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Towards a mechanistic understanding of competence: a missing link in diversity–disease research

Published online by Cambridge University Press:  10 June 2020

Tara E. Stewart Merrill Open the ORCID record for Tara E. Stewart Merrill [Opens in a new window]  and
Pieter T. J. Johnson Open the ORCID record for Pieter T. J. Johnson [Opens in a new window]
Tara E. Stewart Merrill*
Affiliation:
Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, CO80309, USA
Pieter T. J. Johnson
Affiliation:
Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, CO80309, USA
*
Author for correspondence: Tara E. Stewart Merrill, E-mail: Tara.StewartMerrill@colorado.edu
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Abstract

Biodiversity loss may increase the risk of infectious disease in a phenomenon known as the dilution effect. Circumstances that increase the likelihood of disease dilution are: (i) when hosts vary in their competence, and (ii) when communities disassemble predictably, such that the least competent hosts are the most likely to go extinct. Despite the central role of competence in diversity–disease theory, we lack a clear understanding of the factors underlying competence, as well as the drivers and extent of its variation. Our perspective piece encourages a mechanistic understanding of competence and a deeper consideration of its role in diversity–disease relationships. We outline current evidence, emerging questions and future directions regarding the basis of competence, its definition and measurement, the roots of its variation and its role in the community ecology of infectious disease.

Keywords

Competencedilution effectdiversity–diseaseintraspecific variation
Type
Review Article
Information
Parasitology , Volume 147 , Issue 11 , September 2020 , pp. 1159 - 1170
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Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

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References

Adamo, SA (2017) The stress response and immune system share, borrow, and reconfigure their physiological network elements: evidence from the insects. Hormones and Behavior 88, 25–30.CrossRefGoogle ScholarPubMed
Adamo, SA, Easy, RH, Kovalko, I, MacDonald, J, McKeen, A, Swanburg, T, Turnbull, KF and Reeve, C (2016) Predator stress-induced immunosuppression: trade-off, immune redistribution or immune reconfiguration? Journal of Experimental Biology 220, 868–875.Google ScholarPubMed
Adelman, JS and Hawley, DM (2017) Tolerance of infection: a role for animal behavior, potential immune mechanisms, and consequences for parasite transmission. Hormones and Behavior 88, 79–86.CrossRefGoogle ScholarPubMed
Adelman, JS, Moyers, SC, Faine, DR and Hawley, DM (2015) Feeder use predicts both acquisition and transmission of a contagious pathogen in a North American songbird. Proceedings of the Royal Society B: Biological Sciences 282, 20151429.CrossRefGoogle Scholar
Alcaide, M, Rico, C, Ruiz, S, Soriguer, R, Muñoz, J and Figuerola, J (2009) Disentangling vector-borne transmission network: a universal DNA barcoding method to identify vertebrate hosts from arthropod bloodmeals. PLoS ONE 4, e7092.CrossRefGoogle Scholar
Allan, BF, Langerhans, RB, Ryberg, WA, Landesman, WJ, Griffin, NW, Katz, RS, Oberle, BJ, Schutzenhofer, MR, Smyth, KN, de St Maurice, A, Clark, L, Crooks, KR, Hernandez, DE, McLean, RG, Ostfeld, RS and Chase, JM (2009) Ecological correlates of risk and incidence of West Nile virus in the United States. Oecologia 158, 699–708.CrossRefGoogle ScholarPubMed
Altizer, S, Dobson, A, Hosseini, P, Hudson, P, Pascual, M and Rohani, P (2006) Seasonality and the dynamics of infectious diseases. Ecology Letters 9, 467–484.CrossRefGoogle ScholarPubMed
