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Infestation with the parasitic nematode Philometra ovata does not impair behavioral sexual competitiveness or odor attractiveness of the male European minnow (Phoxinus phoxinus)

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Abstract

Our understanding on the role of chemical signals in parasite-mediated sexual selection is still limited, and only some existing studies have focused on fish. Furthermore, published studies on the effect of parasite infection on behavioral sexual competition of the male hosts have yielded contradictory results. Here, we examined whether the infection of the body cavity-dwelling parasitic nematode Philometra ovata influences odor-based female choice and behavioral sexual competition (dominance and courtship behavior) between males in the European minnow (Phoxinus phoxinus), the cyprinid fish host. In contrast to our predictions, we found that naïve females showed no preference between the odors of infected and non-infected males, thus indicating that P. ovata infection may not affect odor-based female choice. Moreover, P. ovata did not impair sexual competitiveness of their hosts either. Our results indicate that despite its relatively large size, P. ovata may not alter sexual cues and the success of the male hosts in sexual selection.

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References

  • Able DJ (1996) The contagion indicator for parasite-mediated sexual selection. Proc Natl Acad Sci U S A 93:2229–2233

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Google Scholar 

  • Bagamian KH, Heins DC, Baker JA (2004) Body condition and reproductive capacity of three-spined stickleback infected with the cestode Schistocephalus solidus. J Fish Biol 64:1568–1576

    Article  Google Scholar 

  • Barber I (2002) Parasite, male-male competition and female mate choice in sand goby. J Fish Biol 21:185–198

    Google Scholar 

  • Barber I, Wright HA (2001) How strong are familiarity preferences in shoaling fish? Anim Behav 61:975–979

    Article  Google Scholar 

  • 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 

  • Barber I, Walker P, Svensson PA (2004) Behavioural responses to simulated avian predation in female three spined sticklebacks: the effect of experimental Schistocephalus solidus infections. Behaviour 141:1425–1440

    Article  Google Scholar 

  • Beltran-Bech S, Richard FJ (2014) Impact of infection on mate choice. Anim Behav 90:159–170

    Article  Google Scholar 

  • Berdoy M, Webster JP, MacDonald DW (1995) Parasite-altered behaviour: is the effect of Toxoplasma gondii on Rattus norvegicus specific? Parasitology 111:403–409

    Article  PubMed  Google Scholar 

  • Bull CM, Burzacott D (1993) The impact of tick load on the fitness of their lizard hosts. Oecologia 96:415–419

    Article  Google Scholar 

  • Candolin U (2003) The use of multiple cues in mate choice. Biol Rev 78:575–595

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Clayton DH (1991) The influence of parasites on host sexual selection. Parasitol Today 7:329–334

    Article  CAS  PubMed  Google Scholar 

  • Dass SAH, Vasudevan A, Dutta D, Soh LJT, Sapolsky RM, Vyas A (2011) Protozoan parasite Toxoplasma gondii manipulates mate choice in rats by enhancing attractiveness of males. PLoS ONE 6:e27229

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Doutrelant C, McGregor PK, Oliveira RF (2001) The effect of an audience on intrasexual communication in male Siamese fighting fish, Betta splendens. Behav Ecol 12:283–286

    Article  Google Scholar 

  • Eilertsen EM, Bårdsen BJ, Liljedal S, Rudolfsen G, Folstad I (2009) Experimental evidence for paternal effects on offspring growth rate in Arctic charr (Salvelinus alpinus). Proc R Soc Lond B 276:129–136

    Article  Google Scholar 

  • Erickson DL, Hightower JE, Grossman GD (1985) The relative gonadal index: an alternative index for quantification of reproductive condition. Comp Biochem Physiol A 18:117–120

    Article  Google Scholar 

  • Evans JP, Kelley JL, Bisazza A, Finazzo E, Pilastro A (2004) Sire attractiveness influences offspring performance in guppies. Proc R Soc Lond B 271:2035–2042

    Article  Google Scholar 

  • Folstad I, Hope AM, Karter A, Skorping A (1994) Sexually selected colour in male stickleback—a signal of both parasite exposure and parasite resistance. Oikos 69:511–515

    Article  Google Scholar 

  • Gil D, Gahr M (2002) The honesty of bird song: multiple constraints for multiple traits. Trends Ecol Evol 17:133–141

    Article  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

    Article  CAS  PubMed  Google Scholar 

  • Hadidi S, Glenney GW, Welch TJ, Silverstein JT, Wiens GD (2008) Spleen size predicts resistance of rainbow trout to Flavobacterium psychrophilum challenge. J Immunol 180:4156–4165

    Article  CAS  PubMed  Google Scholar 

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

  • Hamilton WJ, Poulin R (1995) Parasite, aggression and dominance in male upland bullies. J Fish Biol 47:302–307

