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Demasculinization of male guppies increases resistance to a common and harmful ectoparasite

Published online by Cambridge University Press:  24 September 2015

FELIPE DARGENT ,
ADAM R. REDDON ,
WILLIAM T. SWANEY ,
GREGOR F. FUSSMANN ,
SIMON M. READER ,
MARILYN E. SCOTT  and
MARK R. FORBES
FELIPE DARGENT*
Affiliation:
Department of Biology, McGill University, 1205 Dr. Penfield Av., Montreal, H3A 1B1, QC, Canada Department of Biology, Carleton University, 1125 Colonel By Drive, Ottawa, K1S 5B6, ON, Canada
ADAM R. REDDON
Affiliation:
Department of Biology, McGill University, 1205 Dr. Penfield Av., Montreal, H3A 1B1, QC, Canada
WILLIAM T. SWANEY
Affiliation:
Department of Biology, McGill University, 1205 Dr. Penfield Av., Montreal, H3A 1B1, QC, Canada School of Natural Sciences and Psychology, Liverpool John Moores University, Liverpool, UK
GREGOR F. FUSSMANN
Affiliation:
Department of Biology, McGill University, 1205 Dr. Penfield Av., Montreal, H3A 1B1, QC, Canada
SIMON M. READER
Affiliation:
Department of Biology, McGill University, 1205 Dr. Penfield Av., Montreal, H3A 1B1, QC, Canada
MARILYN E. SCOTT
Affiliation:
Institute of Parasitology and Centre for Host-Parasite Interactions, McGill University, 21111 Lakeshore Road, Ste-Anne de Bellevue, H9X 3V9, QC, Canada
MARK R. FORBES
Affiliation:
Department of Biology, Carleton University, 1125 Colonel By Drive, Ottawa, K1S 5B6, ON, Canada
*
*Corresponding author. Department of Biology, McGill University, 1205 Dr. Penfield Av., Montreal, H3A 1B1, QC, Canada, Department of Biology, Carleton University, 1125 Colonel By Drive, Ottawa, K1S 5B6, ON, Canada. E-mail: [email protected]
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Summary

Parasites are detrimental to host fitness and therefore should strongly select for host defence mechanisms. Yet, hosts vary considerably in their observed parasite loads. One notable source of inter-individual variation in parasitism is host sex. Such variation could be caused by the immunomodulatory effects of gonadal steroids. Here we assess the influence of gonadal steroids on the ability of guppies (Poecilia reticulata) to defend themselves against a common and deleterious parasite (Gyrodactylus turnbulli). Adult male guppies underwent 31 days of artificial demasculinization with the androgen receptor-antagonist flutamide, or feminization with a combination of flutamide and the synthetic oestrogen 17 β-estradiol, and their parasite loads were compared over time to untreated males and females. Both demasculinized and feminized male guppies had lower G. turnbulli loads than the untreated males and females, but this effect appeared to be mainly the result of demasculinization, with feminization having no additional measurable effect. Furthermore, demasculinized males, feminized males and untreated females all suffered lower Gyrodactylus-induced mortality than untreated males. Together, these results suggest that androgens reduce the ability of guppies to control parasite loads, and modulate resistance to and survival from infection. We discuss the relevance of these findings for understanding constraints on the evolution of resistance in guppies and other vertebrates.

Keywords

gonadal steroidsfeminizationsex-biased parasitismtestosteronefishGyrodactylusPoecilia reticulata
Type
Research Article
Information
Parasitology , Volume 142 , Issue 13 , November 2015 , pp. 1647 - 1655
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Copyright
Copyright © Cambridge University Press 2015 

