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Behavioral diversification in a young species flock of pupfish (Cyprionodon spp.): shoaling and aggressive behavior

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Abstract

Increasing empirical and theoretical evidence supports the idea that sympatric speciation is operating, for example, in species flocks comprising several closely related fish species within one lake. Divergent natural selection (promoting spatial and food niche partitioning) and sexual selection (assortative mating) have been identified as key selection factors in intralacustric adaptive radiations. However, the evolution of social behaviors accompanying such adaptive radiations is less well understood. Using a phylogenetically young species flock of pupfish (Cyprinodon spp.) as a model, we examined differences among six sympatric species and compared their shoaling, aggressive, and territorial behaviors with that of a sister species (C. artifrons). Despite an estimated age of the species flock of less than 8,000 years, pronounced behavioral differentiation was found. C. simus, the smallest species in the flock, shoaled more than the other species and was less aggressive and less territorial than C. beltrani. F1-hybrids between C. simus males and C. beltrani females showed an intermediate expression of shoaling and aggressive behavior. Niche partitioning among the members of this species flock appears to be accompanied by rapid divergent evolution of social behaviors. We discuss the potential role of phenotypic plasticity and within-species variation of social behaviors for such rapid behavioral diversifications in sympatric speciation processes.

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References

  • Alvarez J (1949) Una nueva especie de peces Cyprinodontiformes de la Laguna Chichancanab, Quintana Roo. Rev Soc Mex Hist Nat 10:235–240

    Google Scholar 

  • Arnegard ME, Kondrashov AS (2004) Sympatric speciation by sexual selection alone is unlikely. Evolution 58:222–237

    PubMed  Google Scholar 

  • Barlow GW (1961) Social behavior in the desert pupfish, Cyprinodon macularius, in the field and in the aquarium. Am Midl Nat 65:339–359

    Article  Google Scholar 

  • Barluenga M, Meyer A (2004) The Midas cichlid species complex: incipient sympatric speciation in Nicaraguan cichlid fishes? Mol Ecol 13:2061–2076

    Article  PubMed  CAS  Google Scholar 

  • Barluenga M, Stolting KN, Salzburger W, Muschick M, Meyer A (2006) Sympatric speciation in Nicaraguan crater lake cichlid fish. Nature 439:719–723

    Article  PubMed  CAS  Google Scholar 

  • Bell AM, Stamps JA (2004) Development of behavioural differences between individuals and populations of stickleback, Gasterosteus aculeatus. Anim Behav 68:1339–1348

    Article  Google Scholar 

  • Bouton N, Seehausen O, van Alphen JJM (1997) Resource partitioning among rock dwelling haplochromines (pisces: Cichlidae) from Lake Victoria. Ecol Freshw Fish 6:225–240

    Article  Google Scholar 

  • Brown C, Smith R (1996) Foraging trade-offs in fathead minnows (Pimephales promelas, Osteichthyes, Cyprinidae): acquired predator recognition in the absence of an alarm response. Ethology 102:776–785

    Article  Google Scholar 

  • Brown C, Jones F, Braithwaite VA (2005) In situ examination of boldness–shyness traits in the tropical poeciliid, Brachyraphis episcopi. Anim Behav 70:1003–1009

    Article  Google Scholar 

  • Brown C, Burgess F, Braithwaite VA (2007) Heritable and experimental effects on boldness in a tropical poeciliid. Behav Ecol Sociobiol 62:237–243

    Article  Google Scholar 

  • Couldridge VCK, Alexander GJ (2002) Color patterns and species recognition in four closely related species of Lake Malawi cichlid. Behav Ecol 13(1):59–64

    Article  Google Scholar 

  • Covich A, Stuiver M (1974) Changes in oxygen 18 as a measure of long-term fluctuations in tropical lake levels and molluscan populations. Limnol Ocean 19:682–691

    Google Scholar 

  • Diekmann U, Doebeli M (1999) On the origin of species by sympatric speciation. Nature 400:354–357

    Article  Google Scholar 

  • Doebeli M (1996) A quantitative genetic competition model for sympatric speciation. J Evol Biol 9:893–909

    Article  Google Scholar 

  • Dwyer M, Beuling A (1991) Social experience and the development of aggressive behavior in the pupfish (Cyprinodon variegatus). J Comp Psych 105:398–404

    Article  Google Scholar 

  • Echelle AA (1973) Behavior of the pupfish Cyprinodon rubrofluviatilis. Copeia 1973:68–76

