Skip to main content

Advertisement

SpringerLink
Log in

Parallel genotypic adaptation: when evolution repeats itself

  • Published:
Genetica Aims and scope Submit manuscript

Abstract

Until recently, parallel genotypic adaptation was considered unlikely because phenotypic differences were thought to be controlled by many genes. There is increasing evidence, however, that phenotypic variation sometimes has a simple genetic basis and that parallel adaptation at the genotypic level may be more frequent than previously believed. Here, we review evidence for parallel genotypic adaptation derived from a survey of the experimental evolution, phylogenetic, and quantitative genetic literature. The most convincing evidence of parallel genotypic adaptation comes from artificial selection experiments involving microbial populations. In some experiments, up to half of the nucleotide substitutions found in independent lineages under uniform selection are the same. Phylogenetic studies provide a means for studying parallel genotypic adaptation in non-experimental systems, but conclusive evidence may be difficult to obtain because homoplasy can arise for other reasons. Nonetheless, phylogenetic approaches have provided evidence of parallel genotypic adaptation across all taxonomic levels, not just microbes. Quantitative genetic approaches also suggest parallel genotypic evolution across both closely and distantly related taxa, but it is important to note that this approach cannot distinguish between parallel changes at homologous loci versus convergent changes at closely linked non-homologous loci. The finding that parallel genotypic adaptation appears to be frequent and occurs at all taxonomic levels has important implications for phylogenetic and evolutionary studies. With respect to phylogenetic analyses, parallel genotypic changes, if common, may result in faulty estimates of phylogenetic relationships. From an evolutionary perspective, the occurrence of parallel genotypic adaptation provides increasing support for determinism in evolution and may provide a partial explanation for how species with low levels of gene flow are held together.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • D. Andreev M. Kreitman T.W. Phillips R.W. Beeman R.H. ffrench-Constant (1999) ArticleTitleMultiple origins of cyclodiene insecticide resistance in Tribolium castaneum (Coleoptera: Tenbrionidae) J. Mol. Evol. 48 615–624

    Google Scholar 

  • M. Barlow B.G. Hall (2002) ArticleTitlePredicting evolutionary potential: in vitro evolution accurately reproduces natural evolution of the TEM β-lactamase Genetics 160 823–832

    Google Scholar 

  • M. Barlow B.G. Hall (2003) ArticleTitleExperimental prediction of the natural evolution of antibiotic resistance Genetics 163 1237–1241

    Google Scholar 

  • P. Bernasconi A.R. Woodworth B.A. Rosen M.V. Subramanian D.L. Siehl (1995) ArticleTitleA naturally occurring point mutation confers broad range tolerance to herbicides that target acetolactate synthase J. Biol. Chem. 270 17381–17385

    Google Scholar 

  • E.G. Brown H. Liu L. Chang Kit S. Baird M. Nesrallah (2001) ArticleTitlePattern of mutation in the genome of influenza A virus on adaptation to increased virulence in the mouse lung: identification of functional themes Proc. Natl. Acad. Sci. U.S.A. 98 6883–6888

    Google Scholar 

  • J.J. Bull M.R. Badgett H.A. Wichman J.P. Huelsenbeck D.M. Hillis A. Gulati C. Ho I.J. Molineux (1997) ArticleTitleExceptional convergent evolution in a virus Genetics 147 1497–1507

    Google Scholar 

  • L. Chen A.L. DeVries C.-H.C. Cheng (1997) ArticleTitleConvergent evolution of antifreeze glycoproteins in Antarctic notothenioid fish & Arctic cod Proc. Natl. Acad. Sci. U.S.A. 94 3817–3822

    Google Scholar 

  • J.A. Coyne R. Lande (1985) ArticleTitleThe genetic basis of species differences in plants Am. Nat. 126 141–145

    Google Scholar 

  • W.D. Crill H.A. Wichman J.J. Bull (2000) ArticleTitleEvolutionary reversals during viral adaptation to alternating hosts Genetics 154 27–37

    Google Scholar 

  • C.W. Cunningham K. Jeng J. Husti M. Badgett I.J. Molineux D.M. Hillis J.J. Bull (1997) ArticleTitleParallel molecular evolution of deletions & nonsense mutations in bacteriophage T7 Mol. Biol. Evol. 14 113–116

    Google Scholar 

  • R.F. Doolittle (1994) ArticleTitleConvergent evolution: the need to be explicit Trends Biochem. Sci. 19 15–18

