Abstract
Recently diverged species typically have incomplete reproductive barriers, allowing introgression of genetic material from one species into the genomic background of the other. The role of natural selection in preventing or promoting introgression remains contentious. Because of genomic co-adaptation, some chromosomal fragments are expected to be selected against in the new background and resist introgression. In contrast, natural selection should favor introgression for alleles at genes evolving under multi-allelic balancing selection, such as the MHC in vertebrates, disease resistance, or self-incompatibility genes in plants. Here, we test the prediction that negative, frequency-dependent selection on alleles at the multi-allelic gene controlling pistil self-incompatibility specificity in two closely related species, Arabidopsis halleri and A. lyrata, caused introgression at this locus at a higher rate than the genomic background. Polymorphism at this gene is largely shared, and we have identified 18 pairs of S-alleles that are only slightly divergent between the two species. For these pairs of S-alleles, divergence at four-fold degenerate sites (K = 0.0193) is about four times lower than the genomic background (K = 0.0743). We demonstrate that this difference cannot be explained by differences in effective population size between the two types of loci. Rather, our data are most consistent with a five-fold increase of introgression rates for S-alleles as compared to the genomic background, making this study the first documented example of adaptive introgression facilitated by balancing selection. We suggest that this process plays an important role in the maintenance of high allelic diversity and divergence at the S-locus in flowering plant families. Because genes under balancing selection are expected to be among the last to stop introgressing, their comparison in closely related species provides a lower-bound estimate of the time since the species stopped forming fertile hybrids, thereby complementing the average portrait of divergence between species provided by genomic data.
Highlights
The genomes of incipient species diverge at heterogeneous rates, and recently diverged model species are key systems to investigate the causes of this heterogeneity [1,2,3]
As long as reproductive barriers remain incomplete, genetic material from one species is exposed to natural selection into the genomic background of the other species
Theory predicts that the transfer of some chromosomal fragments may be favored by natural selection
Summary
The genomes of incipient species diverge at heterogeneous rates, and recently diverged model species are key systems to investigate the causes of this heterogeneity [1,2,3]. In Helianthus, a recent experimental study reported that herbivore resistance traits have introgressed from Heliantus debilis to H. annuus, thereby increasing adaptation of their naturally occurring hybrid H. annuus taxanus [15] All these documented examples are associated with strong directional selection for adaptive traits recently evolved in one of the species and transmitted horizontally. Theory predicts that adaptive introgression should be a general property of alleles at genes evolving under multiallelic balancing selection, such as the vertebrate MHC system, plant disease resistance or self-incompatibility (SI) genes [16] In these systems, rare alleles enjoy a strong selective advantage [17]. Assuming that a given allele is absent from one of two related species, introgression of this allele would be as strongly favored
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