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Reversed parasite-mediated selection in sticklebacks from eutrophied habitats

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Abstract

Sexual selection is often assumed to increase the viability of populations by increasing the quality of offspring produced. Presently, human-induced environmental changes are altering the process of sexual selection by influencing male–male interactions and female mate choice. Here, we show that increased density of filamentous algae due to eutrophication reverses parasite-mediated selection during reproduction in threespine sticklebacks (Gasterosteus aculeatus). When we manipulated the density of artificial algae in a breeding area in the Baltic Sea, more males nested in dense than in sparse vegetation, but the males in dense vegetation were more parasitized. Interestingly, heavily parasitized males acquired more eggs than less parasitized males in dense vegetation but not in sparse vegetation. The higher probability of reproduction for parasitized males in dense algae growth could be due to impaired visibility relaxing male–male competition or reducing female choosiness. This could favour males in poor condition that often invest more in attracting females than males in good condition. In sparse vegetation, parasitized males may have a lower reproductive success due to intense male–male competition, careful female choice and high predation rate selecting against parasitized males. The results suggest that eutrophication could alter the fraction of the population that reproduces, which could have long-term evolutionary consequences.

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References

  • Andersson M (1994) Sexual selection. Princeton University Press, Princeton

    Google Scholar 

  • Axenrot T, Hansson S (2004) Seasonal dynamics in pelagic fish abundance in a Baltic Sea coastal area. Estuar Coast Shelf Sci 60:541–547

    Article  Google Scholar 

  • Barber I, Ruxton G (1998) Temporal prey distribution affects the competitive ability of parasitized sticklebacks. Anim Behav 56:1477–1483

    Article  PubMed  Google Scholar 

  • Bates D (2007) lme4: linear mixed-effects models using S4 classes (version R package version 0.99875-9)

  • Blais J, Rico C, Bernatchez L (2004) Nonlinear effects of female mate choice in wild threespine sticklebacks. Evolution 58:2498–2510

    PubMed  Google Scholar 

  • Bush A, Lafferty K, Lotz J, Shostak A (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. J Parasitol 83:575–583

    Article  CAS  PubMed  Google Scholar 

  • Candolin U (1999) The relationship between signal quality and physical condition: is sexual signalling honest in the three-spined stickleback? Anim Behav 58:1261–1267

    Article  PubMed  Google Scholar 

  • Candolin U (2000a) Changes in expression and honesty of sexual signalling over the reproductive lifetime of sticklebacks. Proc R Soc Lond B Biol Sci 267:2425–2430

    Article  CAS  Google Scholar 

  • Candolin U (2000b) Increased signalling effort when survival prospects decrease: male–male competition ensures honesty. Anim Behav 60:417–422

    Article  PubMed  Google Scholar 

  • Candolin U (2000c) Male-male competition ensures honest signaling of male parental ability in the three-spined stickleback (Gasterosteus aculeatus). Behav Ecol Sociobiol 49:57–61

    Article  Google Scholar 

  • Candolin U (2004) Effects of algae cover on egg acquisition in male three-spined stickleback. Behaviour 141:1389–1399

    Article  Google Scholar 

  • Candolin U, Heuschele J (2008) Is sexual selection beneficial during adaptation to environmental change? Trends Ecol Evol 23:446–452

    Article  PubMed  Google Scholar 

  • Candolin U, Salesto T (2006) Effects of increased vegetation cover on nesting behavior of sticklebacks (Gasterosteus aculeatus). Behav Ecol Sociobiol 59:689–693

    Article  Google Scholar 

  • Candolin U, Voigt H-R (2001a) Correlation between male size and territory quality: consequence of male competition or predation susceptibility? Oikos 95:225–230

    Article  Google Scholar 

  • Candolin U, Voigt H-R (2001b) No effect of a parasite on reproduction in stickleback males: a laboratory artefact? Parasitology 122:457–464

    Article  CAS  PubMed  Google Scholar 

  • Candolin U, Voigt H-R (2003) Size-dependent selection on arrival times in sticklebacks: why small males arrive first. Evolution 57:862–871

    PubMed  Google Scholar 

  • Candolin U, Salesto T, Evers M (2007) Changed environmental conditions weaken sexual selection in sticklebacks. J Evol Biol 20:233–239

    Article  CAS  PubMed  Google Scholar 

  • Candolin U, Engström-Öst J, Salesto T (2008) Human-induced eutrophication enhances reproductive success through effects on parenting ability in sticklebacks. Oikos 117:459–465

    Article  Google Scholar 

  • Chappell LH, Hardie LJ, Secombes CJ (1994) Diplostomiasis: the disease and host–parasite interactions. In: Pike AW, Lewis JW (eds) Parasitic diseases of fish. Samara Publishing Limited, Dyfed