    Article  Google Scholar 

  • Havlicek J, Roberts SC (2009) MHC-correlated mate choice in humans: a review. Psychoneuroendocrinology 34:497–512

    Article  CAS  PubMed  Google Scholar 

  • Jacob A, Evanno G, Renai E, Sermier R, Wedekind C (2009) Male body size and breeding tubercles are both linked to intrasexual dominance and reproductive success in the minnow. Anim Behav 77:823–829

    Article  Google Scholar 

  • Johnsson JI, Sundström LF (2007) Social transfer of predation risk information reduces food locating ability in European minnows. Ethology 113:166–173

    Article  Google Scholar 

  • Kasuyan AO, Sidorov SS (2002) Individual variability of taste preferences in the minnow Phoxinus phoxinus. J Ichthyol 42:241–254

    Google Scholar 

  • Kavaliers M, Colwell DD, Braun WJ, Choleris E (2003) Brief exposure to the odour of a parasitized male alters the subsequent mate odour responses of female mice. Anim Behav 65:59–68

    Article  Google Scholar 

  • Kekäläinen J, Valkama H, Huuskonen H, Taskinen J (2010) Multiple sexual ornamentation signals male quality and predicts female preference in minnows. Ethology 116:895–903

    Article  Google Scholar 

  • Kekäläinen J, Leppänen HR, Huuskonen H, Lai Y-T, Valkama H, Taskinen J (2011) The information content of odour, colour and tactile cues in the mate choice of minnows. Behaviour 148:909–925

    Article  Google Scholar 

  • Klein SL (2003) Parasite manipulation of the proximate mechanisms that mediate social behavior in vertebrates. Physiol Behav 79:441–449

    Article  CAS  PubMed  Google Scholar 

  • Kortet R, Taskinen J (2004) Parasitism, condition and number of front head breeding tubercles in roach (Rutilus rutilus L.). Ecol Freshw Fish 13:119–124

    Article  Google Scholar 

  • Kortet R, Vainikka A, Rantala MJ, Myntti J, Taskinen J (2004a) In vitro embryo survival and early viability of larvae in relation to male sexual ornaments and parasite resistance in roach, Rutilus rutilus L. J Evol Biol 17:1337–1344

    Article  PubMed  Google Scholar 

  • Kortet R, Taskinen J, Vainikka A, Ylönen H (2004b) Breeding tubercles, papillomatosis and dominance behaviour of male roach (Rutilus rutilus) during the spawning period. Ethology 110:591–601

    Article  Google Scholar 

  • Lai Y-T, Taskinen J, Kekäläinen J, Kortet R (2012) Non-invasive diagnosis for Philometra ovata (Nematoda) infection in the common minnow Phoxinus phoxinus. Parasitol Res 111:2411–2418

    Article  PubMed  Google Scholar 

  • Lai Y-T, Kekäläinen J, Kortet R (2013) Male ornamentation in the European minnow (Phoxinus phoxinus) signals swimming performance. Ethology 119:1077–1085

    Article  Google Scholar 

  • Lai Y-T, Taskinen J, Kekäläinen J, Kortet R (2015) Infection ecology of Philometra ovata (Nematoda:Philometridae) in a wild European minnow (Phoxinus phoxinus) population in Finland. Parasitology 142:926–937

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Magurran AE (1989) Acquired recognition of predator odour in the European minnow (Phoxinus phoxinus). Ethology 82:216–223

    Article  Google Scholar 

  • Maksimowich DS, Mathis A (2000) Parasitized salamanders are inferior competitors for territories and food resources. Ethology 106:319–329

    Article  Google Scholar 

  • Médoc V, Beisel JN (2010) When trophically transmitted parasites combine predation enhancement with predation suppression to optimize their transmission. Oikos 120:1452–1458

    Article  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 (1994) Male ornament size as a reliable cue to enhanced offspring viability in the swallow. Proc Natl Acad Sci U S A 91:6929–6932

    Article  PubMed  PubMed Central  Google Scholar 

  • Møller AP, Alatalo RV (1999) Good-genes effects in sexual selection. Proc R Soc Lond B 266:85–91

    Article  Google Scholar 

  • Møller AP, Saino N (1994) Parasites, immunology of hosts, and host sexual selection. J Parasitol 80:850–858

  • Molnár K (1966) Life-history of Philometra ovata (Zeder, 1803) and Ph. rischta Skrjaben, 1917. Acta Vet Acad Sci Hung 16:227–242

    PubMed  Google Scholar 

  • Moore J (2002) Parasites and behavior of animals. Oxford University Press, Oxford

    Google Scholar 

  • Moravec F (1977) The life history of the nematode Philometra abdominalis in the Rokytka Brook, Czechoslovakia. Acta Soc Zool Bohemoslov 41:114–120

