Genomic implications of the repeated shift to self-fertilization across a species' geographic distribution

Abstract

The ability to self-fertilize often varies among closely related hermaphroditic plant species, though, variation can also exist within species. In the North American Arabidopsis lyrata, the shift from self-incompatibility (SI) to selfing established in multiple regions independently, mostly since recent postglacial range expansion. This has made the species an ideal model for the investigation of the genomic basis of the breakdown of SI and its population genetic consequences. By comparing nearby selfing and outcrossing populations across the entire species' geographic distribution, we investigated variation at the self-incompatibility (S-)locus and across the genome. Furthermore, a diallel crossing experiment on one mixed-mating population was performed to gain insight into the inheritance of mating system variation. We confirmed that the breakdown of SI had evolved in several S-locus backgrounds. The diallel suggested the involvement of biparental contributions with dominance relations. Though, the population-level genome-wide association study did not single out clear-cut candidate genes but several regions with one near the S-locus. On the implication side, selfing as compared to outcrossing populations had less than half of the genomic diversity, while the number and length of runs of homozygosity (ROHs) scaled with the degree of inbreeding. Selfing populations with a history of long expansion had the longest ROHs. The results highlight that mating system shift to selfing, its genetic underpinning and the likely negative genomic consequences for evolutionary potential can be strongly interlinked with past range dynamics.

Keywords: inbreeding; mating system; recombination; runs of homozygosity; self-incompatibility locus.

Fig. 1.

Diversity at the female specificity determinant S-receptor kinase (SRK). A) Depiction of SRK with the respective subdomains. B) Location of the studied populations. The color of the triangles represents the mating system, approximated by the population inbreeding coefficient F_IS, and those of population abbreviations the mating system in categories: outcrossing in black, mixed-mating in pink, and selfing in red. Population abbreviations reflect the respective US state or Canadian province followed by a number. C) Marginal effect (slope; with 95% confidence interval) of a generalized linear mixed-effects model with the predicted probability for being heterozygous for SRK in relationship to F_IS. D) Phylogenetic relationship among populations based on two resequenced genomes per population (left) compared with the phylogenetic relationship of SRK haplotypes. The SRK tree was collapsed to haplotype groups. Lines connect the SRK allele(s) of a respective individual with the detected haplotype group. Gray dots on the phylogenies indicate nodes with >95% bootstrap support. The color of the triangles and the lines connecting the two phylogenies represent F_IS. Indicated in the SRK tree are the number of unique haplotypes found for each group, the dominance class, and the closest matching haplotype from Mable et al. (2017), the latter being italized.

Fig. 2.

Outcome of the genome-wide association study (GWAS) for population-based F_IS. A) Number of HMM outlier SNPs for each chromosome. B) Manhattan plot depicting the Bayes Factor for each SNP included in the GWAS within a 210 kb region around the S-locus on chromosome 7. HMM outliers are depicted in blue.

Fig. 3.

The relationship between mating system shift and genetic diversity. A) Boxplot showing the difference in average genome-wide genetic diversity (Watterson’s θ) between outcrossing and selfing/mixed-mating populations. Marginal effects (with 95% confidence intervals) of Bayesian linear mixed-effects models with B) the number of runs of homozygosity (ROHs) or C) the length of ROHs as the dependent variable.

Fig. 4.

Mating system shifts and recombination across the genome of A. lyrata. A) Density plot depicting the distribution of recombination, estimated as crossovers per base and generation within 100 kb windows from pool-seq data using the software ReLERNN. Line colors depict population-level F_IS (see Fig. 1B). Marginal effects (with 95% confidence intervals) of a linear mixed-effects model with recombination as the dependent variable and the following fixed factors: B) phylogenetic cluster, C) the presence or absence of GWAS outlier SNPs, D) mating system (F_IS), and E) the distance of each window from the centromere (bps, log scale).