    Google Scholar 

  • Chellappa S, Huntingford FA, Strang RHC, Thomson RY (1989) Annual variation in energy reserves in male three-spined stickleback, Gasterosteus aculeatus L. (Pisces, Gasterosteidae). J Fish Biol 35:275–286

    Article  Google Scholar 

  • Ehman KD, Scott ME (2002) Female mice mate preferences with non-parasitized males. Parasitology 124:461–466

    Google Scholar 

  • Emlen S, Oring L (1977) Ecology, sexual selection, and the evolution of mating systems. Science 197:215–223

    Article  CAS  PubMed  Google Scholar 

  • Engström-Öst J, Candolin U (2007) Human-induced water turbidity alters selection on sexual displays in sticklebacks. Behav Ecol 18:393–398

    Article  Google Scholar 

  • Estes J, Duggins D (1995) Sea otters and kelp forests in Alaska—generality and variation in a community ecological paradigm. Ecol Monogr 65:75–100

    Article  Google Scholar 

  • Foster SA, Garcia VB, Town MY (1988) Cannibalism as the cause of an ontogenetic shift in habitat use by fry of the threespine stickleback. Oecologia 74:577–585

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Halpern B, Walbridge S, Selkoe K, Kappel C (2008) A global map of human impact on marine ecosystems. Science 319:948–952

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Hammerschmidt K, Kurtz J (2005) Surface carbohydrate composition of a tapeworm in its consecutive intermediate hosts: individual variation and fitness consequences. Int J Parasitol 35:1499–1507

    Article  CAS  PubMed  Google Scholar 

  • Hammerschmidt K, Kurtz J (2009) Ecological immunology of a tapeworms' interaction with its two consecutive hosts. In: Webster JP (ed) Natural history of host-parasite interactions, 1st edn. Academic, London, pp 111–137

    Google Scholar 

  • Heuschele J, Candolin U (2007) An increase in pH boosts olfactory communication in sticklebacks. Biol Lett 3:411–413

    Article  PubMed  Google Scholar 

  • Järvenpää M, Lindström K (2004) Water turbidity by algal blooms causes mating system breakdown in a shallow-water fish, the sand goby Pomatoschistus minutus. Proc R Soc Lond B Biol Sci 271:2361–2365

    Article  Google Scholar 

  • Kokko H, Rankin D (2006) Lonely hearts or sex in the city? Density-dependent effects in mating systems. Proc R Soc Lond B Biol Sci 361:319–334

    Article  Google Scholar 

  • Kraak SBM, Bakker TCM, Mundwiler B (1999) Sexual selection in sticklebacks in the field: correlates of reproductive, mating, and paternal success. Behav Ecol 10:696–706

    Article  Google Scholar 

  • Kraak SBM, Bakker TCM, Hovecar S (2000) Stickleback males, especially large and red ones, are more likely to nest concealed in macrophytes. Behaviour 137:907–919

    Article  Google Scholar 

  • Kynard BE (1978) Breeding behaviour of a lacustrine population of threespine sticklebacks (Gasterosteus aculeatus L.). Behaviour 67:178–206

    Article  Google Scholar 

  • Kynard B (1979) Nest habitat preference of low plate number morphs in threespine sticklebacks (Gasterosteus aculeatus). Copeia 3:525–528

    Article  Google Scholar 

  • Lehvo A, Bäck S (2001) Survey of macroalgal mats in the Gulf of Finland, Baltic Sea. Aquat Conserv: Mar Freshwat Ecosyst 11:11–18

    Article  Google Scholar 

  • Milinski M (1985) Risk of predation of parasitized sticklebacks (Gasterosteus aculeatus L.) under competition for food. Behaviour 93:203–216

    Article  Google Scholar 

  • Milinski M, Bakker T (1990) Female sticklebacks use male coloration in mate choice and hence avoid parasitized males. Nature 344:330–333

    Article  Google Scholar 

  • Moodie GEE (1972) Morphology, life history and ecology of an unusual stickleback (Gasterosteus aculeatus) in the Queen Charlotte Islands, Canada. Can J Zool 50:721–732

    Article  Google Scholar 

  • Mori S (1993) The breeding system of the three-spined stickleback, Gasterosteus aculeatus (forma leiura) with reference to spatial and temporal patterns of nesting activity. Behaviour 126:97–124

    Article  Google Scholar 

  • Owen SF, Barber I, Hart PJB (1993) Low level infection by eye fluke, Diplostomum spp., affects the vision of three-spined sticklebacks, Gasterosteus aculeatus. J Fish Biol 42:803–806

