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Frequency of Ectodysplasin alleles and limited introgression between sympatric threespine stickleback populations

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Abstract

The threespine stickleback (Gasterosteus aculeatus) is primitively an anadromous or resident marine species but has repeatedly colonized fresh water, where predictable phenotypic divergence usually occurs rapidly. A conspicuous element of this divergence is change of the number and position of lateral armor plates from about 33 that cover the entire flank (complete) to <10 anterior plates (low). This difference is caused primarily by variation at the Ectodysplasin (Eda) locus. The low Eda allele appears to be rarer in two geographically adjacent anadromous populations from Cook Inlet, Alaska than in most marine or anadromous populations reported from elsewhere, and there is no evidence of elevated gene flow for Eda between anadromous and resident lake threespine stickleback populations that breed in sympatry. However, the two anadromous populations are divergent for the frequencies of two complete Eda alleles. It is not clear how monomorphic low-plated freshwater populations in Cook Inlet have almost invariably acquired ancestral low Eda alleles from anadromous ancestors in which this allele appears to be extremely rare.

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References

  • Aguirre WE (2007) The pattern and process of evolutionary diversification. Lessons from a threespine stickleback adaptive radiation. Ph.D. Dissertation, Stony Brook University, New York, USA, 205 pp

  • Aguirre WE, Ellis KE, Kusenda M et al (2008) Phenotypic variation and sexual dimorphism in anadromous threespine stickleback: implications for postglacial adaptive radiation. Biol J Linn Soc 95:465–478

    Article  Google Scholar 

  • Albert AYK, Sawaya S, Vines TH et al (2008) The genetics of adaptive shape shift in stickleback: pleiotropy and effect size. Evolution 62:76–85

    PubMed  Google Scholar 

  • Bańbura J, Bakker TCM (1995) Latral plate morph genetics revisited: evidence for a fourth morph in three-spined sticklebacks. Behaviour 132:1153–1171

    Article  Google Scholar 

  • Barrett RDH, Rogers SM, Schluter D (2008) Natural selection on a major armor gene in threespine stickleback. Science 322:255–257

    Article  CAS  PubMed  Google Scholar 

  • Barrett RDH, Rogers SM, Schluter D (2009a) Environment specific pleiotropy facilitates divergence at the Ectodysplasin locus in threespine stickleback. Evolution 63:2831–2837

    Article  PubMed  Google Scholar 

  • Barrett RDH, Vines TH, Bystriansky JS et al (2009b) Should I stay or should I go? The Ectodysplasin locus is associated with behavioural differences in threespine stickleback. Biol Lett 5:788–791

    Article  PubMed  Google Scholar 

  • Bell MA (1981) Lateral plate polymorphism and ontogeny of the complete plate morph of threespine sticklebacks (Gasterosteus aculeatus). Evolution 35:67–74

    Article  Google Scholar 

  • Bell MA (1982) Differentiation of adjacent stream populations of threespine sticklebacks. Evolution 36:189–199

    Article  Google Scholar 

  • Bell MA (1984) Evolutionary phenetics and genetics: the threespine stickleback, Gasterosteus aculeatus, and related species. In: Turner BJ (ed) Evolutionary genetics of fishes. Plenum, New York, pp 431–528

    Google Scholar 

  • Bell MA (1995) Intraspecific systematics of Gasterosteus aculeatus populations: implications for behavioral ecology. Behaviour 132:1131–1152

    Article  Google Scholar 

  • Bell MA (2001) Lateral plate evolution in the threespine stickleback: getting nowhere fast. Genetica 112(113):45–461

    Google Scholar 

  • Bell MA, Foster SA (1994) Introduction to the evolutionary biology of the threespine stickleback. In: Bell MA, Foster SA (eds) the evolutionary biology of the threespine stickleback. Oxford University Press, Oxford, pp 1–27

    Google Scholar 

  • Bell MA, Aguirre WE, Buck NJ (2004) Twelve years of contemporary armor evolution in a threespine stickleback population. Evolution 58:814–824

    PubMed  Google Scholar 

  • Boughman JW (2007) Speciation in sticklebacks. In: Östlund-Nilsson S, Mayer I, Huntingford FA (eds) Biology of the three-spined stickleback. CRC Press, Boca Raton, pp 83–126

