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.
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
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
M. Barlow B.G. Hall (2003) ArticleTitleExperimental prediction of the natural evolution of antibiotic resistance Genetics 163 1237–1241
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
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
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
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
J.A. Coyne R. Lande (1985) ArticleTitleThe genetic basis of species differences in plants Am. Nat. 126 141–145
W.D. Crill H.A. Wichman J.J. Bull (2000) ArticleTitleEvolutionary reversals during viral adaptation to alternating hosts Genetics 154 27–37
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
R.F. Doolittle (1994) ArticleTitleConvergent evolution: the need to be explicit Trends Biochem. Sci. 19 15–18
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
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
J.A. Endler (1986) Natural Seleciton in the Wild Princeton University Press Princeton
P.R. Ehrlich P.H. Raven (1969) ArticleTitleDifferentiation of populations Science 165 1228–1232
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
R.H. ffrench-Constant (1994) ArticleTitleThe molecular & population genetics of cyclodiene insecticide resistance Insect Bicochem. Mol. Biol. 24 335–345
P.L. Forey C.J. Humphries I.L. Kitching R.W. Scotland D.J. Siebert D.M. Williams (1992) Cladistics Oxford University Press NY
C.J. Goodnight (2000) ArticleTitleQuantitative trait loci & gene interaction: the quantitative genetics of metapopulations Heredity 84 587–598
L.D. Gottlieb (1984) ArticleTitleGenetics & morphological evolution in plants Am. Nat. 123 681–709
V. Grant (1980) ArticleTitleGene flow and the homogeneity of species populations Biol. Zentralbl. 99 157–169
J.B.S. Haldane (1932) The Causes of Evolution Longmans Green London
K.W. Hilu (1983) ArticleTitleThe role of single-gene mutations in the evolution of flowering plants Evol. Biol. 36 97–128
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
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
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
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
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
R. Lande (1983) ArticleTitleThe response to selection on major & minor mutations affecting a metrical trait Heredity 50 47–65
B.R. Levin V. Perrot N. Walker (2000) ArticleTitleCompensatory mutations, antibiotic resistance & the population genetics of adaptive evolution in bacteria Genetics 154 985–997
D.A. Levin (2000) The Origin, Expansion, & Demise of Plant Species Oxford University Press NY
D.A. Levin (2001) ArticleTitleThe recurrent origin of plant races & species Syst. Bot. 26 197–204
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
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
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
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
R. Mauricio (2001) ArticleTitleMapping quantitative trait loci in plants: uses & caveats for evolutionary biology Nat. Rev. Genet. 2 370–381
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
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
S. Ohno (1970) Evolution by Gene Duplication Springer Berlin
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
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
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
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
W.R. Rice E.E. Hostert (1993) ArticleTitleLaboratory experiments on speciation: what have we learned in 40 years Evolution 47 1637–1653
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
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
L.H. Rieseberg J.M. Burke (2001) ArticleTitleThe biological reality of species: gene flow, selection, & collective evolution Taxon 50 47–67
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
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
N. Saitou F. Yamamoto (1997) ArticleTitleEvolution of primate ABO blood group genes & their homologous genes Mol. Biol. Evol. 14 399–411
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
D. Schluter (1996) ArticleTitleAdaptive radiation along genetic lines of least resistance Evolution 50 1766–1774
D. Schluter (2001) ArticleTitleEcology & the origin of species Trends Ecol. Evol. 16 372–380
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
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
G.G. Simpson (1961) Principles of Animal Taxonomy Columbia University Press New York
P.S. Soltis D.S. Soltis (1991) ArticleTitleMultiple origins of the allotetraploid Tragopogon mirus (Compositae): rDNA evidence Syst. Bot. 16 407–413
C.-B. Stewart J.W. Schilling A.C. Wilson (1987) ArticleTitleAdaptive evolution in the stomach lysozymes of foregut fermenters Nature 330 401–404
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
S.D. Tanksley (1993) ArticleTitleMapping polygenes Annual Rev. Genet. 27 205–233
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
M. Ungerer (2000) Selection, genetic envrionment & adaptive evolution: an analysis of microevolutionary dynamics in experimental plant populations Indiana Univ. Bloomington
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
R.S. Wells (1996) ArticleTitleExcessive homoplasy in an evolutionarily constrained protein Proc. R. Soc. Lond. Ser. B Biol. Sci. 263 393–400
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
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
J. Zhang S. Kumar (1997) ArticleTitleDetection of convergent & parallel evolution at the amino acid sequence level Mol. Biol. Evol. 14 527–536
Author information
Authors and Affiliations
Corresponding author
Rights 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
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/s10709-003-2738-9