Hostname: page-component-8448b6f56d-wq2xx Total loading time: 0 Render date: 2024-04-24T10:18:58.367Z Has data issue: false hasContentIssue false
  • English
  • Français

Ecology of fear: environment-dependent parasite avoidance among ovipositing Drosophila

Published online by Cambridge University Press:  15 July 2019

Monika K. Mierzejewski ,
Collin J. Horn Open the ORCID record for Collin J. Horn [Opens in a new window]  and
Lien T. Luong
Monika K. Mierzejewski
Affiliation:
Department of Biological Sciences, University of Alberta, CW405 Biological Sciences Bldg., Edmonton, AB T6G 2E9, Canada
Collin J. Horn*
Affiliation:
Department of Biological Sciences, University of Alberta, CW405 Biological Sciences Bldg., Edmonton, AB T6G 2E9, Canada
Lien T. Luong
Affiliation:
Department of Biological Sciences, University of Alberta, CW405 Biological Sciences Bldg., Edmonton, AB T6G 2E9, Canada
*
Author for correspondence: Collin J. Horn, E-mail: chorn@ualberta.ca
Get access Rights & Permissions [Opens in a new window]

Abstract

Habitat avoidance is an anti-parasite behaviour exhibited by at-risk hosts that can minimize exposure to parasites. Because environments are often heterogeneous, host decision-making with regards to habitat use may be affected by the presence of parasites and habitat quality simultaneously. In this study we examine how the ovipositing behaviour of a cactiphilic fruit fly, Drosophila nigrospiracula, is affected by the presence of an ectoparasitic mite, Macrocheles subbadius, in conjunction with other environmental factors – specifically the presence or absence of conspecific eggs and host plant tissue. We hypothesized that the trade-off between site quality and parasite avoidance should favour ovipositing at mite-free sites even if it is of inferior quality. We found that although flies avoided mites in homogeneous environments (86% of eggs at mite-free sites), site quality overwhelmed mite avoidance. Both conspecific eggs (65% of eggs at infested sites with other Drosophila eggs) and host plant tissue (78% of eggs at infested sites with cactus) overpowered mite avoidance. Our results elucidate the context-dependent decision-making of hosts in response to the presence of parasites in variable environments, and suggest how the ecology of fear and associated trade-offs may influence the relative investment in anti-parasite behaviour in susceptible hosts.

Keywords

Antiparasite behaviourdefensive behaviourecology of fearectoparasiteenvironmental riskhost–parasite interactioninfection risknon-consumptive effectreproductive behaviourrisk trade-off
Type
Research Article
Information
Parasitology , Volume 146 , Issue 12 , October 2019 , pp. 1564 - 1570
Check for updates
Copyright
Copyright © Cambridge University Press 2019 

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.)

Footnotes

*

These authors contributed equally to this work.