    Google Scholar 

  • Boughman JW, Rundle HD, Schluter D (2005) Parallel evolution of sexual isolation in sticklebacks. Evolution 59:361–373

    PubMed  Google Scholar 

  • Bourgeois JF, Blouw DM, Bell MA (1994) Multivariate analysis of geographic covariance between phenotypes and environments in the threespine stickleback, Gasterosteus aculeatus. Can J Zool 72:1497–1509

    Article  Google Scholar 

  • Cano JM, Matsuba C, Mäkinen H et al (2006) The utility of QTL-linked markers to detect selective sweeps in natural populations – a case study of the EDA gene and a linked marker in threespine stickleback. Mol Ecol 15:4613–4621

    Article  CAS  PubMed  Google Scholar 

  • Colosimo PF, Peichel CL, Nereng K et al (2004) The genetic architecture of parallel armor plate reduction in threespine sticklebacks. PLoS Biol 2:0635–0641

    CAS  Google Scholar 

  • Colosimo PF, Hoseman KE, Balabhadra S et al (2005) Widespread parallel evolution in sticklebacks by repeated fixation of Ectodysplasin alleles. Science 307:1928–1933

    Article  CAS  PubMed  Google Scholar 

  • Cresko WA, Amores A, Wilson C et al (2004) Parallel genetic basis for repeated evolution of armor loss in Alaskan threespine stickleback populations. Proc Natl Acad Sci USA 101:6050–6055

    Article  CAS  PubMed  Google Scholar 

  • Francis RC, Havens AC, Bell MA (1985) Unusual lateral plate variation of threespine sticklebacks (Gasterosteus aculeatus) from Knik Lake, Alaska. Copeia 1985:619–624

    Article  Google Scholar 

  • Gow JL, Peichel CL, Taylor EB (2007) Ecological selection against hybrids in natural populations of sympatric threespine sticklebacks. J Evol Biol 20:2173–2180

    Article  CAS  PubMed  Google Scholar 

  • Hagen DW (1967) Isolating mechanisms in threespine sticklebacks (Gasterosteus aculeatus). J Fish Res Board Can 24:1637–1692

    Google Scholar 

  • Hagen DW, Moodie GEE (1982) Polymorphism for plate morphs in Gasterosteus aculeatus on the east coast of Canada and an hypothesis for their global distribution. Can J Zool 60:1032–1042

    Article  Google Scholar 

  • Hay DE, McPhail JD (1975) Mate selection in three-spine sticklebacks (Gasterosteus). Can J Zool 53:441–450

    Article  Google Scholar 

  • Jones FC, Brown C, Pemberton JM et al (2006) Reproductive isolation in threeespine stickleback hybrid zone. J Evol Biol 19:1532–1544

    Article  Google Scholar 

  • Karve AD, von Hippel FA, Bell MA (2007) Isolation between sympatric anadromous and resident threespine stickleback species in Mud Lake, Alaska. Environ Biol Fishes 81:287–296

    Article  Google Scholar 

  • Kitano J, Bolnick DI, Beauchamp DA et al (2008) Reverse evolution of armor plates in the threespine stickleback. Curr Biol 18:769–774

    Article  CAS  PubMed  Google Scholar 

  • Klepaker T (1993) Morphological changes in a marine population of threespine stickleback, Gasterosteus aculeatus, recently isolated in fresh water. Can J Zool 71:1231–1258

    Article  Google Scholar 

  • Klepaker T (1996) Lateral plate polymorphism in marine and estuarine populations of the threespine stickleback (Gasterosteus aculeatus) along the coast of Norway. Copeia 1996:832–838

    Article  Google Scholar 

  • Marchinko KB (2009) Predation’s role in repeated phenotypic and genetic divergence of armor in threespine stickleback. Evolution 63:127–138

    Article  PubMed  Google Scholar 

  • Marchinko KB, Schluter D (2007) Parallel evolution by correlated response: lateral plate reduction in threespine stickleback. Evolution 61:1084–1090

    Article  PubMed  Google Scholar 

  • Mayr E (1942) Systematics and the origin of species. Columbia University Press, New York, p 334

