Recent speciation associated with the evolution of selfing in Capsella

Abstract

The evolution from outcrossing to predominant self-fertilization represents one of the most common transitions in flowering plant evolution. This shift in mating system is almost universally associated with the "selfing syndrome," characterized by marked reduction in flower size and a breakdown of the morphological and genetic mechanisms that prevent self-fertilization. In general, the timescale in which these transitions occur, and the evolutionary dynamics associated with the evolution of the selfing syndrome are poorly known. We investigated the origin and evolution of selfing in the annual plant Capsella rubella from its self-incompatible, outcrossing progenitor Capsella grandiflora by characterizing multilocus patterns of DNA sequence variation at nuclear genes. We estimate that the transition to selfing and subsequent geographic expansion have taken place during the past 20,000 years. This transition was probably associated with a shift from stable equilibrium toward a near-complete population bottleneck causing a major reduction in effective population size. The timing and severe founder event support the hypothesis that selfing was favored during colonization as new habitats emerged after the last glaciation and the expansion of agriculture. These results suggest that natural selection for reproductive assurance can lead to major morphological evolution and speciation on relatively short evolutionary timescales.

Fig. 1.

Floral organs and petals are reduced in C. rubella (Left) compared with C. grandiflora (Right).

Fig. 2.

Comparison of polymorphism patterns between C. grandiflora and C. rubella. Bars represent the median, boxes the interquartile range, and whiskers extend out to 1.5 times the interquartile range. (A) π synonymous, where π is the average pairwise differences (16). (B) The population recombination estimator ρ per base pair, using the composite likelihood estimator of Hudson (32). (C) Tajima's D (16) in C. grandiflora and C. rubella.

Fig. 3.

Derived SNP frequencies in C. grandiflora and C. rubella calculated by using A. thaliana as an outgroup. For this plot, we randomly subsampled the data to include 12 individuals from each species. Values where the derived allele frequencies are >0 and <12 would represent polymorphisms, a frequency of 12 is a derived fixation, and a frequency of zero implies a complete absence of the derived SNP. For example, values with 0 or 12 for one species and not in the other represent unique polymorphism in the other species, whereas derived frequencies >0 and <12 in both species represent shared polymorphisms.

Fig. 4.

Smoothed marginal posterior distributions of speciation parameters estimated by MIMAR, for two models with posterior modes showing good fit to data summaries, assuming either symmetric migration (solid lines) or no migration (dashed lines) and equal effective population sizes in the ancestor as in present-day C. grandiflora. (A) Marginal densities for effective population size (individuals) in C. rubella (gray) and C. grandiflora/the ancestral species. (B) Marginal densities for divergence time (years). (C) Marginal density for migration (4Nm), where N is the effective population size of C. grandiflora.