Data supporting the occurrence of adaptive trait transfer (i.e. the transfer of genes and thus the phenotype of an adaptive trait through viral recombination, lateral gene transfer or introgressive hybridization) are provided in this review. Specifically, we discuss examples of lateral gene transfer and introgressive hybridization that have resulted in the transfer or de novo origin of adaptations. The evolutionary clades in which this process has been identified include all types of organisms. However, we restrict our discussion to bacteria, fungi, plants and animals. Each of these examples reflects the same consequence, namely that the transfer of genetic material, through whatever mechanism, may result in adaptive evolution. In particular, each of the events discussed has been inferred to impact adaptations to novel environmental settings in the recipient lineage.

References

Anderson E. 1948Hybridization of the habitat. Evolution. 2, 1–9.doi:10.2307/2405610. . Crossref, ISI, Google Scholar
Anderson EIntrogressive hybridization. 1949New York, NY:Wiley. Google Scholar
Anderson E& Hubricht L. 1938Hybridization in Tradescantia. III. The evidence for introgressive hybridization. Am. J. Bot. 25, 396–402.doi:10.2307/2436413. . Crossref, Google Scholar
Arnold M.LNatural hybridization and evolution. 1997Oxford, UK:Oxford University Press. Google Scholar
Arnold M.LEvolution through genetic exchange. 2006Oxford, UK:Oxford University Press. Google Scholar
Arnold M.L& Larson E.J. 2004Evolution's new look. Wils. Q. (Autumn)60–72. Google Scholar
Arnold M.L& Meyer A. 2006Natural hybridization in primates: one evolutionary mechanism. Zoology. 109, 261–276.doi:10.1016/j.zool.2006.03.006. . Crossref, PubMed, ISI, Google Scholar
Borge T, Lindroos K, Nádvorník P, Syvänen A.-C& Sætre G.-P. 2005Amount of introgression in flycatcher hybrid zones reflects regional differences in pre and post-zygotic barriers to gene exchange. J. Evol. Biol. 18, 1416–1424. Crossref, PubMed, ISI, Google Scholar
Bouck A.C, Peeler R, Arnold M.L& Wessler S.R. 2005Genetic mapping of species boundaries in Louisiana irises using IRRE retrotransposon display markers. Genetics. 171, 1289–1303.doi:10.1534/genetics.105.044552. . Crossref, PubMed, ISI, Google Scholar
Brasier C.M. 2001Rapid evolution of introduced plant pathogens via interspecific hybridization. BioScience. 51, 123–133.doi:10.1641/0006-3568(2001)051[0123:REOIPP]2.0.CO;2. . Crossref, ISI, Google Scholar
Brasier C.M& Kirk S.A. 2001Designation of the EAN and NAN races of Ophiostoma novo-ulmi as subspecies. Mycol. Res. 105, 547–554.doi:10.1017/S0953756201004087. . Crossref, Google Scholar
Brumfield R.T, Jernigan R.W, McDonald D.B& Braun M.J. 2001Evolutionary implications of divergent clines in an avian (Manacus: Aves) hybrid zone. Evolution. 55, 2070–2087.doi:10.1111/j.0014-3820.2001.tb01322.x. . Crossref, PubMed, ISI, Google Scholar
Claesson M.J, et al.2006Multireplicon genome architecture of Lactobacillus salivarius. Proc. Natl Acad. Sci. USA. 103, 6718–6723.doi:10.1073/pnas.0511060103. . Crossref, PubMed, ISI, Google Scholar
Cornman R.S, Burke J.M, Wesselingh R.A& Arnold M.L. 2004Contrasting genetic structure of adults and progeny in a Louisiana iris hybrid population. Evolution. 58, 2669–2681.doi:10.1554/04-321. . Crossref, PubMed, ISI, Google Scholar