    Google Scholar 

  • Moravec F (2006) Dracunculoid and anguillicoloid nematodes parasitic in vertebrates. Academia, Prague

    Google Scholar 

  • Müller G, Ward PI (1995) Parasitism and heterozygosity influence the secondary sexual characters of the European minnow, Phoxinus phoxinus (L.) (Cyprinidae). Ethology 100:309–319

    Article  Google Scholar 

  • Pelabon C, Borg AA, Bjelvenmark J, Barber I, Forsgren E, Amundsen T (2005) Do microsporidian parasites affect courtship in two-spotted gobies? Mar Biol 148:189–196

    Article  Google Scholar 

  • Penn D (2002) The scent of genetic compatibility: sexual selection and the major histocompatibility complex. Ethology 108:1–21

    Article  Google Scholar 

  • Penn D, Potts WK (1998a) Chemical signals and parasite-mediated sexual selection. Trends Ecol Evol 13:391–396

    Article  CAS  PubMed  Google Scholar 

  • Penn D, Potts WK (1998b) How do major histocompatibility complex genes influence odor and mating preferences? Adv Immunol 69:411–436

    Article  CAS  PubMed  Google Scholar 

  • Rantala MJ, Kortet R (2003) Courtship song and immune function in the field cricket Gryllus bimaculatus. Biol J Linn Soc 79:503–510

    Article  Google Scholar 

  • Rantala MJ, Vainikka A, Kortet R (2003) The role of juvenile hormone in immune function and pheromone production trade-offs: a test of the immunocompetence handicap principle. Proc R Soc Lond B 270:2257–2261

    Article  CAS  Google Scholar 

  • Reusch TBH, Häberli MA, Aeschlimann PB, Milinski M (2001) Female sticklebacks count alleles in a strategy of sexual selection explaining MHC polymorphism. Nature 414:300–302

    Article  CAS  PubMed  Google Scholar 

  • Rowe L, Houle D (1996) The lek paradox and the capture of genetic variance by condition dependent traits. Proc R Soc Lond B 263:1415–1421

    Article  Google Scholar 

  • Saraiva A, Hermida M, Costa MJ, Maia C, Reis AR, Cruz C, Valente A (2008) First record of Philometra ovata (Nematoda) infection in Gobio lozanoi in Portugal. J Fish Biol 73:2288–2292

    Article  Google Scholar 

  • Schall JJ, Dearing MD (1987) Malarial parasitism and male competition for mates in the western fence lizards, Sceloporus occidentalis. Oecologia 73:389–392

    Article  Google Scholar 

  • Sprengel G, Lüchtenberg H (1991) Infection by endoparasites reduces maximum swimming speed of European smelt Osmerus eperlanus and European eel Anguilla anguilla. Dis Aquat Org 11:31–35

    Article  Google Scholar 

  • Thomas F, Lambert A, De Meeüs T, Renaud F, Cézilly F (1995) Influence of Microphallus hoffmanni (Trematoda, Microphallidae) on the survival, sexual selection, and fecundity of Gammarus aequicauda (Amphipoda). Can J Zool 73:1634–1639

    Article  Google Scholar 

  • Umberger CM, De Buron I, Roumillat WA, McElroy EJ (2013) Effects of a muscle-infecting parasitic nematode on the locomotor performance of their fish host. J Fish Biol 82:1250–1258

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Zahavi A (1975) Mate selection: a selection for a handicap. J Theor Biol 53:205–214

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Elli Jelkänen, Ilkka Sirkka, Matti Heep, and Minttu Kivi for their help in the field and lab. We also thank Jouni Taskinen and Antti Oksanen for the inspiring discussions. We also thank the referees for their constructive comments in improving our manuscript. This study was financially supported by Emil Aaltonen Foundation (Y-T.L., grant number 6-15079-13), North Carelia regional fund of Finnish Cultural Foundation (Y-T.L., grant numbers 77138–15725 and 94513–13416), and Kone foundation through Finnish Post-Doc Pool (J.K.).

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Authors and Affiliations

  1. Department of Biology, University of Eastern Finland, P.O. Box 111, FI-80101, Joensuu, Finland

    Yi-Te Lai, Jukka Kekäläinen & Raine Kortet

  2. Centre for Evolutionary Biology, The University of Western Australia, 35 Stirling Hwy, Crawley, WA, 6009, Australia

    Jukka Kekäläinen

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  1. Yi-Te Lai
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Correspondence to Yi-Te Lai.

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Lai, YT., Kekäläinen, J. & Kortet, R. Infestation with the parasitic nematode Philometra ovata does not impair behavioral sexual competitiveness or odor attractiveness of the male European minnow (Phoxinus phoxinus). acta ethol 19, 103–111 (2016). https://doi.org/10.1007/s10211-015-0229-5

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