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Adding parasites to the guppy-predation story: insights from field surveys

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Abstract

Studies of phenotypic variation in nature often consider only a single potential selective agent. In such cases, it remains an open question as to whether variation attributed to that single measured agent might be influenced by some other unmeasured agent. Previous research has shown that phenotypic variation in the Trinidadian guppy (Poecilia reticulata) is strongly influenced by predation regime, and we here ask whether parasitism might represent an additional important selective agent shaping this variation. We performed a field survey of 26 natural guppy populations of known predation regime in northern Trinidad. We quantified levels of parasitism of guppies by the monogenean ecotoparasite, Gyrodactylus, and examined whether this parasite was associated with guppy body size or male colour. Spatial variation in Gyrodactylus parasitism was consistent between years, and parasite prevalence was generally, but not always, higher at high-predation sites than at low-predation sites. Consistent with previous work, predation regime was related to guppy size and some aspects of male colour, whereas parasitism showed few and only minor associations with the same traits. Moreover, a consideration of parasitism did not alter any interpretations regarding associations between guppy traits and predation regimes. These results suggest that parasitism, at least as quantified in the present study, does not play a major role in shaping variation in guppy body size or colour. Nevertheless, considerable variation in these traits, even within a predation regime, suggests the likely importance of other selective agents beyond just predation regime.

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References

  • Bagge AM, Poulin R, Valtonen ET (2004) Fish population size, and not density, as the determining factor of parasite infection: a case study. Parasitology 128:305–313

    Article  PubMed  CAS  Google Scholar 

  • Bakke TA, Cable J, Harris PD (2007) The biology of gyrodactylid monogeneans: the “Russian-doll killers”. In: Baker JR. Muller R, Rollinson D (eds) Advances in parasitology, vol 64. Academic Press, New York, pp 161–460

  • Barber I, Hoare D, Krause J (2000) Effects of parasites on fish behaviour: a review and evolutionary perspective. Rev Fish Biol Fish 10:131–165

    Article  Google Scholar 

  • Cable J, Van Oosterhout C (2007a) The impact of parasites on the life history evolution of guppies (Poecilia reticulata): the effects of host size on parasite virulence. Int J Parasitol 37:1449–1458

    Article  PubMed  CAS  Google Scholar 

  • Cable J, van Oosterhout C (2007b) The role of innate and acquired resistance in two natural populations of guppies (Poecilia reticulata) infected with the ectoparasite Gyrodactylus turnbulli. Biol J Linn Soc 90:647–655

    Article  Google Scholar 

  • Cain AJ, Sheppard PM (1950) Selection in the polymorphic land snail Cepaea nemoralis. Heredity 4:275–294

    Article  PubMed  CAS  Google Scholar 

  • Crispo E, Bentzen P, Reznick DN, Kinnison MT, Hendry AP (2006) The relative influence of natural selection and geography on gene flow in guppies. Mol Ecol 15:49–62

    Article  PubMed  CAS  Google Scholar 

  • Decaestecker E, de Meester L, Ebert D (2002) In deep trouble: habitat selection constrained by multiple enemies in zooplankton. Proc Natl Acad Sci USA 99:5481–5485

    Article  PubMed  CAS  Google Scholar 

  • Dick JTA et al (2010) Parasitism may enhance rather than reduce the predatory impact of an invader. Biol Lett 6:636–638

    Article  PubMed  Google Scholar 

  • Endler JA (1978) A predator’s view of animal color patterns. Evol Biol 11:319–364

    Google Scholar 

  • Endler JA (1980) Natural selection on color patterns in Poecilia reticulata. Evolution 34:76–91

    Article  Google Scholar 

  • Endler JA (1990) On the measurement and classification of color in studies of animal color patterns. Biol J Linn Soc 41:315–352

    Article  Google Scholar 

  • Endler JA (1991) Variation in the appearance of guppy color patterns to guppies and their predators under different visual conditions. Vis Res 31:587–608