Anderson, RM and May, RM (1981) The population dynamics of microparasites and their invertebrate hosts. Philosophical Transactions of the Royal Society B: Biological Sciences 291, 451–524.Google Scholar
Barron, DG, Gervasi, SS, Pruitt, JN and Martin, LB (2015) Behavioral competence: how host behaviors can interact to influence parasite transmission risk. Behavioral Sciences 6, 35–40.Google Scholar
Baucom, RS and de Roode, JC (2011) Ecological immunology and tolerance in plants and animals. Functional Ecology 25, 18–28.CrossRefGoogle Scholar
Becker, DJ, Albery, GF, Kessler, MK, Lunn, TJ, Falvo, CA, Czirják, GA, Martin, LB and Plowright, RK (2019) Macroimmunology: the drivers and consequences of spatial patterns in wildlife immune defence. Journal of Animal Ecology 89, 972–995.CrossRefGoogle Scholar
Beernsten, BT, James, AA and Christensen, BM (2000) Genetics of mosquito vector competence. Microbiology and Molecular Biology Reviews 64, 115–137.CrossRefGoogle Scholar
Bolnick, DI, Amarasekare, P, Araújo, MS, Bürger, R, Levine, JM, Novak, M, Rudolf, VHW, Schreiber, SJ, Urban, MC and Vasseur, D (2011) Why intraspecific trait variation matters in community ecology. Trends in Ecology and Evolution 26, 183–192.CrossRefGoogle ScholarPubMed
Burgan, SC, Gervasi, SS and Martin, LB (2018) Parasite tolerance and host competence in avian host defense to West Nile virus. EcoHealth 15, 360–371.CrossRefGoogle ScholarPubMed
Burgan, SC, Gervasi, SS, Johnson, LR and Martin, LB (2019) How individual variation in host tolerance affects competence to transmit parasites. Physiological and Biochemical Zoology 92, 49–57.CrossRefGoogle ScholarPubMed
Cardillo, M, Mace, GM, Gittleman, JL, Jones, KE, Bielby, J and Purvis, A (2008) The predictability of extinction: biological and external correlates of decline in mammals. Proceedings of the Royal Society B: Biological Sciences 275, 1441–1448.CrossRefGoogle ScholarPubMed
Carver, S, Kuenzi, A, Bagamian, KH, Mills, JN, Rollin, PE, Zanto, SN and Douglass, R (2011) A temporal dilution effect: hantavirus infection in deer mice and the intermittent presence of voles in Montana. Oecologia 166, 713–721.CrossRefGoogle ScholarPubMed
Civitello, DJ, Cohen, J, Fatima, H, Halstead, NT, Liriano, J, McMahon, TA, Ortega, CN, Sauer, EL, Sehgal, T, Young, S and Rohr, JR (2015) Biodiversity inhibits parasites: broad evidence for the dilution effect. Proceedings of the National Academy of Sciences 28, 8667–8671.CrossRefGoogle Scholar
Clay, CA, Lehmer, EM, St. Jeor, S and Dearing, MD (2009) Sin Nombre Virus and rodent species diversity: a test of the dilution and amplification hypotheses. PLoS ONE 4, e6467.CrossRefGoogle ScholarPubMed
Combes, C (2001) Parasitism: The Ecology and Evolution of Intimate Interactions. Chicago, IL: The University of Chicago Press.Google Scholar
Cressler, CE, Nelson, WA, Day, T and McCauley, E (2014) Disentangling the interaction among host resources, the immune system and pathogens. Ecology Letters 17, 284–293.CrossRefGoogle ScholarPubMed
Cronin, JP, Welsh, ME, Dekkers, MG, Abercrombie, ST and Mitchell, CE (2010) Host physiological phenotype explains pathogen reservoir potential. Ecology Letters 13, 1221–1232.CrossRefGoogle ScholarPubMed
de Roode, JC, Rarick, RM, Mongue, AJ, Gerardo, NM and Hunter, MD (2011) Aphids indirectly increase virulence and transmission potential of a monarch butterfly parasite by reducing defensive chemistry of a shared food plant. Ecology Letters 14, 453–461.CrossRefGoogle ScholarPubMed
Des Roches, S, Post, DM, Turley, NE, Bailey, JK, Hendry, AP, Kinnison, MT, Schweitzer, JA and Palkovacs, EP (2018) The ecological importance of intraspecific variation. Nature Ecology and Evolution 2, 57–64.CrossRefGoogle ScholarPubMed
