Hostname: page-component-78c5997874-t5tsf Total loading time: 0 Render date: 2024-11-10T13:12:21.121Z Has data issue: false hasContentIssue false

The influence of infection status and parasitism risk on host dispersal and susceptibility to infection in Drosophila nigrospiracula

Published online by Cambridge University Press:  05 November 2021

Taylor Brophy
Affiliation:
Department of Biological Sciences, University of Alberta, Edmonton, AB, Canada
Lien T. Luong*
Affiliation:
Department of Biological Sciences, University of Alberta, Edmonton, AB, Canada
*
Author for correspondence: Lien Luong, E-mail: lluong@ualberta.ca

Abstract

For many organisms, habitat avoidance provides the first line of defence against parasitic infection. Changes in infection status can shift the cost-benefit ratio of remaining in a given habitat vs dispersing. The aim of this study was to test the hypothesis that the propensity to disperse in Drosophila nigrospiracula is mediated by current parasite load and the risk of further infection by an ectoparasitic mite (Macrocheles subbadius). An activity monitor was used to assess dispersal propensity among infected and uninfected flies. The activity level of uninfected females increased threefold upon exposure to a mite, whereas the activity among uninfected males increased by 17-fold in the presence of a questing mite. Among infected flies, the risk of further infection also generated a change in activity, but the magnitude of the response was dependent on host sex. Current infection status influenced the probability of acquiring more parasites due to increased susceptibility to infection with mite load. The probability of acquiring additional mites among males increased more rapidly compared to female flies. Current infection status can potentially determine the risk of further infection, the host propensity and ability to disperse, with consequence for hosts and parasites at the individual, population and species level.