    Article  PubMed  CAS  Google Scholar 

  • Endler JA (1995) Multiple trait coevolution and environmental gradients in guppies. Trends Ecol Evol 10:22–29

    Article  PubMed  CAS  Google Scholar 

  • Endler JA, Houde AE (1995) Geographic variation in female preferences for male traits in Poecilia reticulata. Evolution 49:456–468

    Article  Google Scholar 

  • Fraser B, Neff B (2010) Parasite mediated homogenizing selection at the MHC in guppies. Genetica 138:273–278

    Article  PubMed  CAS  Google Scholar 

  • Fraser BA, Ramnarine IW, Neff BD (2010) Temporal variation at the MHC class IIB in wild populations of the guppy (Poecilia reticulata). Evolution 64:286–2096

    Google Scholar 

  • Ghalambor CK, McKay JK, Caroll SP, Reznick DN (2007) Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments. Funct Ecol 21:394–407

    Article  Google Scholar 

  • Gheorgiu C, Marcogliese DJ, Scott M (2006) Concentration-dependent effects of waterborne zinc on population dynamics of Gyrodactylus turnbulli (Monogenea) on isolated guppies (Poecilia reticulata). Parasitology 132:225–232

    Article  PubMed  CAS  Google Scholar 

  • Gray SM, Robinson BW (2002) Experimental evidence that competition between stickleback species favours adaptive character divergence. Ecol Lett 5:264–272

    Article  Google Scholar 

  • Grether GF, Hudon J, Millie DF (1999) Carotenoid limitation of sexual coloration along an environmental gradient in guppies. Proc R Soc Lond B 266:1317–1322

    Article  CAS  Google Scholar 

  • Grether GF, Millie DF, Bryant MJ, Reznick DN, Mayea W (2001) Rain forest canopy cover, resource availability, and life history evolution in guppies. Ecology 82:1546–1559

    Article  Google Scholar 

  • Harris PD (1986) Species of Gyrodactylus von Nordmann, 1832 (Monogenea Gyrodactylidae) from poeciliid fishes, with a description of G. turnbulli sp. nov. from the guppy, Poecilia reticulata. Peters. J Nat Hist 20:183–191

    Article  Google Scholar 

  • Harris PD, Lyles AM (1992) Infections of Gyrodactylus bullatarudis and Gyrodactylus turnbulli on guppies (Poecilia reticulata) in Trinidad. J Parasitol 78:912–914

    Article  PubMed  CAS  Google Scholar 

  • Hatcher MJ, Dick JTA, Dunn AM (2006) How parasites affect interactions between competitors and predators. Ecol Lett 9:1253–1271

    Article  PubMed  Google Scholar 

  • Houde AE (1992) Sex-linked heritability of a sexually selected character in a natural popualtion of Poecilia reticulata (Pisces: Poeciliidae) (guppies). Heredity 69:229–235

    Article  Google Scholar 

  • Houde AE (1997) Sex, color, and mate choice in guppies. Princeton University Press, Princeton

    Google Scholar 

  • Houde AE, Torio AJ (1992) Effect of parasitic infection on male color pattern and female choice in guppies. Behav Ecol 3:346–351

    Article  Google Scholar 

  • Hughes KA, Rodd FH, Reznick DN (2005) Genetic and environmental effects on secondary sex traits in guppies (Poecilia reticulata). J Evol Biol 18:35–45

    Article  PubMed  CAS  Google Scholar 

  • Johnson PTJ et al (2010) When parasites become prey: ecological and epidemiological significance of eating parasites. Trends Ecol Evol 25:362–371

    Article  PubMed  Google Scholar 

  • Johnson MB, Lafferty KD, van Oosterhout C, Cable J (2011) Parasite transmission in social interacting hosts: Monogenean epidemics in guppies. PLoS ONE 6:e22634

    Article  PubMed  CAS  Google Scholar 

  • Jones JS, Leith BH, Rawlings P (1977) Polymorphism in Cepaea: a problem with too many solutions? Annu Rev Ecol Syst 8:109–143

