Hymenolepis diminuta (Cestoda) and Moniliformis dubius (Acanthocephala). Effects on growth. Journal of Parasitology, 48, 87–96.Google Scholar
Holmes, J.C. & Price, P.W. (1986) Communities of parasites. In: Kikkawa, J. & Anderson, D.J. (eds.), Community Ecology: Patterns and Processes (pp. 187–213).Oxford: Blackwell Scientific Publishers.Google Scholar
Johnson, P.T.J., De Roode, J.C. & Fenton, A. (2015) Why infectious disease research needs community ecology. Science, 349.Google Scholar
Kennedy, C.R. (2006) Ecology of the Acathocephala. Cambridge: Cambridge University Press.Google Scholar
Knowles, S.C.L., Fenton, A., Petchey, O.L., et al. (2013) Stability of within-host parasite communities in a wild mammal system. Proceedings of the Royal Society of London B, 280, 20130598.Google Scholar
Krasnov, B.R., Matthee, S., Lareschi, M., Korallo-Vinarskaya, N.P. & Vinarski, M.V. (2010) Co-occurrence of ectoparasites on rodent hosts: null model analyses of data from three continents. Oikos, 119, 120–128.Google Scholar
Kreisinger, J., Bastien, G., Hauffe, H.C., Marchesi, J. & Perkins, S.E. (2015) Interactions between multiple helminths and the gut microbiota in wild rodents. Philosophical Transactions of the Royal Society of London B – Biological Sciences, 370, 20150295.Google Scholar
Lello, J., Boag, B., Fenton, A., Stevenson, I.R. & Hudson, P.J. (2004) Competition and mutualism among the gut helminths of a mammalian host. Nature, 428, 840–844.Google Scholar
Lewis, J.W. (1968a) Studies on the helminth parasites of the long-tailed field mouse, Apodemus sylvaticus sylvaticus from Wales. Journal of Zoology, 154, 287–312.Google Scholar
Lewis, J.W. (1968b) Studies on the helminth parasites of voles and shrews from Wales. Journal of Zoology, 154, 313–331.Google Scholar
Lotka, A.J. (1932) The growth of mixed populations: two species competing for a common food supply. Journal of the Washington Academy of Science, 22, 461–469.Google Scholar
Luong, L.T., Perkins, S.E., Grear, D.A., Rizzoli, A. & Hudson, P.J. (2010) The relative importance of host characteristics and co-infection in generating variation in Heligmosomoides polygyrus fecundity. Parasitology, 137, 1003–1012.Google Scholar
Maizels, R.M., Balic, A., Gomez-Escobar, N., et al. (2004) Helminth parasites – masters of regulation. Immunological Reviews, 201, 89–116.Google Scholar
Maurice, C.F., Knowles, S.C.L., Ladau, J., et al. (2015) Marked seasonal variation in the wild mouse gut microbiota. ISME Journal, 9, 2423–2434.Google Scholar
May, R.M. & Nowak, M.A. (1995) Coinfection and the evolution of parasite virulence. Proceedings of the Royal Society of London B, 261, 209–215.Google Scholar
Montgomery, S.S.J. & Montgomery, W.I. (1988) Cyclic and non-cyclic dynamics in populations of the helminth parasites of wood mice, Apodemus sylvaticus. Journal of Helminthology, 62, 78–90.Google Scholar
Montgomery, S.S.J. & Montgomery, W.I. (1990) Structure, stability and species interactions in helminth communities of wood mice, Apodemus sylvaticus. International Journal for Parasitology, 20, 225–242.Google Scholar
Montoya, J.M. & Sole, R.V. (2002) Small world patterns in food webs. Journal of Theoretical Biology, 214, 405–412.Google Scholar
Muller-Graf, C.D.M., Durand, P., Feliu, C., et al. (1999) Epidemiology and genetic variability of two species of nematodes (Heligmosomoides polygyrus and Syphacia stroma) of Apodemus spp. Parasitology, 118, 425–432.Google Scholar
Nieto, N.C., Leonhard, S., Foley, J.E. & Lane, R.S. (2010) Coinfection of western gray squirrel (Sciurus griseus) and other sciurid rodents with Borrelia burgdorferi sensu stricto and Anaplasma phagocytophilum in California. Journal of Wildlife Diseases, 46(1), 291&296. http://dx.doi.org/10.7589/0090-3558-46.1.291.Google Scholar
Nowell, F. & Higgs, S. (1989) Eimeria species infecting wood mice (genus Apodemus) and the transfer of two species to Mus musculus. Parasitology, 98, 329–336.Google Scholar
Pedersen, A.B. & Antonovics, J. (2013) Anthelmintic treatment alters the parasite community in a wild mouse host. Biology Letters, 9, 20130205.Google Scholar
Pedersen, A.B. & Babayan, S.A. (2011) Wild immunology. Molecular Ecology, 20, 872–880.Google Scholar
Pedersen, A.B. & Fenton, A. (2007) Emphasising the ecology in parasite community ecology. Trends in Ecology & Evolution, 22, 133–139.Google Scholar
Pedersen, A.B. & Fenton, A. (2015) The role of antiparasite treatment experiments in assessing the impact of parasites on wildlife. Trends in Parasitology, 31, 200–211.Google Scholar
Petney, T.N. & Andrews, R.H. (1998) Multiparasite communities in animals and humans: frequency, structure and pathogenic significance. International Journal for Parasitology, 28, 377–393.CrossRefGoogle ScholarPubMed
Poulin, R. (1996) Richness, nestedness, and randomness in parasite infracommunity structure. Oecologia, 105, 545–551.Google Scholar
Poulin, R. (1997) Species richness of parasite assemblages: evolution and patterns. Annual Review of Ecology and Systematics, 28, 341–358.Google Scholar
Poulin, R. (2007) Evolutionary Ecology of Parasites, 2nd edition. Princeton, NJ: Princeton University Press.Google Scholar
Price, P.W. (1980) Evolutionary Biology of Parasites. Princeton, NJ: Princeton University Press.Google Scholar
Quinnell, R.J. (1992) The population dynamics of Heligmosomoides polygyrus in an enclosure population of wood mice. Journal of Animal Ecology, 61, 669–679.Google Scholar
Rausch, R. (1952) Studies on the helminth fauna of Alaska. 11. Helminth parasites of microtine rodents – taxonomic considerations. Journal of Parasitology, 38, 415–444.Google Scholar
Rausch, R. & Kuns, M.L. (1950) Studies on some North American shrew cestodes. Journal of Parasitology, 36, 433–438.Google Scholar
Roberts, M.G. & Dobson, A.P. (1995) The population dynamics of communities of parasitic helminths. Mathematical Biosciences, 126, 191–214.Google Scholar
Rynkiewicz, E.C., Pedersen, A.B. & Fenton, A. (2015) An ecosystem approach to understanding and managing within-host parasite community dynamics. Trends in Parasitology, 31, 212–221.Google Scholar
Salvador, A.R., Guivier, E., Xuereb, A., et al. (2011) Concomitant influence of helminth infection and landscape on the distribution of Puumala hantavirus in its reservoir, Myodes glareolus. BMC Microbiology, 11, 30.Google Scholar
Schluter, D. (1984) A variance test for detecting species associations, with some example applications. Ecology, 65, 998–1005.Google Scholar
Sharpe, G.I. (1964) The helminth parasites of some small mammal communities. I. The parasites and their hosts. Parasitology, 54, 145–154.Google Scholar
Shaw, D.J. & Dobson, A.P. (1995) Patterns of macroparasite abundance and aggregation in wildlife populations: a quantitative review. Parasitology, 111, S111–133.Google Scholar
Shaw, D.J., Grenfell, B.T. & Dobson, A.P. (1998) Patterns of macroparasite aggregation in wildlife host populations. Parasitology, 117, 597–610.Google Scholar
Sole, R.V. & Montoya, J.M. (2001) Complexity and fragility in ecological networks. Proceedings of the Royal Society of London B, 268, 2039–2045.Google Scholar
Stanko, M., Miklisova, D., de Bellocq, J.G. & Morand, S. (2002) Mammal density and patterns of ectoparasite species richness and abundance. Oecologia, 131, 289–295.Google Scholar
Stock, T.M. & Holmes, J.C. (1988) Functional relationships and microhabitat distributions of enteric helminths of grebes (Podicipedidae): the evidence for interactive communities. Journal of Parasitology, 74, 214–227.Google Scholar
Strogatz, S.H. (2001) Exploring complex networks. Nature, 410, 268–276.Google Scholar
Telfer, S., Lambin, X., Birtles, R., et al. (2010) Species interactions in a parasite community drive infection risk in a wildlife population. Science, 330, 243–246.Google Scholar
Thomas, R.J. (1953) On the nematode and trematode parasites of some small mammals from the Inner Hebrides. Journal of Helminthology, 27, 143–168.Google Scholar
van Baalen, M. & Sabelis, M.W. (1995) The dynamics of multiple infection and the evolution of virulence. American Naturalist, 146, 881–910.Google Scholar
Watts, D.J. & Strogatz, S.H. (1998) Collective dynamics of ‘small-world’ networks. Nature, 393, 440–442.Google Scholar
Yakob, L., Williams, G.M., Gray, D.J., et al. (2013) Slaving and release in co-infection control. Parasites & Vectors, 6, 157.Google Scholar

References

Abbott, K.A., Taylor, M.A. & Stubbings, L.A. (2012) Sustainable Worm Control Strategies For Sheep: A Technical Manual For Veterinary Surgeons and Advisers. Malvern: UK SCOPS (Sustainable Control of Parasites in Sheep), National Sheep Association.Google Scholar
Albon, S.D., Stien, A., Irvine, R.J., et al. (2002) The role of parasites in the dynamics of a reindeer population. Proceedings of the Royal Society of London B, 269, 1625–1632.Google Scholar
Albrecht, A. (1909) Zur Kenntnis der Entwicklung der Sklerostomen beim Pferde. Zeitschrift fur Veterinarkunde, 21, 161–181.Google Scholar
Anderson, R.M. (1986) The population dynamics and epidemiology of intestinal nematode infections. Transactions of the Royal Society of Tropical Medicine and Hygiene, 80, 686–696.Google Scholar
Anderson, R.M. & May, R.M. (1978) Regulation and stability of host–parasite population interactions. I. Regulatory processes. Journal of Animal Ecology, 47, 219–247.Google Scholar
Anderson, R.M. & May, R.M. (1979) Population biology of infectious diseases: Part I. Nature, 280, 361–367.Google Scholar
Anderson, R.M. & May, R.M. (1982) Coevolution of hosts and parasites. Parasitology, 85, 411–426.Google Scholar
Bancroft, D.R., Pemberton, J.M. & King, P. (1995) Extensive protein and microsatellite variability in an isolated, cyclic ungulate population. Heredity, 74, 326–336.Google Scholar
Behnke, J.M., Barnard, C.J. & Wakelin, D. (1992) Understanding chronic nematode infections: evolutionary considerations, current hypotheses and the way forward. International Journal for Parasitology, 22, 861–907.Google Scholar
Beisel, W.R. (1977) Magnitude of the host nutritional responses to infection. The American Journal of Clinical Nutrition, 30, 1236–1247.Google Scholar
Beldomenico, P.M., Telfer, S., Gebert, S., et al. (2008) Poor condition and infection: a vicious circle in natural populations. Proceedings of the Royal Society of London B, 275, 1753–1759.Google Scholar
Beraldi, D., McRae, A.F., Gratten, J., et al. (2007) Quantitative trait loci (QTL) mapping of resistance to strongyles and coccidea in the free-living Soay sheep (Ovis aries). International Journal for Parasitology, 37, 121–129.Google Scholar
Bérénos, C., Ellis, P.A., Pilkington, J.G., et al. (2015) Heterogeneity of genetic architecture of body size traits in a free-living population. Molecular Ecology, 24, 1810–1830.Google Scholar
Bérénos, C., Ellis, P.A., Pilkington, J.G. & Pemberton, J.M. (2014) Estimating quantitative genetic parameters in wild populations: a comparison of pedigree and genomic approaches. Molecular Ecology, 23, 3434–3451.Google Scholar
Bérénos, C., Ellis, P.A., Pilkington, J.G. & Pemberton, J.M. (2016) Genomic analysis reveals depression due to both individual and maternal inbreeding in a free-living mammal population. Molecular Ecology, 25, 3152–3168.Google Scholar
Best, A., White, A. & Boots, M. (2008) Maintenance of host variation in tolerance to pathogens and parasites. Proceedings of the National Academy of Sciences of the United States of America, 105, 20,786–20,791.Google Scholar
Bishop, S. (2012) A consideration of resistance and tolerance for ruminant nematode infections. Frontiers in Genetics, 3, 168.Google Scholar
Bishop, S.C. & Stear, M.J. (2000) The use of a gamma-type function to assess the relationship between the number of adult Teladorsagia circumcincta and total egg output. Parasitology, 121, 435–440.Google Scholar
Blanchet, S., Rey, O. & Loot, G. (2010) Evidence for host variation in parasite tolerance in a wild fish population. Evolutionary Ecology, 24, 1129–1139.Google Scholar
Boots, M., Best, A., Miller, M.R. & White, A. (2009) The role of ecological feedbacks in the evolution of host defence: what does theory tell us? Philosophical Transactions of the Royal Society of London B: Biological Sciences, 364, 27–36.Google Scholar
Borer, E., Antonovics, J., Kinkel, L., et al. (2011) Bridging taxonomic and disciplinary divides in infectious disease. EcoHealth, 8, 261–267.Google Scholar
Bowers, R.G., Boots, M. & Begon, M. (1994) Life-history trade-offs and the evolution of pathogen resistance: competition between host strains. Proceedings of the Royal Society of London B, 257, 247–253.Google Scholar
Boyd, H.E.G. (1999) The early development of parasitism in Soay sheep on St Kilda. Thesis, University of Cambridge.Google Scholar
Bradley, J.E. & Jackson, J.A. (2008) Measuring immune system variation to help understand host–pathogen community dynamics. Parasitology, 135, 807–823.Google Scholar
