The genetics of speciation and the origin of genomic divergence

Abstract

Speciation involves the origin of trait differences that limit or prevent gene exchange and ultimately results in daughter populations that form monophyletic or exclusive genetic groups. However, for recently diverged populations or species, between which reproductive isolation is often incomplete, gene genealogies will be discordant and most regions of the genome will display nonexclusive genealogical patterns. In these situations, genome regions for which one or both species are exclusive groups may mark the footprint of recent selective sweeps. Alternatively, such regions may include or be closely linked to ?speciation genes,? genes involved in reproductive isolation. Therefore, comparisons of gene genealogies allow inferences about the genetic architectures of both reproductive isolation and adaptation. Contrasting genealogical relationships in sexually isolated Z and E pheromone strains of the European corn borer moth (ECB) demonstrate the relevance of this approach.

Genealogies for five gene regions in ECB are discordant, and for only one molecular marker, the sex-linked gene Tpi, are the two pheromone strains exclusive groups. A genetic linkage map provides the context for understanding genealogical discordance. The factors responsible for sexual isolation, male behavioral response (Resp) and female pheromone production (Pher), and the factor causing temporal isolation, post-diapause development (Pdd), were placed on a linkage map that also contained the mapping positions of the gene genealogies. Pher maps to an autosome, whereas Resp and Pdd are sex-linked. The exclusive gene, Tpi, maps to a position on the sex chromosome that is indistinguishable from Pdd; Resp maps 20-30 cM away. Neutral demography involving population expansion and population substructure can explain most genetic patterns among loci; however, Tpi shows evidence for non-neutral evolution. Because Tpi is tightly linked to Pdd, recent evolution of this reproductive barrier may be responsible for the evolution of genetic divergence between these incipient species.