Type
Research Article
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Baines, CB, Diab, S and McCauley, SJ (2020) Parasitism risk and infection alter host dispersal. American Naturalist 196, 119131.CrossRefGoogle ScholarPubMed
Barrile, GM, Chalfoun, AD and Walters, AW (2021) Infection status as the basis for habitat choices in a wild amphibian. American Naturalist 197, 128137.CrossRefGoogle Scholar
Beresford, DV and Sutcliffe, JF (2009) The effect of Macrocheles muscaedomesticase and M. subbadius (Acarina: Macrochelidae) phoresy on the dispersal of Stomoxys calcitrans (Diptera: Muscidae). Systematic and Applied Acarology Special Publications 23, 130.Google Scholar
Binning, SA, Shaw, AK and Roche, DG (2017) Parasites and host performance: incorporating infection into Our understanding of animal movement. Integrative and Comparative Biology 57, 267280.CrossRefGoogle ScholarPubMed
Boulinier, T, McCoy, KD and Sorci, G (2001). Dispersal and parasitism. In Clobert, J, Danchin, E, Dhondt, AA and Nichols, JD (eds), Dispersal. Oxford: Oxford University Press, pp. 169179.Google Scholar
Brophy, T and Luong, L T (2021) Ectoparasite-induced increase inDrosophilahost metabolic rate. Physiological Entomology 46, 17. doi: 10.1111/phen.12334.CrossRefGoogle Scholar
Buck, JC, Weinstein, SB and Young, HS (2018) Ecological and evolutionary consequences of parasite avoidance. Trends in Ecology & Evolution 33, 619632.CrossRefGoogle ScholarPubMed
Cicolani, B, Passariello, S and Petrelli, G (1978) Influence of temperature on population increase of Macrocheles-subbadius (berlese) (Acarina-Mesostigmata). Acarologia 19, 563578.Google Scholar
Clay, PA, Duffy, MA and Rudolf, VHW (2020) Within-host priority effects and epidemic timing determine outbreak severity in co-infected populations. Proceedings of the Royal Society B-Biological Sciences 287: 20200046. doi: 10.1098/rspb.2020.0046.Google Scholar
Clobert, J, Le Galliard, JF, Cote, J, Meylan, S and Massot, M (2009) Informed dispersal, heterogeneity in animal dispersal syndromes and the dynamics of spatially structured populations. Ecology Letters 12, 197209.CrossRefGoogle ScholarPubMed
Cote, J, Clobert, J, Brodin, T, Fogarty, S and Sih, A (2010) Personality-dependent dispersal: characterization, ontogeny and consequences for spatially structured populations. Philosophical Transactions of the Royal Society B-Biological Sciences 365, 40654076.CrossRefGoogle ScholarPubMed
Curtis, VA (2014) Infection-avoidance behaviour in humans and other animals. Trends in Immunology 35, 457464.CrossRefGoogle ScholarPubMed
Davidar, P, Wilson, M and Ribeiro, JMC (1989) Differential distribution of immature Ixodes dammani (Acarai, Ixodidae) on rodent hosts. Journal of Parasitology 75, 898904.CrossRefGoogle Scholar
Deshpande, JN, Kaltz, O and Fronhofer, EA (2021) Host-parasite dynamics set the ecological theatre for the evolution of state- and context-dependent dispersal in hosts. Oikos 130, 121132.CrossRefGoogle Scholar
Dobson, A and Hudson, P (1995) The interaction between the parasites and predators of red grouse Lagopus-Lagopus-Scoticus. Ibis 137, S87S96.CrossRefGoogle Scholar
Egan, ME, Barth, RH and Hanson, FE (1975) Chemically-mediated host selection in a parasitic mite. Nature 257, 788790.CrossRefGoogle Scholar
Halliday, FW, Penczykowski, RM, Barres, B, Eck, JL, Numminen, E and Laine, AL (2020). Facilitative priority effects drive parasite assembly under coinfection. Nature Ecology & Evolution 4, 1510–1521. doi: 10.1038/s41559-020-01289-9.CrossRefGoogle ScholarPubMed
Hanski, I, Saastamoinen, M and Ovaskainen, O (2006) Dispersal-related life-history trade-offs in a butterfly metapopulation. Journal of Animal Ecology 75, 91100.CrossRefGoogle Scholar
Horn, CJ and Luong, LT (2019) Current parasite resistance trades off with future defenses and flight performance. Behavioral Ecology and Sociobiology 73, 7377. doi: 10.1007/s00265-019-2697-5CrossRefGoogle Scholar
Horn, CJ and Luong, LT (2021) Trade-offs between reproduction and behavioural resistance against ectoparasite infection. Physiology & Behavior 239. doi: 10.1016/j.physbeh.2021.113524Google ScholarPubMed
Horn, CJ, Mierzejewski, MK and Luong, LT (2018) Host respiration rate and injury-derived cues drive host preference by an ectoparasite of fruit flies. Physiological and Biochemical Zoology 91, 896903. doi: 10.1086/697466CrossRefGoogle ScholarPubMed
Horn, CJ, Mierzejewski, MK, Elahi, ME and Luong, LT (2020) Extending the ecology of fear: parasite-mediated sexual selection drives host response to parasites. Physiology & Behavior 224, 7.CrossRefGoogle ScholarPubMed
Hoverman, JT, Hoye, BJ and Johnson, PTJ (2013) Does timing matter? How priority effects influence the outcome of parasite interactions within hosts. Oecologia 173, 14711480.CrossRefGoogle ScholarPubMed
Iritani, R (2015) How parasite-mediated costs drive the evolution of disease state-dependent dispersal. Ecological Complexity 21, 113.CrossRefGoogle Scholar
