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The genetic basis of adaptation: lessons from concealing coloration in pocket mice

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Abstract

Recent studies on the genetics of adaptive coat-color variation in pocket mice (Chaetodipus intermedius) are reviewed in the context of several on-going debates about the genetics of adaptation. Association mapping with candidate genes was used to identify mutations responsible for melanism in four different populations of C. intermedius. Here, I review four main results (i) a single gene, the melanocortin-1-receptor (Mc1r), appears to be responsible for most of the phenotypic variation in color in one population, the Pinacate site; (ii) four or fewer nucleotide changes at Mc1r appear to be responsible for the difference in receptor function; (iii) studies of migration-selection balance suggest that the selection coefficient associated with the dark Mc1r allele at the Pinacate site is large; and (iv) different (unknown) genes underlie the evolution of melanism on three other lava flows. These findings are discussed in light of the evolution of convergent phenotypes, the average size of phenotypic effects underlying adaptation, the evolution of dominance, and the distinction between adaptations caused by changes in gene dosage versus gene structure.

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References

  • M.D.F.S. Barbosa Q.A. Nguyen V.T. Tchernev J.A. Ashley J.C. Detter S.M. Blaydes S.J. Brandt D. Chotai C. Hodgman R.C.E. Solari M. Lovett S.F. Kingsmore (1996) ArticleTitleIdentification of the homologous beige and Chediak-Higashi-Syndrome genes Nature 382 262–265

    Google Scholar 

  • G.S. Barsh (1996) ArticleTitleThe genetics of pigmentation: from fancy genes to complex traits Trend. Genet. 12 299–305

    Google Scholar 

  • S.B. Benson (1933) ArticleTitleConcealing coloration among some desert rodents of the southwestern United States Univ. Calif. Pub. Zool. 40 1–70

    Google Scholar 

  • R.J. Britten E.H. Davidson (1969) ArticleTitleGene regulation for higher cells: a theory Science 165 349–357

    Google Scholar 

  • M. Bronner-Fraser (1995) ArticleTitleOrigins and developmental potential of the neural crest Exp. Cell Res. 218 405–417

    Google Scholar 

  • S.J. Bultman M.L. Klebig E.J. Michaud H.O. Sweet M.T. Davisson R.P. Woychik (1994) ArticleTitleMolecular analysis of reverse mutations from nonagouti (a) to black-and-tan (at) and white-bellied agouti (Aw) reveals alternative forms of agouti transcripts Genes Develop. 8 481–490

    Google Scholar 

  • B. Charlesworth (1992) ArticleTitleEvolutionary rates in partially self-fertilizing species Am. Nat. 140 126–148

    Google Scholar 

  • B. Charlesworth (1994) ArticleTitleThe genetics of adaptation: lessons from mimicry Am. Nat. 144 839–847

    Google Scholar 

  • B. Charlesworth J.A. Coyne N.H. Barton (1987) ArticleTitleThe relative rates of evolution of sex chromosomes and autosomes Am. Nat. 130 113–146

    Google Scholar 

  • L.E. Cowen J.B. Anderson L.M. Kohn (2002) ArticleTitleEvolution of drug resistance in Candida albicans Ann. Rev. Microbiol. 56 139–165

    Google Scholar 

  • P.J. Daborn J.L. Yen M.R. Bogwitz G. LeGoff E. Feil S. Jeffers N. Tijet T. Perry D. Heckel P. Batterham et al. (2002) ArticleTitleA single P450 allele associated with insecticide resistance in Drosophila Science 297 2253–2256

    Google Scholar 

  • C. Darwin (1859) The Origin of Species by Mean of Natural Selection John Murray London

    Google Scholar 

  • L.R. Dice (1940) ArticleTitleEcologic and genetic variability within species of Peromyscus Am. Nat. 74 212–221

    Google Scholar 

  • L.R. Dice (1947) ArticleTitleEffectiveness of selection by owls of deer-mice (Peromyscus maniculatus) which contrast in color with their background Contr. Lab. Vert. Biol., Univ. Michigan 34 1–20

    Google Scholar 

  • L.R. Dice P.M. Blossom (1937) ArticleTitleStudies of mammalian ecology in southwestern North America with special attention to the colors of desert mammals Publ. Carnegie Inst. Washington 485 1–129

    Google Scholar 

  • J. Doebley A. Stec L. Hubbard (1997) ArticleTitleThe evolution of apical dominance in maize Nature 386 485–488 Occurrence Handle10.1038/386485a0 Occurrence Handle1:CAS:528:DyaK2sXisVSqurc%3D Occurrence Handle9087405

    Article  CAS  PubMed  Google Scholar 

  • T. Dobzhansky (1937) Genetics and the Origin of Species Columbia University Press New York

    Google Scholar 

  • T. Dobzhansky (1970) Genetics of the Evolutionary Process Columbia University Press New York