    Google Scholar 

  • McKinnon JS, Rundle HD (2002) Speciation in nature: the threespine stickleback model systems. Trends Ecol Evol 17:480–488

    Article  Google Scholar 

  • McKinnon JS, Mori S, Blackman BK et al (2004) Evidence for ecology’s role in speciation. Nature 429:294–298

    Article  CAS  PubMed  Google Scholar 

  • McPhail JD (1994) Speciation and the evolution of reproductive isolation in the sticklebacks (Gasterosteus) of south-western British Columbia. In: Bell MA, Foster SA (eds) The evolutionary biology of the threespine stickleback. Oxford University Press, Oxford, pp 399–437

    Google Scholar 

  • McPhial JD (1969) Predation and the evolution of a stickleback (Gasterosteus). J Fish Res Board Can 26:3183–3208

    Google Scholar 

  • Münzing J (1963) The evolution of variation and distributional patterns in European populations of the three-spined stickleback, Gasterosteus aculeatus. Evolution 17:320–332

    Article  Google Scholar 

  • Nagel L, Schluter D (1998) Body size, natural selection, and speciation in sticklebacks. Evolution 52:209–218

    Article  Google Scholar 

  • Reimchen TE (2000) Predator handling failures of lateral plate morphs in Gasterosteus aculeatus: implications for stasis and distribution of the ancestral plate condition. Behaviour 137:1081–1096

    Article  Google Scholar 

  • Schluter D (1995) Adaptive radiation in sticklebacks: trade-offs in feeding performance and growth. Ecology 76:82–90

    Article  Google Scholar 

  • Sokal RR, Rohlf FJ (1995) Biometry, 3rd edn. W.H. Freeman, New York, p 887

    Google Scholar 

  • Taylor EB, McPhail JD (1999) Evolutionary history of an adaptive radiation in species pairs of threespine sticklebacks (Gasteroteus): insights from mitochondrial DNA. Biol J Linn Soc 66:271–291

    Article  Google Scholar 

  • Taylor EB, McPhail JD (2000) Historical contingency and ecological determinism interact to prime speciation in sticklebacks, Gasterosteus. Proc Roy Soc, B Biol Sci 267:2375–2384

    Article  CAS  Google Scholar 

  • Vamosi SM (2006) Contemporary evolution of armor and body size in a recently introduced population of threespine stickleback Gasterosteus aculeatus. Acta Zool Sin 52:483–490

    Google Scholar 

  • Withler RE, McPhail JD (1985) Genetic variability in freshwater and anadromous stickleabckcs (Gasterosteus aculeatus) of southern British Columbia. Can J Zool 63:528–533

    Article  Google Scholar 

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Acknowledgments

We thank M. Bobb, K. E. Ellis, P. J. Park, and A. Plaunova for field assistance, E. Hughes and A. Litewka for help with Eda genotyping, C. L. Peichel, J. Kitano, and D. Schluter for providing Eda frequencies from their studies, F.J. Rohlf for advice on calculating frequency limits for rare alleles, M. Fisher-Reid, X. Hua, D. Moen, K. Slovak, C. Ulloa, and J. Wiens for comments on an earlier version of the manuscript, and two anonymous reviewers for constructive criticism. Support to WEA from the W. Burghardt Turner Fellowship and Alliance for Graduate Education and the Professoriate is gratefully acknowledged. Howard Hughes Medical Institute grant 52005887 to the Long Island Group Advancing Science Education (LIGASE) at Stony Brook University supported AB and AKG for this research, and several undergraduate assistants were supported by National Institutes of Health grant GM50070 to LIGASE. Field sampling was supported by National Science Foundation grants DEB0211391 and DEB0322818 to MAB and F. J. Rohlf. This is contribution 1203 from Ecology and Evolution at Stony Brook University.

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Correspondence to Michael A. Bell.

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Bell, M.A., Gangavalli, A.K., Bewick, A. et al. Frequency of Ectodysplasin alleles and limited introgression between sympatric threespine stickleback populations. Environ Biol Fish 89, 189–198 (2010). https://doi.org/10.1007/s10641-010-9712-z

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  • DOI: https://doi.org/10.1007/s10641-010-9712-z

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