Braisher, T.L., Gemmell, N.J., Grenfell, B.T. & Amos, W. (2004) Host isolation and patterns of genetic variability in three populations of Teladorsagia from sheep. International Journal for Parasitology, 34, 1197–1204.Google Scholar
Brown, E.A., Pilkington, J.G., Nussey, D.H., et al. (2013) Detecting genes for variation in parasite burden and immunological traits in a wild population: testing the candidate gene approach. Molecular Ecology, 22, 757–773.Google Scholar
Bruno, J.F., Ellner, S.P., Vu, I., Kim, K. & Harvell, C.D. (2011) Impacts of aspergillosis on sea fan coral demography: modeling a moving target. Ecological Monographs, 81, 123–139.Google Scholar
Carval, D. & Ferriere, R. (2010) A unified model for the coevolution of resistance, tolerance and virulence. Evolution, 64, 2988–3009.Google Scholar
Caswell, H. (2001) Matrix Population Models, 2nd edition. Sunderland, MA: Sinauer Associates.Google Scholar
Cattadori, I.M., Albert, R. & Boag, B. (2007) Variation in host susceptibility and infectiousness generated by co-infection: the myxoma–Trichostrongylus retortaeformis case in wild rabbits. Journal of The Royal Society Interface, 4, 831–840.Google Scholar
Cattadori, I.M., Boag, B., Bjørnstad, O.N., Cornell, S.J. & Hudson, P.J. (2005) Peak shift and epidemiology in a seasonal host–nematode system. Proceedings of the Royal Society of London B, 272, 1163–1169.Google Scholar
Caudron, Q., Garnier, R., Pilkington, J.G., et al. (2017) Robust extraction of quantitative structural information from high-variance histological images of livers from necropsied Soay sheep. Royal Society Open Science, 4, 170111.Google Scholar
Chessa, B., Pereira, F., Arnaud, F., et al. (2009) Revealing the history of sheep domestication using retrovirus integrations. Science, 324, 532–536.Google Scholar
Chevin, L.-M. (2015) Evolution of adult size depends on genetic variance in growth trajectories: a comment on analyses of evolutionary dynamics using integral projection models. Methods in Ecology and Evolution, 6, 981–986.Google Scholar
Childs, D.Z., Coulson, T.N., Pemberton, J.M., Clutton-Brock, T.H. & Rees, M. (2011) Predicting trait values and measuring selection in complex life histories: reproductive allocation decisions in Soay sheep. Ecology Letters, 14, 985–992.Google Scholar
Childs, D.Z., Sheldon, B.C. & Rees, M. (2016) The evolution of labile traits in sex- and age-structured populations. Journal of Animal Ecology, 85, 329–342.Google Scholar
Christensen, L.L., Selman, C., Blount, J.D., et al. (2015) Plasma markers of oxidative stress are uncorrelated in a wild mammal. Ecology and Evolution, 5, 5096–5108.Google Scholar
Clark, D. & Bruelisauer, F. (2008) Mapping the Prevalence of JSRV and Other Endemic Infections. Inverness: Scottish Government.Google Scholar
Clutton-Brock, T.H., Illius, A.W., Wilson, K., et al. (1997) Stability and instability in ungulate populations: an empirical analysis. American Naturalist, 149, 195–219.Google Scholar
Clutton-Brock, T.H. & Pemberton, J.M. (2004) Individuals and populations. In: Clutton-Brock, T.H. & Pemberton, J.M. (eds.), Soay Sheep: Dynamics and Selection in an Island Population (pp. 1–13). Cambridge: Cambridge University Press.Google Scholar
Clutton-Brock, T.H., Pemberton, J.M., Coulson, T., Stevenson, I.R. & MacColl, A.D.C. (2004) The sheep of St Kilda. In: Clutton-Brock, T.H. & Pemberton, J.M. (eds.), Soay Sheep: Dynamics and Selection in an Island Population (pp. 17–51). Cambridge: Cambridge University Press.Google Scholar
Clutton-Brock, T. & Sheldon, B.C. (2010) Individuals and populations: the role of long-term, individual-based studies of animals in ecology and evolutionary biology. Trends in Ecology & Evolution, 25, 562–573.Google Scholar
Clutton-Brock, T.H., Stevenson, I.R., Marrow, P., et al. (1996) Population fluctuations, reproductive costs and life-history tactics in female Soay sheep. Journal of Animal Ecology, 65, 675–689.Google Scholar
Colditz, I.G. (2008) Six costs of immunity to gastrointestinal nematode infections. Parasite Immunology, 30, 63–70.Google Scholar
Coltman, D.W., Pilkington, J.G., Kruuk, L.E.B., Wilson, K. & Pemberton, J.M. (2001a) Positive genetic correlation between parasite resistance and body size in a free-living ungulate population. Evolution, 55, 2116–2125.Google Scholar
Coltman, D.W., Pilkington, J.G. & Pemberton, J.M. (2003) Fine-scale genetic structure in a free-living ungulate population. Molecular Ecology, 12, 733–742.Google Scholar
Coltman, D.W., Pilkington, J.G., Smith, J.A. & Pemberton, J.M. (1999) Parasite-mediated selection against inbred Soay sheep in a free-living, island population. Evolution, 53, 1259–1267.Google Scholar
Coltman, D.W., Wilson, K., Pilkington, J.G., Stear, M.J. & Pemberton, J.M. (2001b) A microsatellite polymorphism in the gamma interferon gene is associated with resistance to gastrointestinal nematodes in a naturally parasitized population of Soay sheep. Parasitology, 122, 571–582.Google Scholar
Connelly, L., Craig, B.H., Jones, B. & Alexander, C.L. (2013) Genetic diversity of Cryptosporidium spp. within a remote population of Soay Sheep on St. Kilda Islands, Scotland. Applied and Environmental Microbiology, 79, 2240–2246.Google Scholar
Cornell, S.J. (2010) Modelling stochastic transmission processes in helminth infections. In: Michael, E. & Spear, R.C. (eds.), Modelling Parasite Transmission & Control (pp. 66–78). New York, NY: Springer.Google Scholar
Coulson, T. (2012) Integral projections models, their construction and use in posing hypotheses in ecology. Oikos, 121, 1337–1350.Google Scholar
Coulson, T., Albon, S., Pilkington, J.G. & Clutton-Brock, T.H. (1999) Small-scale spatial dynamics in a fluctuating ungulate population. Journal of Animal Ecology, 68, 658–671.Google Scholar
Coulson, T., Catchpole, E.A., Albon, S.D., et al. (2001) Age, sex, density, winter weather, and population crashes in Soay sheep. Science, 292, 1528–1531.Google Scholar
Coulson, T., Kendall, B.E., Barthold, J., et al. (2017) Modeling adaptive and nonadaptive responses of populations to environmental change. The American Naturalist, 190, 313–336.Google Scholar
Coulson, T., Tuljapurkar, S. & Childs, D.Z. (2010) Using evolutionary demography to link life history theory, quantitative genetics and population ecology. Journal of Animal Ecology, 79, 1226–1240.Google Scholar
Craig, B.H. (2005) Parasite diversity in a free-living host population. Thesis, University of Edinburgh.Google Scholar
Craig, B.H., Jones, O.R., Pilkington, J.G. & Pemberton, J.M. (2009) Re-establishment of nematode infra-community and host survivorship in wild Soay sheep following anthelmintic treatment. Veterinary Parasitology, 161, 47–52.Google Scholar
Craig, B.H., Pilkington, J.G., Kruuk, L.E.B. & Pemberton, J.M. (2007) Epidemiology of parasite protozoan infections in Soay sheep (Ovis aries L.) on St Kilda. Parasitology, 134, 9–21.Google Scholar
Craig, B.H., Pilkington, J.G. & Pemberton, J.M. (2006) Gastrointestinal nematode species burdens and host mortality in a feral sheep population. Parasitology, 133, 485–496.Google Scholar
Craig, B.H., Tempest, L.J., Pilkington, J.G. & Pemberton, J.M. (2008) Metazoan–protozoan parasite co-infections and host body weight in St Kilda Soay sheep. Parasitology, 135, 433–441.Google Scholar
Crawley, M., Albon, S., Bazely, D., et al. (2004) Vegetation and sheep population dynamics. In: Clutton-Brock, T.H. & Pemberton, J.M. (eds.), Soay Sheep: Dynamics and Selection in an Island Population (pp. 89–112). Cambridge: Cambridge University Press.Google Scholar
Cressler, C.E., Graham, A.L. & Day, T. (2015) Evolution of hosts paying manifold costs of defence. Proceedings of the Royal Society of London B, 282, 20150065.Google Scholar
Day, T., Alizon, S. & Mideo, N. (2011) Bridging scales in the evolution of infectious disease life-histories: theory. Evolution, 65, 3448–3461.Google Scholar
Denham, D.A. (1969) The development of Ostertagia circumcincta in lambs. Journal of Helminthology, 43, 299–310.Google Scholar
Doeschl-Wilson, A.B., Bishop, S., Kyriazakis, I. & Villanueva, B. (2012) Novel methods for quantifying individual host response to infectious pathogens for genetic analyses. Frontiers in Genetics, 3, 266.Google Scholar
Doeschl-Wilson, A.B. & Kyriazakis, I. (2012) Should we aim for genetic improvement in host resistance or tolerance to infectious pathogens? Frontiers in Genetics, 3, 272.Google Scholar
Doeschl-Wilson, A.B., Villanueva, B. & Kyriazakis, I. (2012) The first step towards genetic selection for host tolerance to infectious pathogens: obtaining the tolerance phenotype through group estimates. Frontiers in Genetics, 3, 265.Google Scholar
Easterling, M.R., Ellner, S.P. & Dixon, P.M. (2000) Size-specific sensitivity: applying a new structured population model. Ecology, 81, 694–708.Google Scholar
Ezenwa, V.O., Etienne, R.S., Gordon, L., Beja‐Pereira, A. & Jolles, A.E. (2010) Hidden consequences of living in a wormy world: nematode‐induced immune suppression facilitates tuberculosis invasion in African buffalo. The American Naturalist, 176, 613–624.Google Scholar
Ezenwa, V.O. & Jolles, A.E. (2015) Opposite effects of anthelmintic treatment on microbial infection at individual versus population scales. Science, 347, 175–177.Google Scholar
Fairlie, J., Holland, R., Pilkington, J.G., et al. (2016) Lifelong leukocyte telomere dynamics and survival in a free-living mammal. Aging Cell, 15, 140–148.Google Scholar
Feulner, P.G.D., Gratten, J., Kijas, J.W., et al. (2013) Introgression and the fate of domesticated genes in a wild mammal population. Molecular Ecology, 22, 4210–4221.Google Scholar
Fineblum, W.L. & Rausher, M.D. (1995) Tradeoff between resistance and tolerance to herbivore damage in a morning glory. Nature, 377, 517–520.Google Scholar
Garnier, R., Bento, A.I., Hansen, C., et al. (2017a) Physiological proteins in resource-limited herbivores experiencing a population die-off. The Science of Nature, 104, 68.Google Scholar
Garnier, R., Cheung, C.K., Watt, K.A., et al. (2017b) Joint associations of blood plasma proteins with overwinter survival of a large mammal. Ecology Letters, 20, 175–183.Google Scholar
Garnier, R. & Graham, A.L. (2014) Insights from parasite-specific serological tools in eco-immunology. Integrative and Comparative Biology, 54, 363–376.Google Scholar
Garnier, R., Grenfell, B.T., Nisbet, A.J., Matthews, J.B. & Graham, A.L. (2016) Integrating immune mechanisms to model nematode worm burden: an example in sheep. Parasitology, 143, 894–904.Google Scholar
Gibson, W., Pilkington, J.G. & Pemberton, J.M. (2010) Trypanosoma melophagium from the sheep ked Melophagus ovinus on the island of St Kilda. Parasitology, 137, 1799–1804.Google Scholar
Graham, A.L., Allen, J.E. & Read, A.F. (2005) Evolutionary causes and consequences of immunopathology. Annual Review of Ecology, Evolution, and Systematics, 36, 373–397.Google Scholar
Graham, A.L., Hayward, A.D., Watt, K.A., et al. (2010) Fitness correlates of heritable variation in antibody responsiveness in a wild mammal. Science, 330, 662–665.Google Scholar
Graham, A.L., Nussey, D.H., Lloyd-Smith, J.O., et al. (2016) Exposure to viral and bacterial pathogens among Soay sheep (Ovis aries) of the St Kilda archipelago. Epidemiology and Infection, 144, 1–10.Google Scholar
Graham, A.L., Shuker, D.M., Pollitt, L.C., et al. (2011) Fitness consequences of immune responses: strengthening the empirical framework for ecoimmunology. Functional Ecology, 25, 5–17.Google Scholar
Gratten, J., Beraldi, D., Lowder, B.V., et al. (2007) Compelling evidence that a single nucleotide substitution in TYRP1 is responsible for coat-colour polymorphism in a free-living population of Soay sheep. Proceedings of the Royal Society of London B, 274, 619–626.Google Scholar
Gratten, J., Pilkington, J.G., Brown, E.A., et al. (2010) The genetic basis of recessive self-colour pattern in a wild sheep population. Heredity, 104, 206–214.Google Scholar
Grenfell, B. & Dobson, A. (1995) Ecology of Infectious Diseases in Natural Populations. Cambridge: Cambridge University Press.Google Scholar
Grenfell, B.H., Price, O.F., Albon, S.D. & Clutton-Brock, T.H. (1992) Overcompensation and population cycles in an ungulate. Nature, 355, 823–826.Google Scholar
Grenfell, B.T., Wilson, K., Finkelstadt, B.F., et al. (1998) Noise and determinism in synchronized sheep dynamics. Nature, 394, 674–677.Google Scholar
Grenfell, B.T., Wilson, K., Isham, V.S., Boyd, H.E.G. & Dietz, K. (1995) Modelling patterns of parasite aggregation in natural populations: trichostrongylid nematode–ruminant interactions as a case study. Parasitology, 111, S135–S151.Google Scholar
Gulland, F.M.D. (1992) The role of nematode parasites in Soay sheep (Ovis aries L.) mortality during a population crash. Parasitology, 105, 493–503.Google Scholar
Gulland, F.M.D., Albon, S.D., Pemberton, J.M., Moorcroft, P.R. & Clutton-Brock, T.H. (1993) Parasite-associated polymorphism in a cyclic ungulate population. Proceedings of the Royal Society of London B, 254, 7–13.Google Scholar
Gulland, F.M.D. & Fox, M. (1992) Epidemiology of nematode infections of Soay sheep (Ovis aries L.) on St Kilda. Parasitology, 105, 481–492.Google Scholar