References

Arvanitis, L, Wiklund, C and Ehrlen, J (2007) Butterfly seed predation: effects of landscape characteristics, plant ploidy level and population structure. Oecologia 152, 275–285.Google Scholar
Atkinson, RJ, McVean, GAT and Stone, GN (2002) Use of population genetic data to infer oviposition behaviour: species-specific patterns in four oak gallwasps (Hymenoptera : Cynipidae). Proceedings of the Royal Society B-Biological Sciences 269, 383–390.Google Scholar
Barber, I and Dingemanse, NJ (2010) Parasitism and the evolutionary ecology of animal personality. Philosophical Transactions of the Royal Society B 365, 4077–4088.Google Scholar
Bonneaud, C, Mazuc, J, Gonzalez, G, Haussy, C, Chastel, O, Faivre, B and Sorci, G (2003) Assessing the cost of mounting an immune response. American Naturalist 161, 367–379.Google Scholar
Brunner, FS and Eizaguirre, C (2016) Can environmental change affect host/parasite-mediated speciation? Zoology 119, 384–394.Google Scholar
Buck, JC, Weinstein, SB and Young, HS (2018) Ecological and evolutionary consequences of parasite avoidance. Trends in Ecology & Evolution 33, 619–632.Google Scholar
Coulson, G, Cripps, JK, Garnick, S, Bristow, V and Beveridge, I (2018) Parasite insight: assessing fitness costs, infection risks and foraging benefits relating to gastrointestinal nematodes in wild mammalian herbivores. Philosophical Transactions of the Royal Society B-Biological Sciences 373, 1–10. doi:10.1098/rstb.2017.0197.Google Scholar
Coyne, JA and Orr, HA (1997) ‘Patterns of speciation in Drosophila’ revisited. Evolution 51, 295–303.Google Scholar
Dainese, M, Schneider, G, Krauss, J and Steffan-Dewenter, I (2017) Complementarity among natural enemies enhances pest suppression. Scientific Reports 7, 1–8. doi:10.1038/s41598-017-08316-z.Google Scholar
Davis, JM and Stamps, JA (2004) The effect of natal experience on habitat preferences. Trends in Ecology & Evolution 19, 411–416.Google Scholar
de Jong, G (1995) Phenotypic plasticity as a product of selection in a variable environment. The American Naturalist 145, 493–512.Google Scholar
de la Flor, M, Chen, LJ, Manson-Bishop, C, Chu, TC, Zamora, K, Robbins, D, Gunaratne, G and Roman, G (2017) Drosophila increase exploration after visually detecting predators. PLoS ONE 12, 1–17. doi:10.1371/journal.pone.0180749.Google Scholar
de Roode, JC and Lefèvre, T (2012) Behavioral immunity in insects. Insects 3, 789–820.Google Scholar
Duménil, C, Woud, D, Pinto, F, Alkema, JT, Jansen, I, Van der Geest, AM, Roessingh, S and Billeter, JC (2016) Pheromonal cues deposited by mated females convey social information about egg-laying sites in Drosophila melanogaster. Journal of Chemical Ecology 42, 259–269.Google Scholar
Fanara, JJ, Fontdevila, A and Hasson, E (1999) Oviposition preference and life history traits in cactophilic Drosophila koepferae and D-buzzatii in association with their natural hosts. Evolutionary Ecology 13, 173–190.Google Scholar
Fellows, DP and Heed, WB (1972) Factors affecting host plant selection in desert-adapted cactiphilic Drosophila. Ecology 53, 850–858.Google Scholar
French, SS, DeNardo, DF and Moore, MC (2007) Trade-offs between the reproductive and immune systems: facultative responses to resources or obligate responses to reproduction? American Naturalist 170, 79–89.Google Scholar
Gaudry, Q, Nagel, KI and Wilson, RI (2012) Smelling on the fly: sensory cues and strategies for olfactory navigation in Drosophila. Current Opinion in Neurobiology 22, 216–222.Google Scholar
Geraldi, NR and Macreadie, PI (2013) Restricting prey dispersal can overestimate the importance of predation in trophic cascades. PLoS ONE 8, 1–9.Google Scholar
Grostal, P and Dicke, M (1999) Direct and indirect cues of predation risk influence behavior and reproduction of prey: a case for acarine interactions. Behavioral Ecology 10, 422–427.Google Scholar
Hall, AR, Scanlan, PD, Morgan, AD and Buckling, A (2011) Host-parasite coevolutionary arms races give way to fluctuating selection. Ecology Letters 14, 635–642.Google Scholar
