Abstract
Adaptation and reproductive isolation, the engines of biological diversity, are still elusive when discussing the genetic bases of speciation. Namely, the number of genes and magnitude of selection acting positively or negatively on genomic traits implicated in speciation is contentious. Here, we describe the first steps of an ongoing research program aimed at understanding the genetic bases of population divergence and reproductive isolation in the lake whitefish (Coregonus clupeaformis). A preliminary linkage map originating from a hybrid cross between dwarf and normal ecotypes is presented, whereby some of the segregating AFLP markers were found to be conserved among natural populations. Maximum-likelihood was used to estimate hybrid indices from non-diagnostic markers at 998 AFLP loci. This allowed identification of the most likely candidate loci that have been under the influence of selection during the natural hybridisation of whitefish originating from different glacial races. As some of these loci could be identified on the linkage map, the possibility that selection of traits in natural populations may eventually be correlated to specific chromosomal regions was demonstrated. The future prospects and potential of these approaches to elucidate the genetic bases of adaptation and reproductive isolation among sympatric ecotypes of lake whitefish is discussed.
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Allendorf, F.W. & G.H. Thorgaard, 1984. Tetraploidy and the evolution of salmonid fishes, in Evolutionary Genetics of Fishes, edited by B.J. Turner. Plenum Press, New York.
Barton, N.H., 1998. The geometry of adaptation. Nature 395: 751–752.
Barton, N.H. & K.S. Gale, 1993. Genetic analysis of hybrid zones, pp. 13–45 in Hybrid Zones and the Evolutionary Process, edited by R.G. Harrison. Oxford University Press, Oxford.
Bernatchez, L., A. Chouinard & G. Lu, 1999. Integrating molecular genetics and ecology in studies of adaptive radiation: whitefish, Coregonus sp., as a case study. Biol. J. Linnean Soc. 68: 173–194.
Bernatchez, L. & J.J. Dodson, 1990. Allopatric origin of sympatric populations of lake whitefish (Coregonus clupeaformis) as revealed by mitochondrial DNA restriction analysis. Evolution 44: 1263–1271.
Bernatchez, L. & J.J. Dodson, 1994. Phylogenetic relationships among paleartic and neartic whitefish (Coregonus sp.) populations as revealed by mitochondrial DNA variation. Can. J. Fish. Aquat. Sci. 51: 240–251.
Bernatchez, L., J.A. Vuorinen, R.A. Bodaly & J.J. Dodson, 1996. Genetic evidence for reproductive isolation and multiple origins of sympatric trophic ecotypes of whitefish (Coregonus). Evolution 50: 624–635.
Bernatchez, L. & C.C. Wilson, 1998. Comparative phylogeography of Nearctic and Palearctic fishes. Mol. Ecol. 7: 431–452.
Bradshaw, H.D., K.G. Otto, B. Frewen, J. McKay & D.W. Schemske, 1998. Quantitative trait loci affecting differences in floral morphology between two species of monkeyflower (Mimulus). Genetics 149: 367–382.
Bradshaw, H.D., S.M. Wilbert, K.G. Otto & D.W. Schemske, 1995. Genetic mapping of floral traits associated with reproductive isolation in monkeyflowers (Minulus). Nature 376: 762–765.
Bush, G.L. & J. Smith, 1998. The genetics and ecology of sympatric speciation: a case study. Res. Populat. Ecol. 40: 175–187.
Carney S.E., K.A. Gardner & L.H. Rieseberg, 2000. Evolutionary changes over the fifty-year history of a hybrid population of sunflowers (Helianthus). Evolution 54: 462–474.
Cloutier, S., M. Cappadocia & B.S. Landry, 1997. Analysis of RFLP mapping inaccuracy in Brassica napus L. Theor. Appl. Genet. 95: 83–91.
Coyne, J.A., 1995. Speciation in monkeyflowers. Nature 376: 726–727.
Darwin, C., 1859. On the Origin of Species By Means of Natural Selection. Random House, USA, Modern Library edn. (1998).
Diekmann, U. & M. Doebeli, 1999. On the origin of species by sympatric speciation. Nature 400: 354–357.
Edwards, A.W.F., 1972. Likelihood. Cambridge University Press, Cambridge.