Halliday, A.M., Routledge, C.M., Smith, S.K., Matthews, J.B. & Smith, W.D. (2007) Parasite loss and inhibited development of Teladorsagia circumcincta in relation to the kinetics of the local IgA response in sheep. Parasite Immunology, 29, 425–434.Google Scholar
Hayward, A.D., Garnier, R., Watt, K.A., et al. (2014a) Heritable, heterogeneous, and costly resistance of sheep against nematodes and potential feedbacks to epidemiological dynamics. The American Naturalist, 184, S58–S76.Google Scholar
Hayward, A.D., Nussey, D.H., Wilson, A.J., et al. (2014b) Natural selection on individual variation in tolerance of gastrointestinal nematode infection. PLoS Biology, 12, e1001917.Google Scholar
Hayward, A.D., Pemberton, J.M., Bérénos, C., et al. (2018) Evidence for selection-by-environment but not genotype-by-environment interactions for fitness-related traits in a wild mammal population. Genetics, 208, 349–364.Google Scholar
Hayward, A.D., Wilson, A.J., Pilkington, J.G., et al. (2011) Natural selection on a measure of parasite resistance varies across ages and environmental conditions in a wild mammal. Journal of Evolutionary Biology, 24, 1664–1676.Google Scholar
Hayward, A.D., Wilson, A.J., Pilkington, J.G., Pemberton, J.M. & Kruuk, L.E.B. (2009) Ageing in a variable habitat: environmental stress affects senescence in parasite resistance in St Kilda Soay sheep. Proceedings of the Royal Society of London B, 276, 3477–3485.Google Scholar
Henderson, C.R. (1950) Estimation of genetic parameters. Annals of Mathematical Statistics, 21, 309–310.Google Scholar
Henrichs, B., Oosthuizen, M.C., Troskie, M., et al. (2016) Within guild co-infections influence parasite community membership: a longitudinal study in African Buffalo. Journal of Animal Ecology, 85, 1025–1034.Google Scholar
Hong, C., Michel, J.F. & Lancaster, M.B. (1987) Observations on the dynamics of worm burdens in lambs infected daily with Ostertagia circumcincta. International Journal for Parasitology, 17, 951–956.Google Scholar
Houdijk, J.G.M., Kyriazakis, I., Jackson, F., Huntley, J.F. & Coop, R.L. (2005) Effects of protein supply and reproductive status on local and systemic immune responses to Teladorsagia circumcincta in sheep. Veterinary Parasitology, 129, 105–117.Google Scholar
Hudson, P.J., Dobson, A.P. & Newborn, D. (1998) Prevention of population cycles by parasite removal. Science, 282, 2256–2258.Google Scholar
Hutchings, M.R., Milner, J.M., Gordon, I.J., Kyriazakis, I. & Jackson, F. (2002) Grazing decisions of Soay sheep, Ovis aries, on St Kilda: a consequence of parasite distribution? Oikos, 96, 235–244.Google Scholar
Jackson, J.A., Hall, A.J., Friberg, I.M., et al. (2014) An immunological marker of tolerance to infection in wild rodents. PLoS Biology, 12, e1001901.Google Scholar
Janeiro, M.J., Coltman, D.W., Festa-Bianchet, M., Pelletier, F. & Morrissey, M.B. (2017) Towards robust evolutionary inference with integral projection models. Journal of Evolutionary Biology, 30, 270–288.Google Scholar
Jewell, P.A., Milner, C. & Boyd, J.M. (1974) Island Survivors: The Ecology of the Soay Sheep of St Kilda. London: Athlone Press.Google Scholar
Johnston, S.E., Bérénos, C., Slate, J. & Pemberton, J.M. (2016) Conserved genetic architecture underlying individual recombination rate variation in a wild population of Soay sheep (Ovis aries). Genetics, 203, 583–598.Google Scholar
Johnston, S.E., Gratten, J., Berenos, C., et al. (2013) Life history trade-offs at a single locus maintain sexually selected genetic variation. Nature, 502, 93–95.Google Scholar
Johnston, S.E., McEwan, J.C., Pickering, N.K., et al. (2011) Genome-wide association mapping identifies the genetic basis of discrete and quantitative variation in sexual weaponry in a wild sheep population. Molecular Ecology, 20, 2555–2566.Google Scholar
Jolles, A.E., Ezenwa, V.O., Etienne, R.S., Turner, W.C. & Olff, H. (2008) Interactions between macroparasites and microparasites drive infection patterns in free-ranging African buffalo. Ecology, 89, 2239–2250.Google Scholar
Jones, O.R., Anderson, R.M. & Pilkington, J.G. (2006) Parasite-induced anorexia in a free-ranging mammalian herbivore: an experimental test using Soay sheep. Canadian Journal of Zoology, 84, 685–692.Google Scholar
Jones, O.R., Crawley, M.J., Pilkington, J.G. & Pemberton, J.M. (2005) Predictors of early survival in Soay sheep: cohort-, maternal-, and individual-level variation. Proceedings of the Royal Society of London B, 272, 2619–2625.Google Scholar
Kause, A. (2011) Genetic analysis of tolerance to infections using random regressions: a simulation study. Genetics Research, 93, 291–302.Google Scholar
Kause, A., van Dalen, S. & Bovenhuis, H. (2012) Genetics of ascites resistance and tolerance in chicken: a random regression approach. G3: Genes|Genomes|Genetics, 2, 527–535.Google Scholar
Kenyon, F., Sargison, N.D., Skuce, P.J. & Jackson, F. (2009) Sheep helminth parasitic disease in south eastern Scotland arising as a possible consequence of climate change. Veterinary Parasitology, 163, 293–297.Google Scholar
Kijas, J.W., Lenstra, J.A., Hayes, B., et al. (2012) Genome-wide analysis of the world’s sheep breeds reveals high levels of historic mixture and strong recent selection. PLoS Biology, 10, e1001258.Google Scholar
Klasing, K.C. (2004) The costs of immunity. Acta Zoologica Sinica, 50, 961–969.Google Scholar
Koski, K.G. & Scott, M.E. (2001) Gastrointestinal nematodes, nutrition and immunity: breaking the negative spiral. Annual Review of Nutrition, 21, 297–321.Google Scholar
Kruuk, L.E.B. (2004) Estimating genetic parameters in natural populations using the ‘animal model’. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, 359, 873–890.Google Scholar
Lawson Handley, L.-J., Byrne, K., Santucci, F., et al. (2007) Genetic structure of European sheep breeds. Heredity, 99, 620–631.Google Scholar
Lello, J., Boag, B., Fenton, A., Stevenson, I.R. & Hudson, P.J. (2004) Competition and mutualism among the gut helminths of a mammalian host. Nature, 428, 840–844.Google Scholar
Lippens, C., Guivier, E., Faivre, B. & Sorci, G. (2016) Reaction norms of host immunity, host fitness and parasite performance in a mouse–intestinal nematode interaction. International Journal for Parasitology, 46, 133–140.Google Scholar
Liu, W.-C., Bonsall, M.B. & Godfray, H.C.J. (2007) The form of host density-dependence and the likelihood of host–pathogen cycles in forest–insect systems. Theoretical Population Biology, 72, 86–95.Google Scholar
Lloyd-Smith, J.O., Schreiber, S.J., Kopp, P.E. & Getz, W.M. (2005) Superspreading and the effect of individual variation on disease emergence. Nature, 438, 355–359.Google Scholar
Lochmiller, R.L. & Deerenberg, C. (2000) Tradeoffs in evolutionary immunology: just what is the cost of immunity? Oikos, 88, 87–98.Google Scholar
Martinez-Valldares, M., Vara-Del Rio, M.P., Cruz-Rojo, M.A. & Rojo-Vazquez, F.A. (2005) Genetic resistance to Teladorsagia circumcincta: IgA and parameters at slaughter in Churra sheep. Parasite Immunology, 27, 213–218.Google Scholar
May, R.M. & Anderson, R.M. (1978) Regulation and stability of host–parasite population interactions: II. Destabilizing processes. Journal of Animal Ecology, 47, 249–267.Google Scholar
May, R.M. & Anderson, R.M. (1979) Population biology of infectious diseases: Part II. Nature, 280, 455–461.Google Scholar
Mazé-Guilmo, E., Loot, G., Páez, D.J., Lefèvre, T. & Blanchet, S. (2014) Heritable variation in host tolerance and resistance inferred from a wild host–parasite system. Proceedings of the Royal Society of London B, 281, 20132567.Google Scholar
McNeilly, T.N., Devaney, E. & Matthews, J.B. (2009) Teladorsagia circumcincta in the sheep abomasum: defining the role of dendritic cells in T cell regulation and protective immunity. Parasite Immunology, 31, 347–356.Google Scholar
McRae, K.M., Stear, M.J., Good, B. & Keane, O.M. (2015) The host immune response to gastrointestinal nematode infection in sheep. Parasite Immunology, 37, 605–613.Google Scholar
Medzhitov, R., Schneider, D.S. & Soares, M.P. (2012) Disease tolerance as a defense strategy. Science, 335, 936–941.Google Scholar
Metcalf, C.J.E., Graham, A.L., Martinez-Bakker, M. & Childs, D.Z. (2016) Opportunities and challenges of Integral Projection Models for modelling host–parasite dynamics. Journal of Animal Ecology, 85, 343–355.Google Scholar
Mideo, N., Nelson, W.A., Reece, S.E., et al. (2011) Bridging scales in the evolution of infectious disease life histories: application. Evolution, 65, 3298–3310.Google Scholar
Miller, M.R., White, A. & Boots, M. (2005) The evolution of host resistance: tolerance and control as distinct strategies. Journal of Theoretical Biology, 236, 198–207.Google Scholar
Miller, M.R., White, A. & Boots, M. (2006) The evolution of parasites in response to tolerance in their hosts: the good, the bad, and apparent commensalism. Evolution, 60, 945–956.Google Scholar
Milner, J.M., Albon, S.D., Illius, A.W., Pemberton, J.M. & Clutton-Brock, T.H. (1999) Repeated selection of morphometric traits in the Soay sheep on St Kilda. Journal of Animal Ecology, 68, 472–488.Google Scholar
Milner, J.M., Elston, D.A. & Albon, S.D. (1999) Estimating the contributions of population density and climatic fluctuations to interannual variation in survival of Soay sheep. Journal of Animal Ecology, 68, 1235–1247.Google Scholar
Moore, S.L. & Wilson, K. (2002) Parasites as a viability cost of sexual selection in natural populations of mammals. Science, 297, 2015–2018.Google Scholar
Morales-Montor, J., Chavarria, A., De León, M.A., et al. (2004) Host gender in parasitic infections of mammals: an evaluation of the female host supremacy paradigm. Journal of Parasitology, 90, 531–546.Google Scholar
Morgan, E.R. & van Dijk, J. (2012) Climate and the epidemiology of gastrointestinal nematode infections of sheep in Europe. Veterinary Parasitology, 189, 8–14.Google Scholar
Murphy, L., Pathak, A.K. & Cattadori, I.M. (2013) A co-infection with two gastrointestinal nematodes alters host immune responses and only partially parasite dynamics. Parasite Immunology, 35, 421–432.Google Scholar
Murray, D.L., Cox, E.W., Ballard, W.B., et al. (2006) Pathogens, nutritional deficiency, and climate influences on a declining moose population. Wildlife Monographs, 166, 1–30.Google Scholar
Nielsen, M.K., Kaplan, R.M., Thamsborg, S.M., Monrad, J. & Olsen, S.N. (2007) Climatic influences on development and survival of free-living stages of equine strongyles: implications for worm control strategies and managing anthelmintic resistance. The Veterinary Journal, 174, 23–32.Google Scholar
Nieuwhof, G.J. & Bishop, S.C. (2005) Costs of the major endemic diseases of sheep in Great Britain and the potential benefits of reduction in disease impact. Animal Science, 81, 23–29.Google Scholar
Nisbet, A.J., McNeilly, T.N., Wildblood, L.A., et al. (2013) Successful immunization against a parasitic nematode by vaccination with recombinant proteins. Vaccine, 31, 4017–4023.Google Scholar
Nussey, D.H., Watt, K., Pilkington, J.G., Zamoyska, R. & McNeilly, T.N. (2012) Age-related variation in immunity in a wild mammal population. Aging Cell, 11, 178–180.Google Scholar
Nussey, D.H., Watt, K.A., Clark, A., et al. (2014) Multivariate immune defences and fitness in the wild: complex but ecologically important associations among plasma antibodies, health and survival. Proceedings of the Royal Society of London B, 281, 20132931.Google Scholar
Ozgul, A., Childs, D.Z., Oli, M.K., et al. (2010) Coupled dynamics of body mass and population growth in response to environmental change. Nature, 466, 482–485.Google Scholar
Ozgul, A., Coulson, T., Reynolds, A., Cameron, T.C. & Benton, T.G. (2012) Population responses to perturbations: the importance of trait-based analysis illustrated through a microcosm experiment. The American Naturalist, 179, 582–594.Google Scholar
Pacala, S.W. & Dobson, A.P. (1988) The relation between the number of parasites/host and host age: population dynamic causes and maximum likelihood estimation. Parasitology, 96, 197–210.Google Scholar
Paterson, S., Wilkes, C., Bleay, C. & Viney, M.E. (2008) Immunological responses elicited by different infection regimes with Strongyloides ratti. PLoS ONE, 3, e2509.Google Scholar
Paterson, S., Wilson, K. & Pemberton, J.M. (1998) Major histocompatibility complex variation associated with juvenile survival and parasite resistance in a large unmanaged ungulate population (Ovis aries L.). Proceedings of the National Academy of Sciences of the United States of America, 95, 3714–3719.Google Scholar
Pathak, A.K., Pelensky, C., Boag, B. & Cattadori, I.M. (2012) Immuno-epidemiology of chronic bacterial and helminth co-infections: observations from the field and evidence from the laboratory. International Journal for Parasitology, 42, 647–655.Google Scholar
Pedersen, A.B. & Greives, T.J. (2008) The interaction of parasites and resources cause crashes in a wild mouse population. Journal of Animal Ecology, 77, 370–377.Google Scholar