    Article  Google Scholar 

  • Karino K, Haijima Y (2001) Heritability of male secondary sexual traits in feral guppies in Japan. J Ethol 19:33–37

    Article  Google Scholar 

  • Kemp DJ, Reznick DN, Grether GF (2008) Ornamental evolution in Trinidadian guppies (Poecilia reticulata): insights from sensory processing-based analyses of entire colour patterns. Biol J Linn Soc 95:734–747

    Article  Google Scholar 

  • Kennedy CR, Guégan JF (1994) Regional versus local helminth parasite richness in British freshwater fish—saturated or unsaturated parasite communities. Parasitology 109:175–185

    Article  PubMed  Google Scholar 

  • Kennedy CEJ, Endler JA, Poynton SL, McMinn H (1987) Parasite load predicts mate choice in guppies. Behav Ecol Sociobiol 21:291–295

    Article  Google Scholar 

  • Kerfoot WC, Sih A (1987) Predation: direct and indirect impacts on aquatic communities. University Press of New England, Hanover

    Google Scholar 

  • Kodric-Brown A (1989) Dietary carotenoids and male mating success in the guppy—an environmental component to female choice. Behav Ecol Sociobiol 25:393–401

    Article  Google Scholar 

  • Kolluru GR, Grether GF, Dunlop E, South SH (2009) Food availability and parasite infection influence mating tactics in guppies (Poecilia reticulata). Behav Ecol 20:131–137

    Article  Google Scholar 

  • Langerhans RB, Layman CA, Shokrollahi AM, DeWitt TJ (2004) Predator-driven phenotypic diversification in Gambusia affinis. Evolution 58:2305–2318

    PubMed  Google Scholar 

  • Lopez S (1998) Acquired resistance affects male sexual diplay and female choice in guppies in Trinindad. Proc R Soc Lond B 265:717–723

    Article  Google Scholar 

  • Lozano GA (1994) Carotenoids, parasites, and sexual selection. Oikos 70:309–311

    Article  Google Scholar 

  • MacColl ADC (2011) The ecological causes of evolution. Trends Ecol Evol 26:514–522

    Article  PubMed  Google Scholar 

  • Magurran AE (1990) The adaptive significance of schooling as an anti-predator derence in fish. Ann Zool Fenn 27:51–66

    Google Scholar 

  • Magurran AE (2005) Evolutionary ecology: the Trinidadian guppy. Oxford University Press, New York

    Book  Google Scholar 

  • Mandic M, Todgham AE, Richards JG (2009) Mechanisms and evolution of hypoxia tolerance in fish. Proc R Soc Lond B 276:735–744

    Google Scholar 

  • Martin CH, Johnsen S (2007) A field test of the Hamilton-Zuk hypothesis in the Trinidadian guppy (Poecilia reticulata). Behav Ecol Sociobiol 61:1897–1909

    Article  Google Scholar 

  • Millar N, Hendry A (2012) Population divergence of private and non-private signals in wild guppies. Environ Biol Fish 513–525

  • Millar NP, Reznick DN, Kinnison MT, Hendry AP (2006) Disentangling the selective factors that act on male colour in wild guppies. Oikos 113:1–12

    Article  Google Scholar 

  • Otti O, Gantenbein-Ritter I, Jacot A, Brinkhof MWG (2012) Immune response increases predation risk. Evolution 66:732–739

    Article  PubMed  Google Scholar 

  • Pérez-Jvostov F, Hendry AP, Fussmann GF, Scott ME (2012) Are host-parasite interactions influenced by adaptation to predators? A test with guppies and Gyrodactylus in experimental stream channels. Oecologia 170:77–88

    Article  PubMed  Google Scholar 

  • Porter JW, Muscatine L, Dubinsky Z, Falkowski PG (1984) Primary production and photoadaptation in light- and shade-adapted colonies of the symbiotic coral, Stylophora pistillata. Proc R Soc Lond B 222:161–180