    Article  Google Scholar 

  • Echelle AA, Carson EW, Echelle AF, Van den Busche RA, Dowling TE, Meyer A (2005) Historical biogeograohy of the New World pupfish genus Cyprinodon (Teleostei, Cyprinodontidae). Copeia 2005:220–239

    Article  Google Scholar 

  • Feulner PGD, Kirschbaum F, Schugardt C, Ketmaier V, Tiedemann R (2006) Electrophysiological and molecular genetic evidence for sympatrically occurring cryptic species in African weakly electric fishes (Teleostei: Mormyridae: Campylomormyrus). Mol Phylogenet Evol 39:198–208

    Article  PubMed  CAS  Google Scholar 

  • Feulner PGD, Kirschbaum F, Mamonekene V, Ketmaier V, Tiedemann R (2007) Adaptive radiation in African weakly electric fish (Teleostei: Mormyridae: Campylomormyrus): a combined molecular and morphological approach. J Evol Biol 20:403–414

    Article  PubMed  CAS  Google Scholar 

  • Fusilier L (2001) Impacts of Oreochromis mossambicus (Perciformes: Cichlidae) upon habitat segregation among cyprinidontids (Cyprinodontiformes) of a species flock in Mexico. Rev Biol Trop 49:647–656

    Google Scholar 

  • Godin J-GJ (1986) Antipredator function of shoaling in teleost fishes: a selective review. Naturaliste Can 113:241–250

    Google Scholar 

  • Greenwood PH (1981) The haplochromine species of East African Lakes. Cornell University Press, Ithaka, NY

    Google Scholar 

  • Greenwood PH (1984) What is a species flock? In: Echelle AA, Kornfield I (eds) Evolution of fish species flocks. University of Maine at Orono Press, Orono, pp 13–19

    Google Scholar 

  • Griffith SW, Maggurran AE (1997) Familiarity in schooling fish: how long does it take to acquire? Anim Behav 53:945–949

    Article  Google Scholar 

  • Herre AWT (1933) The fishes of Lake Lanao: a problem in evolution. Am Nat 67:154–162

    Article  Google Scholar 

  • Higashi M, Takimoto G, Yamamura N (1999) Sympatric speciation by sexual selection. Nature 402:523–526

    Article  PubMed  CAS  Google Scholar 

  • Hodell DA, Curtis JH, Brenner M (1995) Possible role of climate in the collapse of Classic Maya civilization. Nature 375:391–394

    Article  CAS  Google Scholar 

  • Hodell DA, Brenner M, Curtis JH, Guilderson T (2001) Solar forcing of drought frequency in the Maya lowlands. Science 292:1367–1370

    Article  PubMed  CAS  Google Scholar 

  • Horstkotte J, Strecker U (2005) Trophic differentiation in the phylogenetically young Cyprinodon species flock (Cyprinodontidae, Teleostei) from Laguna Chichancanab (Mexico). Biol J Linn Soc 85:125–134

    Article  Google Scholar 

  • Humphries JM, Miller RR (1981) A remarkable species flock of pupfishes, genus Cyprinodon, from Yucatan, Mexico. Copeia 1981:52–64

    Article  Google Scholar 

  • Humphries JM (1984a) Cyprinodon verecundus, n. sp., a fifth species of pupfish from Laguna Chichancanab. Copeia 1984:58–68

    Article  Google Scholar 

  • Humphries JM (1984b) Genetics of speciation in pupfishes from Laguna Chichancanab, Mexico. In: Echelle AA, Kornfield I (eds) Evolution of fish species flocks. University of Maine at Orono Press, Orono, pp 129–139

    Google Scholar 

  • Itzkowitz M (1977) Interrelationships of dominance and territorial behaviour in the pupfish, Cyprinodon variegatus. Behav Proc 2:383–391

    Article  Google Scholar 

  • Itzkowitz M (1979) Territorial tactics and habitat quality. Am Nat 114:585–590

    Article  Google Scholar 

  • Johnson TC, Scholz CA, Talbot MR, Kelts K, Ricketts RD, Ngobi G, Beuning K, Ssemmanda I, McGill JW (1996) Late Pleistocene desiccation of Lake Victoria and rapid evolution of cichlid fishes. Science 273:1091–1093

    Article  PubMed  CAS  Google Scholar 

  • Kodric-Brown A (1977) Reproductive success and the evolution of breeding territories in pupfish (Cyprinodon). Evolution 31:750–766