    Google Scholar 

  • S.R. Downie J.D. Palmer (1992) Use of chloroplast DNA rearrangements in reconstructing plant phylogeny P.S. Soltis D.E. Soltis J.J. Doyle (Eds) Molecular Systematics of Plants Chapman & Hall N.Y

    Google Scholar 

  • L. Elard A.M. Comes J.F. Humbert (1996) ArticleTitleSequences of B-tubulin cDNA from benzimidazole-susceptible and -resistant strains of Teladorsagia cirumcincta, a nematode parasite of small ruminants Mol. Biochem. Parasitol. 79 249–253

    Google Scholar 

  • J.A. Endler (1986) Natural Seleciton in the Wild Princeton University Press Princeton

    Google Scholar 

  • P.R. Ehrlich P.H. Raven (1969) ArticleTitleDifferentiation of populations Science 165 1228–1232

    Google Scholar 

  • C.A. Fatokun D.I. Menancio-Hautea D. Danesh N.D. Young (1992) ArticleTitleEvidence for orthologous seed weight genes in cowpea & mung bean based on RFLP mapping Genetics 132 841–846

    Google Scholar 

  • R.H. ffrench-Constant (1994) ArticleTitleThe molecular & population genetics of cyclodiene insecticide resistance Insect Bicochem. Mol. Biol. 24 335–345

    Google Scholar 

  • P.L. Forey C.J. Humphries I.L. Kitching R.W. Scotland D.J. Siebert D.M. Williams (1992) Cladistics Oxford University Press NY

    Google Scholar 

  • C.J. Goodnight (2000) ArticleTitleQuantitative trait loci & gene interaction: the quantitative genetics of metapopulations Heredity 84 587–598

    Google Scholar 

  • L.D. Gottlieb (1984) ArticleTitleGenetics & morphological evolution in plants Am. Nat. 123 681–709

    Google Scholar 

  • V. Grant (1980) ArticleTitleGene flow and the homogeneity of species populations Biol. Zentralbl. 99 157–169

    Google Scholar 

  • J.B.S. Haldane (1932) The Causes of Evolution Longmans Green London

    Google Scholar 

  • K.W. Hilu (1983) ArticleTitleThe role of single-gene mutations in the evolution of flowering plants Evol. Biol. 36 97–128

    Google Scholar 

  • F.Y. Hu D.Y. Tao E. Sacks B.Y. Fu P. Xu J. Li Y. Yang K. McNally G.S. Khush A.H. Paterson Z.-K. Li (2003) ArticleTitleConvergent evolution of perenniality in rice & sorghum Proc. Natl. Acad. Sci. U.S.A. 100 4050–4054

    Google Scholar 

  • U. Johanson J. West C. Lister S. Michaels R. Amasino C. Dean (2001) ArticleTitleMolecular analysis of FRIGIDA, a major determinant of natural variation in Arabidopsis flowering time Science 290 344–347

    Google Scholar 

  • E. Jouvin-Marche A. Cuddihy S. Butler J.N. Hansen W.M. Fitch S. Rudikoff (1988) ArticleTitleModern Evolution of a single-copy gene: the immunoglobulin Ck locus in wild mice Mol. Biol. Evol. 5 500–511

    Google Scholar 

  • N. Kermarrec F. Roubinet P.-A. Apoil A. Blancher (1999) ArticleTitleComparison of allele O sequences of the human & non-human primate ABO system Immunogenetics 49 517–526

    Google Scholar 

  • K. Kriener C. O’hUigin H. Tichy J. Klein (2000) ArticleTitleConvergent evolution of major histocompatibility complex molecules in humans & New World monkeys Immunogenetics 51 169–178

    Google Scholar 

  • R. Lande (1983) ArticleTitleThe response to selection on major & minor mutations affecting a metrical trait Heredity 50 47–65

    Google Scholar 

  • B.R. Levin V. Perrot N. Walker (2000) ArticleTitleCompensatory mutations, antibiotic resistance & the population genetics of adaptive evolution in bacteria Genetics 154 985–997

    Google Scholar 

  • D.A. Levin (2000) The Origin, Expansion, & Demise of Plant Species Oxford University Press NY

    Google Scholar 

  • D.A. Levin (2001) ArticleTitleThe recurrent origin of plant races & species Syst. Bot. 26 197–204

    Google Scholar 

  • H. Liao T. McKenzie R. Hageman (1986) ArticleTitleIsolation of a thermostable enzyme variant by cloning & selection in a thermophile Proc. Natl. Acad. Sci. U.S.A. 83 576–580