Cruzan M.B& Arnold M.L. 1993Ecological and genetic associations in an Iris hybrid zone. Evolution. 47, 1432–1445.doi:10.2307/2410158. . Crossref, PubMed, ISI, Google Scholar
Doolittle W.F& Bapteste E. 2007Pattern pluralism and the Tree of Life hypothesis. Proc. Natl Acad. Sci. USA. 104, 2043–2049.doi:10.1073/pnas.0610699104. . Crossref, PubMed, ISI, Google Scholar
Evans P.D, Anderson J.R, Vallender E.J, Choi S.S& Lahn B.T. 2004Reconstructing the evolutionary history of microcephalin, a gene controlling human brain size. Hum. Mol. Genet. 13, 1139–1145.doi:10.1093/hmg/ddh126. . Crossref, PubMed, ISI, Google Scholar
Evans P.D, Gilbert S.L, Mekel-Bobrov N, Vallender E.J, Anderson J.R, Vaez-Azizi L.M, Tishkoff S.A, Hudson R.R& Lahn B.T. 2005Microcephalin, a gene regulating brain size, continues to evolve adaptively in humans. Science. 309, 1717–1720.doi:10.1126/science.1113722. . Crossref, PubMed, ISI, Google Scholar
Evans P.D, Mekel-Bobrov N, Vallender E.J, Hudson R.R& Lahn B.T. 2006Evidence that the adaptive allele of the brain size gene microcephalin introgressed into Homo sapiens from an archaic Homo lineage. Proc. Natl Acad. Sci. USA. 103, 18 178–18 183.doi:10.1073/pnas.0606966103. . Crossref, ISI, Google Scholar
Finlayson C. 2005Biogeography and evolution of the genus Homo. Trends Ecol. Evol. 20, 457–463.doi:10.1016/j.tree.2005.05.019. . Crossref, PubMed, ISI, Google Scholar
Flynn S, van Sinderen D, Thornton G.M, Holo H, Nes I.F& Collins J.K. 2002Characterization of the genetic locus responsible for the production of ABP-118, a novel bacteriocin produced by the probiotic bacterium Lactobacillus salivarius subsp. salivarius UCC118. Microbiology. 148, 973–984. Crossref, PubMed, ISI, Google Scholar
Garrigan D, Mobasher Z, Severson T, Wilder J.A& Hammer M.F. 2005Evidence for archaic Asian ancestry on the human X chromosome. Mol. Biol. Evol. 22, 189–192.doi:10.1093/molbev/msi013. . Crossref, PubMed, ISI, Google Scholar
Grant P.R& Grant B.R. 1992Hybridization of bird species. Science. 256, 193–197.doi:10.1126/science.256.5054.193. . Crossref, PubMed, ISI, Google Scholar
Grant B.R& Grant P.R. 2008Fission and fusion of Darwin's finches populations. Phil. Trans. R. Soc. B. 363, 2821–2829.doi:10.1098/rstb.2008.0051. . Link, ISI, Google Scholar
Jackson A.P, et al.2002Identification of microcephalin, a protein implicated in determining the size of the human brain. Am. J. Hum. Genet. 71, 136–142.doi:10.1086/341283. . Crossref, PubMed, ISI, Google Scholar
Jiggins C.D, McMillan W.O, King P& Mallet J. 1997The maintenance of species differences across a Heliconius hybrid zone. Heredity. 79, 495–505. Crossref, ISI, Google Scholar
Jiggins C.D, Naisbit R.E, Coe R.L& Mallet J. 2001Reproductive isolation caused by colour pattern mimicry. Nature. 411, 302–305.doi:10.1038/35077075. . Crossref, PubMed, ISI, Google Scholar
Jiggins C.D, Mallarino R, Willmott K.R& Bermingham E. 2006The phylogenetic pattern of speciation and wing pattern change in neotropical Ithomia butterflies (Lepidoptera: Nymphalidae). Evolution. 60, 1454–1466.doi:10.1554/05-483.1. . Crossref, PubMed, ISI, Google Scholar
Johnston J.A, Wesselingh R.A, Bouck A.C, Donovan L.A& Arnold M.L. 2001Intimately linked or hardly speaking? The relationship between genotypic variation and environmental gradients in a Louisiana iris hybrid population. Mol. Ecol. 10, 673–681.doi:10.1046/j.1365-294x.2001.01217.x. . Crossref, PubMed, ISI, Google Scholar
