Hostname: page-component-586b7cd67f-rdxmf Total loading time: 0 Render date: 2024-11-24T12:44:20.292Z Has data issue: false hasContentIssue false
  • English
  • Français

Proximity to parasites reduces host fitness independent of infection in a Drosophila–Macrocheles system

Published online by Cambridge University Press:  13 March 2018

Collin J. Horn Open the ORCID record for Collin J. Horn [Opens in a new window]  and
Lien T. Luong
Collin J. Horn*
Affiliation:
Department of Biological Sciences, CW405 Biological Sciences Bldg., University of Alberta, Edmonton, AB T6G 2E9Canada
Lien T. Luong
Affiliation:
Department of Biological Sciences, CW405 Biological Sciences Bldg., University of Alberta, Edmonton, AB T6G 2E9Canada
*
Author for correspondence: Collin J. Horn, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Parasites are known to have direct negative effects on host fitness; however, the indirect effects of parasitism on host fitness sans infection are less well understood. Hosts undergo behavioural and physiological changes when in proximity to parasites. Yet, there is little experimental evidence showing that these changes lead to long-term decreases in host fitness. We aimed to determine if parasite exposure affects host fitness independent of contact, because current approaches to parasite ecology may underestimate the effect of parasites on host populations. We assayed the longevity and reproductive output of Drosophila nigrospiracula exposed or not exposed to ectoparasitic Macrocheles subbadius. In order to preclude contact and infection, mites and flies were permanently separated with a mesh screen. Exposed flies had shorter lives and lower fecundity relative to unexposed flies. Recent work in parasite ecology has argued that parasite–host systems show similar processes as predator–prey systems. Our findings mirror the non-consumptive effects observed in predator–prey systems, in which prey species suffer reduced fitness even if they never come into direct contact with predators. Our results support the perspective that there are analogous effects in parasite–host systems, and suggest new directions for research in both parasite ecology and the ecology of fear.

Keywords

Fruit flyhost fitnessnon-consumptive effectsparasite exposureparasite avoidanceectoparasites
Type
Research Article
Information
Parasitology , Volume 145 , Issue 12 , October 2018 , pp. 1564 - 1569
Check for updates
Copyright
Copyright © Cambridge University Press 2018 