Horn, CJ and Luong, LT (2018). Proximity to parasites reduces host fitness independent of infection in a Drosophila-Macrocheles system. Parasitology 145, 1–6. doi:10.1017/s0031182018000379.Google Scholar
Horn, CJ and Luong, LT (2019) Current parasite resistance trades off with future defenses and flight performance. Behavioral Ecology and Sociobiology 73, 1–10.Google Scholar
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, 896–903.Google Scholar
Jaenike, J (1982) Environmental modification of oviposition behavior in Drosophila. American Naturalist 119, 784–802.Google Scholar
Jaenike, J and Holt, RD (1991) Genetic-variation for habitat preference – evidence and explanations. American Naturalist 137, S67–S90.Google Scholar
Janssen, A, Vanalphen, JJM, Sabelis, MW and Bakker, K (1995) Specificity of odor mediated avoidance of competition in Drosophila parasitoids. Behavioral Ecology and Sociobiology 36, 229–235.Google Scholar
Johnston, JS and Heed, WB (1976) Dispersal of desert-adapted Drosophila: the Saguaro-breeding D. nigrospiracula. American Naturalist 110, 629–651.Google Scholar
Joseph, RM, Devineni, AV, King, IFG and Heberlein, U (2009) Oviposition preference for and positional avoidance of acetic acid provide a model for competing behavioral drives in Drosophila. Proceedings of the National Academy of Sciences of the United States of America 106, 11352–11357.Google Scholar
Karvonen, A and Seehausen, O (2012) The role of parasitism in adaptive radiations – when might parasites promote and when might they constrain ecological speciation? International Journal of Ecology 2012, 280169.Google Scholar
Klemme, I and Karvonen, A (2016) Learned parasite avoidance is driven by host personality and resistance to infection in a fish-trematode interaction. Proceedings of the Royal Society B-Biological Sciences 283, 1–7. doi:10.1098/rspb.2016.1148.Google Scholar
Kortet, R, Hedrick, AV and Vainikka, A (2010) Parasitism, predation and the evolution of animal personalities. Ecology Letters 13, 1449–1458.Google Scholar
Koprivnikar, J and Urichuk, TMY (2017) Time-lagged effect of predators on tadpole behaviour and parasite infection. Biology Letters 13, 1–4.Google Scholar
Koskella, B (2018) Resistance gained, resistance lost: an explanation for host-parasite coexistence. PLoS Biology 16, e3000013–e3000013.Google Scholar
Lefèvre, T, de Roode, JC, Kacsoh, BZ and Schlenke, TA (2012) Defence strategies against a parasitoid wasp in Drosophila: fight or flight? Biology Letters 8, 230–233.Google Scholar
Lindstrom, KM, Foufopoulos, J, Parn, H and Wikelski, M (2004) Immunological investments reflect parasite abundance in island populations of Darwin's finches. Proceedings of the Royal Society B-Biological Sciences 271, 1513–1519.Google Scholar
Luong, LT and Polak, M (2007) Environment-dependent trade-offs between ectoparasite resistance and larval competitive ability in the Drosophila–Macrocheles system. Heredity 99, 632–640.Google Scholar
Luong, LT, Horn, CJ and Brophy, T (2017) Mitey costly: energetic costs of parasite avoidance and infection. Physiological and Biochemical Zoology 90, 471–477.Google Scholar
Markow, TA (1988) Reproductive behavior of Drosophila melanogaster and Drosophila nigrospiracula in the field and in the laboratory. Journal of Comparative Psychology 102, 169–173.Google Scholar
Mikheev, VN, Pasternak, AF, Taskinen, J and Valtonen, TE (2013). Grouping facilitates avoidance of parasites by fish. Parasites & Vectors 6, 1–8. doi:10.1186/1756-3305-6-301.Google Scholar
Pascua, LL, Hall, AR, Best, A, Morgan, AD, Boots, M and Buckling, A (2014) Higher resources decrease fluctuating selection during host-parasite coevolution. Ecology Letters 17, 1380–1388.Google Scholar
Patterson, JEH and Ruckstuhl, KE (2013) Parasite infection and host group size: a meta-analytical review. Parasitology 140, 803–813.Google Scholar
Peacor, SD and Werner, EE (2008) Nonconsumptive effects of predators and trait-mediated indirect effects. In Encyclopedia of Life Sciences (ELS). Chichester, UK: John Wiley & Sons, Ltd, pp. 1–8.Google Scholar