Pemberton, J.M., Coltman, D.W., Bancroft, D.R., Smith, J.A. & Paterson, S. (2004) Molecular genetic variation and selection on phenotype. In: Clutton-Brock, T.H. & Pemberton, J.M. (eds.), Soay Sheep: Dynamics and Selection in an Island Population (pp. 217–242). Cambridge: Cambridge University Press.Google Scholar
Penczykowski, R.M., Walker, E., Soubeyrand, S. & Laine, A.-L. (2015) Linking winter conditions to regional disease dynamics in a wild plant–pathogen metapopulation. New Phytologist, 205, 1142–1152.Google Scholar
Pernthaner, A., Cole, S.-A., Morrison, L., et al. (2006) Cytokine and antibody subclass responses in the intestinal lymph of sheep during repeated experimental infections with the nematode parasite Trichostrongylus colubriformis. Veterinary Immunology and Immunopathology, 114, 135–148.Google Scholar
Preston, B.T., Stevenson, I.R., Pemberton, J.M., Coltman, D.W. & Wilson, K. (2003) Overt and covert competition in a promiscuous mammal: the importance of weaponry and testes size to male reproductive success. Proceedings of the Royal Society of London B, 270, 633–640.Google Scholar
Råberg, L., Graham, A.L. & Read, A.F. (2009) Decomposing health: tolerance and resistance to parasites in animals. Philosophical Transactions of the Royal Society of London B, 364, 37–49.Google Scholar
Råberg, L., Sim, D. & Read, A.F. (2007) Disentangling genetic variation for resistance and tolerance to infectious diseases in animals. Science, 318, 812–814.Google Scholar
Rees, M., Childs, D.Z. & Ellner, S.P. (2014) Building integral projection models: a user’s guide. Journal of Animal Ecology, 83, 528–545.Google Scholar
Rees, M. & Ellner, S.P. (2009) Integral projection models for populations in temporally varying environments. Ecological Monographs, 79, 575–594.Google Scholar
Rees, M. & Ellner, S.P. (2016) Evolving integral projection models: evolutionary demography meets eco-evolutionary dynamics. Methods in Ecology and Evolution, 7, 157–170.Google Scholar
Restif, O. & Koella, J.C. (2003) Shared control of epidemiological traits in a coevolutionary model of host–parasite interactions. The American Naturalist, 161, 827–836.Google Scholar
Restif, O. & Koella, J.C. (2004) Concurrent evolution of resistance and tolerance to pathogens. The American Naturalist, 164, E90–E102.Google Scholar
Robinson, M.R., Pilkington, J.G., Clutton-Brock, T.H., Pemberton, J.M. & Kruuk, L.E.B. (2008) Environmental heterogeneity generates fluctuating selection on a secondary sexual trait. Current Biology, 18, 751–757.Google Scholar
Robinson, M.R., Wilson, A.J., Pilkington, J.G., et al. (2009) The impact of environmental heterogeneity on genetic architecture in a wild population of Soay sheep. Genetics, 181, 1639–1648.Google Scholar
Roy, B.A. & Kirchner, J.W. (2000) Evolutionary dynamics of pathogen resistance and tolerance. Evolution, 54, 51–63.Google Scholar
Sahoo, A., Pattanaik, A.K. & Goswami, T.K. (2009) Immunobiochemical status of sheep exposed to periods of experimental protein deficit and realimentation. Journal of Animal Science, 87, 2664–2673.Google Scholar
Sand, K.M.K., Bern, M., Nilsen, J., et al. (2015) Unraveling the interaction between FcRn and albumin: opportunities for design of albumin-based therapeutics. Frontiers in Immunology, 5, 682.Google Scholar
Sayre, B.L. & Harris, G.C. (2012) Systems genetics approach reveals candidate genes for parasite resistance from quantitative trait loci studies in agricultural species. Animal Genetics, 43, 190–198.Google Scholar
Schmid-Hempel, P. (2003) Variation in immune defence as a question of evolutionary ecology. Proceedings of the Royal Society of London B, 270, 357–366.Google Scholar
Schneider, D.S. & Ayres, J.S. (2008) Two ways to survive infection: what resistance and tolerance can teach us about treating infectious disease. Nature Reviews Immunology, 8, 889–895.Google Scholar
Scott, M.E. (1991) Heligmosomoides polygyrus (Nematoda): susceptible and resistant strains of mice are indistinguishable following natural infection. Parasitology, 103, 429–438.Google Scholar
Scott, M.E. (2006) High transmission rates restore expression of genetically determined susceptibility of mice to nematode infections. Parasitology, 132, 669–679.Google Scholar
Shaw, D.J. & Dobson, A.P. (1995) Patterns of macroparasite abundance and aggregation in wildlife populations: a quantitative review. Parasitology, 111, S111–S133.Google Scholar
Shaw, D.J., Grenfell, B.T. & Dobson, A.P. (1998) Patterns of macroparasite aggregation in wildlife host populations. Parasitology, 117, 597–610.Google Scholar
Sheldon, B.C. & Verhulst, S. (1996) Ecological immunity: costly parasite defences and tradeoffs in evolutionary ecology. Trends in Ecology and Evolution, 11, 317–321.Google Scholar
Simms, E. (2000) Defining tolerance as a norm of reaction. Evolutionary Ecology, 14, 563–570.Google Scholar
Simpson, H.V. (2000) Pathophysiology of abomasal parasitism: is the host or parasite responsible? The Veterinary Journal, 160, 177–191.Google Scholar
Smith, J.A., Wilson, K., Pilkington, J.G. & Pemberton, J.M. (1999) Heritable variation in resistance to gastrointestinal nematodes in an unmanaged mammal population. Proceedings of the Royal Society of London B, 266, 1283–1290.Google Scholar
Smith, W.D., Jackson, F., Jackson, E. & Williams, J. (1985) Age immunity to Ostertagia circumcincta: comparison of the local immune responses of 4 1/2- and 10-month-old lambs. Journal of Comparative Pathology, 95, 235–245.Google Scholar
Sparks, A.M., Watt, K., Sinclair, R., et al. (2019) The genetic architecture of helminth-specific immune responses in a wild population of Soay sheep (Ovis aries). bioRxiv 02871.Google Scholar
Stear, M.J., Bishop, S.C., Doligalska, M., et al. (1995) Regulation of egg production, worm burden, worm length and worm fecundity by host responses in sheep infected with Ostertagia circumcincta. Parasite Immunology, 17, 643–652.Google Scholar
Steele, T. (1979) The Life and Death of St Kilda. Glasgow: Fontana/Collins.Google Scholar
Tate, A.T. & Graham, A.L. (2015) Dynamic patterns of parasitism and immunity across host development influence optimal strategies of resource allocation. The American Naturalist, 186, 495–512.Google Scholar
Tate, A.T. & Rudolf, V.H.W. (2012) Impact of life stage specific immune priming on invertebrate disease dynamics. Oikos, 121, 1083–1092.Google Scholar
Tempest, L.J. (2005) Parasites and the cost of reproduction in Soay sheep. PhD thesis, University of Stirling.Google Scholar
Thrall, P. & Antonovics, J. (1994) The cost of resistance and the maintenance of genetic polymorphisms in host–pathogen systems. Proceedings of the Royal Society of London B, 257, 105–110.Google Scholar
Tidbury, H.J., Best, A. & Boots, M. (2012) The epidemiological consequences of immune priming. Proceedings of the Royal Society of London B, 279, 4505–4512.Google Scholar
Torgerson, P.R., Pilkington, J., Gulland, F.M.D. & Gemmell, M.A. (1995) Further evidence for the long distance dispersal of taeniid eggs. International Journal for Parasitology, 25, 265–267.Google Scholar
Traill, L.W., Schindler, S. & Coulson, T. (2014) Demography, not inheritance, drives phenotypic change in hunted bighorn sheep. Proceedings of the National Academy of Sciences of the United States of America, 111, 13,223–13,228.Google Scholar
Watson, M.J. (2013) What drives population-level effects of parasites? Meta-analysis meets life-history. International Journal for Parasitology: Parasites and Wildlife, 2, 190–196.Google Scholar
Watson, R.L., Bird, E.J., Underwood, S., et al. (2017) Sex differences in leucocyte telomere length in a free-living mammal. Molecular Ecology, 26, 3230–3240.Google Scholar
Watson, R.L., McNeilly, T.N., Watt, K.A., et al. (2016) Cellular and humoral immunity in a wild mammal: variation with age & sex and association with overwinter survival. Ecology and Evolution, 6, 8695–8705.Google Scholar
Watt, K.A., Nussey, D.H., Maclellan, R., Pilkington, J.G. & McNeilly, T.N. (2016) Fecal antibody levels as a noninvasive method for measuring immunity to gastrointestinal nematodes in ecological studies. Ecology and Evolution, 6, 56–67.Google Scholar
Westra, E.R., van Houte, S., Oyesiku-Blakemore, S., et al. (2015) Parasite exposure drives selective evolution of constitutive versus inducible defense. Current Biology, 25, 1043–1049.Google Scholar
Wilber, M.Q., Knapp, R.A., Toothman, M. & Briggs, C.J. (2017) Resistance, tolerance and environmental transmission dynamics determine host extinction risk in a load-dependent amphibian disease. Ecology Letters, 20, 1169–1181.Google Scholar
Wilber, M.Q., Langwig, K.E., Kilpatrick, A.M., McCallum, H.I. & Briggs, C.J. (2016) Integral projection models for host–parasite systems with an application to amphibian chytrid fungus. Methods in Ecology and Evolution, 7, 1182–1194.Google Scholar
Wilson, A.J., Pemberton, J.M., Pilkington, J.G., et al. (2006) Environmental coupling of selection and heritability limits evolution. PLoS Biology, 4, 1270–1275.Google Scholar
Wilson, A.J., Réale, D., Clements, M.N., et al. (2010) An ecologist’s guide to the animal model. Journal of Animal Ecology, 79, 13–26.Google Scholar
Wilson, K., Bjornstad, O.N., Dobson, A.P., et al. (2002) Heterogeneities in macroparasite infections: patterns and processes. In: Hudson, P.J., Rizzoli, A., Grenfell, B.T., Heesterbeek, H. & Dobson, A.P. (eds.), The Ecology of Wildlife Diseases (pp. 6–44). Oxford: Oxford University Press.Google Scholar
Wilson, K., Grenfell, B.T., Pilkington, J.G., Boyd, H.E.G. & Gulland, F.M.D. (2004) Parasites and their impact. In: Clutton-Brock, T.H. & Pemberton, J.M. (eds.), Soay Sheep: Dynamics and Selection in an Island Population (pp. 113–165). Cambridge: Cambridge University Press.Google Scholar
Wilson, K., Grenfell, B.T. & Shaw, D.J. (1996) Analysis of aggregated parasite distributions: a comparison of methods. Functional Ecology, 10, 592–601.Google Scholar
Zuk, M. & McKean, K.A. (1996) Sex differences in parasite infections: patterns and processes. International Journal for Parasitology, 26, 1009–1024.Google Scholar

References

Abu Samra, N., Jori, F., Xiao, L.H., Rikhotso, O. & Thompson, P.N. (2013) Molecular characterization of Cryptosporidium species at the wildlife/livestock interface of the Kruger National Park, South Africa. Comparative Immunology, Microbiology and Infectious Diseases, 36, 295–302.Google Scholar
Allen, J.E. & Maizels, R.M. (2011) Diversity and dialogue in immunity to helminths. Nature Reviews Immunology, 11, 375–388.Google Scholar
Anderson, E.C. & Rowe, L.W. (1998) The prevalence of antibody to the viruses of bovine virus diarrhoea, bovine herpes virus 1, rift valley fever, ephemeral fever and bluetongue and to Leptospira sp. in free-ranging wildlife in Zimbabwe. Epidemiology and Infection, 121, 441–449.Google Scholar
Anderson, R.M. & May, R.M. (1991) Infectious Diseases of Humans:Dynamics and Control. Oxford: Oxford University Press.Google Scholar
Atherstone, C., Picozzi, K. & Kalema-Zikusoka, G. (2014) Short Report: Seroprevalence of Leptospira Hardjo in cattle and African buffalos in Southwestern Uganda. American Journal of Tropical Medicine and Hygiene, 90, 288–290.Google Scholar
Ayebazibwe, C., Mwiine, F.N., Balinda, S.N., Tjornehoj, K. & Alexandersen, S. (2012) Application of the Ceditest (R) FMDV type O and FMDV-NS enzyme-linked immunosorbent assays for detection of antibodies against foot-and-mouth disease virus in selected livestock and wildlife species in Uganda. Journal of Veterinary Diagnostic Investigation, 24, 270–276.Google Scholar
Beechler, B.R., Bengis, R., Swanepoel, R., et al. (2015a) Rift Valley Fever in Kruger National Park: do buffalo play a role in the inter-epidemic circulation of virus? Transboundary and Emerging Diseases, 62, 24–32.Google Scholar
Beechler, B.R., Manore, C.A., Reininghaus, B., et al. (2015b) Enemies and turncoats: bovine tuberculosis exposes pathogenic potential of Rift Valley fever virus in a common host, African buffalo (Syncerus caffer). Proceedings of the Royal Society of London B, 282, 20142942.Google Scholar
Bender, E.A., Case, T.J. & Gilpin, M.E. (1984) Perturbation experiments in community ecology: theory and practice. Ecology, 65, 1–13.Google Scholar
Beura, L.K., Hamilton, S.E., Bi, K., et al. (2016) Normalizing the environment recapitulates adult human immune traits in laboratory mice. Nature, 532, 512–516.Google Scholar
Biron, C.A., Nguyen, K.B., Pien, G.C., Cousens, L.P. & Salazar-Mather, T.P. (1999) Natural killer cells in antiviral defense: function and regulation by innate cytokines. Annual Review of Immunology, 17, 189–220.Google Scholar
Brown, J.H., Whitham, T.G., Morgan Ernest, S.K. & Gehring, C.A. (2001) Complex species interactions and the dynamics of ecological systems: long-term experiments. Science, 293, 643.Google Scholar