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References

REFERENCES

Amo, L., López, P. and Martín, J. (2005). Prevalence and intensity of haemogregarine blood parasites and their mite vectors in the common wall lizard, Podarcis muralis . Parasitology Research 96, 378–381.Google Scholar
Arnold, A. P. (2009). The organizational–activational hypothesis as the foundation for a unified theory of sexual differentiation of all mammalian tissues. Hormones and Behavior 55, 570–578. doi: http://dx.doi.org/10.1016/j.yhbeh.2009.03.011.Google Scholar
Baatrup, E. and Junge, M. (2001). Antiandrogenic pesticides disrupt sexual characteristics in the adult male guppy Poecilia reticulata . Environmental Health Perspectives 109, 1063–1070.Google Scholar
Bakke, T. A., Cable, J. and Harris, P. D. (2007). The biology of gyrodactylid monogeneans: The ‘Russian-doll killers’. Advances in Parasitology, 64, 161–376.Google Scholar
Bayley, M., Junge, M. and Baatrup, E. (2002). Exposure of juvenile guppies to three antiandrogens causes demasculinization and a reduced sperm count in adult males. Aquatic Toxicology 56, 227–239.CrossRefGoogle Scholar
Bayley, M., Larsen, P. F., Baekgaard, H. and Baatrup, E. (2003). The effects of vinclozolin, an anti-androgenic fungicide, on male guppy secondary sex characters and reproductive success. Biology of Reproduction 69, 1951–1956.Google Scholar
Bjerselius, R., Lundstedt-Enkel, K., Olsén, H., Mayer, I. and Dimberg, K. (2001). Male goldfish reproductive behaviour and physiology are severely affected by exogenous exposure to 17 β-estradiol. Aquatic Toxicology 53, 139–152.Google Scholar
Blas, J., Pérez-Rodríguez, L., Bortolotti, G. R., Viñuela, J. and Marchant, T. A. (2006). Testosterone increases bioavailability of carotenoids: Insights into the honesty of sexual signaling. Proceedings of the National Academy of Sciences 103, 18633–18637.Google Scholar
Buchmann, K. (1997). Population increase of Gyrodactylus derjavini on rainbow trout induced by testosterone treatment of the host. Diseases of Aquatic Organisms 30, 145–150.Google Scholar
Cable, J., Scott, E. C., Tinsley, R. C. and Harris, P. D. (2002). Behavior favoring transmission in the viviparous Monogenean Gyrodactylus turnbulli . Journal of Parasitology 88, 183–184.CrossRefGoogle ScholarPubMed
Cable, J. and van Oosterhout, C. (2007). The impact of parasites on the life history evolution of guppies (Poecilia reticulata): The effects of host size on parasite virulence. International Journal for Parasitology 37, 1449–1458.Google Scholar
Chaves-Pozo, E., García-Ayala, A. and Cabas, I. (2012). Sex steroids modulate fish immune response. In Sex Steroids (ed. Kahn, S. M.), pp. 199–220. InTech. http://www.intechopen.com/books/sex-steroids Google Scholar
Cuesta, A., Vargas-Chacoff, L., García-López, A., Arjona, F. J., Martínez-Rodríguez, G., Meseguer, J., Mancera, J. M. and Esteban, M. A. (2007). Effect of sex-steroid hormones, testosterone and estradiol, on humoral immune parameters of gilthead seabream. Fish & Shellfish Immunology 23, 693–700.Google Scholar
Dargent, F. (2015). The wild side: Assessing evolutionary ecology of defence against parasites in nature . Ph.D. Thesis. pp. 223. McGill University, Montreal.Google Scholar
Dargent, F., Scott, M. E., Hendry, A. P. and Fussmann, G. F. (2013 a). Experimental elimination of parasites in nature leads to the evolution of increased resistance in hosts. Proceedings of the Royal Society B: Biological Sciences 280, 1–9.Google Scholar
Dargent, F., Torres-Dowdall, J., Scott, M. E., Ramnarine, I. and Fussmann, G. F. (2013 b). Can mixed-species groups reduce individual parasite load? A field test with two closely related poeciliid fishes Poecilia reticulata and Poecilia picta . PLoS ONE 8, e56789.CrossRefGoogle ScholarPubMed
de Waal, P. P., Wang, D. S., Nijenhuis, W. A., Schulz, R. W. and Bogerd, J. (2008). Functional characterization and expression analysis of the androgen receptor in zebrafish (Danio rerio) testis. Reproduction 136, 225–234.Google Scholar
Fitzpatrick, S. W., Torres-Dowdall, J., Reznick, D. N., Ghalambor, C. K. and Funk, W. C. (2014). Parallelism isn't perfect: Could disease and flooding drive a life-history anomaly in Trinidadian guppies? The American Naturalist 183, 290–300.Google Scholar
Forbes, M. R. (2007). On sex differences in optimal immunity. Trends in Ecology & Evolution 22, 111–113.CrossRefGoogle ScholarPubMed