Dobson, A, Cattadori, I, Holt, RD, Ostfeld, RS, Keesing, F, Krichbaum, K, Rohr, JR, Perkins, SE and Hudson, PJ (2006) Sacred cows and sympathetic squirrels: the importance of biological diversity to human health. PLoS Medicine 3, e231.CrossRefGoogle ScholarPubMed
Downs, CJ, Schoenle, LA, Han, BA, Harrison, JF and Martin, LB (2019) Scaling of host competence. Trends in Parasitology 35, 182–192.CrossRefGoogle ScholarPubMed
Ebert, D (1994) Virulence and local adaptation of a horizontally transmitted parasite. Science (New York, N.Y.) 265, 1084–1086.CrossRefGoogle ScholarPubMed
Ezenwa, VO, Archie, EA, Craft, ME, Hawley, DM, Martin, LB, Moore, J and White, L (2016) Host-behaviour-parasite feedback: an essential link between animal behaviour and disease ecology. Proceedings of the Royal Society B: Biological Sciences 283, 20153078.CrossRefGoogle ScholarPubMed
Gervasi, SS, Civitello, DJ, Klivitis, HJ and Martin, LB (2015) The context of host competence: a role for plasticity in host-parasite dynamics. Trends in Parasitology 31, 419–425.CrossRefGoogle ScholarPubMed
Gervasi, SS, Burgan, SC, Hofmeister, E, Unnasch, TR and Martin, LB (2017) Stress hormones predict a host superspreader phenotype in the West Nile virus system. Proceedings of the Royal Society B: Biological Sciences 284, 20171090.CrossRefGoogle ScholarPubMed
Gottdenker, NL, Chaves, LF, Calzada, JE, Saldaña, A and Carroll, CR (2012) Host life history strategy, species diversity, and habitat influence Trypanosoma cruzi vector infection in changing landscapes. PLoS Neglected Tropical Diseases 6, e1884.CrossRefGoogle ScholarPubMed
Hall, SR, Becker, CR, Simons, JL, Duffy, MA, Tessier, AJ and Cáceres, CE (2009) Friendly competition: evidence for a dilution effect among competitors in a planktonic host-parasite system. Ecology 90, 791–801.CrossRefGoogle Scholar
Hall, EM, Crespi, EJ, Goldberg, CS and Brunner, JL (2016) Evaluating environmental DNA-based quantification of ranavirus infection in wood frog populations. Molecular Ecology Resources 16, 423–433.CrossRefGoogle ScholarPubMed
Halliday, FW and Rohr, JR (2019) Measuring the shape of the biodiversity-disease relationship across systems reveals new findings and key gaps. Nature Communications 10, 1–10.CrossRefGoogle ScholarPubMed
Halliday, FW, Umbanhowar, J and Mitchell, CE (2018) A host immune hormone modifies parasite species interactions and epidemics: insights from a field manipulation. Proceedings of the Royal Society B: Biological Sciences 285, 20182075.CrossRefGoogle ScholarPubMed
Halsey, S (2019) Defuse the dilution effect debate. Nature Ecology & Evolution 3, 145–146.CrossRefGoogle ScholarPubMed
Han, BA, Schmidt, JP, Bowden, SE and Drake, JM (2015) Rodent reservoirs of future zoonotic diseases. Proceedings of the National Academy of Sciences 112, 7039–7044.CrossRefGoogle ScholarPubMed
Hawley, DM, Etienne, RS, Ezenwa, VO and Jolles, AE (2011) Does animal behavior underlie covariation between host exposure to infectious agents and susceptibility to infection? Implications for disease dynamics. Integrative and Comparative Biology 51, 528–539.CrossRefGoogle ScholarPubMed
Huang, ZYX, de Boer, WF, van Langevelde, F, Olson, V, Blackburn, TM and Prins, HHT (2013) Species’ life-history traits explain interspecific variation in reservoir competence: a possible mechanism underlying the dilution effect. PLoS ONE 8, e54341.CrossRefGoogle ScholarPubMed
Huang, ZYX, Langevelde, FV, Estrada-Pena, A, Suzán, G and De Boer, WF (2016) The diversity-disease relationship: evidence for and criticisms of the dilution effect. Parasitology 143, 1075–1086.CrossRefGoogle ScholarPubMed