    Google Scholar 

  • W. Enard P. Khaitovich J. Klose S. Zollner F. Heissig P. Giavalisco K. Nieselt-Struwe E. Muchmore A. Varki R. Ravid G.M. Doxiadis R.E. Bontrop S. Paabo (2002) ArticleTitleIntra- and interspecific variation in primate gene expression patterns Science 296 340–343 Occurrence Handle10.1126/science.1068996 Occurrence Handle1:CAS:528:DC%2BD38XjtVWhsrs%3D Occurrence Handle11951044

    Article  CAS  PubMed  Google Scholar 

  • C.A. Erickson (1993) ArticleTitleFrom the crest to the pheriphery: control of pigment-cell migration and lineage segregation Pigment Cell Res. 6 336–347

    Google Scholar 

  • G.H. Feng T. Bailin J. Oh R.A. Spritz (1997) ArticleTitleMouse pale ear (ep) is homologous to human Hermasky-Pudlak syndrome and contains a rare AT-AC intron Hum. Mol. Genet. 6 793–797

    Google Scholar 

  • D.A. Fidock T. Nomura A.K. Talley R.A. Cooper S.M. Dzekunov M.T. Ferdig L.M.B. Ursos A.B.S. Sidhu B. Naude K.W. Deitsch X.Z. Su J.C. Wootton P.D. Roepe T.E. Wellems (2000) ArticleTitleMutations in the P-falciparum digestive vacuole transmembrane protein PfCRT and evidence for their role in chloroquine resistance Mol. Cell. 6 861–871

    Google Scholar 

  • R.A. Fisher (1930) The Genetical Theory of Natural Selection Oxford University Press Oxford

    Google Scholar 

  • E.S. Haag J.R. True (2001) ArticleTitlePerspective: from mutants to mechanisms Assessing the candidate gene paradigm in evolutionary biology. Evolution 55 1077–1084

    Google Scholar 

  • J.B.S. Haldane (1924) ArticleTitleA mathematical theory of natural and artificial selection, Part 1 Trans. Camb. Philos. Soc. 23 19–41

    Google Scholar 

  • J.B.S. Haldane (1932) The Causes of Evolution Longmans, Green & Co, Ltd. New York

    Google Scholar 

  • H.E. Hoekstra K.E. Drumm M.W. Nachman (2004) ArticleTitleEcological genetics of adaptive color polymorphism in pocket mice: geographic variation in selected and neutral genes Evolution 58 1329–1341

    Google Scholar 

  • H.E. Hoekstra M.W. Nachman (2003) ArticleTitleDifferent genes underlie adaptive melanism in different populations of rock pocket mice Mol. Ecol. 12 1185–1194

    Google Scholar 

  • D. Hughes (2003) ArticleTitleExploiting genomics, genetics and chemistry to combat antibiotic resistance Nat. Rev. Genet. 4 432–441

    Google Scholar 

  • I.J. Jackson (1994) ArticleTitleMolecular and developmental genetics of mouse coat color Ann. Rev. Genet. 28 189–217

    Google Scholar 

  • I.J. Jackson (1997) ArticleTitleHomologous pigmentation mutations in human, mouse and other model organisms Human Mol. Genet. 6 1613–1624

    Google Scholar 

  • M. Jasieniuk A.L. Brule-Babel I.N. Morrison (1996) ArticleTitleThe evolution and genetics of herbicide resistance in weeds Weed Sci. 44 176–193

    Google Scholar 

  • M. Kimura (1983) The Neutral Theory of Molecular Evolution Cambridge University Press Cambridge

    Google Scholar 

  • A.S. Kondrashov S. Sunyaev F.A. Kondrashov (2002) ArticleTitleDobzhansky-Muller incompatibilities in protein evolution Proc. Nat. Acad. Sci. 99 14878–14883

    Google Scholar 

  • D.L. Lack (1947) Darwin’s Finches University Press Cambridge

    Google Scholar 

  • R. Mauricio (2001) ArticleTitleMapping quantitative trait loci in plants: uses and caveats for evolutionary biology Nat. Rev. Genet. 2 370–381

    Google Scholar 

  • E. Mayr (1942) Systematics and the Origin of Species Columbia University Press New York

    Google Scholar 

  • E. Mayr (1963) Animal Species and Evolution Harvard University Press Cambridge, Massachusetts

    Google Scholar 

  • D.J. Merrell (1969) ArticleTitleThe evolutionary role of dominant genes Genet. Lect. (Oregon State University, Corvalis) 1 167–194

    Google Scholar 

  • M.W. Nachman H.E. Hoekstra S.L. D’Agostino (2003) ArticleTitleThe genetic basis of adaptive melanism in pocket mice Proc. Nat. Acad. Sci. USA 100 5268–5273

    Google Scholar 

  • J.M. Newton A.L. Wilkie L. He S.A. Jordan D.L. Metallinos N.G. Holmes I.J. Jackson G.S. Barsh (2000) ArticleTitleMelanocortin 1 receptor variation in the domestic dog Mamm. Genome 11 24–30

