Joint inference of evolutionary transitions to self-fertilization and demographic history using whole-genome sequences

Abstract

The evolution from outcrossing to selfing occurred recently across the eukaryote tree of life in plants, animals, fungi, and algae. Despite short-term advantages, selfing is hypothetically an evolutionary dead-end reproductive strategy. The tippy distribution on phylogenies suggests that most selfing species are of recent origin. However, dating such transitions is challenging yet central for testing this hypothesis. We build on previous theories to disentangle the differential effect of past changes in selfing rate or from that of population size on recombination probability along the genome. This allowed us to develop two methods using full-genome polymorphisms to (1) test if a transition from outcrossing to selfing occurred and (2) infer its age. TheteSMCandtsABCmethods use a transition matrix summarizing the distribution of times to the most recent common ancestor along the genome to estimate changes in the ratio of population recombination and mutation rates overtime. First, we demonstrate that our methods distinguish between past changes in selfing rate and demographic history. Second, we assess the accuracy of our methods to infer transitions to selfing approximately up to 2.5Negenerations ago. Third, we demonstrate that our estimates are robust to the presence of purifying selection. Finally, as a proof of principle, we apply both methods to threeArabidopsis thalianapopulations, revealing a transition to selfing approximately 600,000 years ago. Our methods pave the way for studying recent transitions to self-fertilization and better accounting for variation in mating systems in demographic inferences.