Huver, JR, Koprivnikar, J, Johnson, PTJ and Whyard, S (2015) Development and application of an eDNA method to detect and quantify a pathogenic parasite in aquatic ecosystems. Ecological Applications 25, 991–1002.CrossRefGoogle ScholarPubMed
Isaac, NJ and Cowlishaw, G (2004) How species respond to multiple extinction threats. Proceedings of the Royal Society B: Biological Sciences 271, 1135–1141.CrossRefGoogle ScholarPubMed
Johnson, PTJ and Thieltges, DW (2010) Diversity, decoys and the dilution effect: how ecological communities affect disease risk. Journal of Experimental Biology 213, 961–970.CrossRefGoogle ScholarPubMed
Johnson, PTJ, Kellermanns, E and Bowerman, J (2011) Critical windows of disease risk: amphibian pathology driven by developmental changes in host resistance and tolerance. Functional Ecology 25, 726–734.CrossRefGoogle Scholar
Johnson, PTJ, Rohr, JR, Hoverman, JT, Kellermanns, E, Bowerman, J and Lunde, KB (2012) Living fast and dying of infection: host life history drives interspecific variation in infection and disease risk. Ecology Letters 15, 235–242.CrossRefGoogle ScholarPubMed
Johnson, PTJ, Preston, DL, Hoverman, JT and Richgels, KLD (2013) Biodiversity reduces disease through predictable changes in host community competence. Nature 494, 230–234.CrossRefGoogle ScholarPubMed
Johnson, PTJ, Ostfeld, RS and Keesing, F (2015) Frontiers in research on biodiversity and disease. Ecology Letters 18, 1119–1133.CrossRefGoogle ScholarPubMed
Johnson, PTJ, Calhoun, DM, Riepe, TB and Koprivnikar, J (2019a) Chance or choice? Understanding parasite selection and infection in multi-host communities. International Journal for Parasitology 49, 407–415.CrossRefGoogle Scholar
Johnson, PTJ, Calhoun, DM, Riepe, T, McDevitt-Galles, T and Koprivnikar, J (2019b) Community disassembly and disease: realistic – but not randomized – biodiversity losses enhance parasite transmission. Proceedings of the Royal Society B: Biological Sciences 286, 20190260.CrossRefGoogle Scholar
Joseph, MB, Mihaljevic, JR, Orlofske, SA and Paull, SA (2013) Does life history mediate changing disease risk when communities disassemble? Ecology Letters 16, 1405–1412.CrossRefGoogle ScholarPubMed
Kalbe, M and Kurtz, J (2006) Local differences in immunocompetence reflect resistance of sticklebacks against the eye fluke Diplostomum pseudopathaceum. Parasitology 132, 105–116.CrossRefGoogle Scholar
Keesing, F, Holt, RD and Ostfeld, RS (2006) Effects of species diversity on disease risk. Ecology Letters 9, 485–498.CrossRefGoogle ScholarPubMed
Keesing, F, Belden, LK, Daszak, P, Dobson, A, Harvell, CD, Holt, RD, Hudson, P, Jolles, A, Jones, KE, Mitchell, CE, Myers, SS, Bogich, T and Ostfeld, RS (2010) Impacts of biodiversity on the emergence and transmission of infectious diseases. Nature 468, 647–652.CrossRefGoogle ScholarPubMed
Kilpatrick, AM, Daszak, P, Jones, MJ, Marra, PP and Kramer, LD (2006) Host heterogeneity dominates West Nile virus transmission. Proceedings of the Royal Society B: Biology Sciences 273, 2327–2333.CrossRefGoogle ScholarPubMed
Kilpatrick, AM, Fonseca, DM, Ebel, GD, Reddy, MR and Kramer, LD (2010) Spatial and temporal variation in vector competence of Culex pipiens and Cx. restuans mosquitoes for West Nile virus. The American Journal of Tropical Medicine and Hygiene 83, 607–613.CrossRefGoogle ScholarPubMed
Komar, N, Langevin, S, Hinten, S, Nemeth, NM, Edwards, E, Hettler, DL, Davis, BS, Bowen, RA and Bunning, ML (2003) Experimental infection of North American birds with the New York 1999 strain of West Nile Virus. Emerging Infectious Diseases 9, 311–322.CrossRefGoogle ScholarPubMed
LaCroix, C, Jolles, A, Seabloom, EW, Power, AG, Mitchell, CE and Borer, ET (2013) Non-random biodiversity loss underlies predictable increases in viral disease prevalence. Journal of the Royal Society Interface 11, 20130947.CrossRefGoogle ScholarPubMed
