Divergent sorting of a balanced ancestral polymorphism underlies the establishment of gene-flow barriers in Capsella

Abstract

In the Bateson–Dobzhansky–Muller model of genetic incompatibilities post-zygotic gene-flow barriers arise by fixation of novel alleles at interacting loci in separated populations. Many such incompatibilities are polymorphic in plants, implying an important role for genetic drift or balancing selection in their origin and evolution. Here we show that NPR1 and RPP5 loci cause a genetic incompatibility between the incipient species Capsella grandiflora and C. rubella, and the more distantly related C. rubella and C. orientalis. The incompatible RPP5 allele results from a mutation in C. rubella, while the incompatible NPR1 allele is frequent in the ancestral C. grandiflora. Compatible and incompatible NPR1 haplotypes are maintained by balancing selection in C. grandiflora, and were divergently sorted into the derived C. rubella and C. orientalis. Thus, by maintaining differentiated alleles at high frequencies, balancing selection on ancestral polymorphisms can facilitate establishing gene-flow barriers between derived populations through lineage sorting of the alternative alleles.

Endosperm‐based postzygotic hybridization barriers: developmental mechanisms and evolutionary drivers

“…; Sicard et al . ). While a locus generating an endosperm‐based hybridization barrier between species remains to be discovered, the evolutionary drivers building these barriers have been intensively discussed (Gutierrez‐Marcos et al .…”

A two‐locus hybrid incompatibility is widespread, polymorphic, and active in natural populations of Mimulus *

“…; Sicard et al. ) or incomplete selective sweeps (Sweigart and Flagel ). Alternatively, polymorphism might result from interspecific gene flow, with incompatible alleles being replaced by introgression of compatible alleles.…”

A two-locus hybrid incompatibility is widespread, polymorphic, and active in natural populations of Mimulus

“…A natural starting point for determining whether hybrid incompatibilities affect rates of contemporary interspecific gene flow is to assess their distribution and frequency within species, which can indicate whether incompatibilities are expressed in natural hybrids. In diverse taxa, incompatibility loci are often polymorphic within species, with both incompatible and compatible alleles existing at a single locus (e.g., Reed and Markow 2004;Shuker et al 2005;Sweigart et al 2007;Seidel et al 2008;Good et al 2008;Cutter 2012;Sicard et al 2015;Larson et al 2018). Such polymorphism may exist because of evolutionary processes acting within species, such as balancing selection maintaining multiple alleles (Seidel et al 2008;Sicard et al 2015) or incomplete selective sweeps (Sweigart and Flagel 2015).…”