Budischak, S.A., Hoberg, E.P., Abrams, A., Jolles, A.E. & Ezenwa, V.O. (2015) A combined parasitological molecular approach for noninvasive characterization of parasitic nematode communities in wild hosts. Molecular Ecology Resources, 15, 1112–1119.Google Scholar
Budischak, S.A., Hoberg, E.P., Abrams, A., Jolles, A.E. & Ezenwa, V.O. (2016) Experimental insight into the process of parasite community assembly. Journal of Animal Ecology, 85, 1222–1233.Google Scholar
Budischak, S.A., Jolles, A.E. & Ezenwa, V.O. (2012) Direct and indirect costs of co-infection in the wild: linking gastrointestinal parasite communities, host hematology, and immune function. International Journal for Parasitology: Parasites and Wildlife, 1, 2–12.Google Scholar
Budischak, S.A., O’Neal, D., Jolles, A.E. & Ezenwa, V.O. (2018) Differential host responses to parasitism shape divergent fitness costs of infection. Functional Ecology, 32, 324–333.Google Scholar
Callaway, R.M. & Walker, L.R. (1997) Competition and facilitation: a synthetic approach to interactions in plant communities. Ecology, 78, 1958–1965.Google Scholar
Chaisi, M.E., Sibeko, K.P., Collins, N.E., Potgieter, F.T. & Oosthuizen, M.C. (2011) Identification of Theileria parva and Theileria sp. (buffalo) 18S rRNA gene sequence variants in the African Buffalo (Syncerus caffer) in southern Africa. Veterinary Parasitology, 182, 150–162.Google Scholar
Chenine, A.L., Shai-Kobiler, E., Steele, L.N., et al. (2008) Acute Schistosoma mansoni infection increases susceptibility to systemic SHIV clade C infection in rhesus macaques after mucosal virus exposure. PLoS Neglected Tropical Diseases, 2, e265.Google Scholar
Cousins, D.V., Huchzermeyer, H., Griffin, J., Van Rensburg, I.B.J.B.G. & Kriek, N. (2004) Tuberculosis. In: Coetzer, J. & Tustin, R.C. (eds.), Infectious Diseases of Livestock. (pp. 1973–1991). Oxford: Oxford University Press.Google Scholar
Cox, F.E.G. (2001) Concomitant infections, parasites and immune responses. Parasitology, 122, S23–S38.Google Scholar
Dini-Andreote, F., Stegen, J.C., van Elsas, J.D. & Salles, J.F. (2015) Disentangling mechanisms that mediate the balance between stochastic and deterministic processes in microbial succession. Proceedings of the National Academy of Sciences of the United States of America, 112, E1326–E1332.Google Scholar
Else, K.J. & Finkelman, F.D. (1998) Intestinal nematode parasites, cytokines and effector mechanisms. International Journal for Parasitology, 28, 1145–1158.Google Scholar
Entrican, G. (2002) Immune regulation during pregnancy and host–pathogen interactions in infectious abortion. Journal of Comparative Pathology, 126, 79–94.Google Scholar
Eygelaar, D., Jori, F., Mokopasetso, M., et al. (2015) Tick-borne haemoparasites in African buffalo (Syncerus caffer) from two wildlife areas in Northern Botswana. Parasites & Vectors, 8, 26.Google Scholar
Ezenwa, V.O. (2004) Host social behavior and parasitic infection: a multifactorial approach. Behavioral Ecology, 15, 446–454.Google Scholar
Ezenwa, V.O., Etienne, R.S., Luikart, G., Beja-Pereira, A. & Jolles, A.E. (2010) Hidden consequences of living in a wormy world: nematode-induced immune suppression facilitates tuberculosis invasion. American Naturalist, 176, 613–624.Google Scholar
Ezenwa, V.O. & Jolles, A.E. (2015) Opposite effects of anthelmintic treatment on microbial infection at individual versus population scales. Science, 347, 175–177.Google Scholar
Ezenwa, V.O., Price, S.A., Altizer, S., Vitone, N.D. & Cook, K.C. (2006) Host traits and parasite species richness in even and odd‐toed hoofed mammals, Artiodactyla and Perissodactyla. Oikos, 115, 526–536.Google Scholar
Fagbo, S., Coetzer, J.A.W. & Venter, E.H. (2014) Seroprevalence of Rift Valley fever and lumpy skin disease in African buffalo (Syncerus caffer) in the Kruger National Park and Hluhluwe-iMfolozi Park, South Africa. Journal of the South African Veterinary Association, 85, e1–e7.Google Scholar
Fayle, T.M., Eggleton, P., Manica, A., Yusah, K.M. & Foster, W.A. (2015) Experimentally testing and assessing the predictive power of species assembly rules for tropical canopy ants. Ecology Letters, 18, 254–262.Google Scholar
Fenton, A., Knowles, S.C.L., Petchey, O.L. & Pedersen, A.B. (2014) The reliability of observational approaches for detecting interspecific parasite interactions: comparison with experimental results. International Journal for Parasitology, 44, 437–445.Google Scholar
Fischer, N., Indenbirken, D., Meyer, T., et al. (2015) Evaluation of unbiased next-generation sequencing of RNA (RNA-seq) as a diagnostic method in influenza virus-positive respiratory samples. Journal of Clinical Microbiology, 53, 2238–2250.Google Scholar
Fitzgerald, S.D. & Kaneene, J.B. (2013) Wildlife reservoirs of bovine tuberculosis worldwide: hosts, pathology, surveillance, and control. Veterinary Pathology, 50, 488–499.Google Scholar
Flick, R. & Bouloy, M. (2005) Rift Valley fever virus. Current Molecular Medicine, 5, 827–834.Google Scholar
Flynn, J.L. & Chan, J. (2001) Immunology of tuberculosis. Annual Review of Immunology, 19, 93–129.Google Scholar
Gomo, C., de Garine-Wichatitsky, M., Caron, A. & Pfukenyi, D.M. (2012) Survey of brucellosis at the wildlife–livestock interface on the Zimbabwean side of the Great Limpopo Transfrontier Conservation Area. Tropical Animal Health and Production, 44, 77–85.Google Scholar
Gradwell, D.V., Schutte, A.P., Vanniekerk, C.A. & Roux, D.J. (1977) Isolation of Brucella abortus biotype 1 from African buffalo in Kruger National Park. Journal of the South African Veterinary Association, 48, 41–43.Google Scholar
Graham, A.L. (2008) Ecological rules governing helminth–microparasite coinfection. Proceedings of the National Academy of Sciences of the United States of America, 105, 566–570.Google Scholar
Griffiths, E.C., Pedersen, A.B., Fenton, A. & Petchey, O.L. (2014) Analysis of a summary network of co-infection in humans reveals that parasites interact most via shared resources. Proceedings of the Royal Society of London B, 281, 20132286.Google Scholar
Hamblin, C., Anderson, E.C., Jago, M., Mlengeya, T. & Hipji, K. (1990) Antibodies to some pathogenic agents in free-living wild species in Tanzania. Epidemiology and Infection, 105, 585–594.Google Scholar
Hamblin, C., Hedger, R.S. & Condy, J.B. (1980) The isolation of parainfluenza 3 virus from free-living African buffalo (Syncerus caffer). Veterinary Record, 107, 18.Google Scholar
Henrichs, B., Oosthuizen, M.C., Troskie, M., et al. (2016) Within guild co-infections influence parasite community membership: a longitudinal study in African Buffalo. Journal of Animal Ecology, 85, 1025–1034.Google Scholar
Hoberg, E.P., Abrams, A. & Ezenwa, V.O. (2008) An exploration of diversity among the Ostertagiinae (Nematoda: Trichostrongyloidea) in ungulates from sub-Saharan Africa with a proposal for a new genus. Journal of Parasitology, 94, 230–251.Google Scholar
Hoberg, E.P., Abrams, A. & Pilitt, P.A. (2010) A new species of trichostrongyloid in African buffalo (Syncerus caffer). The Journal of Parasitology, 96, 129–136.Google Scholar
Hoverman, J.T., Hoye, B.J. & Johnson, P.T.J. (2013) Does timing matter? How priority effects influence the outcome of parasite interactions within hosts. Oecologia, 173, 1471–1480.Google Scholar
Jolles, A.E., Etienne, R.S. & Olff, H. (2006) Independent and competing disease risks: implications for host populations in variable environments. American Naturalist, 167, 745–757.Google Scholar
Jolles, A.E., Ezenwa, V.O., Etienne, R.S., Turner, W.C. & Olff, H. (2008) Interactions between macroparasites and microparasites drive infection patterns in free-ranging African buffalo. Ecology, 89, 2239–2250.Google Scholar
Jolles, A.E., Le Roex, N.I.C.K.I., Flacke, G., et al. (2017) Wildlife disease dynamics in carnivore and herbivore hosts in the Hluhluwe-iMfolozi Park. In: Cromsigt, J.P., Archibald, S. & Owen-Smith, N. (eds.), Conserving Africa’s Mega-Diversity in the Anthropocene: The Hluhluwe-iMfolozi Park Story. Cambridge: Cambridge University Press.Google Scholar
Knowles, S.C., Fenton, A., Petchey, O.L., et al. (2013) Stability of within-host–parasite communities in a wild mammal system. Proceedings of the Royal Society of London B, 280, 20130598.Google Scholar
Krasnov, B.R., Pilosof, S., Stanko, M., et al. (2014) Co-occurrence and phylogenetic distance in communities of mammalian ectoparasites: limiting similarity versus environmental filtering. Oikos, 123, 63–70.Google Scholar
Kreisinger, J., Bastien, G., Hauffe, H.C., Marchesi, J. & Perkins, S.E. (2015) Interactions between multiple helminths and the gut microbiota in wild rodents. Philosophical Transactions of the Royal Society of London B:Biological Sciences, 370, 20140295.Google Scholar
Kuris, A.M. (1990) Guild structure of larval trematodes in molluscan hosts: Prevalence, dominance, and significance of competition. In: Esch, G.W., Bush, A.O. & Aho, J.M. (eds.), Parasite Communities: Patterns and Processes (pp. 69–100). London: Chapman and Hall.Google Scholar
Lello, J., Boag, B., Fenton, A., Stevenson, I.R. & Hudson, P.J. (2004) Competition and mutualism among the gut helminths of a mammalian host. Nature, 428, 840–844.Google Scholar
Levitt, B., Obala, A., Langdon, S., et al. (2017) Overlap extension barcoding for the next generation sequencing and genotyping of Plasmodium falciparum in individual patients in Western Kenya. Scientific Reports, 7, 41108.Google Scholar
Lowry, E., Rollinson, E.J., Laybourn, A.J., et al. (2013) Biological invasions: a field synopsis, systematic review, and database of the literature. Ecology & Evolution, 3, 182–196.Google Scholar
Maggioli, M.F., Palmer, M.V., Thacker, T.C., Vordermeier, H.M. & Waters, W.R. (2015) Characterization of effector and memory T cell subsets in the immune response to bovine tuberculosis in cattle. PLoS ONE, 10, e0122571.Google Scholar
Maizels, R.M., Hewitson, J.P., Murray, J., et al. (2012) Immune modulation and modulators in Heligmosomoides polygyrus infection. Experimental Parasitology, 132, 76–89.Google Scholar
Manore, C.A. & Beechler, B.R. (2015) Inter-epidemic and between-season persistence of rift valley fever: vertical transmission or cryptic cycling? Transboundary Emerging Diseases, 62, 13–23.Google Scholar
McSorley, H.J. & Maizels, R.M. (2012) Helminth infections and host immune regulation. Clinical Microbiology Reviews, 25, 585–608.Google Scholar
Michel, A.L. & Bengis, R.G. (2012) The African buffalo: a villain for inter-species spread of infectious diseases in southern Africa. Onderstepoort Journal of Veterinary Research, 79(2).Google Scholar
Miguel, E., Grosbois, V., Caron, A., et al. (2013) Contacts and foot and mouth disease transmission from wild to domestic bovines in Africa. Ecosphere, 4, art51.Google Scholar
Mollot, G., Pantel, J.H. & Romanuk, T.N. (2017) The effects of invasive species on the decline in species richness: a global meta-analysis. In: Bohan, D.A., Dumbrell, A.J. & Massol, F. (eds.), Advances in Ecological Research (pp. 61–83). New York, NY: Academic Press.Google Scholar
Morton, E.R., Lynch, J., Froment, A., et al. (2015) Variation in rural African gut microbiota is strongly correlated with colonization by Entamoeba and subsistence. PLOS Genetics, 11, e1005658.Google Scholar
Mosmann, T.R. & Sad, S. (1996) The expanding universe of T-cell subsets: Th1, Th2 and more. Immunology Today, 17, 138–146.Google Scholar
Nanyingi, M.O., Munyua, P., Kiama, S.G., et al. (2015) A systematic review of Rift Valley Fever epidemiology 1931–2014. Infection Ecology & Epidemiology, 5, 28024.Google Scholar
Newbold, L.K., Burthe, S.J., Oliver, A.E., et al. (2017) Helminth burden and ecological factors associated with alterations in wild host gastrointestinal microbiota. ISME Journal, 11, 663–675.Google Scholar
Osborne, L.C., Monticelli, L.A., Nice, T.J., et al. (2014) Virus–helminth coinfection reveals a microbiota-independent mechanism of immunomodulation. Science, 345, 578.Google Scholar
Pawlowski, A., Jansson, M., Sköld, M., Rottenberg, M.E. & Källenius, G. (2012) Tuberculosis and HIV co-infection. PLOS Pathogens, 8, e1002464.Google Scholar
Pedersen, A.B. & Fenton, A. (2007) Emphasizing the ecology in parasite community ecology. Trends in Ecology & Evolution, 22, 133–139.Google Scholar
Pedersen, A.B. & Fenton, A. (2015) The role of antiparasite treatment experiments in assessing the impact of parasites on wildlife. Trends in Parasitology, 31, 200–211.Google Scholar
Pepin, M., Bouloy, M., Bird, B.H., Kemp, A. & Paweska, J. (2010) Rift Valley fever virus (Bunyaviridae: Phlebovirus): an update on pathogenesis, molecular epidemiology, vectors, diagnostics and prevention. Veterinary Research, 41, 61.Google Scholar
Petney, T.N. & Andrews, R.H. (1998) Multiparasite communities in animals and humans: frequency, structure and pathogenic significance. International Journal for Parasitology, 28, 377–393.Google Scholar
Pienaar, N.J. & Thompson, P.N. (2013) Temporal and spatial history of Rift Valley fever in South Africa: 1950 to 2011. Onderstepoort Journal of Veterinary Research, 80(1).Google Scholar