LaDeau, SL, Kilpatrick, AM and Marra, PP (2007) West Nile virus emergence and large-scale declines of North American bird populations. Nature 447, 710–713.CrossRefGoogle ScholarPubMed
LaFonte, BE and Johnson, PTJ (2013) Experimental infection dynamics: using immunosuppression and in vivo parasite tracking to understand resistance in an amphibian-trematode system. Journal of Experimental Biology 216, 3700–3708.CrossRefGoogle Scholar
Langwig, KE, Frick, WF, Hoyt, JR, Parise, KL, Drees, KP, Kunz, TH, Foster, JT and Kilpatrick, AM (2017) Drivers of variation in species impacts for a multi-host fungal disease of bats. Philosophical Transactions of the Royal Society B: Biological Sciences 371, 20150456.CrossRefGoogle Scholar
Lee, KA (2006) Linking immune defense and life history at the levels of the individual and the species. Integrative and Comparative Biology 46, 1000–1015.CrossRefGoogle ScholarPubMed
Lloyd-Smith, JO, Schreiber, SJ, Kopp, PE and Getz, WM (2005) Superspreading and the effect of individual variation on disease emergence. Nature 438, 355–359.CrossRefGoogle ScholarPubMed
Luis, AD, Kuenzi, AJ and Mills, JN (2018) Species diversity concurrently dilutes and amplifies transmission in a zoonotic host-pathogen system through competing mechanisms. Proceedings of the National Academy of Sciences of the USA 115, 7979–7984.CrossRefGoogle Scholar
Manlove, KR, Cassirer, EF, Plowright, RK, Cross, PC and Hudson, PJ (2017) Contact and contagion: probability of transmission given contact varies with demographic state in bighorn sheep. Journal of Animal Ecology 86, 908–920.CrossRefGoogle Scholar
Martin, LB, Hopkins, WA, Mydlarz, LD and Rohr, JR (2010) The effects of anthropogenic global changes on immune functions and disease resistance. Annals of the New York Academy of Sciences 1195, 129–148.CrossRefGoogle ScholarPubMed
Martin, LB, Burgan, SC, Adelman, JS and Gervasi, SS (2016) Host competence: an organismal trait to integrate immunology and epidemiology. Integrative and Comparative Biology 56, 1225–1237.CrossRefGoogle ScholarPubMed
Martin, LB, Addison, BA, Bean, AGD, Buchanan, KL, Crino, OL, Eastwood, JR, Flies, AS, Hamede, R, Hill, GE, Klaasen, M, Koch, RE, Martens, JM, Napolitano, C, Narayan, EJ, Peacock, L, Peel, AJ, Peters, A, Raven, N, Risely, A, Roast, MJ, Rollins, LA, Ruiz-Aravena, M, Selechnik, D, Stokes, HS, Ujvari, B and Grogan, LF (2019) Extreme competence: keystone hosts of infections. Trends in Ecology and Evolution 34, 303–314.CrossRefGoogle ScholarPubMed
Mather, TM, Wilson, ML, Moore, SI, Ribeiro, JMC and Spielman, A (1989) Comparing the relative potential of rodents as reservoirs of the Lyme disease spirochete (Borrelia burgdorferi). American Journal of Epidemiology 130, 143–150.CrossRefGoogle Scholar
McCallum, H, Fenton, A, Hudson, PJ, Lee, B, Levick, B, Norman, R, Perkins, SE, Viney, M, Wilson, AJ and Lello, J (2017) Breaking beta: deconstructing the parasite transmission function. Philosophical Transactions of the Royal Society of London B: Biological Sciences 372, 20160084. doi: 10.1098/rstb.2016/0084.CrossRefGoogle ScholarPubMed
McGill, BJ, Enquist, BJ, Weiher, E and Westoby, M (2006) Rebuilding community ecology from functional traits. Trends in Ecology and Evolution 21, 178–185.CrossRefGoogle ScholarPubMed
Merrill, L, Stewart Merrill, TE, Barger, AM and Benson, TJ (2019) Avian health across the landscape: nestling immunity covaries with changing landcover. Integrative and Comparative Biology 59, 1150–1164.CrossRefGoogle ScholarPubMed
Messier, J, McGill, BJ and Lechowicz, MJ (2010) How do traits vary across ecological scales? A case for trait-based ecology. Ecology Letters 13, 838–848.CrossRefGoogle Scholar