Gotanda, K. M., Delaire, L. C., Raeymaekers, J. A. M., Pérez-Jvostov, F., Dargent, F., Bentzen, P., Scott, M. E., Fussmann, G. F. and Hendry, A. P. (2013). Adding parasites to the guppy-predation story: insights from field surveys. Oecologia 172, 155–166.Google Scholar
Grossman, C. (1989). Possible underlying mechanisms of sexual dimorphism in the immune response, fact and hypothesis. Journal of Steroid Biochemistry 34, 241–251.Google Scholar
Guégan, J.-F., Lambert, A., Lévêque, C., Combes, C. and Euzet, L. (1992). Can host body size explain the parasite species richness in tropical freshwater fishes? Oecologia 90, 197–204.Google Scholar
Hamilton, W. (1982). Pathogens as causes of genetic diversity in their host populations. In Population Biology of Infectious Diseases (eds. Anderson, R. M., and May, R. M.), pp. 269–296. Springer, Berlin.Google Scholar
Hamilton, W. D. and Zuk, M. (1982). Heritable true fitness and bright birds – a role for parasites. Science 218, 384–387.CrossRefGoogle Scholar
Harris, P. D. and Lyles, A. M. (1992). Infections of Gyrodactylus bullatarudis and Gyrodactylus turnbulli on guppies (Poecilia reticulata) in Trinidad. Journal of Parasitology 78, 912–914.Google Scholar
Houde, A. E. and Endler, J. A. (1990). Correlated evolution of female mating preferences and male color patterns in the guppy Poecilia reticulata . Science 248, 1405–1408.Google Scholar
Houde, A. E. and Torio, A. J. (1992). Effect of parasitic infection on male color pattern and female choice in guppies. Behavioral Ecology 3, 346–351.Google Scholar
Jensen, K. M., Kahl, M. D., Makynen, E. A., Korte, J. J., Leino, R. L., Butterworth, B. C. and Ankley, G. T. (2004). Characterization of responses to the antiandrogen flutamide in a short-term reproduction assay with the fathead minnow. Aquatic Toxicology 70, 99–110.Google Scholar
Jolly, C., Katsiadaki, I., Le Belle, N., Mayer, I. and Dufour, S. (2006). Development of a stickleback kidney cell culture assay for the screening of androgenic and anti-androgenic endocrine disrupters. Aquatic Toxicology 79, 158–166.Google Scholar
Kennedy, C. E. J., Endler, J. A., Poynton, S. L. and McMinn, H. (1987). Parasite load predicts mate choice in guppies. Behavioral Ecology and Sociobiology 21, 291–295.Google Scholar
Kinnberg, K. and Toft, G. (2003). Effects of estrogenic and antiandrogenic compounds on the testis structure of the adult guppy (Poecilia reticulata). Ecotoxicology and Environmental Safety 54, 16–24.Google Scholar
Klein, S. L. (2000). Hormones and mating system affect sex and species differences in immune function among vertebrates. Behavioural Processes 51, 149–166.Google Scholar
Klein, S. L. (2004). Hormonal and immunological mechanisms mediating sex differences in parasite infection. Parasite Immunology 26, 247–264.Google Scholar
Kodric-Brown, A. and Nicoletto, P. (2001). Female choice in the guppy (Poecilia reticulata): the interaction between male color and display. Behavioral Ecology and Sociobiology 50, 346–351.Google Scholar
Kolluru, G. R., Grether, G. F., South, S. H., Dunlop, E., Cardinali, A., Liu, L. and Carapiet, A. (2006). The effects of carotenoid and food availability on resistance to a naturally occurring parasite (Gyrodactylus turnbulli) in guppies (Poecilia reticulata). Biological Journal of the Linnean Society 89, 301–309.Google Scholar
Krasnov, B., Morand, S., Hawlena, H., Khokhlova, I. and Shenbrot, G. (2005). Sex-biased parasitism, seasonality and sexual size dimorphism in desert rodents. Oecologia 146, 209–217.Google Scholar
Krasnov, B. R., Bordes, F., Khokhlova, I. S. and Morand, S. (2012). Gender-biased parasitism in small mammals: patterns, mechanisms, consequences. Mammalia 76, 1–13.CrossRefGoogle Scholar
Lafferty, K. D., Allesina, S., Arim, M., Briggs, C. J., De Leo, G., Dobson, A. P., Dunne, J. A., Johnson, P. T. J., Kuris, A. M., Marcogliese, D. J., Martinez, N. D., Memmott, J., Marquet, P. A., McLaughlin, J. P., Mordecai, E. A., Pascual, M., Poulin, R. and Thieltges, D. W. (2008). Parasites in food webs: the ultimate missing links. Ecology Letters 11, 533–546.Google Scholar
Lazzaro, B. P. and Little, T. J. (2009). Immunity in a variable world. Philosophical Transactions of the Royal Society B 364, 15–26.Google Scholar
Magurran, A. E. (2005). Evolutionary Ecology: The Trinidadian Guppy, Oxford University Press, New York.CrossRefGoogle Scholar
McGraw, K. J. and Ardia, D. R. (2007). Do carotenoids buffer testosterone-induced immunosuppression? An experimental test in a colourful songbird. Biology Letters 3, 375–378.Google Scholar