Pilosof, S., Morand, S., Krasnov, B.R. & Nunn, C.L. (2015) Potential parasite transmission in multi-host networks based on parasite sharing. PLoS ONE, 10, e0117909.Google Scholar
Pirson, C., Jones, G.J., Steinbach, S., Besra, G.S. & Vordermeier, H.M. (2012) Differential effects of Mycobacterium bovis-derived polar and apolar lipid fractions on bovine innate immune cells. Veterinary Research, 43, 54.Google Scholar
Pitchford, R.J. (1976) Preliminary observations on the distribution, definitive hosts and possible relation with other schistosomes, of Schistosoma margrebowiei, Le Roux, 1933 and Schistosoma leiperi, Le Roux, 1955. Journal of Helminthology, 50, 111–123.Google Scholar
Pollock, J.M., Rodgers, J.D., Welsh, M.D. & McNair, J. (2006) Pathogenesis of bovine tuberculosis: experimental models of infection. Veterinary Microbiology, 112, 141–150.Google Scholar
Pospischil, A., Kaiser, C., Hofmann-Lehmann, R., et al. (2012) Evidence for Chlamydia in wild mammals of the Serengeti. Journal of Wildlife Diseases, 48, 1074–1078.Google Scholar
Poulin, R. (1996) Richness, nestedness, and randomness in parasite infracommunity structure. Oecologia, 105, 545–551.Google Scholar
Prins, H.H.T. (1996) Ecology and Behaviour of the African Buffalo: Social Inequality and Decision Making. London: Chapman and Hall.Google Scholar
Reese, T.A., Bi, K., Kambal, A., et al. (2016) Sequential infection with common pathogens promotes human-like immune gene expression and altered vaccine response. Cell Host & Microbe, 19, 713–719.Google Scholar
Regidor-Cerrillo, J., Arranz-Solís, D., Benavides, J., et al. (2014) Neospora caninum infection during early pregnancy in cattle: how the isolate influences infection dynamics, clinical outcome and peripheral and local immune responses. Veterinary Research, 45, 10.Google Scholar
Renwick, A.R., White, P.C.L. & Bengis, R.G. (2007) Bovine tuberculosis in southern African wildlife: a multi-species host–pathogen system. Epidemiology and Infection, 135, 529–540.Google Scholar
Rodwell, T.C., Kriek, N.P., Bengis, R.G., et al. (2001) Prevalence of bovine tuberculosis in African buffalo at Kruger National Park. Journal of Wildlife Diseases, 37, 258–264.Google Scholar
Romano, A., Doria, N.A., Mendez, J., Sacks, D.L. & Peters, N.C. (2015) Cutaneous infection with Leishmania major mediates heterologous protection against visceral infection with Leishmania infantum. The Journal of Immunology, 195, 3816.Google Scholar
Roug, A., Muse, E.A., Smith, W.A., et al. (2016) Demographics and parasites of African buffalo (Syncerus caffer Sparrman, 1779) in Ruaha National Park, Tanzania. African Journal of Ecology, 54, 146–153.Google Scholar
Schmid-Hempel, P. (2017) Parasites and their social hosts. Trends in Parasitology, 33, 453–462.Google Scholar
Segre, H., Ron, R., De Malach, N., et al. (2014) Competitive exclusion, beta diversity, and deterministic vs. stochastic drivers of community assembly. Ecology Letters, 17, 1400–1408.Google Scholar
Sinclair, A.R.E. (1977) The African Buffalo, A Study of Resource Limitation of Populations. Chicago, IL: Chicago University Press.Google Scholar
Stock, T. & Holmes, J.C. (1987) Dioecocestus asper (Cestoda: Dioecocestidae): an interference competitor in an enteric helminth community. The Journal of Parasitology, 73, 1116–1123.Google Scholar
Stock, T. & Holmes, J.C. (1988) Functional relationships and microhabitat distributions of enteric helminths of grebes (Podicipedidae): the evidence for interactive communities. The Journal of Parasitology, 74, 214–227.Google Scholar
Su, Z., Segura, M., Morgan, K., Loredo-Osti, J.C. & Stevenson, M.M. (2005) Impairment of protective immunity to blood-stage malaria by concurrent nematode infection. Infection and Immunity, 73, 3531–3539.Google Scholar
Swanepoel, R. & Coetzer, J. (2004) Rift valley fever. Infectious Diseases of Livestock, 2, 1037–1070.Google Scholar
Taylor, M.D., van der Werf, N. & Maizels, R.M. (2012) T cells in helminth infection: the regulators and the regulated. Trends in Immunology, 33, 181–189.Google Scholar
Taylor, W.A., Skinner, J.D. & Boomker, J. (2013) Nematodes of the small intestine of African buffaloes, Syncerus caffer, in the Kruger National Park, South Africa. Onderstepoort Journal of Veterinary Research, 80, 1–4.Google Scholar
Telfer, S. & Bown, K. (2012) The effects of invasion on parasite dynamics and communities. Functional Ecology, 26, 1288–1299.Google Scholar
Telfer, S., Lambin, X., Birtles, R., et al. (2010) Species interactions in a parasite community drive infection risk in a wildlife population. Science (New York, N.Y.), 330, 243–246.Google Scholar
Thacker, T.C., Palmer, M.V. & Waters, W.R. (2007) Associations between cytokine gene expression and pathology in Mycobacterium bovis infected cattle. Veterinary Immunology and Immunopathology, 119, 204–213.Google Scholar
Tilman, D. (1994) Competition and biodiversity in spatially structured habitats. Ecology, 75, 2–16.Google Scholar
Walsh, J.R., Carpenter, S.R. & Vander Zanden, M.J. (2016) Invasive species triggers a massive loss of ecosystem services through a trophic cascade. Proceedings of the National Academy of Sciences of the United States of America, 113, 4081–4085.Google Scholar
Walson, J.L., Otieno, P.A., Mbuchi, M., et al. (2008) Albendazole treatment of HIV-1 and helminth co-infection: a randomized, double blind, placebo-controlled trial. AIDS (London, England), 22, 1601–1609.Google Scholar
Waters, W.R., Palmer, M.V., Thacker, T.C., et al. (2011) Tuberculosis immunity: opportunities from studies with cattle. Clinical Developmental Immunology, 2011, 768542.Google Scholar
Welsh, M.D., Cunningham, R.T., Corbett, D.M., et al. (2005) Influence of pathological progression on the balance between cellular and humoral immune responses in bovine tuberculosis. Immunology, 114, 101–111.Google Scholar
Xu, D.-H., Pridgeon, J.W., Klesius, P.H. & Shoemaker, C.A. (2012) Parasitism by protozoan Ichthyophthirius multifiliis enhanced invasion of Aeromonas hydrophila in tissues of channel catfish. Veterinary Parasitology, 184, 101–107.Google Scholar

References

Alexander, H.M. (1989) An experimental field study of anther-smut disease of Silene alba caused by Ustilago violacea: genotypic variation and disease incidence. Evolution, 43, 835–847.Google Scholar
Alexander, H.M. (1990) Epidemiology of anther-smut infection of Silene alba caused by Ustilago violacea: patterns of spore deposition and disease incidence. Journal of Ecology, 78, 166–179.Google Scholar
Alexander, H.M. & Antonovics, J. (1988) Disease spread and population dynamics of anther-smut infection of Silene alba caused by the fungus Ustilago violacea. Journal of Ecology, 76, 91–104.Google Scholar
Alexander, H.M. & Antonovics, J. (1995) Spread of anther-smut disease (Ustilago violacea) and character correlations in a genetically variable experimental population of Silene alba. Journal of Ecology, 83, 783–794.Google Scholar
Alexander, H.M., Antonovics, J. & Kelly, A.W. (1993) Genotypic variation in plant disease resistance–physiological resistance in relation to field disease transmission. Journal of Ecology, 81, 325–333.Google Scholar
Altizer, S., Davis, A.K., Cook, K.C. & Cherry, J.J. (2004) Age, sex, and season affect the risk of mycoplasmal conjunctivitis in a southeastern house finch population. Canadian Journal of Zoology, 82, 755–763.Google Scholar
Antonovics, A.J., Stratton, D., Thrall, P.H. & Jarosz, A.M. (1996) An anther-smut disease (Ustilago violacea) of Fire-pink (Silene virginica): its biology and relationship to the anther-smut disease of white campion (Silene alba). American Midland Naturalist, 135, 130–143.Google Scholar
Antonovics, J. (2004) Long-term study of a plant-pathogen metapopulation. In: Ecology, Genetics, and Evolution of Metapopulations (pp. 471–488). Amsterdam: Elsevier.Google Scholar
Antonovics, J. & Alexander, H.M. (1992) Epidemiology of anther-smut infection of Silene alba (= S. latifolia) caused by Ustilago violacea: patterns of spore deposition in experimental populations. Proceedings of the Royal Society of London B, 250, 157–163.Google Scholar
Antonovics, J., Hood, M.E., Thrall, P.H., Abrams, J.Y. & Duthie, G.M. (2003) Herbarium studies on the distribution of anther-smut fungus (Microbotryum violaceum) and Silene species (Caryophyllaceae) in the eastern United States. American Journal of Botany, 90, 1522–1531.Google Scholar
Antonovics, J. & Thrall, P.H. (1994) The cost of resistance and maintenance of genetic polymorphism in host–pathogen systems. Proceedings of the Royal Society of London B, 257, 105–110.Google Scholar
Armitage, S.A.O., Thompson, J.J.W., Rolff, J. & Siva-Jothy, M.T. (2003) Examining costs of induced and constitutive immune investment in Tenebrio molitor. Journal of Evolutionary Biology, 16, 1038–1044.Google Scholar
Baird, J.K. (1998) Age-dependent characteristics of protection v. susceptibility to Plasmodium falciparum. Annals of Tropical Medicine and Parasitology, 92, 367–390.Google Scholar
Barton, K.E. & Koricheva, J. (2010) The ontogeny of plant defense and herbivory: characterizing general patterns using meta-analysis. The American Naturalist, 175, 481–493.Google Scholar
Bergelson, J. & Purrington, C.B. (1996) Surveying patterns in the cost of resistance in plants. The American Naturalist, 148, 536–558.Google Scholar
Bernasconi, G., Antonovics, J., Biere, A., et al. (2009) Silene as a model system in ecology and evolution. Heredity, 103, 5–14.Google Scholar
Biere, A. & Antonovics, J. (1996) Sex-specific costs of resistance to the fungal pathogen Ustilago violacea (Microbotryum violaceum) in Silene alba. Evolution, 50, 1098–1110.Google Scholar
Boege, K. & Marquis, R.J. (2005) Facing herbivory as you grow up: the ontogeny of resistance in plants. Trends in Ecology and Evolution, 20, 441–448.Google Scholar
Boots, M., Donnelly, R. & White, A. (2013) Optimal immune defence in the light of variation in lifespan. Parasite Immunology, 35, 331–338.Google Scholar
Brambell, F.W.R. (1970) The Transmission of Passive Immunity from Mother to Young. Amsterdam: North Holland.Google Scholar
Bruns, E., Hood, M.E. & Antonovics, J. (2015) Rate of resistance evolution and polymorphism in long- and short-lived hosts. Evolution, 69, 551–560.Google Scholar
Bruns, E.L., Antonovics, J., Carasso, V. & Hood, M. (2017) Transmission and temporal dynamics of anther-smut disease (Microbotryum) on alpine carnation (Dianthus pavonius). Journal of Ecology, 105, 1413–1424.Google Scholar
Buono, L., López-Villavicencio, M., Shykoff, J.A., Snirc, A. & Giraud, T. (2014) Influence of multiple infection and relatedness on virulence: disease dynamics in an experimental plant population and its castrating parasite. PLoS ONE, 9, e98526.Google Scholar
Burdon, J.J., Oates, J.D. & Marshall, D.R. (1983) Interactions between Avena and Puccinia species. I. The wild hosts: Avena barbata Pott Ex Link, A. fatua L. and A. ludoviciana Durieu. Journal of Applied Ecology, 20, 571–584.Google Scholar
Cafuir, L., Antonovics, J. & Hood, M.E. (2007) Tissue culture and quantification of individual‐level resistance to anther‐smut disease in Silene vulgaris.International Journal of Plant Sciences, 168, 415–419.Google Scholar
Carlsson-Granér, U. (1997) Anther-smut disease in Silene dioica: variation in susceptibility among genotypes and populations, and patterns of disease within populations. Evolution, 51, 1416–1426.Google Scholar
Carlsson-Granér, U. (2006) Disease dynamics, host specificity and pathogen persistence in isolated host populations. Oikos, 112, 174–184.Google Scholar
Carlsson-Granér, U. & Thrall, P.H. (2006) The impact of host longevity on disease transmission: host–pathogen dynamics and the evolution of resistance. Evolutionary Ecology Research, 8, 659–675.Google Scholar
Charlesworth, B. (1980) Evolution in Age-structured Populations. Cambridge: Cambridge University Press.Google Scholar
Chen, X. (2013) High-temperature adult-plant resistance, key for sustainable control of stripe rust. American Journal of Plant Science and Biotechnology, 4, 608–627.Google Scholar
Chung, E., Petit, E., Antonovics, J., Pedersen, A.B. & Hood, M.E. (2012) Variation in resistance to multiple pathogen species: anther smuts of Silene uniflora. Ecology and Evolution, 2, 2304–2314.Google Scholar
Develey-Rivière, M.P. & Galiana, E. (2007) Resistance to pathogens and host developmental stage: a multifaceted relationship within the plant kingdom. New Phytologist, 175, 405–416.Google Scholar
Diamond, J. (1997) Guns, Germs and Steel: The Fates of Human Societies. New York, NY: Norton.Google Scholar
Donnelly, R., White, A. & Boots, M. (2015) The epidemiological feedbacks critical to the evolution of host immunity. Journal of Evolutionary Biology, 28, 2042–2053.Google Scholar
Fellous, S. & Lazzaro, B.P. (2011) Potential for evolutionary coupling and decoupling of larval and adult immune gene expression. Molecular Ecology, 20, 1558–1567.Google Scholar
Flor, H.H. (1956) The complementary genic systems in flax and flax rust. Advances in Genetics, 8, 29–54.Google Scholar