Messina, S, Edwards, DP, Eens, M and Constantini, D (2018) Physiological and immunological responses of birds and mammals to forest degradation: a meta-analysis. Biological Conservation 224, 223–229.CrossRefGoogle Scholar
Mihaljevic, JR, Joseph, MB, Orlofske, SA and Paull, SH (2014) The scaling of host density with richness affects the direction, shape, and detectability of diversity-disease relationships. PLoS ONE 9, e97812.CrossRefGoogle ScholarPubMed
Montiglio, P-O, Dammhahn, M, Messier, GD and Réale, DJF (2018) The pace-of-life syndrome revisited: the role of ecological conditions and natural history on the slow-fast continuum. Behavioral Ecology and Sociobiology 72, 116.CrossRefGoogle Scholar
Mordecai, EA, Caldwell, JM, Grossman, MK, Lippi, CA, Johnson, LR, Neira, M, Rohr, JR, Ryan, SJ, Savage, V, Shocket, MS, Sippy, R, Stewart Ibarra, AM, Thomas, MB and Villena, O (2019) Thermal biology of mosquito-borne disease. Ecology Letters 22, 1690–1708.CrossRefGoogle ScholarPubMed
Nemeth, N, Thomsen, B, Spraker, T, Benson, J, Bosco-Lauth, A, Oesterle, P, Bright, J, Muth, J, Gidlewski, T, Campbell, T and Bowen, R (2011) Clinical and pathologic responses of American crows (Corvus brachyrhynchos) and fish crows (C. ossifragus) to experimental West Nile virus infection. Veterinary Pathology 48, 1061–1074.CrossRefGoogle Scholar
Ostfeld, RS and Keesing, F (2000) The function of biodiversity in the ecology of vector-borne zoonotic diseases. Canadian Journal of Zoology 78, 2061–2078.CrossRefGoogle Scholar
Ostfeld, RS and Keesing, F (2012) Effects of host diversity on infectious disease. Annual Review of Ecology Evolution and Systematics 43, 157–182.CrossRefGoogle Scholar
Ostfeld, RS and LoGiudice, K (2003) Community disassembly, biodiversity loss, and the erosion of an ecosystem service. Ecology 84, 1421–1427.CrossRefGoogle Scholar
Paaijmans, K, Blanford, S, Chan, B and Thomas, MB (2012) Warmer temperatures reduce the vectorial capacity of malaria mosquitoes. Biology Letters 8, 465–468.CrossRefGoogle ScholarPubMed
Previtali, MA, Ostfeld, RS, Keesing, F, Jolles, AE, Hanselmann, R and Martin, LB (2012) Relationship between pace of life and immune responses in wild rodents. Oikos 121, 1483–1492.CrossRefGoogle Scholar
Råberg, L, Grahn, M, Hasselquist, D and Svensson, E (1998) On the adaptive significance of stress-induced immunosuppression. Proceedings of the Royal Society B: Biological Sciences 265, 1637–1641.CrossRefGoogle ScholarPubMed
Råberg, L, Sim, D and Read, AF (2007) Disentangling genetic variation for resistance and tolerance to infectious diseases in animals. Science (New York, N.Y.) 318, 812–814.CrossRefGoogle ScholarPubMed
Randolph, SE and Dobson, AD (2012) Pangloss revisited: a critique of the dilution effect and the biodiversity-buffers-disease paradigm. Parasitology 139, 847–863.CrossRefGoogle ScholarPubMed
Rohr, JR, Raffel, TR and Hall, CA (2010) Developmental variation in resistance and tolerance in a multi-host-parasite system. Functional Ecology 24, 1110–1121.CrossRefGoogle Scholar
Rohr, JR, Civitello, DJ, Halliday, FW, Hudson, PJ, Lafferty, KD, Wood, CL and Mordecai, EA (2020) Towards common ground in the biodiversity-disease debate. Nature Ecology and Evolution 4, 24–33.CrossRefGoogle ScholarPubMed
Stearns, SC (1992) The Evolution of Life Histories. London, UK: Oxford University Press.Google Scholar
Stewart Merrill, TE (2019) Variable Immunity and Its Consequences for Parasite Dynamics (PhD thesis). University of Illinois at Urbana-Champaign, Urbana, Illinois.Google Scholar
Stewart Merrill, TE, Hall, SR, Merrill, L and Cáceres, CE (2019) Variation in immune defense shapes disease outcomes in laboratory and wild Daphnia. Integrative and Comparative Biology 59, 1203–1219.CrossRefGoogle ScholarPubMed