Jolly C.J. 2001A proper study for mankind: analogies from the papionin monkeys and their implications for human evolution. Yearb. Phys. Anthropol. 44, 177–204.doi:10.1002/ajpa.10021. . Crossref, Google Scholar
Jordan I.K, Makarova K.S, Spouge J.L, Wolf Y.I& Koonin E.V. 2001Lineage-specific gene expansions in bacterial and archaeal genomes. Genome Res. 11, 555–565.doi:10.1101/gr.GR-1660R. . Crossref, PubMed, ISI, Google Scholar
Kentner E.K, Arnold M.L& Wessler S.R. 2003Characterization of high copy number retrotransposons from the large genomes of the Louisiana iris species and their use as molecular markers. Genetics. 164, 685–697. Crossref, PubMed, ISI, Google Scholar
Kronforst M.R, Young L.G, Blume L.M& Gilbert L.E. 2006Multilocus analyses of admixture and introgression among hybridizing Heliconius butterflies. Evolution. 60, 1254–1268. Crossref, PubMed, ISI, Google Scholar
Makarova K, et al.2006Comparative genomics of the lactic acid bacteria. Proc. Natl Acad. Sci. USA. 103, 15 611–15 616.doi:10.1073/pnas.0607117103. . Crossref, ISI, Google Scholar
Mallet J. 2005Hybridization as an invasion of the genome. Trends Ecol. Evol. 20, 229–237.doi:10.1016/j.tree.2005.02.010. . Crossref, PubMed, ISI, Google Scholar
Martin N.H, Bouck A.C& Arnold M.L. 2005Loci affecting long-term hybrid survivability in Louisiana irises: implications for reproductive isolation and introgression. Evolution. 59, 2116–2124. Crossref, PubMed, ISI, Google Scholar
Martin N.H, Bouck A.C& Arnold M.L. 2006Detecting adaptive trait introgression between Iris fulva and I. brevicaulis in highly selective field conditions. Genetics. 172, 2481–2489.doi:10.1534/genetics.105.053538. . Crossref, PubMed, ISI, Google Scholar
Mavárez J, Salazar C.A, Bermingham E, Salcedo C, Jiggins C.D& Linares M. 2006Speciation by hybridization in Heliconius butterflies. Nature. 441, 868–871.doi:10.1038/nature04738. . Crossref, PubMed, ISI, Google Scholar
McCarthy J, et al.2003Double blind, placebo controlled trial of two probiotic strains in interleukin 10 knockout mice and mechanistic link with cytokine balance. Gut. 52, 975–980.doi:10.1136/gut.52.7.975. . Crossref, PubMed, ISI, Google Scholar
McDonald D.B, Clay R.P, Brumfield R.T& Braun M.J. 2001Sexual selection on plumage and behavior in an avian hybrid zone: experimental tests of male–male interactions. Evolution. 55, 1443–1451.doi:10.1111/j.0014-3820.2001.tb00664.x. . Crossref, PubMed, ISI, Google Scholar
Navarro A& Barton N.H. 2003Chromosomal speciation and molecular divergence—accelerated evolution in rearranged chromosomes. Science. 300, 321–324.doi:10.1126/science.1080600. . Crossref, PubMed, ISI, Google Scholar
Ochman H. 2005Genomes on the shrink. Proc. Natl Acad. Sci. USA. 102, 11 959–11 960.doi:10.1073/pnas.0505863102. . Crossref, ISI, Google Scholar
Ochman H, Lawrence J.G& Groisman E.A. 2000Lateral gene transfer and the nature of bacterial innovation. Nature. 405, 299–304.doi:10.1038/35012500. . Crossref, PubMed, ISI, Google Scholar
Osada N& Wu C.-I. 2005Inferring the mode of speciation from genomic data: a study of the great apes. Genetics. 169, 259–264.doi:10.1534/genetics.104.029231. . Crossref, PubMed, ISI, Google Scholar
Paoletti M, Buck K.W& Brasier C.M. 2006Selective acquisition of novel mating type and vegetative incompatibility genes via interspecies gene transfer in the globally invading eukaryote Ophiostoma novo-ulmi. Mol. Ecol. 15, 249–262.doi:10.1111/j.1365-294X.2005.02728.x. . Crossref, PubMed, ISI, Google Scholar