    Google Scholar 

  • H.A. Orr (1998) ArticleTitleThe population genetics of adaptation: the distribution of factors fixed during adaptive evolution Evolution 52 935–949

    Google Scholar 

  • H.A. Orr J.A. Coyne (1992) ArticleTitleThe genetics of adaptation: a reassessment Am. Nat. 140 725–742

    Google Scholar 

  • H.A. Orr (1999) ArticleTitleThe evolutionary genetics of adaptation: a simulation study Genet. Res. Camb. 74 207–214

    Google Scholar 

  • H.A. Orr A.J. Betancourt (2001) ArticleTitleHaldane’s sieve and adaptation from the standing genetic variation Genetics 157 875–884

    Google Scholar 

  • M.F. Palopoli N.H. Patel (1996) ArticleTitleNeo-Darwinian developmental evolution: can we bridge the gap between pattern and process Curr. Op. Genet. Dev. 6 502–508

    Google Scholar 

  • S.R. Palumbi (2001) ArticleTitleHumans as the world’s greatest evolutionary force Science 293 1786–1790

    Google Scholar 

  • G. Prota (1992) Melanins and Melanogenesis Academic Press Inc. San Diego, CA

    Google Scholar 

  • M. Raymond C. Berticat M. Weill N. Pasteur C. Chevillon (2001) ArticleTitleInsecticide resistance in the mosquito Culex pipiens: what have we learned about adaptation? Genetica 112–113 287–296

    Google Scholar 

  • D.N. Reznick C.K. Ghalambor (2001) ArticleTitleThe population ecology of contemporary adaptations: what empirical studies reveal about the conditions that promote adaptive evolution Genetics 112–113 183–198

    Google Scholar 

  • L.S. Robbins J.H. Nadeau K.R. Johnson M.A. Kelly L. Rosellirehfuss E. Baack K.G. Mountjoy R.D. Cone (1993) ArticleTitlePigmentation phenotypes of variant extension locus alleles result from point mutations that alter receptor function Cell 72 827–834

    Google Scholar 

  • W.K. Silvers (1979) The Coat Colors of Mice: A Model for Mammalian Gene Action and Interaction Springer-Verlag New York

    Google Scholar 

  • G.L. Stebbins SuffixJr. (1950) Variation and Evolution in Plants Columbia University press New York

    Google Scholar 

  • K.P. Steel D.R. Davidson I.J. Jackson (1992) ArticleTitleTRP-2/DT, a new early melnoblast marker shows that the steel growth factor (c-kit ligand) is a survival factor Development 115 1111–1119 Occurrence Handle1:STN:280:ByyD1czkt1I%3D Occurrence Handle1280558

    CAS  PubMed  Google Scholar 

  • J.R.G. Turner (1981) ArticleTitleAdaptation and evolution in Heliconius: a defense of NeoDarwinism Ann. Rev. Ecol. Syst. 12 99–121

    Google Scholar 

  • H. Vrieling D.M.J. Duhl S.E. Millar K.A. Miller G.S. Barsh (1994) ArticleTitleDifferences in dorsal and ventral pigmentation result from regional expression of the mouse agouti gene Proc. Natl. Acad. Sci. 91 5667–5671

    Google Scholar 

  • C. Walsh (2000) ArticleTitleMolecular mechanisms that confer antibacterial drug resistance Nature 406 775–781

    Google Scholar 

  • R.L. Wang A. Stec J. Hey L. Lukens J. Doebley (1999) ArticleTitleThe limits of selection during maize domestication Nature 398 236–239 Occurrence Handle10.1038/18435 Occurrence Handle1:CAS:528:DyaK1MXitVGkt7g%3D Occurrence Handle10094045

    Article  CAS  PubMed  Google Scholar 

  • J.C. Wootton X. Feng M.T. Ferdig R.A. Cooper J. Mu D.I. Baruch A.J. Magill X.Z. Su (2002) ArticleTitleGenetic diversity and chloroquine selective sweeps in Plasmodium falciparum Nature 418 320–323 Occurrence Handle10.1038/nature00813 Occurrence Handle1:CAS:528:DC%2BD38XltlGms7w%3D Occurrence Handle12124623

    Article  CAS  PubMed  Google Scholar 

  • S. Wright (1929) ArticleTitleFisher’s theory of dominance Am. Nat. 63 274–279

    Google Scholar 

  • S. Wright (1931) ArticleTitleEvolution in Mendelian populations Genetics 16 97–159

    Google Scholar 

  • S. Wright (1934) ArticleTitlePhysiological and evolutionary theories of dominance Am. Nat. 68 25–53

    Google Scholar 

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Correspondence to Michael W. Nachman.

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Nachman, M.W. The genetic basis of adaptation: lessons from concealing coloration in pocket mice. Genetica 123, 125–136 (2005). https://doi.org/10.1007/s10709-004-2723-y

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