    Article  Google Scholar 

  • Kodric-Brown A (1978) Establishment and defence of breeding territories in a pupfish (Cyprinodontidae: Cyprinodon). Anim Behav 26:818–834

    Article  Google Scholar 

  • Kodric-Brown A (1981) Variable breeding systems in pupfishes (genus Cyprinodon): adaptations to changing environments. In: Nauman RJ, Soltz DL (eds) Fishes in North American deserts. Wiley, New York, pp 205–235

    Google Scholar 

  • Kodric-Brown A (1983) Determinants of male reproductive success in pupfish (Cyprinodon pecosensis). Anim Behav 31:128–137

    Article  Google Scholar 

  • Kodric-Brown A (1986) Satellites and sneakers: opportunistic male breeding tactics in pupfish (Cyprinodon pecosensis). Behav Ecol Sociobiol 19:425–432

    Article  Google Scholar 

  • Kodric-Brown A (1988) Effect of population density, size of habitat and oviposition substrate on the breeding system of pupfish (Cyprinodon pecosensis). Ethology 77:28–43

    Article  Google Scholar 

  • Kodric-Brown A, Strecker U (2001) Responses of Cyprinodon maya and C. labiosus females to visual and olfactory cues of conspecific and heterospecific males. Biol J Linn Soc 74:541–548

    Google Scholar 

  • Kondrashov AS, Kondrashov FA (1999) Interactions among quantitative traits in the course of sympatric speciation. Nature 400:351–354

    Article  PubMed  CAS  Google Scholar 

  • Kornfield I, Carpenter KE (1984) Cyprinids of Lake Lanao, Philippines: taxonomic validity, evolutionary rates and speciation scenarios. In: Echelle AA, Kornfield I (eds) Evolution of fish species flocks. University of Maine at Orono Press, Orono, pp 69–84

    Google Scholar 

  • Krause J, Ruxton GD (2002) Living in groups. Oxford University Press, Oxford

    Google Scholar 

  • Lauzanne L (1982) Les Orestias (Pisces, Cyprinodontidae) du Petit Lac Titicaca. Rev Hydrobiol Trop 15:39–70

    Google Scholar 

  • Lauzanne L (1992) The Orestias. VI.5 fish fauna, VI5a native species. In: Dejoux C, Iltis A (eds) Lake Titicaca. A synthesis of limnological knowledge. Monographiae biologiae 68. Kluwer, Leiden

    Google Scholar 

  • Lindström K, Ranta E (1993) Social preferences by male guppies, Poecilia reticulata, based on shoal size and sex. Anim Behav 46:1029–1031

    Article  Google Scholar 

  • Losos JB (2000) Ecological character displacement and the study of adaptation. Proc Natl Acad Sci USA 97:5693–5695

    Article  PubMed  CAS  Google Scholar 

  • McKaye KR (1980) Seasonality in habitat selection by the gold color morph of Cichlasoma citrinellum and its relevance to sympatric speciation in the family Cichlidae. Environ Biol Fish 5:75–78

    Article  Google Scholar 

  • McPhail JD (1984) Ecology and evolution of sympatric sticklebacks (Gasterosteus): Morphological and genetic evidence for a species pair at Enos Lake, British Columbia. Can J Zool 62:1402–1408

    Google Scholar 

  • McPhail JD (1992) Ecology and evolution of sympatric sticklebacks (Gasterosteus): evidence for a species-pair in Paxton Lake, Texas Island, British Columbia. Can J Zool 70:361–369

    Article  Google Scholar 

  • Magnhagen C (2006) Risk-taking behaviour in foraging young-of-the-year perch varies with population size structure. Oecologia 147:734–743

    Article  PubMed  Google Scholar 

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

    Google Scholar 

  • Magurran AE, Seghers BH (1991) Variation in schooling and aggression amongst guppy (Poecilia reticulata) populations in Trinidad. Behaviour 118:214–234

    Article  Google Scholar 

  • Magurran AE, Seghers BH, Carvalho GR, Shaw PW (1992) Behavioural consequences on an artificial introduction of guppies (Poecilia reticulata) in N. Trinidad: evidence for the evolution of antipredator behaviour in the wild. Proc R Soc Lond B 248:260–277

    Article  Google Scholar 

  • Maynard-Smith J (1966) Sympatric speciation. Am Nat 100:637–650

    Article  Google Scholar 

  • Mayr E (1942) Systematics and the origin of species. Colombia University Press, New York