Parsons T.J, Olson S.L& Braun M.J. 1993Unidirectional spread of secondary sexual plumage traits across an avian hybrid zone. Science. 260, 1643–1646.doi:10.1126/science.260.5114.1643. . Crossref, PubMed, ISI, Google Scholar
Rieseberg L.H. 1997Hybrid origins of plant species. Annu. Rev. Ecol. Syst. 28, 359–389.doi:10.1146/annurev.ecolsys.28.1.359. . Crossref, Google Scholar
Riley H.P. 1938A character analysis of colonies of Iris fulva, Iris hexagona var. giganticaerulea and natural hybrids. Am. J. Bot. 25, 727–738.doi:10.2307/2436599. . Crossref, Google Scholar
Riley M.A& Wertz J.E. 2002Bacteriocin diversity: ecological and evolutionary perspectives. Biochimie. 84, 357–364.doi:10.1016/S0300-9084(02)01421-9. . Crossref, PubMed, ISI, Google Scholar
Sætre G.-P, Borge T, Lindell J, Moum T, Primmer C.R, Sheldon B.C, Johnsen A& Ellegren H. 2001Speciation, introgressive hybridization and nonlinear rate of molecular evolution in flycatchers. Mol. Ecol. 10, 737–749.doi:10.1046/j.1365-294x.2001.01208.x. . Crossref, PubMed, ISI, Google Scholar
Sætre G.-P, Borge T, Lindroos K, Haavie J, Sheldon B.C, Primmer C& Syvänen A.-C. 2003Sex chromosome evolution and speciation in Ficedula flycatchers. Proc. R. Soc. B. 270, 53–59.doi:10.1098/rspb.2002.2204. . Link, ISI, Google Scholar
Seehausen O. 2004Hybridization and adaptive radiation. Trends Ecol. Evol. 19, 198–207.doi:10.1016/j.tree.2004.01.003. . Crossref, PubMed, ISI, Google Scholar
Sheil B, McCarthy J, O'Mahony L, Bennett M.W, Ryan P, Fitzgibbon J.J, Kiely B, Collins J.K& Shanahan F. 2004Is the mucosal route of administration essential for probiotic function? Subcutaneous administration is associated with attenuation of murine colitis and arthritis. Gut. 53, 694–700.doi:10.1136/gut.2003.027789. . Crossref, PubMed, ISI, Google Scholar
Stein A.C& Uy J.A.C. 2006Unidirectional introgression of a sexually selected trait across an avian hybrid zone: a role for female choice?. Evolution. 60, 1476–1485.doi:10.1554/05-575.1. . PubMed, ISI, Google Scholar
Stringer C.B& Andrews P. 1988Genetic and fossil evidence for the origin of modern humans. Science. 239, 1263–1268.doi:10.1126/science.3125610. . Crossref, PubMed, ISI, Google Scholar
Tegelström H& Gelter H.P. 1990Haldane's rule and sex biased gene flow between two hybridizing flycatcher species (Ficedula albicollis and F. hypoleuca, Aves: Muscicapidae). Evolution. 44, 2012–2021.doi:10.2307/2409611. . PubMed, ISI, Google Scholar
Viosca P. 1935The irises of southeastern Louisiana—a taxonomic and ecological interpretation. Bull. Am. Iris Soc. 57, 3–56. Google Scholar
Wang Y.-Q& Su B. 2004Molecular evolution of microcephalin, a gene determining human brain size. Hum. Mol. Genet. 13, 1131–1137.doi:10.1093/hmg/ddh127. . Crossref, PubMed, ISI, Google Scholar

This Issue

Philosophical Transactions of the Royal Society B: Biological Sciences cover image

12 September 2008

Volume 363Issue 1505

Theme Issue ‘Hybridization in animals: extent, processes and evolutionary impact’ compiled by Klaus Schwenk, Nora Brede and Bruno Streit

Article Information

DOI:https://doi.org/10.1098/rstb.2008.0021
PubMed:18522920
Published by:Royal Society
Print ISSN:0962-8436
Online ISSN:1471-2970

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Published online16/06/2008
Published in print12/09/2008

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