Perez-Leanos, A, Loustalot-Laclette, MR, Nazario-Yepiz, N and Markow, TA (2017) Ectoparasitic mites and their Drosophila hosts. Fly 11, 10–18.Google Scholar
Polak, M (1996) Ectoparasitic effects on host survival and reproduction: the Drosophila–Macrocheles association. Ecology 77, 1379–1389.Google Scholar
Poulin, R and Morand, S (2000) The diversity of parasites. Quarterly Review of Biology 75, 277–293.Google Scholar
Quan, AS and Eisen, MB (2018) The ecology of the Drosophila-yeast mutualism in wineries. PLoS One 13, e0196440–e0196440.Google Scholar
Raffel, TR, Rohr, JR, Kiesecker, JM and Hudson, PJ (2006) Negative effects of changing temperature on amphibian immunity under field conditions. Functional Ecology 20, 819–828.Google Scholar
Raffel, TR, Martin, LB and Rohr, JR (2008) Parasites as predators: unifying natural enemy ecology. Trends in Ecology 23, 610–618.Google Scholar
Rodrigues, MA, Martins, NE, Balance, LF, Broom, LN, Dias, AJS, Fernandes, ASD, Rodrigues, F, Sucena, E and Mirth, CK (2015) Drosophila melanogaster larvae make nutritional choices that minimize developmental time. Journal of Insect Physiology 81, 69–80.Google Scholar
Rosa, E, van Nouhuys, S and Saastamoinen, M (2017) The more the merrier: conspecific density improves performance of gregarious larvae and reduces susceptibility to a pupal parasitoid. Ecology and Evolution 7, 10710–10720.Google Scholar
RStudio Team (2015) RStudio: Integrated Development for R. Boston, MA: RStudio, Inc. Available at http://www.rstudio.com/.Google Scholar
Sang, JH and King, RC (1961) Nutritional requirements of axenically cultured Drosophila melanogaster adults. Journal of Experimental Biology, 38, 793–809.Google Scholar
Sarin, S and Dukas, R (2009) Social learning about egg-laying substrates in fruitflies. Proceedings of the Royal Society B-Biological Sciences 276, 4323–4328.Google Scholar
Schulenburg, H, Kurtz, J, Moret, Y and Siva-Jothy, MT (2009) Introduction. Ecological immunology. The Royal Society, Philosophical Transactions of the Royal Society B 364, 3–14.Google Scholar
Schwenke, RA, Lazzaro, BP and Wolfner, MF (2016) Reproduction-immunity trade-offs in insects. Annual Review of Entomology 61, 239–256.Google Scholar
Singer, MC, Ng, D and Thomas, CD (1988) Heritability of oviposition preference and its relationship to offspring performance within a single insect population. Evolution 42, 977–985.Google Scholar
Siva-Jothy, JA, Monteith, KM and Vale, PF (2018) Navigating infection risk during oviposition and cannibalistic foraging in a holometabolous insect. Behavioral Ecology 29, 1426–1435.Google Scholar
Smith, LA, White, PCL and Hutchings, MR (2006) Effect of the nutritional environment and reproductive investment on herbivore-parasite interactions in grazing environments. Behavioral Ecology 17, 591–596.Google Scholar
Soto, IM, Carreira, VP, Corio, C, Padro, J, Soto, EM and Hasson, E (2014). Differences in tolerance to host cactus alkaloids in Drosophila koepferae and D. buzzatii. PLoS ONE 9, 1–9. doi:10.1371/journal.pone.0088370.Google Scholar
Stearns, SC (1989) Trade-offs in life-history evolution. Functional Ecology 3, 259–268.Google Scholar
Thompson, JN (1988) Evolutionary ecology of the relationship between oviposition preference and performance of offspring in phytophagous insects. Entomologia Experimentalis Et Applicata 47, 3–14.Google Scholar
Vilcinskas, A (2013) Evolutionary plasticity of insect immunity. Journal of Insect Physiology 59, 123–129.Google Scholar
Weiner, J (1992) Physiological limits to sustainable energy budgets in birds and mammals – ecological implications. Trends in Ecology & Evolution 7, 384–388.Google Scholar
Wertheim, B, Marchais, J, Vet, LEM and Dicke, M (2002) Allee effect in larval resource exploitation in Drosophila: an interaction among density of adults, larvae, and micro-organisms. Ecological Entomology 27, 608–617.Google Scholar
Zhukovskaya, M, Yanagawa, A and Forschler, BT (2013) Grooming behavior as a mechanism of insect disease defense. Insects 4, 609–630.Google Scholar