Garbutt, J.S., O’Donoghue, A.J.P., McTaggart, S.J., Wilson, P.J. & Little, T.J. (2014) The development of pathogen resistance in Daphnia magna: implications for disease spread in age-structured populations. The Journal of Experimental Biology, 217, 3929–3934.Google Scholar
Garnier, R., Gandon, S., Harding, K.C. & Boulinier, T. (2014) Length of intervals between epidemics: evaluating the influence of maternal transfer of immunity. Ecology and Evolution, 4, 568–575.Google Scholar
Getz, W.M. & Pickering, J. (1983) Epidemic models: thresholds and population regulation. The American Naturalist, 121, 892–898.Google Scholar
Hanssen, S.A., Hasselquist, D., Folstad, I. & Erikstad, K.E. (2004) Costs of immunity: immune responsiveness reduces survival in a vertebrate. Proceedings of the Royal Society of London B, 271, 925–930.Google Scholar
Härkönen, T., Harding, K., Rasmussen, T.D., Teilmann, J. & Dietz, R. (2007) Age- and sex-specific mortality patterns in an emerging wildlife epidemic: the phocine distemper in European harbour seals. PLoS ONE, 2, e887.Google Scholar
Hendrix, F.F. & Campbell, W. (1973) Pythiums as plant pathogens. Annual Review of Phytopathology, 11, 77–98.Google Scholar
Hood, M.E., Mena-Alí, J.I., Gibson, A.K., et al. (2010). Distribution of the anther-smut pathogen Microbotryum on species of the Caryophyllaceae. The New Phytologist, 187, 217–229.Google Scholar
Jarosz, A.M. & Burdon, J.J. (1990) Predominance of a single major gene for resistance to Phakopsora pachyrhizi in a population of Glycine argyrea. Heredity, 64, 347–353.Google Scholar
Jayakar, S.D. (1970) A mathematical model for interaction of gene frequencies in a parasite and its host. Theoretical Population Biology, 1, 140–164.Google Scholar
Kallio, E.R., Begon, M., Henttonen, H., et al. (2010) Hantavirus infections in fluctuating host populations: the role of maternal antibodies. Proceedings of the Royal Society of London B, 277, 3783–3791.Google Scholar
Kaltz, O., Gandon, S., Michalakis, Y. & Shykoff, J.A. (1999) Local maladaptation in the anther-smut fungus Microbotryum violaceum to its host plant Silene latifolia: evidence from a cross-inoculation experiment. Evolution, 53, 395–407.Google Scholar
Kaltz, O. & Shykoff, J.A. (2001) Male and female Silene latifolia plants differ in per-contact risk of infection by a sexually transmitted disease. Journal of Ecology, 89, 99–109.Google Scholar
Kubi, C., Van Den Abbeele, J., De Deken, R., et al. (2006) The effect of starvation on the susceptibility of teneral and non-teneral tsetse flies to trypanosome infection. Medical and Veterinary Entomology, 20, 388–392.Google Scholar
Kurtis, J.D., Onyango, F.K. & Duffy, P.E. (2001) Human resistance to Plasmodium falciparum increases during puberty and is predicted by dehyroepiandrosterone sulfate levels. Infection and Immunity, 69, 123–128.Google Scholar
le Gac, M., Hood, M.E., Fournier, E. & Giraud, T. (2007) Phylogenetic evidence of host-specific cryptic species in the anther smut fungus. Evolution, 61, 15–26.Google Scholar
Line, R.F. & Chen, X. (1995) Successes in breeding for and managing durable resistance to wheat rusts. Plant Breeding, 79, 1254–1255.Google Scholar
Lochmiller, R.L. & Deerenberg, C. (2000) Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos, 88, 87–98.Google Scholar
Marr, D.L. & Delph, L.F. (2005) Spatial and temporal pattern of a pollinator-transmitted pathogen in a long-lived perennial, Silene acaulis. Evolutionary Ecology Research, 7, 335–352.Google Scholar
McDade, T.W. (2003) Life history theory and the immune system: steps toward a human ecological immunology. American Journal of Physical Anthropology, 122(Suppl. 46), 100–125.Google Scholar
McNeill, W.H. (1976) Plagues and Peoples. New York, NY: Anchor Books.Google Scholar
Miller, M.R., White, A. & Boots, M. (2007) Host life span and the evolution of resistance characteristics. Evolution, 61, 2–14.Google Scholar
Morris, W. & Doak, D. (1998) Life history of the long-lived gynodioecious cushion plant Silene acaulis (Caryophyllaceae), inferred from size-based population projection matrices. American Journal of Botany, 85, 784–793.Google Scholar
Müller-Graf, C., Collins, D., Packer, C. & Woolhouse, M. (1997) Schistosoma mansoni infection in a natural population of olive baboons (Papio cynocephalus anubis) in Gombe Stream National Park, Tanzania. Parasitology, 115, 621–627.Google Scholar
Nunn, C. & Altizer, S. (2006) Infectious Diseases in Primates. Oxford: Oxford University Press.Google Scholar
Oppelt, C., Starkloff, A., Rausch, P., Von Holst, D. & Rodel, H. (2010) Major histocompatibility complex variation and age-specific endoparasite load in subadult European rabbits.Molecular Ecology, 19, 4155–4167.Google Scholar
Packer, A. & Clay, K. (2000) Soil pathogens and spatial patterns of seedling mortality in a temperate tree. Nature, 404, 278–281.Google Scholar
Panter, S. & Jones, D.A. (2002) Age-related resistance to plant pathogens. Advances in Botanical Research, 38, 251–280.Google Scholar
Parker, M.A. (1988) Polymorphism for disease resistance in the annual legume Amphicarpaea bracteata. Heredity, 60, 27–31.Google Scholar
Petit, E., Silver, C., Cornille, A., et al. (2017) Co-occurrence and hybridization of anther-smut pathogens specialized on Dianthus hosts. Molecular Ecology, 26, 1877–1890.Google Scholar
Poland, J.A., Balint-Kurti, P.J., Wisser, R.J., Pratt, R.C. & Nelson, R.J. (2009) Shades of gray: the world of quantitative disease resistance. Trends in Plant Science, 14, 21–29.Google Scholar
Raberg, L., Nilsson, J.A., Ilmonen, P., Stjernman, M. & Hasselquist, D. (2000) The cost of an immune response: vaccination reduces parental effort. Ecology Letters, 3, 382–386.Google Scholar
Rosengaus, R.B. & Traniello, J.F.A. (2001) Disease susceptibility and the adaptive nature of colony demography in the dampwood termite Zootermopsis angusticollis. Behavioral Ecology and Sociobiology, 50, 546–556.Google Scholar
Sait, S., Begon, M. & Thompson, D.J. (1994) The influence of larval age on the response of Plodia interpunctella to a granulosis virus. Journal of Invertebrate Pathology, 63, 107–110.Google Scholar
Schäfer, A.M., Kemler, M., Bauer, R. & Begerow, D. (2010) The illustrated life cycle of Microbotryum on the host plant Silene latifolia. Botany, 88, 875–885.Google Scholar
Susi, H. & Laine, A.-L. (2015) The effectiveness and costs of pathogen resistance strategies in a perennial plant. Journal of Ecology, 103, 303–315.Google Scholar
Thrall, P.H., Biere, A. & Antonovics, J. (1993) Plant life-history and disease susceptibility – the occurrence of Ustilago violacea on different species within the Caryophyllaceae. Journal of Ecology, 81, 489–498.Google Scholar

References

Abbot, P. & Dill, L.M. (2001) Sexually transmitted parasites and sexual selection in the milkweed leaf beetle, Labidomera clivicollis. Oikos, 92, 91–100.Google Scholar
Adamo, S.A., Kovalko, I., Easy, R.H. & Stoltz, D. (2014) A viral aphrodisiac in the cricket Gryllus texensis. Journal of Experimental Biology, 217, 1970–1976.Google Scholar
Alexander, H.M. & Maltby, A. (1990) Anther-smut infection of Silene alba caused by Ustilago violacea: factors determining fungal reproduction. Oecologia, 84, 249–253.Google Scholar
Amiri, E., Meixner, M.D. & Kryger, P. (2016) Deformed wing virus can be transmitted during natural mating in honey bees and infect the queens. Scientific Reports, 6, 33065.Google Scholar
Anderson, R.M. & May, R.M. (1991) Infectious Diseases of Humans: Dynamics and Control. Oxford: Oxford University Press.Google Scholar
Apari, P., De Sousa, J.D. & Müller, V. (2014) Why sexually transmitted infections tend to cause infertility: an evolutionary hypothesis. PLoS Pathogens, 10, e1004111.Google Scholar
Ashby, B. & Boots, M. (2015) Coevolution of parasite virulence and host mating strategies. Proceedings of the National Academy of Sciences of the United States of America, 112, 13,290–13,295.Google Scholar
Ashby, B. & Gupta, S. (2013) Sexually transmitted infections in polygamous mating systems. Philosophical Transactions of the Royal Society B, 368, e20120048.Google Scholar
Augustine, D.J. (1998) Modelling Chlamydia–koala interactions: coexistence, population dynamics and conservation implications. Journal of Applied Ecology, 35, 261–272.Google Scholar
Bateman, A.J. (1948) Intra-sexual selection in Drosophila. Heredity, 2, 349–368.Google Scholar
Bauch, C.T. & McElreath, R. (2016) Disease dynamics and costly punishment can foster socially imposed monogamy. Nature Communications, 7, 11219.Google Scholar
Baverud, V., Nystrom, C. & Johansson, K.E. (2006) Isolation and identification of Taylorella asinigenitalis from the genital tract of a stallion, first case of a natural infection. Veterinary Microbiology, 116, 294–300.Google Scholar
Boots, M. & Knell, R.J. (2002) The evolution of risky behaviour in the presence of a sexually transmitted disease. Proceedings of the Royal Society of London B, 269, 585–589.Google Scholar
Brown, A. & Grice, R. (1984) Isolation of Chlamydia psiltaci from koalas (Phascolarctos cinereus). Australian Veterinary Journal, 61, 413–413.Google Scholar
Chahroudi, A., Permar, S. & Pandrea, I. (2014) Chapter 13 – SIV transmission in natural hosts A2 – Ansari, Aftab A. In: Silvestri, G. (ed.), Natural Hosts of SIV. Amsterdam: Elsevier.Google Scholar
Cockram, F. & Jackson, A. (1974) Isolation of a Chlamydia from cases of keratoconjunctivitis in koalas. Australian Veterinary Journal, 50, 82–83.Google Scholar
Cohen, M.S. (1998) Sexually transmitted diseases enhance HIV transmission: no longer a hypothesis. Lancet, 351, 5–7.Google Scholar
Eames, K.T.D. & Keeling, M.J. (2002) Modeling dynamic and network heterogeneities in the spread of sexually transmitted diseases. Proceedings of the National Academy of Sciences of the United States of America, 99, 13,330–13,335.Google Scholar
Escallón, C., Becker, M.H., Walke, J.B., et al. (2017) Testosterone levels are positively correlated with cloacal bacterial diversity and the relative abundance of Chlamydiae in breeding male rufous-collared sparrows. Functional Ecology, 31, 192–203.Google Scholar
Ezenwa, V.O., Etienne, R.S., Luikart, G., Beja-Pereira, A. & Jolles, A.E. (2010) Hidden consequences of living in a wormy world: nematode-induced immune suppression facilitates tuberculosis invasion in African buffalo. American Naturalist, 176, 613–624.Google Scholar
Fauvergue, X. (2013) A review of mate-finding Allee effects in insects: from individual behavior to population management. Entomologia Experimentalis et Applicata, 146, 79–92.Google Scholar
Gascoigne, J., Berec, L., Gregory, S. & Courchamp, F. (2009) Dangerously few liaisons: a review of mate-finding Allee effects. Population Ecology, 51, 355–372.Google Scholar
Getz, W.M. & Pickering, J. (1983) Epidemic models: thresholds and population regulation. American Naturalist, 121, 892–898.Google Scholar
Grassl, J., Peng, Y., Baer-Imhoof, B., et al. (2017) Infections with the sexually transmitted pathogen Nosema apis trigger an immune response in the seminal fluid of honey bees (Apis mellifera). Journal of Proteome Research, 16, 319–334.Google Scholar
Grassly, N.C., Fraser, C. & Garnett, G.P. (2005) Host immunity and synchronized epidemics of syphilis across the United States. Nature, 433, 417–421.Google Scholar
Gupta, S., Anderson, R.M. & May, R.M. (1989) Networks of sexual contacts – implications for the pattern of spread of HIV. AIDS, 3, 807–817.Google Scholar
Haddrill, P.R., Majerus, M.E.N. & Shuker, D.M. (2013) Variation in male and female mating behaviour among different populations of the two-spot ladybird, Adalia bipunctata (Coleoptera: Coccinellidae). European Journal of Entomology, 110, 87–93.Google Scholar
Haddrill, P.R., Shuker, D.M., Amos, W., Majerus, M.E.N. & Mayes, S. (2008) Female multiple mating in wild and laboratory populations of the two-spot ladybird, Adalia bipunctata. Molecular Ecology, 17, 3189–3197.Google Scholar
Hagos, A., Abebe, G., Buscher, P., Goddeeris, B.M. & Claes, F. (2010) Serological and parasitological survey of dourine in the Arsi-Bale highlands of Ethiopia. Tropical Animal Health and Production, 42, 769–776.Google Scholar
Hamilton, W.D. (1990) Mate choice near or far? American Zoologist, 30, 341–352.Google Scholar
Handasyde, K.A. (1986) Factors affecting reproduction in the female koala “Phascolarctos cinereus”. PhD thesis, Monash University.Google Scholar
Handsfield, H.H., Lipman, T.O., Harnisch, J.P., Tronca, E. & Holmes, K.K. (1974) Asymptomatic gonorrhea in men. New England Journal of Medicine, 290, 117–123.Google Scholar
Hart, B.L., Korinek, E. & Brennan, P. (1987) Postcopulatory genital grooming in male-rats – prevention of sexually-transmitted infections. Physiology & Behavior, 41, 321–325.Google Scholar
Hethcote, H. & Yorke, J.A. (1984) Gonorrhea Transmission Dynamics and Control. Berlin: Springer-Verlag.Google Scholar