    Article  Google Scholar 

  • Palumbi SR (2001) Humans as the world's greatest evolutionary force. Science 293:1786–1790

    Article  CAS  PubMed  Google Scholar 

  • Pinheiro J, Bates D, DebRoy S, Sarkar D, the R Core team (2007) nlme: linear and nonlinear mixed effects models. R package version 3.1-83

  • Poulin R, FitzGerald FG (1989) Risk of parasitism and microhabitat selection in juvenile sticklebacks. Can J Zool 67:14–18

    Article  Google Scholar 

  • Poulin R, Vickery WL (1993) Parasite distribution and virulence: implications for parasite-mediated sexual selection. Behav Ecol Sociobiol 33:429–436

    Article  Google Scholar 

  • R Development Core Team (2009) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, http://www.R-project.org. ISBN 3-900051-07-0

    Google Scholar 

  • Rantala MJ, Jokinen I, Kortet R, Vainikka A, Suhonen J (2002) Do pheromones reveal male immuncompetence? Proc R Soc Lond B Biol Sci 269:1681–1685

    Article  Google Scholar 

  • Real L (1990) Search theory and mate choice 1. Models of single-sex discrimination. Am Nat 136:376–405

    Article  Google Scholar 

  • Ricker WE (1975) Computation and interpretation of biological statistics of fish populations. Bull Fish Res Board Can 191:1–382

    Google Scholar 

  • Rowland WJ (1989) The effects of body size, aggression and nuptial coloration on competition for territories in male threespine sticklebacks, Gasterosteus aculeatus. Anim Behav 132:282–289

    Article  Google Scholar 

  • Sargent RC (1982) Territory quality, male quality, courtship intrusions, and female nestchoice in the threespine stickleback, Gasterosteus aculeatus. Anim Behav 30:364–374

    Article  Google Scholar 

  • Sargent RC, Gebler JB (1980) Effects of nest site concealment on hatching success, reproductive successs, and paternal behaviour of the threespine stickleback, Gasterosteus aculeatus. Behav Ecol Sociobiol 7:137–142

    Article  Google Scholar 

  • Seehausen O, Alphen J, Witte F (1997) Cichlid fish diversity threatened by eutrophication that curbs sexual selection. Science 277:1808–1811

    Article  CAS  Google Scholar 

  • Seppälä O, Karvonen A, Valtonen ET (2004) Parasite-induced change in host behaviour and susceptibility to predation in an eye fluke–fish interaction. Anim Behav 68:257–263

    Article  Google Scholar 

  • Shuster SM, Wade MJ (2003) Mating systems and strategies. Princeton University Press, Princeton

    Google Scholar 

  • Smith V (2003) Eutrophication of freshwater and coastal marine ecosystems—a global problem. Environ sci pollut Res Int 10:126–139

    Article  CAS  PubMed  Google Scholar 

  • Wall T, Bjerkås E (1999) A simplified method of scoring cataracts in fish. Bull Eur Assoc Fish Pathol 19:162–165

    Google Scholar 

  • Wong B, Candolin U, Lindström K (2007) Environmental deterioration compromises socially enforced signals of male quality in three-spined sticklebacks. Am Nat 170:184–189

    Article  PubMed  Google Scholar 

  • Wootton RJ (1984) A functional biology of sticklebacks. Croom Helm, London

    Google Scholar 

  • Worden BD, Parker PG, Pappas PW (2000) Parasites reduce attractiveness and reproductive success in grain beetles. Anim Behav 59:543–550

    Article  PubMed  Google Scholar 

  • Zander CD, Reimer LW, Barz K (1999) Parasite communities of the Salzhaff (Northwest Mecklenburg, Baltic Sea). I. Structure and dynamics of communities of littoral fish, especially small-sized fish. Parasitol Res 85:356–372

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We thank U. Tuomainen, B. Diaz Pauli and S. Greger for help in the field; B. Diaz Pauli and J. Zuckerman for producing artificial algae; M. Kalbe, C.D. Zander, C. Eizaguirre and especially P. Jacobsen for advice on the parasitological investigation; B. Wong, J.W. Boughman and two anonymous reviewers for helpful comments on the manuscript. P. Gienapp kindly helped with parts of the statistical analysis. The work was funded by the Academy of Finland (to UC) and conducted at Tvärminne Zoological Station.

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Correspondence to Jan Heuschele.

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Communicated by K. Lindström

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Heuschele, J., Candolin, U. Reversed parasite-mediated selection in sticklebacks from eutrophied habitats. Behav Ecol Sociobiol 64, 1229–1237 (2010). https://doi.org/10.1007/s00265-010-0937-9

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  • DOI: https://doi.org/10.1007/s00265-010-0937-9

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