Role of Natural Selection in Chromosomal Speciation

Abstract

Abstract Speciation can occur in the face of gene flow if there are mechanisms that are able to neutralise it. Two such mechanisms or forces are divergent selection and the suppression of recombination. New data and theory suggest that chromosomal rearrangements (CRs) facilitate speciation with gene flow mainly by suppressing recombination. However, the role of natural selection in chromosomal speciation is less clear. According to recent models, natural selection can play a role in speciation by facilitating the fixation of CRs; and later, acting synergistically with CRs, by allowing the accumulation of incompatibilities along large regions of the genome. Interestingly, instead of resulting exclusively from disruptive selection among populations, a potential signal of selection within CRs may also result from the inability of favourable mutations to migrate between populations. However, empirical evidence for natural selection in suppressed‐recombination chromosomal speciation is scarce, reinforcing the need for further multidisciplinary studies. Key Concepts: For evolutionary biologists, speciation has always been a controversial topic, both in terms of mechanisms and geographical context. Although allopatry has been the most consensual geographic context of speciation, the divergence of taxa in the face of gene flow is not a rare observation. In purely genetic terms, speciation can be viewed as the evolution of restrictions on the freedom of genetic recombination. Recombination originates new genetic combinations upon which natural selection can act, transforming the genomes of lineages connected by gene flow into a mosaic of genetic information. The molecular characterisation of genes involved in reproductive isolation between some Drosophila species suggests that natural selection has shaped their evolution. The functional characterisation of genes involved in reproductive isolation suggests that genetic conflicts may have a more important role in speciation than what it was initially thought. The formalisation of suppressed‐recombination models of speciation was highly influenced by research performed in fruit flies and sunflowers ( Drosophila and Helianthus ). CRs may play an important role in the origin and accumulation of incompatibilities between parapatric populations but also by avoiding species fusion after a secondary contact. Signatures of selection within CRs may result from divergent environmental conditions but also from universally advantageous alleles. Although, in theory, natural selection facilitates the role of CRs in speciation, signatures of natural selection within CRs have not been universally found in the species so far investigated.