Fenderson O.C., 1964. Evidence of subpopulations of lake white-fish, Coregonus clupeaformis, involving a dwarf form. Trans. Am. Fish. Soc. 93: 77–94.
Fisher, R.A., 1925. Statistical Methods for Research Workers. Oliver and Boyd, Edinburgh.
Fisher, R.A., 1930. The Genetical Theory of Natural Selection. Oxford University Press, Oxford.
Hilborn, R. & M. Mangel, 1997. The Ecological Detective: Confronting Models with Data. Princeton University Press, Princeton.
Huxley, J., 1942. Evolution, the Modern Synthesis. Allen and Unwin, London.
Jiggens, C.D. & J. Mallet, 2000. Bimodal hybrid zones and speciation. Trends Ecol. Evol. 15: 250–255.
Kim S.-C. & L.H. Rieseberg, 1999. Genetic architecture of species differences in annual sunflowers: implications for adaptive trait introgression. Genetics 153: 965–977.
Kimura, M., 1983. The Neutral Theory of Molecular Evolution, Cambridge University Press, Cambridge.
Knapik, E.W., A. Goodman, M. Ekker, M. Chevrette, J. Delgado, S. Neuhaus, N. Shimoda, W. Driever, M.C. Fishman & H.J. Jacob, 1998. A microsatellite genetic linkage map for zebrafish (Danio rerio). Nature Genet. 18: 338–343.
Kocher, T., W.-J. Lee, H. Sobolewska, D. Penman & B. McAndrew, 1998. A genetic linkage map of a cichlid fish, the tilapia (Oreochromis niloticus). Genetics 148: 1225–1232.
Kondrashov, A.S. & F.A. Kondrashov, 1999. Interactions among quantitative traits in the course of sympatric speciation. Nature 400: 351–354.
Lander, E., P. Green, J. Abrahamson, A. Barlow, M. Daly, S. Lincoln & L. Newburg, 1987. MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1: 174–181.
Long, J.C., 1991. The genetic structure of admixed populations. Genetics 127: 417–428.
Lu, G., D. Basley & L. Bernatchez, 2001. Complex evolutionary history of lake whitefish (Coregonus clupeaformis) in northeastern North America assessed with mtDNA and microsatellite markers. Mol. Ecol. 10: 965–985.
Lu, G. & L. Bernatchez, 1998. Experimental evidence for reduced hybrid viability between dwarf and normal ecotypes of lake whitefish (Coregonus clupeaformis, Mitchill). Proc. Roy. Soc. London B 265: 1025–1030.
Lu, G. & L. Bernatchez, 1999. Correlated trophic specialization and genetic divergence in sympatric lake whitefish ecotypes (Coregonus clupeaformis): support for the ecological speciation hypothesis. Evolution 53: 1491–1505.
Mayr, E., 1942. Systematics and the Origin of Species from the Viewpoint of a Zoologist. Columbia University Press, New York.
Mueller, U. & L. Wolfenbarger, 1999. AFLP genotyping and fingerprinting. Trends Ecol. Evol. 14: 389–394.
Orr, H.A., 1998. The population genetics of adaptation: the distribution of factors fixed during adaptive evolution. Evolution 52: 935–949.
Orr, H.A. & T.B. Smith, 1998. Ecology and speciation. Trends Ecol. Evol. 13: 502–506.
Ott, J., 1991. Analysis of Human Genetic Linkage. The Johns Hopkins University Press, Baltimore, Revised edn.
Pigeon, D., A. Chouinard & L. Bernatchez, 1997. Multiple modes of speciation involved in the parallel evolution of sympatric dwarf and normal morphotypes of lake whitefish (Coregonus clupeaformis, Salmonidae). Evolution 51: 196–205.
Rice, W.R., 1989. Analysing tables of statistical tests. Evolution 43: 223–225.
Rieseberg, L.H., 1998a. Genetic mapping as a tool for studying speciation, pp. 459–487 in Molecular Systematics of Plants, edited by D.E. Soltis, P.S. Soltis & J.J. Doyle. Chapman and Hall, New York, 2nd edn.
Rieseberg, L.H., 1998b. Molecular ecology of hybridization, pp. 243–265 in Advances in Molecular Ecology, edited by G.R. Carvalho. IOS Press.