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

Adamo, SA, Easy, RH, Kovalko, I, MacDonald, J, McKeen, A, Swanburg, T, Turnbull, KF and Reeve, C (2017) Predator exposure-induced immunosuppression: trade-off, immune redistribution or immune reconfiguration? Journal of Experimental Biology 220, 868–875.Google Scholar
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.Google Scholar
Auld, S, Penczykowski, RM, Ochs, JH, Grippi, DC, Hall, SR and Duffy, MA (2013) Variation in costs of parasite resistance among natural host populations. Journal of Evolutionary Biology 26, 2479–2486.Google Scholar
Beckerman, AP, de Roij, J, Dennis, SR and Little, TJ (2013) A shared mechanism of defense against predators and parasites: chitin regulation and its implications for life-history theory. Ecology and Evolution 3, 5119–5126.Google Scholar
Bergland, AO, Genissel, A, Nuzhdin, SV and Tatar, M (2008) Quantitative trait loci affecting phenotypic plasticity and the allometric relationship of ovariole number and thorax length in Drosophila melanogaster. Genetics 180, 567–582.Google Scholar
Buchanan, AL, Hermann, SL, Lund, M and Szendrei, Z (2017) A meta-analysis of non-consumptive predator effects in arthropods: the influence of organismal and environmental characteristics. Oikos 126, 1233–1240.Google Scholar
Careau, V, Thomas, DW and Humphries, MM (2010) Energetic cost of bot fly parasitism in free-ranging eastern chipmunks. Oecologia 162, 303–312.Google Scholar
Clinchy, M, Schulkin, J, Zanette, LY, Sheriff, MJ, McGowan, PO and Boonstra, R (2011) The neurological ecology of fear: insights neuroscientists and ecologists have to offer one another. Frontiers in Behavioral Neuroscience 5, 1–6.Google Scholar
Ekengren, S, Tryselius, Y, Dushay, MS, Liu, G, Steiner, HÅK and Hultmark, D (2001) A humoral stress response in Drosophila. Current Biology 11, 714–718.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
Hart, BL (2011) Behavioural defences in animals against pathogens and parasites: parallels with the pillars of medicine in humans. Philosophical Transactions of the Royal Society B-Biological Sciences 366, 3406–3417.Google Scholar
Koutroumpa, FA, Monsempes, C, Francois, MC, de Cian, A, Royer, C, Concordet, JP and Jacquin-Joly, E (2016) Heritable genome editing with CRISPR/Cas9 induces anosmia in a crop pest moth. Scientific Reports 6, 1–9.Google Scholar
Kubrak, OI, Lushchak, OV, Zandawala, M and Nassel, DR (2016) Systemic corazonin signalling modulates stress responses and metabolism in Drosophila. Open Biology 6, 272–283.Google Scholar
Kulkarni, PS and Gramapurohit, NP (2017) Effect of corticosterone on larval growth, antipredator behaviour and metamorphosis of Hylarana indica. General and Comparative Endocrinology 251, 21–29.Google Scholar
Larsson, MC, Domingos, AI, Jones, WD, Chiappe, ME, Amrein, H and Vosshall, LB (2004) Or83b encodes a broadly expressed odorant receptor essential for Drosophila olfaction. Neuron 43, 703–714.Google Scholar
Lu, ZC, Wang, YM, Zhu, SG, Yu, H, Guo, JY and Wan, FH (2014) Trade-offs between survival, longevity, and reproduction, and variation of survival tolerance in Mediterranean Bemisia tabaci after temperature stress. Journal of Insect Science 14, 1–14.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 (1996) Evolution of Drosophila mating systems. Evolutionary Biology 29, 73–106.Google Scholar
Moret, Y and Schmid-Hempel, P (2000) Survival for immunity: the price of immune system activation for bumblebee workers. Science 290, 1166–1168.Google Scholar
Nakhleh, J, Moussawi, LE and Osta, MA (2017) The melanization response in insect immunity. In Ligoxygakis, P. (ed). Advances in Insect Physiology, Vol. 52. Cambridge, MA: Academic Press, pp. 83–109.Google Scholar
Odiere, MR, Koski, KG, Weiler, HA and Scott, ME (2010) Concurrent nematode infection and pregnancy induce physiological responses that impair linear growth in the murine foetus. Parasitology 137, 991–1002.Google Scholar
Peacor, SD and Werner, EE (2008) Nonconsumptive effects of predators and trait-mediated indirect effects. In Encyclopedia of Life Sciences (ELS). Chichester, United Kingdom: John Wiley & Sons, Ltd, pp. 1–8.Google Scholar
Peckarsky, B, Cowan, C, Penton, M and Anderson, C (1993) Sublethal consequences of stream-dwelling predatory stoneflies on mayfly growth and fecundity. Ecology 74, 1836–1846.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
Preisser, EL and Bolnick, DI (2008) The many faces of fear: comparing the pathways and impacts of nonconsumptive predator effects on prey populations. PLoS ONE 3, 1–8.Google Scholar
Raffel, TR, Martin, LB and Rohr, JR (2008) Parasites as predators: unifying natural enemy ecology. Trends in Ecology & Evolution 23, 610–618.Google Scholar
Robar, N, Burness, G and Murray, DL (2010) Tropics, trophics and taxonomy: the determinants of parasite-associated host mortality. Oikos 119, 1273–1280.Google Scholar
Rohr, JR, Swan, A, Raffel, TR and Hudson, PJ (2009) Parasites, info-disruption, and the ecology of fear. Oecologia 159, 447–454.Google Scholar
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.Google Scholar
Rohr, JR, Raffel, TR, Halstead, NT, McMahon, TA, Johnson, SA, Boughton, RK and Martin, LB (2013) Early-life exposure to a herbicide has enduring effects on pathogen-induced mortality. Proceedings of the Royal Society B-Biological Sciences 280, 1–7.Google Scholar
Sadd, BM and Schmid-Hempel, P (2009) Principles of ecological immunology. Evolutionary Applications 2, 113–121.Google Scholar
Sadd, BM and Siva-Jothy, MT (2006) Self-harm caused by an insect's innate immunity. Proceedings of the Royal Society B-Biological Sciences 273, 2571–2574.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
Sears, BF, Snyder, PW and Rohr, JR (2015) Host life history and host-parasite syntopy predict behavioural resistance and tolerance of parasites. Journal of Animal Ecology 84, 625–636.Google Scholar
Slos, S and Stoks, R (2008) Predation risk induces stress proteins and reduces antioxidant defense. Functional Ecology 22, 637–642.Google Scholar
Smith, RL (1980) Ecology and Field Biology, 3rd edn. New York, New York, United States of America: Harper & Row, Publishers.Google Scholar
Wilber, MQ, Weinstein, SB and Briggs, CJ (2016) Detecting and quantifying parasite-induced host mortality from intensity data: method comparisons and limitations. International Journal for Parasitology 46, 59–66.Google Scholar