Skip to main content
SpringerLink
Log in

A field test of the Hamilton–Zuk hypothesis in the Trinidadian guppy (Poecilia reticulata)

  • Original Paper
  • Published:
Behavioral Ecology and Sociobiology Aims and scope Submit manuscript

Abstract

The Hamilton–Zuk hypothesis proposes that females prefer male secondary sexual traits because they are honest indicators of parasite resistance. Despite the attention that this hypothesis has received, its role in sexual selection remains equivocal. This study presents the first field test in guppies of two key predictions of the Hamilton–Zuk hypothesis: (1) that within populations, the most highly ornamented males have the fewest parasites and (2) that among populations, males in high parasite populations have the most conspicuous ornaments. Five hundred male guppies from 19 distinct populations in the Northern Range of Trinidad were inspected for Gyrodactylus parasites and photographed. Eight measures of orange spot ornamentation were used to test the predictions: hue, saturation, lightness, relative area, number, and area-weighted hue, saturation, and lightness. Parasite load had no significant effect on any of these measures. There was also no relationship between orange spot ornamentation and parasite abundance among populations. Guppies from high-predation environments had significantly more parasites, and their orange coloration was lighter and less saturated than that in guppies from low-predation environments. Despite previous lab results, this study found no relationship between parasite load and male orange spot ornamentation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Basolo AL (1990) Female preference predates the evolution of the sword in swordtail fish. Science 250:808–810

    Article  PubMed  Google Scholar 

  • Brooks R, Endler JA (2001) Direct and indirect sexual selection and quantitative genetics of male traits in guppies (Poecilia reticulata). Evolution 55:1002–1015

    Article  PubMed  CAS  Google Scholar 

  • Cohen J (1988) Statistical power analysis for the behavioral sciences. Lawrence Erlbaum, Hilldale

    Google Scholar 

  • Darwin C (1871) The descent of man, and selection in relation to sex. Appleton, London

    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 (1983) Natural and sexual selection on color patterns in poeciliid fishes. Environ Biol Fishes 9:173–190

    Article  Google Scholar 

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

    Article  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 

  • Endler JA, Lyles AM (1989) Bright ideas about parasites. Trends Ecol Evol 4:246–248

    Article  Google Scholar 

  • Faul F, Erdfelder E, Lang A-G, Buchner A (2007) G*Power 3: a flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behav Res Meth (in press)

  • Fisher RA (1930) The genetical theory of natural selection. Clarendon, Oxford

    Google Scholar 

  • Folstad I, Karter AJ (1992) Parasites, bright males, and the immunocompetence handicap. Am Nat 139:603–622

    Article  Google Scholar 

  • Getty T (2002) Signaling health versus parasites. Am Nat 159:363–371

    Article  PubMed  Google Scholar 

  • Goodwin TW (1984) The biochemistry of the carotenoids. Chapman & Hall, London

    Google Scholar 

  • Grether GF (2000) Carotenoid limitation and mate preference evolution: a test of the indicator hypothesis in guppies (Poecilia reticulata) Evolution 54:1712–1724

    PubMed  CAS  Google Scholar 

  • Grether GF, Hudon J, Endler JA (2001) Carotenoid scarcity, synthetic pteridine pigments and the evolution of sexual coloration in guppies (Poecilia reticulata). Proc R Soc Lond B 268:1245–1253

    Article  CAS  Google Scholar 

  • Grether GF, Kasahara S, Kolluru GR, Cooper EL (2003) Sex-specific effects of carotenoid intake on the immunological response to allografts in guppies (Poecilia reticulata). Proc R Soc Lond B 271:45–49

    Article  CAS  Google Scholar 

  • Grether GF, Kolluru GR, Rodd FH, Cerda J, Shimazaki K (2005) Carotenoid availability affects the development of a colour-based mate preference and the sensory bias to which it is genetically linked. Proc R Soc Lond B 272:2181–2188

    Article  Google Scholar 

  • Godin JGJ, Briggs SE (1996) Female mate choice under predation risk in the guppy. Anim Behav 51:117–130

    Article  Google Scholar 

  • Hamilton WJ, Poulin R (1997) The Hamilton and Zuk hypothesis revisited: a meta-analytical approach. Behaviour 134:299–320

    Google Scholar 

  • Hamilton WD, Zuk M (1982) Heritable true fitness and bright birds: a role for parasites? Science 218:384–387

    Article  PubMed  CAS  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 

  • 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 

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

    Article  Google Scholar 

  • Karino K, Haijima Y (2004) Algal-diet enhances sexual ornament, growth and reproduction in the guppy. Behaviour 141:585–601

    Article  Google Scholar 

  • Karino K, Shinjo S (2004) Female mate preference based on male orange spot patterns in the feral guppy Poecilia reticulata in Japan. Ichthyol Res 51:316–320

    Article  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 

  • 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 

  • Kodric-Brown A, Brown JH (1984) Truth in advertising: the kinds of traits favored by sexual selection. Am Nat 124:305–322

    Google Scholar 

  • Kodric-Brown A, Nicoletto PF (2001) Female choice in the guppy (Poecilia reticulata): the interaction between male color and display. Behav Ecol Sociobiol 50:346–351

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Luyten PH, Liley NR (1985) Geographic variation in the sexual behaviour of the guppy, Poecilia reticulata (Peters). Behaviour 95:164–179

