The evolution of self-compatibility and its genetic consequences in Leavenworthia alabamica (Brassicaceae)

Abstract

The evolution of self-fertilization from the outcrossing condition is a common transition in flowering plants which strongly alters the genetic structure of populations. In general, it is thought that self-fertilization may evolve in response to its innate transmission advantage or pollen limitation, and that this mating system may endanger the long-term viability of populations through mutation accumulation. The purpose of this dissertation was to evaluate the costs and benefits of self-fertilization in the species Leavenworthia alabamica, which exhibits variation among populations in the presence or absence of self-incompatibility. This variation in mating-system made it possible to directly answer the following questions: 1) what are the agents of selection driving the fixation of self-compatibility alleles in populations?; 2) does inbreeding depression selectively maintain self-incompatibility in nature, and if so, what happens to these deleterious alleles following the transition to self-compatibility?; and 3) does a history of self-fertilization cause populations to accumulate deleterious mutations and potentially experience extinction?

In L. alabamica, self-incompatibility predominates in large, stable and geographically central populations. In contrast, self-compatibility and adaptations for self-fertilization evolve in the small, disturbed, and geographically peripheral populations of this species. A field experiment shows that self-compatible genotypes are selectively favored in all environments, but that reductions in mate availability likely favor their spread and fixation in the smallest of populations. This model of mating-system evolution is supported by the nearly complete or complete loss of sequence diversity in all of the independently derived self-compatible taxa of Leavenworthia. Inbreeding depression plays a role in the maintenance of self-incompatibility in L. alabamica, and the spread and fixation of self-compatibility alleles purge populations of these strongly deleterious mutations. Nearly all of the populations of this species do not suffer from a substantial local drift load caused by the fixation of mildly deleleterious mutations. That being said, the oldest and most isolated self-fertilizing population showed a dramatic increase in fitness following crosses between populations. Overall, these results suggests that mutation accumulation may eliminate highly inbreeding plant populations as the stochastic fixation of mildly deleterious mutations depresses fitness over many generations.