Genetic Architecture of a Reinforced, Postmating, Reproductive Isolation Barrier between Neurospora Species Indicates Evolution via Natural Selection

Abstract

A role for natural selection in reinforcing premating barriers is recognized, but selection for reinforcement of postmating barriers remains controversial. Organisms lacking evolvable premating barriers can theoretically reinforce postmating isolation, but only under restrictive conditions: parental investment in hybrid progeny must inhibit subsequent reproduction, and selected postmating barriers must restore parents' capacity to reproduce successfully. We show that reinforced postmating isolation markedly increases maternal fitness in the fungus Neurospora crassa, and we detect the evolutionary genetic signature of natural selection by quantitative trait locus (QTL) analysis of the reinforced barrier. Hybrid progeny of N. crassa and N. intermedia are highly inviable. Fertilization by local N. intermedia results in early abortion of hybrid fruitbodies, and we show that abortion is adaptive because only aborted maternal colonies remain fully receptive to future reproduction. In the first QTL analysis of postmating reinforcement in microbial eukaryotes, we identify 11 loci for abortive hybrid fruitbody development, including three major QTLs that together explain 30% of trait variance. One of the major QTLs and six QTLs of lesser effect are found on the mating-type determining chromosome of Neurospora. Several reinforcement QTLs are flanked by genetic markers showing either segregation distortion or non-random associations with alleles at other loci in a cross between N. crassa of different clades, suggesting that the loci also are associated with local effects on same-species reproduction. Statistical analysis of the allelic effects distribution for abortive hybrid fruitbody development indicates its evolution occurred under positive selection. Our results strongly support a role for natural selection in the evolution of reinforced postmating isolation in N. crassa.

Author Summary

Although Darwin believed that natural selection could not drive intersterility between species, it is now well established that there is a role for natural selection in the evolution of premating discrimination that reinforces barriers to hybridization. However, natural selection for postmating barriers, like hybrid inviability, is still controversial, because it can only occur when overall maternal fitness is increased by the inviability of hybrid offspring. Constraint on adaptive evolution of postmating barriers poses a problem when organisms without premating preferences must adapt to the presence of related species and ensure that reproduction occurs only between members of the same species. We studied the evolutionary genetics of a reinforced, postmating barrier between two species of mold, Neurospora crassa and N. intermedia. Although hybrids have low fitness, Neurospora females do not discriminate against different-species sex partners before mating. Instead, N. crassa has adapted to the presence of the N. intermedia in its range by selectively aborting hybrid fruitbodies. We show that abortion increases maternal fitness because N. crassa can mate again after hybridization only if fruitbodies abort. Abortion is controlled by 11 loci, whose genetic effects are consistent with an adaptive evolution model, confirming that abortion evolved via natural selection against hybridization.