    Article  Google Scholar 

  • Raffel TR, Hoverman JT, Halstead NT, Michel PJ, Rohr JR (2010) Parasitism in a community context: trait-mediated interactions with competition and predation. Ecology 91:1900–1907

    Article  PubMed  Google Scholar 

  • Reardon EE, Chapman LJ (2010) Hypoxia and energetics of mouth brooding: is parental care a costly affair? Comp Biochem Physiol A Comp Physiol 156:400–406

    Google Scholar 

  • Reznick D, Endler JA (1982) The impact of predation on life history evolution in Trinidadian guppies (Poecilia reticulata). Evolution 36:160–177

    Article  Google Scholar 

  • Reznick DN, Butler MJ, Rodd FH, Ross P (1996) Life-history evolution in guppies (Poecilia reticulata). VI. Differential mortality as a mechanism for natural selection. Evolution 50:1651–1660

    Article  Google Scholar 

  • Reznick D, Butler MJ IV, Rodd FH (2001) Life-history evolution in guppies. VII. The comparative ecology of high- and low-predation environments. Am Nat 157:126–140

    Article  PubMed  CAS  Google Scholar 

  • Rifkin JL, Nunn CL, Garamszegi LZ (2012) Do animals living in larger groups experience greater parasitism? A meta-analysis. Am Nat 180:70–82

    Article  PubMed  Google Scholar 

  • Rodd FH, Reznick DN (1997) Variation in the demography of guppy populations: the importance of predation and life histories. Ecology 78:405–418

    Google Scholar 

  • Rodd FH, Hughes KA, Grether GF, Baril CT (2002) A possible non-sexual origin of mate preference: are male guppies mimicking fruit? Proc R Soc Lond B 269:475–481

    Article  Google Scholar 

  • Roff DA (1992) The evolution of life histories: theory and analysis. Chapman and Hall, New York

    Google Scholar 

  • Schluter D (1994) Experimental evidence that competition promotes divergence in adaptive radiation. Science 266:798–801

    Article  PubMed  CAS  Google Scholar 

  • Schwartz AK, Hendry AP (2007) A test for the parallel co-evolution of male colour and female preference in Trinidadian guppies (Poecilia reticulata). Evol Ecol Res 9:71–90

    Google Scholar 

  • Schwartz AK, Hendry AP (2010) Testing the influence of local forest canopy clearing on phenotypic variation in Trinidadian guppies. Funct Ecol 24:354–364

    Article  Google Scholar 

  • Scott ME (1985) Dynamics of challenge infections of Gyrodactylus bullatarudis Turnbull (Monogenea) on guppies, Poecilia reticulata (Peters). J Fish Dis 8:495–503

    Article  Google Scholar 

  • Scott ME (1987) Temporal changes in aggregation: a laboratory study. Parasitology 94:583–595

    Article  PubMed  Google Scholar 

  • Scott ME, Anderson RM (1984) The population dynamics of Gyrodactylus bullatarudis within laboratory populations of the fish host Poecilia reticulata. Parasitology 89:159–195

    Article  PubMed  Google Scholar 

  • Scott ME, Nokes DJ (1984) Temperature-dependent reproduction and survival of Gyrodactylus bullatarudis (Monogenea) on guppies (Poecilia reticulata). Parasitology 89:221–229

    Article  Google Scholar 

  • Strauss RE (1990) Predation and life-history variation in Poecilia reticulata (Cyprinodontiformes: Poeciliidae). Environ Biol Fish 27:121–130

    Article  Google Scholar 

  • Thomas F, Renaud F, Meeüs TD, Cézilly F, Cézilly F (2009) Parasites, age and the Hamilton-Zuk hypothesis: inferential fallacy? Oikos 74:305–309