    Google Scholar 

  • A.S. Low F.M. MacKenzie I.M. Gould I.R. Booth (2001) ArticleTitleProtected environments allow parallel evolution of a bacterial pathogen in a patient subjected to long-term antibiotic therapy Mol. Microbiol. 42 619–630

    Google Scholar 

  • M. Lynch J.S. Conery (2000) ArticleTitleThe evolutionary fate & consequences of duplicate genes Science 290 1151–1155 Occurrence Handle10.1126/science.290.5494.1151 Occurrence Handle1:CAS:528:DC%2BD3cXotVChsb8%3D Occurrence Handle11073452

    Article  CAS  PubMed  Google Scholar 

  • I. Malcuit W. Jong ParticleDe D.C. Baulcombe D.C. Shields T.A. Kavanagh (2000) ArticleTitleAcquisition of multiple virulence/avirulence determinants by potato virus X (PVX) has occurred through convergent evolution rather than through recombination Virus Genes 20 165–172

    Google Scholar 

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

    Google Scholar 

  • A. Molla M. Korneyeva Q. Gao S. Vasavanonda P.J. Schipper et al. (1996) ArticleTitleOrdered accumulation of mutations in HIV protease confers resistance to ritonavir Nat. Med. 2 760–766

    Google Scholar 

  • A. Morris J.K. Bowmaker D.M. Hunt (1993) ArticleTitleThe molecular basis of a spectral shift in the rhodopsins of two species of squid from different photic environments Proc. R. Soc. Lond. Ser. B Biol. Sci. 254 233–240

    Google Scholar 

  • S. Ohno (1970) Evolution by Gene Duplication Springer Berlin

    Google Scholar 

  • C. O’hUigin A. Sato J. Klein (1997) ArticleTitleEvidence for convergent evolution of A & B blood group antigens in primates Hum. Genet. 101 141–148

    Google Scholar 

  • E. Palacios L. Digilio H.M. McClure Z. Chen P.A. Marx M.A. Goldsmith R.M. Grant (1998) ArticleTitleParallel evolution of CCR5-null phenotypes in humans & in a natural host of simian immunodeficiency virus Curr. Biol. 8 943–946

    Google Scholar 

  • A.H. Paterson Y.-R. Lin Z. Li K.F. Schertz J.F. Doebley S.R.M. Pinson S.-C. Liu J.W. Stansel J.E. Irivine (1995) ArticleTitleConvergent domestication of cereal crops by independent mutations at corresponding genetic loci Science 269 1714–1718 Occurrence Handle1:CAS:528:DyaK2MXot1aitbg%3D

    CAS  Google Scholar 

  • S.D. Reid C.J. Herbelin A.C. Bumbaugh R.K. Selander T.S. Whittam (2000) ArticleTitleParallel evolution of virulence in pathogenic Escherichia coli Nature 406 64–67

    Google Scholar 

  • W.R. Rice E.E. Hostert (1993) ArticleTitleLaboratory experiments on speciation: what have we learned in 40 years Evolution 47 1637–1653

    Google Scholar 

  • M.M. Riehle A.F. Bennett A.D. Long (2001) ArticleTitleGenetic architecture of thermal adaptation in Escherichia coli Proc. Natl. Acad. Sci. U.S.A. 98 525–530

    Google Scholar 

  • L.H. Rieseberg B. Sinervo C.R. Linder M.C. Ungerer D.M. Arias (1996) ArticleTitleRole of gene interactions in hybrid speciation: evidence from ancient & experimental hybrids Science 272 741–745

    Google Scholar 

  • L.H. Rieseberg J.M. Burke (2001) ArticleTitleThe biological reality of species: gene flow, selection, & collective evolution Taxon 50 47–67

    Google Scholar 

  • A.E. Romero-Herrera H. Lehmann K.A. Josey A.E. Friday (1978) ArticleTitleOn the evolution of myoglobin Philos. Trans. R Soc. Lond. Ser. B Biol. Sci. 283 61–163

    Google Scholar 

  • H.D. Rundle L. Nagel J.W. Boughman D. Schluter (2000) ArticleTitleNatural selection & parallel speciation in sympatric sticklebacks Science 287 306–308 Occurrence Handle10.1126/science.287.5451.306

    Article  Google Scholar 

  • N. Saitou F. Yamamoto (1997) ArticleTitleEvolution of primate ABO blood group genes & their homologous genes Mol. Biol. Evol. 14 399–411

