Recent and Ancient Signature of Balancing Selection around the S-Locus in Arabidopsis halleri and A. lyrata

Abstract

Balancing selection can maintain different alleles over long evolutionary times. Beyond this direct effect on the molecular targets of selection, balancing selection is also expected to increase neutral polymorphism in linked genome regions, in inverse proportion to their genetic map distances from the selected sites. The genes controlling plant self-incompatibility are subject to one of the strongest forms of balancing selection, and they show clear signatures of balancing selection. The genome region containing those genes (the S-locus) is generally described as nonrecombining, and the physical size of the region with low recombination has recently been established in a few species. However, the size of the region showing the indirect footprints of selection due to linkage to the S-locus is only roughly known. Here, we improved estimates of this region by surveying synonymous polymorphism and estimating recombination rates at 12 flanking region loci at known physical distances from the S-locus region boundary, in two closely related self-incompatible plants Arabidopsis halleri and A. lyrata. In addition to studying more loci than previous studies and using known physical distances, we simulated an explicit demographic scenario for the divergence between the two species, to evaluate the extent of the genomic region whose diversity departs significantly from neutral expectations. At the closest flanking loci, we detected signatures of both recent and ancient indirect effects of selection on the S-locus flanking genes, finding ancestral polymorphisms shared by both species, as well as an excess of derived mutations private to either species. However, these effects are detected only in a physically small region, suggesting that recombination in the flanking regions is sufficient to quickly break up linkage disequilibrium with the S-locus. Our approach may be useful for distinguishing cases of ancient versus recently evolved balancing selection in other systems.

What causes mating system shifts in plants? Arabidopsis lyrata as a case study

“…Pollen grains that express a variant of SCR matching that of the SRK expressed on the receiving stigma are rejected. The genes encoding these female and male proteins are physically linked and form the S- locus, which is found in a genomic region that shows restricted recombination between a U-box domain protein (At4g21350; B80) and a member of the SRK gene family ( ARK 3) (Goubet et al , 2012; Roux et al , 2013). There is a complex downstream signalling reaction that is still not completely understood (Goring, 2000; Iwano et al , 2015), but self-compatibility (SC) species typically lack activity of some of these downstream components (for example, Arm-Repeat-Containing Protein 1 (ARC1)) (Indriolo et al , 2012).…”

Nucleotide diversity inflation as a genome-wide response to experimental lifespan extension in Drosophila melanogaster

“…However, despite longstanding interest in the process of balancing selection, its prevalence, the extent of footprints in the genome, and evolutionary significance remain largely unknown due to challenges related to its detection [43–46]. Balancing selection is expected to boost neutral polymorphism in linked genome regions, in inverse proportion to their genetic map distances from the selected site, but the size and distribution of genomic regions showing indirect footprints of balancing selection have been unknown [45]. Our results prove that such effects at the genome-wide level can be pervasive and rapid, invoking newly established neutral polymorphisms from standing genetic variation.…”

Genome-Wide Detection of Selective Signatures in Chicken through High Density SNPs

“…Selection signatures are the selective footprints across the organism genome due to the effect of artificial selection, which displayed the long range linkage disequilibrium in chromosome or genetic diversity reduction [2, 3]. Thus, identifying selection signatures in chicken, we could effectively and efficiently uncovered the selected genes and genomic regions, which would contribute to understand the relationships between genotype and phenotype.…”