    Google Scholar 

  • Mayr E (1963) Animal species and evolution. Belknap of Harvard University Press, Cambridge, MA

    Google Scholar 

  • Meyer A, Kocher TD, Basasibwaki P, Wilson AC (1990) Monophyletic origin of Lake Victoria cichlid fishes suggested by mitochondrial DNA sequences. Nature 347:550–553

    Article  PubMed  CAS  Google Scholar 

  • Parenti LR (1984) Biogeography of the Andean killifish genus Orestias with comments on the species flock concept. In: Echelle AA, Kornfield I (eds) Evolution of fish species flocks. University of Maine at Orono, Orono, pp 85–92

    Google Scholar 

  • Pigliucci M (2001) Phenotypic plasticity: beyond nature and nurture. John Hopkins University Press, Baltimore, MD

    Google Scholar 

  • Pigliucci M (2005) Evolution of phenotypic plasticity: where are we going now? Trends Ecol Evol 20:481–486

    Article  PubMed  Google Scholar 

  • Pitcher TJ, Parrish JK (1993) Functions of shoaling behaviour in teleosts. In: Pitcher TJ (ed) Behaviour of teleost fishes. 2nd edn. Chapman & Hall, London

    Google Scholar 

  • Raney EC, Backus RH, Crawford RW, Robins CR (1953) Reproductive behaviour in Cyprinodon variegatus Lacépède, in Florida. Zoologica 38:97–104

    Google Scholar 

  • Ribbink AJ (1984) Is the species flock concept tenable? In: Echelle AA, Kornfield I (eds) Evolution of fish species flocks. University of Maine at Orono, Orono, pp 21–25

    Google Scholar 

  • Rosenzweig ML (1978) Competitive speciation. Biol J Linn Soc 10:275–289

    Article  Google Scholar 

  • Sandlund OT, Gunnarsson K, Jonasson PM, Jonasson B, Lindem T, Magnusson KP, Malmquist HJ, Sigurjonsdottir H, Skulasson S, Snorrason SS (1992) The Arctic charr Salvelinis alpinus in Thingvallavatn. Oikos 64:305–352 (special edition: Jonasson P (ed) Ecology of oligotrophic, subarctic Thingvallavatn)

    Article  Google Scholar 

  • Schliewen U, Tautz D, Pääbo S (1994) Sympatric speciation suggested by monophyly of crater lake cichlids. Nature 386:629–632

    Article  Google Scholar 

  • Schluter D (1996) Ecological causes of adaptive radiation. Am Nat 148:S40–S64

    Article  Google Scholar 

  • Schluter D (2000) The ecology of adaptive radiation. Oxford University Press, Oxford

    Google Scholar 

  • Schmitter-Soto JJ, Caro CI (1997) Distribution of tilapia, Oreochromis mossambicus (Perciformes: Cichlidae), and water body characteristics in Quintana Roo, Mexico. Rev Biol Trop 45:1257–1261

    Google Scholar 

  • Seehausen O, Bouton N (1997) Microdistribution and fluctuations in niche overlap in a rocky shore community in Lake Victoria. Ecol Freshw Fish 6:161–173

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Seghers BH (1974) Schooling behaviour in the guppy Poecilia reticulata: an evolutionary response to predation. Evolution 28:486–489

    Article  Google Scholar 

  • Stevenson MM (1992) Food habits within the Laguna Chichancanab Cyprinodon (Pisces: Cyprinodontidae) species flock. Southwest Nat 37:337–343

    Article  Google Scholar 

  • Strecker U (1996) Molekulargenetische und ethologische Untersuchungen zur Speziation eines Artenschwarmes der Gattung Cyprinodon (Cyprinodontidae, Teleostei). Ph.D. thesis, Universität Hamburg

  • Strecker U (2002) Cyprinodon esconditius, a new pupfish from Laguna Chichancanab, Yucatan, Mexico (Cyprinodontidae). Cybium 26:301–307

    Google Scholar 

  • Strecker U (2004) The Cyprinodon species flock from Laguna Chichancanab, Mexico (Teleostei): sexual and disruptive selection driving adaptive radiation. Mitteil Hamb Zool Mus Inst 101:65–74

    Google Scholar 

  • Strecker U (2005) Description of a new species from Laguna Chichancanab, Yucatan, Mexico: Cyprinodon suavium (Pisces: Cyprinodontidae). Hydrobiologia 541:107–115