    Google Scholar 

  • H. Schat R. Voous E. Kuiper (1996) ArticleTitleIdentical major gene loci for heavy metal tolerances that have independently evolved in different local populations & subspecies of Silene vulagaris Evolution 50 1888–1895

    Google Scholar 

  • D. Schluter (1996) ArticleTitleAdaptive radiation along genetic lines of least resistance Evolution 50 1766–1774

    Google Scholar 

  • D. Schluter (2001) ArticleTitleEcology & the origin of species Trends Ecol. Evol. 16 372–380

    Google Scholar 

  • J. Shafqat M. El-Ahmad O. Danielsson M.C. Martinez B. Persson X. Pares H. Jornvall (1996) ArticleTitlePea formaldehyde-active class III alcohol dehydrogenase: common derivation of the plant & animal forms but not of the corresponding ethanol-active forms (classes I & P) Proc. Natl. Acad. Sci. U.S.A. 93 5595–5599

    Google Scholar 

  • S.-K. Shyue D. Hewett-Emmett H.G. Sperling D.M. Hunt J.K. Bowmaker J.D. Mollon W.-H. Li (1995) ArticleTitleAdaptive evolution of color vision genes in higher primates Science 269 1265–1267

    Google Scholar 

  • G.G. Simpson (1961) Principles of Animal Taxonomy Columbia University Press New York

    Google Scholar 

  • P.S. Soltis D.S. Soltis (1991) ArticleTitleMultiple origins of the allotetraploid Tragopogon mirus (Compositae): rDNA evidence Syst. Bot. 16 407–413

    Google Scholar 

  • C.-B. Stewart J.W. Schilling A.C. Wilson (1987) ArticleTitleAdaptive evolution in the stomach lysozymes of foregut fermenters Nature 330 401–404

    Google Scholar 

  • E. Sucena I. Delon I. Jones F. Payre D.L. Stern (2003) ArticleTitleRegulatory evolution of shavenbaby/ovo underlies multiple cases of morphological parallelism Nature 424 935–938

    Google Scholar 

  • S.D. Tanksley (1993) ArticleTitleMapping polygenes Annual Rev. Genet. 27 205–233

    Google Scholar 

  • A.R. Templeton (1989) The meaning of species & speciation: a genetic perspective D. Otte J.A. Endler (Eds) Speciation & Its Consequences Sunderland MA 3–27

    Google Scholar 

  • M. Ungerer (2000) Selection, genetic envrionment & adaptive evolution: an analysis of microevolutionary dynamics in experimental plant populations Indiana Univ. Bloomington

    Google Scholar 

  • M.J. Wade C.J. Goodnight (1998) ArticleTitlePerspective: the theories of Fisher & Wright in the context of metapopulations: when nature does many small experiments Evolution 52 1537–1553

    Google Scholar 

  • R.S. Wells (1996) ArticleTitleExcessive homoplasy in an evolutionarily constrained protein Proc. R. Soc. Lond. Ser. B Biol. Sci. 263 393–400

    Google Scholar 

  • H.A. Wichman M.R. Badgett L.A. Scott C.M. Boulianne J.J. Bull (2001) ArticleTitleDifferent trajectories of parallel evolution during viral adaptation Science 285 422–424

    Google Scholar 

  • R. Yokoyama S. Yokoyama (1990) ArticleTitleConvergent evolution of the red- & green-like visual pigment genes in fish, Astyanax fasciatus & human Proc. Natl. Acad. Sci. U.S.A. 87 9315–9318

    Google Scholar 

  • J. Zhang S. Kumar (1997) ArticleTitleDetection of convergent & parallel evolution at the amino acid sequence level Mol. Biol. Evol. 14 527–536

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Indiana University, 1001 E. Third St, Jordan Hall 142, Bloomington, IN, 47405, U.S.A

    Troy E. Wood & Loren H. Rieseberg

  2. Department of Biological Sciences, Vanderbilt University, VU Station B 351634, Nashville, TN, 37235, U.S.A

    John M. Burke

Authors
  1. Troy E. Wood
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. John M. Burke
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Loren H. Rieseberg
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Troy E. Wood.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wood, T.E., Burke, J.M. & Rieseberg, L.H. Parallel genotypic adaptation: when evolution repeats itself. Genetica 123, 157–170 (2005). https://doi.org/10.1007/s10709-003-2738-9

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10709-003-2738-9

Keywords

Search

Navigation