Stockwell, MP, Clulow, J and Mahony, MJ (2010) Host species determines whether infection load increases beyond disease-causing thresholds following exposure to the amphibian chytrid fungus. Animal Conservation 13, 62–71.CrossRefGoogle Scholar
Strauss, AT, Bowling, AM, Duffy, MA, Cáceres, CE and Hall, SR (2018) Linking host traits, interactions with competitors and disease: mechanistic foundations for disease dilution. Functional Ecology 32, 1271–1279.CrossRefGoogle Scholar
Telfer, S, Brown, KJ, Sekules, R, Begon, M, Hayden, T and Birtles, R (2005) Disruption of a host-parasite system following the introduction of an exotic host species. Parasitology 130, 661–668.CrossRefGoogle ScholarPubMed
Telford, SR and Spielman, A (1993) Reservoir competence of white-footed mice for Babesia microti. Journal of Entomology 30, 223–227.Google ScholarPubMed
Thompson, JN (2005) Coevolution: the geographic mosaic of coevolutionary arms races. Current Biology 15, R992–R994.CrossRefGoogle ScholarPubMed
Van Buskirk, J and Ostfeld, RS (1995) Controlling Lyme disease by modifying the density and species composition of tick hosts. Ecological Applications 5, 1133–1140.CrossRefGoogle Scholar
VanderWaal, KL and Ezenwa, VO (2016) Heterogeneity in pathogen transmission: mechanisms and methodology. Functional Ecology 30, 1606–1622.CrossRefGoogle Scholar
Vazquez-Prokopec, GM, Perkins, TA, Waller, LA, Lloyd, AL, Reiner, AC Jr, Scott, TW and Kitron, U (2016) Coupled heterogeneities and their impact on parasite transmission and control. Trends in Parasitology 32, 356–367.CrossRefGoogle ScholarPubMed
Violle, C, Enquist, BJ, McGill, BJ, Jiang, L, Albert, CH, Hulshof, C, Jung, V and Messier, J (2012) The return of the variance: intraspecific variability in community ecology. Trends in Ecology and Evolution 27, 244–252.CrossRefGoogle ScholarPubMed
Voyles, J, Woodhams, DC, Saenz, V, Byrne, AQ, Perez, R, Rios-Sotlea, G, Ryan, MJ, Bletz, MC, Sobell, FA, McLetchie, S, Reinert, L, Rosenblum, EB, Rollins-Smith, LA, Ibáñez, R, Ray, JM, Griffith, EJ, Ross, H and Richards-Zawacki, CL (2018) Shifts in disease dynamics in a tropical assemblage are not due to pathogen attenuation. Science (New York, N.Y.) 359, 1517–1519.CrossRefGoogle Scholar
Weinstein, SB, Moura, CW, Mendez, JF and Lafferty, KD (2018) Fear of feces? Tradeoffs between disease risk and foraging drive animal activity around raccoon latrines. Oikos 127, 927–934.CrossRefGoogle Scholar
Wood, CL and Lafferty, KD (2013) Biodiversity and disease: a synthesis of ecological perspectives on Lyme disease transmission. Trends in Ecology and Evolution 28, 239–247.CrossRefGoogle ScholarPubMed
Wood, CL, Lafferty, KD, DeLeo, G, Young, HS, Hudson, PJ and Kuris, AM (2014) Does biodiversity protect humans against infectious disease? Ecology 95, 817–832.CrossRefGoogle ScholarPubMed
Woolhouse, MEJ, Dye, C, Etard, J-F, Smith, T, Charlwood, JD, Garnett, GP, Hagan, P, Hii, JLK, Ndhlovu, PD, Quinnell, RJ, Watts, CH, Chandiwana, SK and Anderson, RM (1997) Heterogeneities in the transmission of infectious agents: Implications for the design of control programs. Proceedings of the National Academy of Sciences of the United States of America 94, 338–342.CrossRefGoogle Scholar
Young, H, Griffin, RH, Wood, CL and Nunn, CL (2013) Does habitat disturbance increase infectious disease risk for primates? Ecology Letters 16, 656–663.CrossRefGoogle ScholarPubMed
Zuk, M and McKean, KA (1996) Sex differences in parasite infections: patterns and processes. International Journal for Parasitology 26, 1009–1023.CrossRefGoogle ScholarPubMed
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