Rieseberg, L.H., S.J.E. Baird & A.M. Desrochers, 1998. Patterns of mating in wild sunflower hybrid zones. Evolution 52: 713–726.
Rieseberg, L.H., H. Choi, R. Chan & C. Spore, 1993. Genomic map of a diploid hybrid species. Heredity 70: 285–293.
Rieseberg, L.H. & C.R. Linder, 1999. Hybrid classification: insights from genetic map-based studies experimental hybrids. Ecology 80: 351–370.
Rieseberg, L.H., J. Whitton & K.A. Gardner, 1999. Hybrid zones and the genetic architecture of a barrier to gene flow between two sunflower species. Genetics 152: 713–727.
Robinson, B.W. & D. Schluter, 2000. Natural selection and the evolution of adaptive genetic variation in northern freshwater fishes, pp. 65–94 in Adaptive Genetic Variation in the Wild, edited by T.A. Mousseau, B. Sinervo & J.A. Endler. Oxford University Press, New York.
Sakamoto, T., R.G. Danzmann, K. Gharbi, P. Howard, A. Ozaki, S.-K. Khoo, R.A. Woram, N. Okamoto, M.M. Ferguson, L.-E. Holm, R. Guyomard & B. Hoyheim, 2000. A microsatellite linkage map of rainbow trout (Oncorhynchus mykiss). Genetics 155: 1331–1345.
Sawamura, K., A. Davis & C.-L.Wu, 2000. Genetic analysis of speciation by means of introgression into Drosophila melanogaster. Proc. Nat. Acad. Sci. 97: 2652–2655.
Schemske, D.W. & H.D. Bradshaw, 1999. Pollinator preference and the evolution of floral traits in monkeyflowers (Mimulus). Proc. Nat. Acad. Sci. 96: 11910–11915.
Schluter, D., 1996a. Ecological speciation in postglacial fishes. Philos. Trans. Roy. Soc. London B 351: 807–814.
Schluter, D., 1996b. Ecological causes of adaptive radiation. Am. Naturalist 148: 540–564.
Schluter, D., 1998. Ecological causes of speciation, pp. 114–129 in Endless Forms: Species and Speciation, edited by D.J. Howard & S.H. Berlocher. Oxford University Press, New York.
Schluter, D., 2000. Ecological character displacement in adaptive radiation. Am. Naturalist 156: S4–S16.
Scott, W. & E. Crossman, 1973. Freshwater fishes of Canada. Fish. Res. Board Can. 184: 269–277.
Tanksley, S., 1993. Mapping polygenes. Ann. Rev. Genet. 27: 205–233.
Taylor, E. & J. McPhail, 1999. Evolutionary history of an adaptive radiation in species pairs of three spine sticklebacks (Gasterosteus): insights from mitochondrial DNA. Biol. J. Linnean Soc. 66: 271–291.
Turgeon, J., A. Estoup & L. Bernatchez, 1999. Species flock in the North American Great Lakes: molecular ecology of Lake Nipigon ciscoes (Teleostei: Coregonidae: Coregonus). Evolution 53: 1857–1871.
Van der Lee, T., I. De Witte, A. Drenth, C. Alfonso & F. Govers, 1997. AFLP linkage map of the oomycete Phytophthora infestans. Fungal Genet. Biol. 21: 278–291.
Vos, P., R. Hogers, M. Bleeker, M. Reijans, T. van de Lee, M. Hornes, A. Frijters, J. Pot, J. Peleman, M. Kuiper & M. Zabeau, 1995. AFLP: a new technique for DNA fingerprinting. Nucl. Acids Res. 23: 4407–4414.
Wolfram, S., 1992. Mathematica: A System for Doing Mathematics by Computer. Addison-Wesley Publishing Company, Redwood City.
Young, W., P. Wheeler, V. Coryell, P. Keim & G. Thorgaard, 1998. A detailed linkage map of rainbow trout produced using doubled haploids. Genetics 148: 839–850.
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Rogers, S., Campbell, D., Baird, S. et al. Combining the analyses of introgressive hybridisation and linkage mapping to investigate the genetic architecture of population divergence in the lake whitefish (Coregonus clupeaformis, Mitchill). Genetica 111, 25–41 (2001). https://doi.org/10.1023/A:1013773600304
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DOI: https://doi.org/10.1023/A:1013773600304