Iritani, R and Iwasa, Y (2014) Parasite infection drives the evolution of state-dependent dispersal of the host. Theoretical Population Biology 92, 113.CrossRefGoogle ScholarPubMed
Johnson, PTJ and Hoverman, JT (2014) Heterogeneous hosts: how variation in host size, behaviour and immunity affects parasite aggregation. Journal of Animal Ecology 83, 11031112.CrossRefGoogle ScholarPubMed
Koenraadt, CJM and Dicke, M (2010) The role of volatiles in aggregation and host-seeking of the haematophagous poultry red mite Dermanyssus gallinae (Acari: Dermanyssidae). Experimental and Applied Acarology 50, 191199.CrossRefGoogle Scholar
Luong, LT, Penoni, LR, Horn, CJ and Polak, M (2015) Physical and physiological costs of ectoparasitic mites on host flight endurance. Ecological Entomology 40, 518524.CrossRefGoogle Scholar
Luong, LT, Brophy, T, Stolz, E and Chan, SJ (2017) State-dependent parasitism by a facultative parasite of fruit flies. Parasitology 144, 14681475.CrossRefGoogle ScholarPubMed
McElroy, EJ and de Buron, I (2014) Host performance as a target of manipulation by parasites: a meta-analysis. Journal of Parasitology 100, 399410.CrossRefGoogle ScholarPubMed
Mideo, N (2009) Parasite adaptations to within-host competition. Trends in Parasitology 25, 261268.CrossRefGoogle ScholarPubMed
Mierzejewski, MK, Horn, CJ and Luong, LT (2019) Ecology of fear: environment-dependent parasite avoidance among ovipositing Drosophila. Parasitology 146, 15641570.CrossRefGoogle ScholarPubMed
Ogden, NH, Casey, ANJ, French, NP, Adams, JDW and Woldehiwet, Z (2002) Field evidence for density-dependent facilitation amongst Ixodes ricinus ticks feeding on sheep. Parasitology 124, 117125.CrossRefGoogle ScholarPubMed
Parker, BJ, Barribeau, SM, Laughton, AM, de Roode, JC and Gerardo, NM (2011) Non-immunological defense in an evolutionary framework. Trends in Ecology & Evolution 26, 242248.CrossRefGoogle Scholar
Polak, M (1996) Ectoparasitic effects on host survival and reproduction: the Drosophila-Macrocheles association. Ecology 77, 13791389.CrossRefGoogle Scholar
Polak, M (2003) Heritability of resistance against ectoparasitism in the Drosophila-Macrocheles system. Journal of Evolutionary Biology 16, 7482.CrossRefGoogle ScholarPubMed
Polak, M and Markow, TA (1995) Effect of ectoparasitic mites on sexual selection in a Sonoran desert fruit fly. Evolution 49, 660669.CrossRefGoogle Scholar
Polak, M and Starmer, WT (1998). Parasite induced risk of mortality elevates reproductive effort in male Drosophila. Proceedings of the Royal Society of London 265, 21972201.CrossRefGoogle ScholarPubMed
Polak, M, Luong, LT and Starmer, WT (2007) Parasites physically block host copulation: a potent mechanism of parasite-mediated sexual selection. Behavioral Ecology 18, 952957.CrossRefGoogle Scholar
Poulin, R (1996) Sexual inequalities in the helminth infections: a cost of being male? The American Naturalist 147, 287295.CrossRefGoogle Scholar
Poulin, R (2007) Evolutionary Ecology of Parasites. Princeton, NJ: Princeton University Press.CrossRefGoogle Scholar
R Development Core Team (2016). R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing. http://www.R-project.org/.Google Scholar
Schmid-Hempel, P (2011) Evolutionary Parasitology: The Integrated Study of Infections, Immunology, Ecology, and Genetics. Oxford, UK: Oxford University Press.Google Scholar
Sonenshine, DE (1991) Biology of Ticks. New York: Oxford University Press.Google Scholar
Suhonen, J, Honkavaara, J and Rantala, MJ (2010) Activation of the immune system promotes insect dispersal in the wild. Oecologia 162, 541547.CrossRefGoogle ScholarPubMed
Tung, S, Mishra, A, Gogna, N, Sadiq, MA, Shreenidhi, PM, Sruti, VRS, Dorai, K and Dey, S (2018) Evolution of dispersal syndrome and its corresponding metabolomic changes. Evolution 72, 18901903.CrossRefGoogle ScholarPubMed
Wang, H, Hails, RS, Cui, WW and Nuttall, PA (2001) Feeding aggregation of the tick Rhipicephalus appendiculatus (Ixodidae): benefits and costs in the contest with host responses. Parasitology 123, 447453.CrossRefGoogle ScholarPubMed
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, 927934.CrossRefGoogle Scholar
Wertheim, B, van Baalen, EJA, Dicke, M and Vet, LEM (2005) Pheromone-mediated aggregation in nonsocial arthropods: an evolutionary ecological perspective. Annual Review of Entomology, vol. 50. Palo Alto: Annual Reviews, pp. 321346.Google Scholar
Wilson, K, Bjornstad, ON, Dobson, AP, Merler, S, Poglayen, G, Randolf, SE, AF, R and Skorping, A (2002). Heterogeneities in macroparasite infections: patterns and processes. In Hudson, PJ, Rizzoli, A, Grenfell, BT, Heesterbeek, H and Dobson, AP (eds), The Ecology of Wildlife Disease. Oxford: Oxford University Press, pp. 644.Google Scholar
Zilio, G, Norgaard, LS, Petrucci, G, Zeballos, N, Gougat-Barbera, C, Fronhofer, EA and Kaltz, O (2021) Parasitism and host dispersal plasticity in an aquatic model system. Journal of Evolutionary Biology. doi: 10.1111/jeb.13893.CrossRefGoogle Scholar