    Google Scholar 

  • Luyten PH, Liley NR (1991) Sexual selection and competitive mating success of male guppies (Poecilia reticulata) from four Trinidad populations. Behav Ecol Sociobiol 28:329–336

    Article  Google Scholar 

  • Lyles AM (1990) Genetic variation and susceptibility to parasites: Poecilia reticulata infected with Gyrodactylus turnbulli. Ph.D. Thesis, Princeton University, New Jersey

  • Magurran AE (1999) The causes and consequences of geographic variation in antipredator behavior: perspectives from fish populations. In: Foster SA, Endler JA (eds) Geographic variation in behavior: perspectives on evolutionary mechanisms. Oxford University Press, Oxford, pp 139–163

    Google Scholar 

  • Maynard Smith J (1978) The evolution of sex. Cambridge University Press, London

    Google Scholar 

  • McLennan DA, Brooks DR (1991) Parasites and sexual selection: a macroevolutionary perspective. Q Rev Biol 66:255–286

    Article  PubMed  CAS  Google Scholar 

  • McMinn H (1990) Effects of the nematode parasite Camallanus cotti on sexual and non-sexual behaviors in the guppy (Poecilia reticulata). Am Zool 30:245–249

    Google Scholar 

  • Møller AP (1990) Parasites and sexual selection: current status of the Hamilton and Zuk hypothesis. J Evol Biol 3:319–328

    Article  Google Scholar 

  • Møller AP, Christie P, Lux E (1999) Parasitism, host immune function, and sexual selection. Q Rev Biol 74:3–20

    Article  PubMed  Google Scholar 

  • Nicoletto PF (1993) Females respond to condition-dependent ornaments in the guppy, Poecilia reticulata Anim Behav 46:441–450

    Article  Google Scholar 

  • Oosterhout CV, Harris PD, Cable J (2003) Marked variation in parasite resistance between two wild populations of the Trinidadian guppy, Poecilia reticulata. Biol J Linn Soc 79:645–651

    Article  Google Scholar 

  • Pomiankowski A (1987) The costs of choice in sexual selection. J Theor Biol 128:195–218

    Article  PubMed  CAS  Google Scholar 

  • Read AF (1990) Parasites and the evolution of host sexual behavior. In: Barnard CJ, Harvey PH (eds) Parasitism and host behaviour. Taylor and Francis, London, pp 117–157

    Google Scholar 

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

    Article  Google Scholar 

  • Reznick DN, Shaw FH, Rodd FH, Shaw RG (1997) Evaluation of the rate of evolution in natural populations of guppies (Poecilia reticulata). Science 275:1934–1937

    Article  PubMed  CAS  Google Scholar 

  • Rodd HF, Hughes KA, Grether GF (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 

  • Ryan MJ (1990) Sexual selection, sensory systems, and sensory exploitation. Oxf Surv Evol Biol 7:157–195

    Google Scholar 

  • Schall JJ, Staats CM (1997) Parasites and the evolution of extravagant male characters: Anolis lizards on Caribbean islands as a test of the Hamilton–Zuk hypothesis. Oecologia 111:543–548

    Article  Google Scholar 

  • Scott ME, Anderson RM (1984) The population dynamics of Gyrodactylus bullatarudis (Monogenea) within laboratory populations of the fish host Poecilia reticulata. Parasitology 90:159–194

    Article  Google Scholar 

  • Thomas L (1997) Retrospective power analysis. Conserv Biol 11:276–280

    Article  Google Scholar 

  • Trivers RL (1972) Parental investment and sexual selection. In: Campbell (ed) Sexual selection and the descent of man. Aldine, Chicago, pp 1871–1971

    Google Scholar 

Download references

Acknowledgements

O. Lau and R. Hernandez provided excellent support with fieldwork in Trinidad. K. Hughes, G. Grether, and H. Rodd gave advice on project design and logistics. S. Alberts, M. Cummings, K. Hughes, H. Rodd, W. Morris, T. Getty, and one anonymous reviewer offered valuable criticism of the manuscript. K. Hughes, W. Morris, M. Lavine, D. Stangl, and G. Puggioni were consulted on statistical analyses. The Simla Research Station run by the ASA Wright Nature Center provided accommodation in Trinidad. Trinidad’s Water and Sewage Authority generously allowed work in the Quare drainage. This work was funded by a Summer Enrichment Grant from the Duke University Scholars Program, a Latin American Studies Grant from the Mellon Foundation, a Deans’ Summer Fellowship, and the Undergraduate Research Support Program, all at Duke University. SJ was supported in part by a grant from the National Science Foundation (IOB-0444674). All protocols used in this study were approved by the Duke Institutional Animal Care and Use Committee (registry #A078-04-03) and comply with the current laws of Trinidad and Tobago.

Author information

Authors and Affiliations

  1. Biology Department, Duke University, Box 90338, Durham, NC, USA

    Christopher H. Martin & Sönke Johnsen

Authors
  1. Christopher H. Martin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sönke Johnsen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sönke Johnsen.

Additional information

Communicated by C. St. Mary

Appendix

Appendix

Table 4 Data for populations sampled
Full size table

Rights and permissions

Reprints and permissions

About this article

Cite this article

Martin, C.H., Johnsen, S. A field test of the Hamilton–Zuk hypothesis in the Trinidadian guppy (Poecilia reticulata). Behav Ecol Sociobiol 61, 1897–1909 (2007). https://doi.org/10.1007/s00265-007-0430-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00265-007-0430-2

Keywords

Search

Navigation