Minchella, D. J. and Scott, M. E. (1991). Parasitism: A cryptic determinant of animal community structure. Trends in Ecology & Evolution 6, 250–254.Google Scholar
Nunn, C. L., Lindenfors, P., Pursall, E. R. and Rolff, J. (2009). On sexual dimorphism in immune function. Philosophical Transactions of the Royal Society B: Biological Sciences 364, 61–69.Google Scholar
Perez-Jvostov, F., Hendry, A. P., Fussmann, G. F. and Scott, M. E. (2012). Are host-parasite interactions influenced by adaptation to predators? A test with guppies and Gyrodactylus in experimental stream channels. Oecologia 170, 77–88.Google Scholar
Pérez-Jvostov, F., Hendry, A. P., Fussmann, G. F. and Scott, M. E. (2015). Testing for local host–parasite adaptation: an experiment with Gyrodactylus ectoparasites and guppy hosts. International Journal for Parasitology 45, 409–417.Google Scholar
Poulin, R. and Rohde, K. (1997). Comparing the richness of metazoan ectoparasite communities of marine fishes: Controlling for host phylogeny. Oecologia 110, 278–283.Google Scholar
Price, P. W. (1980). Evolutionary Biology of Parasites, Princeton University Press, New Jersey, USA.Google Scholar
R Development Core Team (2014). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.Google Scholar
Raberg, L., Sim, D. and Read, A. F. (2007). Disentangling genetic variation for resistance and tolerance to infectious diseases in animals. Science 318, 812–814.Google Scholar
Ramírez, R., Harris, P. D. and Bakke, T. A. (2012). An agent-based modelling approach to estimate error in gyrodactylid population growth. International Journal for Parasitology 42, 809–817.Google Scholar
Schmid-Hempel, P. (2011). Evolutionary Parasitology: the Integrated Study of Infections, Immunology, Ecology, and Genetics, Oxford University Press, Oxford.Google Scholar
Scott, M. E. and Anderson, R. M. (1984). The population-dynamics of Gyrodactylus bullatarudis (Monogenea) within laboratory populations of the fish host Poecilia reticulata . Parasitology 89, 159–194.Google Scholar
Sheldon, B. C. and Verhulst, S. (1996). Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends in Ecology & Evolution 11, 317–321.CrossRefGoogle ScholarPubMed
Stephenson, J. F., van Oosterhout, C., Mohammed, R. S. and Cable, J. (2015). Parasites of Trinidadian guppies: evidence for sex- and age-specific trait-mediated indirect effects of predators. Ecology 96, 489–498.Google Scholar
Tadiri, C. P., Dargent, F. and Scott, M. E. (2013). Relative host body condition and food availability influence epidemic dynamics: a Poecilia reticulata-Gyrodactylus turnbulli host-parasite model. Parasitology 140, 343–351.Google Scholar
Tinsley, R. C. (1989). The effects of host sex on transmission success. Parasitology Today 5, 190–195.CrossRefGoogle ScholarPubMed
Travis, J., Reznick, D., Bassar, R. D., López-Sepulcre, A., Ferriere, R. and Coulson, T. (2014). Do eco-evo feedbacks help us understand nature? Answers from studies of the Trinidadian guppy. In Advances in Ecological Research, Volume 50 (eds. Moya-Laraño, J. R., Rowntree, J. and Woodward, G.), pp. 1–40. Academic Press, London.Google Scholar
van Oosterhout, C., Mohammed, R. S., Hansen, H., Archard, G. A., McMullan, M., Weese, D. J. and Cable, J. (2007 a). Selection by parasites in spate conditions in wild Trinidadian guppies (Poecilia reticulata). International Journal for Parasitology 37, 805–812.Google Scholar
van Oosterhout, C., Smith, A. M., Haenfling, B., Ramnarine, I. W., Mohammed, R. S. and Cable, J. (2007 b). The guppy as a conservation model: implications of parasitism and inbreeding for reintroduction success. Conservation Biology 21, 1573–1583.Google Scholar
Wallen, K. and Baum, M. J. (2002). Masculinization and defeminization in altricial and precocial mammals: comparative aspects of steroid hormone action. Hormones, Brain and Behavior 4, 385–423.Google Scholar
Watanuki, H., Yamaguchi, T. and Sakai, M. (2002). Suppression in function of phagocytic cells in common carp Cyprinus carpio L. injected with estradiol, progesterone or 11-ketotestosterone. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology 132, 407–413.Google ScholarPubMed
Zuk, M. (1990). Reproductive strategies and disease susceptibility: an evolutionary viewpoint. Parasitology Today 6, 231–233.Google Scholar
Zuk, M. and McKean, K. A. (1996). Sex differences in parasite infections: patterns and processes. International Journal for Parasitology 26, 1009–1023.Google Scholar
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