    Article  Google Scholar 

  • Strecker U (2006a) Genetic differentiation and reproductive isolation in a Cyprinodon fish species flock from Laguna Chichancanab, Mexico. Mol Phylogenet Evol 39:865–872

    Article  PubMed  CAS  Google Scholar 

  • Strecker U (2006b) The impact of invasive fish on an endemic Cyprinodon species flock (Teleostei) from Laguna Chichancanab, Yucatan, Mexico. Ecol Freshw Fish 15:408–418

    Article  Google Scholar 

  • Strecker U, Kodric-Brown A (1999) Mate recognition systems in a species flock of Mexican pupfish. J Evol Biol 12:927–935

    Article  Google Scholar 

  • Strecker U, Kodric-Brown A (2000) Mating preferences in a species flock of Mexican pupfishes (Cyprinodon, Teleostei). Biol J Linn Soc 71:677–687

    Article  Google Scholar 

  • Strecker U, Meyer CG, Sturmbauer C, Wilkens H (1996) Genetic divergence and speciation in an extremely young species flock in Mexico formed by the genus Cyprinodon (Cyprinodontidae, Teleostei). Mol Phylogenet Evol 6:143–149

    Article  PubMed  CAS  Google Scholar 

  • Sturmbauer C, Meyer CG (1992) Genetic divergence, speciation and morphological stasis in a lineage of African cichlid fishes. Nature 358:578–581

    Article  PubMed  CAS  Google Scholar 

  • Templeton CN, Shriner WM (2004) Multiple selection pressures influence Trinidadian guppy (Poecilia reticulata) antipredator behavior. Behav Ecol 15:673–678

    Article  Google Scholar 

  • Tobler M, Schlupp I, Heubel KU, Riesch R, García de León FJ, Giere O, Plath M (2006) Life on the edge: hydrogen sulfide and the fish communities of a Mexican cave and surrounding waters. Extremophiles 10(6):577–585

    Article  PubMed  CAS  Google Scholar 

  • van Oers K, Drent PJ, de Goede P, van Norrdwijk AJ (2004) Realized heritability and repeatability of risk-taking behaviour in relation to avian personalities. Proc R Soc Lond B 271:65–73

    Article  Google Scholar 

  • Villwock W (1986) Speciation and adaptive radiation in Andean Orestias fishes. In: Vuilleumier F, Monasterio MM (eds) High altitude tropical biography. Oxford University Press, Oxford, NY, pp 387–403

    Google Scholar 

  • West-Eberhard MJ (2003) Developmental plasticity and evolution. Oxford University Press, Oxford

    Google Scholar 

  • Wilson DS, Clark AB, Coleman K, Dearstyne T (1994) Shyness and boldness in humans and other animals. Trends Ecol Evol 9:442–446

    Article  Google Scholar 

  • Yamaoka K (1991) Feeding relationships. In: Keenleyside MHA (ed) Cichlid fishes: behaviour, ecology and evolution. Chapman & Hall, London, pp 151–172

    Google Scholar 

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Acknowledgments

We thank H. Wilkens and J. Horstkotte for valuable comments and discussions. M. Hänel provided the drawings for Fig. 1. C. St. Mary, T. Czeschlik, and two anonymous reviewers greatly helped to improve the manuscript with their extremely constructive comments. D. Teege and S. Baumann provided help with fish care. Financial support came from the University of Hamburg to M.P. The experiments reported in this paper comply with the current laws of Germany.

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  1. Martin Plath

    Present address: Unit of Animal Ecology, Institute of Biochemistry and Biology, University of Potsdam, Maulbeerallee 1, 14469, Potsdam, Germany

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  1. Unit of Evolutionary Biology and Systematic Zoology, Institute of Biochemistry and Biology, University of Potsdam, Karl-Liebknecht Str. 24–25, 14476, Potsdam, Germany

    Martin Plath

  2. Biozentrum Grindel und Zoologisches Museum der Universität Hamburg, Martin-Luther-King Platz 3, 20146, Hamburg, Germany

    Ulrike Strecker

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Plath, M., Strecker, U. Behavioral diversification in a young species flock of pupfish (Cyprionodon spp.): shoaling and aggressive behavior. Behav Ecol Sociobiol 62, 1727–1737 (2008). https://doi.org/10.1007/s00265-008-0601-9

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