    Article  Google Scholar 

  • Tripathi N, Hoffmann M, Willing EM, Lanz C, Weigel D, Dreyer C (2009) Genetic linkage map of the guppy, Poecilia reticulata, and quantitative trait loci analysis of male size and colour variation. Proc R Soc Lond B 276:2195–2208

    Article  CAS  Google Scholar 

  • van Oosterhout C et al (2006) Balancing selection, random genetic drift, and genetic variation at the major histocompatibility complex in two wild populations of guppies (Poecilia reticulata). Evolution 60:2562–2574

    Article  PubMed  Google Scholar 

  • van Oosterhout C et al (2007) Selection by parasites in spate conditions in wild Trinidadian guppies (Poecilia reticulata). Int J Parasitol 37:805–812

    Article  PubMed  Google Scholar 

  • van Oosterhout C, Potter R, Wright H, Cable J (2008) Gyro-scope: an individual-based computer model to forecast gyrodactylid infections on fish hosts. Int J Parasitol 38:541–548

    Article  PubMed  Google Scholar 

  • Vergara P, Martinez-Padilla J, Redpath SM, Mougeot F (2011) The ornament-condition relationship varies with parasite abundance at population level in a female bird. Naturwissenschaften 98:897–902

    Article  PubMed  CAS  Google Scholar 

  • Weese DJ, Gordon SP, Hendry AP, Kinnison MT (2010) Spatiotemporal variation in linear natural selection on body color in wild guppies (Poecilia reticulata). Evolution 64:1802–1815

    Article  PubMed  Google Scholar 

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Acknowledgments

Fieldwork was aided by Shahin Muttalib, Lyndsey Baillie, and Ian Paterson. Photoshop analysis was performed by Cameron Mojarrad. Special thanks to Indar Ramnarine for field support and Mauricio Torres for producing Online Resource 1. We sincerely thank three anonymous reviewers and David J. Marcogliese for their comments which greatly improved the manuscript. Funding for field work was provided by the Natural Sciences and Engineering Research Council of Canada (NSERC) in the form of a Special Research Opportunity Grant to G.F.F., M.E.S., P.B., and A.P.H.. NSERC also provided a Canada Graduate Scholarship—Masters and Vanier Canada Graduate Scholarship to K.M.G. J.A.M.R. was funded by the Research Foundation—Flanders and the University of Leuven, F.D. was funded by a Richard H. Tomlinson Fellowship, and F.P.J. was funded by the Consejo Nacional de Ciencia y Tecnología (Mexico). Research at the Institute of Parasitology is supported by a regroupement stratégique from Fonds Québecois pour la Recherche sur la Nature et les Technologies (FQRNT).

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Authors and Affiliations

  1. Department of Biology, McGill University, Montreal, QC, H3A 1B1, Canada

    Kiyoko M. Gotanda, Lari C. Delaire, Felipe Pérez-Jvostov, Felipe Dargent, Gregor F. Fussmann & Andrew P. Hendry

  2. Redpath Museum, McGill University, 859 Sherbrooke Street West, Montreal, QC, H3A 0C4, Canada

    Kiyoko M. Gotanda, Lari C. Delaire & Andrew P. Hendry

  3. Laboratory of Biodiversity and Evolutionary Genomics, Katholieke Universiteit Leuven, 3000, Leuven, Belgium

    Joost A. M. Raeymaekers

  4. Institute of Parasitology, Macdonald Campus of McGill University, Ste-Anne de Bellevue, QC, H9X 3V9, Canada

    Felipe Pérez-Jvostov & Marilyn E. Scott

  5. Department of Biology, Dalhousie University, Halifax, NS, B3H 4R2, Canada

    Paul Bentzen

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  1. Kiyoko M. Gotanda
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Correspondence to Kiyoko M. Gotanda.

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Communicated by David Marcogliese.

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Gotanda, K.M., Delaire, L.C., Raeymaekers, J.A.M. et al. Adding parasites to the guppy-predation story: insights from field surveys. Oecologia 172, 155–166 (2013). https://doi.org/10.1007/s00442-012-2485-7

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