Speciation with gene flow

Long Z, Zhang X, Yu Y, Owens GL, Rennison DJ, Palma‐Silva C, Ortiz‐Barrientos D and Rieseberg LH

Plants People Planet
https://doi.org/10.1002/ppp3.70144

Abstract

Societal Impact Statement

Biodiversity is threatened by human activities, with extinction debt accumulating rapidly. Many of these activities change the connectivity of populations, fragmenting existing population systems or bringing previously isolated populations or species into contact. Speciation research offers insights into both the short- and long-term outcomes of changes in isolation and connectivity and thus provides fundamental knowledge that can inform biodiversity management. Here, we review what is known about the role of gene flow in speciation, highlighting that gene flow does not appear to be a major impediment to speciation in plants and instead often contributes to diversification.

Summary

  • The likelihood of speciation with gene flow represents one of the longest running debates in evolutionary biology. Gene flow can hamper speciation by disrupting associations between loci under divergent natural selection and those causing assortative mating. Conversely, variation introduced by gene flow can facilitate speciation, and some modes of speciation require interspecific gene flow.
  • Here, we first describe the history of this debate. Next, we review theoretical models of speciation with gene flow, along with empirical evidence, emphasizing studies of plants. Our review includes both primary divergence with gene flow, as well as gene flow following secondary contact, including different forms of hybrid speciation.
  • We find that plants have several characteristics that can promote the formation of associations between ecological and assortative mating traits, including magic traits (divergently selected traits that also cause assortative mating) and abundant recombination suppressors, such as inversions. Biogeographic studies of several plant groups show patterns of greater range overlap and range asymmetry in sister species compared with more distantly related species. This pattern suggests that geographic isolation is not required for speciation in plants and also that speciation by budding may be important. Genomic data further indicate that gene flow is frequent, but often intermittent, during the speciation process in plants and that speciation triggered by secondary gene flow (introgression) is common.
  • We conclude that Darwin's skepticism about the necessity of geographic isolation in speciation is warranted, especially in the plant kingdom.
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