Hurst, G.D.D., Jiggins, F.M., Schulenburg, J.H.G.V.D., et al. (1999a) Male-killing Wolbachia in two species of insect. Proceedings of the Royal Society of London B, 266, 735–740.Google Scholar
Hurst, G.D.D., Sharpe, R.G., Broomfield, A.H., et al. (1995) Sexually transmitted disease in a promiscuous insect, Adalia bipunctata. Ecological Entomology, 20, 230–236.Google Scholar
Hurst, G.D.D., Von Der Schulenburg, J.H.G., Majerus, T.M.O., et al. (1999b) Invasion of one insect species, Adalia bipunctata, by two different male-killing bacteria. Insect Molecular Biology, 8, 133–139.Google Scholar
Jackson, M., White, N., Giffard, P. & Timms, P. (1999) Epizootiology of Chlamydia infections in two free-range koala populations. Veterinary Microbiology, 65, 225–234.Google Scholar
Ji, W., White, P.C.L. & CLout, M.N. (2005) Contact rates between possums revealed by proximity data loggers. Journal of Applied Ecology, 42, 595–604.Google Scholar
Jones, S.L., Pastok, D. & Hurst, G.D.D. (2015) No evidence that presence of sexually transmitted infection selects for reduced mating rate in the two spot ladybird, Adalia bipunctata. Peer J, 3, e1148.Google Scholar
Keeling, M. (2005) The implications of network structure for epidemic dynamics. Theoretical Population Biology, 67, 1–8.Google Scholar
Keeling, M.J. (1999) The effects of local spatial structure on epidemiological invasions. Proceedings of the Royal Society of London B, 266, 859–867.Google Scholar
Knell, R.J. (1999) Sexually transmitted disease and parasite mediated sexual selection. Evolution, 53, 957–961.Google Scholar
Knell, R.J. & Webberley, K.M. (2004) Sexually transmitted diseases of insects: distribution, ecology, evolution and host behaviour. Biological Reviews, 79, 557–581.Google Scholar
Kokko, H. & Rankin, D.J. (2006) Lonely hearts or sex in the city? Density-dependent effects in mating systems. Philosophical Transactions of the Royal Society of London B, 361, 319–334.Google Scholar
Kokko, H., Ranta, E., Ruxton, G. & Lundberg, P. (2002) Sexually transmitted disease and the evolution of mating systems. Evolution, 56, 1091–1100.Google Scholar
Kulkarni, S. & Heeb, P. 2007. Social and sexual behaviours aid transmission of bacteria in birds. Behavioural Processes, 74, 88–92.Google Scholar
Lockhart, A.B., Thrall, P.H. & Antonovics, J. (1996) Sexually transmitted diseases in animals: ecological and evolutionary implications. Biological Reviews, 71, 415–471.Google Scholar
Loehle, C. (1995) Social barriers to pathogen transmission in wild animal populations. Ecology, 76, 326–335.Google Scholar
Lombardo, M.P., Thorpe, P.A. & Power, H.W. (1999) The beneficial sexually transmitted microbe hypothesis of avian copulation. Behavioral Ecology, 10, 333–337.Google Scholar
Lunney, D., Crowther, M.S., Wallis, I., et al. (2012) Koalas and climate change: a case study on the Liverpool Plains, north-west New South Wales. In: Lunney, D. & Hutchings, P. (eds.), Wildlife and Climate Change: Towards Robust Conservation Strategies for Australian Fauna (pp. 150–168). Mosman, NSW: Royal Zoological Society of New South Wales.Google Scholar
Luong, L.T., Platzer, E.G., Zuk, M. & Giblin-Davis, R.M. (2000) Venereal worms: sexually transmitted nematodes in the decorated cricket. Journal of Parasitology, 86, 471–477.Google Scholar
May, R.M. & Anderson, R.M. (1979) Population biology of infectious diseases: Part II. Nature, 280, 455–461.Google Scholar
May, R.M. & Anderson, R.M. (1987) Transmission dynamics of HIV infection. Nature, 326, 137–142.Google Scholar
May, R.M., Gupta, S. & McLean, A.R. (2001) Infectious disease dynamics: what characterizes a successful invader? Philosophical Transactions of the Royal Society of London B, 356, 901–910.Google Scholar
McColl, K., Martin, R., Gleeson, L., Handasyde, K. & Lee, A. (1984) Chlamydia infection and infertility in the female koala (Phascolarctos cinereus). Veterinary Record, 115, 655–655.Google Scholar
Mitchell, P., Bilney, R. & Martin, R. (1988) Population-structure and reproductive status of koalas on Raymond Island, Victoria. Wildlife Research, 15, 511–514.Google Scholar
Moore, S.L. & Wilson, K. (2002) Parasites as a viability cost of sexual selection in natural populations of mammals. Science, 297, 2015–2018.Google Scholar
Morand, S. (1993) Sexual transmission of a nematode: study of a model. Oikos, 66, 48–54.Google Scholar
Morand, S. & Faliex, E. (1994) Study on the life cycle of a sexually transmitted nematode parasite of a terrestrial snail. Journal of Parasitology, 80, 1049–1052.Google Scholar
Nahrung, H.F. & Allen, G.R. (2004) Sexual selection under scramble competition: mate location and mate choice in the eucalypt leaf beetle Chrysophtharta agricola (Chapuis) in the field. Journal of Insect Behavior, 17, 353–366.Google Scholar
Nahrung, H.F. & Clarke, A.R. (2007) Sexually-transmitted disease in a sub-tropical eucalypt beetle: infection of the fittest? Evolutionary Ecology, 21, 143–156.Google Scholar
Nunn, C.L. (2003) Behavioural defenses against sexually transmitted diseases in primates. Animal Behaviour, 66, 37–48.Google Scholar
Nunn, C.L. & Altizer, S. (2004) Sexual selection, behaviour and sexually transmitted diseases. In: Kappeler, P.M. & van Schaik, C.P. (eds.), Sexual Selection in Primates: New and Comparative Perspectives (pp. 117–130). Cambridge: Cambridge University Press.Google Scholar
Nunn, C.L., Scully, E.J., Kutsukake, N., et al. (2014) Mating competition, promiscuity, and life history traits as predictors of sexually transmitted disease risk in primates. International Journal of Primatology, 35, 764–786.Google Scholar
Otti, O., McTighe, A.P. & Reinhardt, K. (2013) In vitro antimicrobial sperm protection by an ejaculate-like substance. Functional Ecology, 27, 219–226.Google Scholar
Pastok, D., Hoare, M.J., Ryder, J.J., et al. (2016) The role of host phenology in determining the incidence of an insect sexually transmitted infection. Oikos, 125, 636–643.Google Scholar
Peng, Y., Grassl, J., Millar, A.H. & Baer, B. (2016) Seminal fluid of honeybees contains multiple mechanisms to combat infections of the sexually transmitted pathogen Nosema apis. Proceedings of the Royal Society of London B, 283, 2015.1785.Google Scholar
Perry, J.C., Sharpe, D.M.T. & Rowe, L. (2009) Condition-dependent female remating resistance generates sexual selection on male size in a ladybird beetle. Animal Behaviour, 77, 743–748.Google Scholar
Poiani, A. & Wilks, C. (2000) Sexually transmitted diseases: a possible cost of promiscuity in birds? The Auk, 117, 1061–1065.Google Scholar
Poinar, G.O.J. (1970) Orycetonema genitalis gen. et sp. nov. (Rhabditidae: Nematoda) from the genital system of Orycetes monoceros L. (Scarabaeidae: Coleoptera) in West Africa. Journal of Helminthology, 44, 1–10.Google Scholar
Riddick, E.W. (2010) Ectoparasitic mite and fungus on an invasive lady beetle: parasite coexistence and influence on host survival. Bulletin of Insectology, 63, 13–20.Google Scholar
Rowe, L. (1992) Convenience polyandry in a water strider – foraging conflicts and female control of copulation frequency and guarding duration. Animal Behaviour, 44, 189–202.Google Scholar
Rushmore, J., Caillaud, D., Hall, R.J., et al. (2014) Network-based vaccination improves prospects for disease control in wild chimpanzees. Journal of the Royal Society Interface, 11(97), 20140349.Google Scholar
Rushmore, J., Caillaud, D., Matamba, L., et al. (2013) Social network analysis of wild chimpanzees provides insights for predicting infectious disease risk. Journal of Animal Ecology, 82, 976–986.Google Scholar
Ryder, J.J., Hoare, M.-J., Pastok, D., et al. (2014) Disease epidemiology in arthropods is altered by the presence of nonprotective symbionts. American Naturalist, 183, E89–E104.Google Scholar
Ryder, J.J., Miller, M.R., White, A., Knell, R.J. & Boots, M. (2007) Host–parasite population dynamics under combined frequency- and density-dependent transmission. Oikos, 116, 2017–2026.Google Scholar
Ryder, J.J., Pastok, D., Hoare, M.-J., et al. (2013) Spatial variation in food supply, mating behavior, and sexually transmitted disease epidemics. Behavioral Ecology, 24, 723–729.Google Scholar
Ryder, J.J., Webberley, K.M., Boots, M. & Knell, R.J. (2005) Measuring the transmission dynamics of a sexually transmitted disease. Proceedings of the National Academy of Sciences of the United States Of America, 102, 15,140–15,143.Google Scholar
Samakovlis, C., Kylsten, P., Kimbrell, D.A., Engström, A. & Hultmark, D. (1991) The Andropin gene and its product, a male-specific antibacterial peptide in Drosophila melanogaster. EMBO J, 10, 163–169.Google Scholar
Schmid-Hempel, P. (1998) Parasites of Social Insects, Princeton, NJ: Princeton University Press.Google Scholar
Seeman, O.D. & Nahrung, H.F. (2004) Female biased parasitism and the importance of host generation overlap in a sexually transmitted parasite of beetles. Journal of Parasitology, 90, 114–118.Google Scholar
Simmons, A.M. & Rogers, C.E. (1990) Distribution and prevalence of an ectoparasitic nematode, Noctuidonema guyanese, on moths of the fall armyworm (Lepidoptera: Noctuidae) in the tropical Americas. Journal of Entomological Science, 25, 510–518.Google Scholar
Simmons, A.M. & Rogers, C.E. (1994) Effects of an ectoparasitic nematode, Noctuidonema guyanese on adult longevity and egg fertility in Spodoptera frugiperda (Lepidoptera: Noctuidae). Biological Control, 4, 285–289.Google Scholar
Smith, C.C. & Mueller, U.G. (2015) Sexual transmission of beneficial microbes. Trends in Ecology & Evolution, 30, 438–440.Google Scholar
Stalder, K., Vaz, P.K., Gilkerson, J.R., et al. (2015) Prevalence and clinical significance of Herpesvirus infection in populations of Australian marsupials. PLoS ONE, 10.Google Scholar
Suganuma, K., Narantsatsral, S., Battur, B., et al. (2016) Isolation, cultivation and molecular characterization of a new Trypanosoma equiperdum strain in Mongolia. Parasites & Vectors, 9, 481.Google Scholar
Sugimoto, C., Isayama, Y., Sakazaki, R. & Kuramochi, S. (1983) Transfer of Hemophilus equigenitalis Taylor et al. 1978 to the genus Taylorella gen-nov as Taylorella equigenitalis comb. nov. Current Microbiology, 9, 155–162.Google Scholar
Telfer, S., Lambin, X., Birtles, R., et al. (2010) Species interactions in a parasite community drive infection risk in a wildlife population. Science, 330, 243–246.Google Scholar
Waterman, J.M. (2010) The adaptive function of masturbation in a promiscuous African ground squirrel. PLoS ONE, 5, e13060.Google Scholar
Webberley, K.M., Buszko, J., Isham, V. & Hurst, G.D.D. (2006a) Sexually transmitted disease epidemics in a natural insect population. Journal of Animal Ecology, 75, 33–43.Google Scholar
Webberley, K.M. & Hurst, G.D.D. (2002) The effect of aggregative overwintering on an insect sexually transmitted parasite system. Journal of Parasitology, 88, 707–712.Google Scholar
Webberley, K.M., Hurst, G.D.D., Buszko, J. & Majerus, M.E.N. (2002) Lack of parasite-mediated sexual selection in a ladybird/sexually transmitted disease system. Animal Behaviour, 63, 131–141.Google Scholar
Webberley, K.M., Hurst, G.D.D., Husband, R.W., et al. (2004) Host reproduction and a sexually transmitted disease: causes and consequences of Coccipolipus hippodamiae distribution on coccinellid beetles. Journal of Animal Ecology, 73, 1–10.Google Scholar
Webberley, K.M., Tinsley, M.C., Sloggett, J.J., Majerus, M.E.N. & Hurst, G.D.D. (2006b) Spatial variation in the incidence of a sexually transmitted parasite of the ladybird beetle Adalia bipunctata (Coleoptera: Coccinellidae). European Journal of Entomology, 103, 793–797.Google Scholar
Weigler, B.J., Girjes, A.A., White, N.A., et al. (1988) Aspects of the epidemiology of Chlamydia psittaci infection in a population of koalas (Phascolarctos cinereus) in southeastern Queensland, Australia. Journal of Wildlife Diseases, 24, 282–291.Google Scholar
Welch, V.L., Sloggett, J.J., Webberley, K.M. & Hurst, G.D.D. (2001) Short-range clinal variation in the prevalence of a sexually transmitted fungus associated with urbanisation. Ecological Entomology, 26, 547–550.Google Scholar
Werren, J.H., Hurst, G.D.D., Zhang, W., et al. (1994) Rickettsial relative associated with male killing in the ladybird beetle (Adalia bipunctata). Journal of Bacteriology, 176, 388–394.Google Scholar
White, J., Richard, M., Massot, M. & Meylan, S. (2011) Cloacal bacterial diversity increases with multiple mates: evidence of sexual transmission in female common lizards. PLoS ONE, 6, e22339.Google Scholar
White, N. & Timms, P. (1994) Chlamydia psittaci in a koala (Phascolarctos cinereus) population in south-east Queensland. Wildlife Research, 21, 41–47.Google Scholar
Xiang, J., Wünschmann, S., Diekema, D.J., et al. (2001) Effect of coinfection with GB virus C on survival among patients with HIV infection. New England Journal of Medicine, 345, 707–714.Google Scholar
Yorke, J.A., Hethcote, H.W. & Nold, A. (1978) Dynamics and control of the transmission of gonnorhea. Sexually Transmitted Diseases, 5, 51–56.Google Scholar

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