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

Michael Lenhard,Cindy Marona,Adrien Sicard,John R. Stinchcombe,Stephen I. Wright,Emily B. Josephs,Christian Kappel,Young Wha Lee

doi:10.1038/ncomms8960

Michael Lenhard, Cindy Marona + Show 6 more

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https://doi.org/10.1038/ncomms8960

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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.

Highlights

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
We focussed our subsequent analysis on these near-isogenic lines (NILs), as no suitable inbred lines are available for the obligate outbreeder C. grandiflora; as a result, genetic background variation between C. grandiflora individuals could confound any comparisons between the parental species and the NILs
As RECOGNITION OF PERONOSPORA PARASITICA 5 (RPP5) homologues in A. thaliana have been identified as strongly overrepresented among loci causing hybrid necrosis[14], our findings suggest that their propensity for giving rise to incompatible alleles is an evolutionarily more wide-spread phenomenon that can give rise to between-species incompatibilities

Summary

Introduction

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. Such post-zygotic barriers to gene flow often result from the establishment of Bateson–Dobzhansky–Muller incompatibilities (BDMIs)[1,2,3,4] According to this model, novel alleles at one or more loci become fixed in separated populations, either due to genetic drift or selection, and produce detrimental consequences when combined in hybrid offspring after crossing[2]. Once fixed for alternative, functionally differentiated alleles, only one novel incompatible mutation to an interacting locus would be required to establish a BDMI between the derived populations[5] This scenario could explain the observation that the transition to selfing appears to accelerate the establishment of post-zygotic gene-flow barriers between different selfing lineages and with the ancestral outbreeding species[17,18,19,20]. Independent transitions to selfing have led to the fixation of alternative alleles in the derived selfers C. rubella and C. orientalis, contributing to a genetic incompatibility between them

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