The origin of interspecific genomic incompatibility via gene duplication

Michael Lynch, A. G. Force

Research output: Contribution to journalArticle

219 Scopus citations

Abstract

One of the great unsolved mysteries of evolutionary biology concerns the genetic mechanisms underlying the origin of genomic incompatibilities between species. Two prevailing thoughts are that such incompatibilities often result from epistatically interacting genes that act as loss-of-function alleles in hybrid backgrounds or from chromosomal rearrangements that result in mis-segregation during meiosis in hybrids. However, it is unclear how genes that cause a radical breakdown in hybrids arise without reducing fitness within species, and numerous cases of speciation appear to be unassociated with obvious chromosomal rearrangements. Here we suggest that duplicate genes, and more generally any kind of genomic redundancies, provide a powerful substrate for the origin of genomic incompatibilities in isolated populations. The divergent resolution of genomic redundancies, such that one population loses function from one copy while the second population loses function from a second copy at a different chromosomal location, leads to chromosomal repatterning such that gametes produced by hybrid individuals can be completely lacking in functional genes for a duplicate pair. Under this model, incompatibility factors accumulate with essentially no loss of fitness within populations as postulated under the Bateson-Dobzhansky-Muller (BDM) model of speciation and despite the fact that they arise from degenerative mutations. However, unlike the situation often envisioned under the BDM model, no change in the mode of gene action in hybrid backgrounds need be invoked. The plausibility of this model derives from a number of recent observations, including the fact that most genomes harbor substantial numbers of gene duplicates whose turnover is common and ongoing process and the fact that many genes have complex regulatory regions that facilitate their divergent resolution in sister taxa.

Original languageEnglish (US)
Pages (from-to)590-605
Number of pages16
JournalAmerican Naturalist
Volume156
Issue number6
DOIs
StatePublished - Dec 1 2000
Externally publishedYes

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Keywords

  • Complementation
  • Gene duplication
  • Gene expression patterns
  • Genomic redundancy
  • Reproductive incompatibility
  • Speciation

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics

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