Abstract
BackgroundEvolutionary transitions from outcrossing between individuals to selfing are partly responsible for the great diversity of animal and plant reproduction systems. The hypothesis of ‘reproductive assurance’ suggests that transitions to selfing occur because selfers that are able to reproduce on their own ensure the persistence of populations in environments where mates or pollination agents are unavailable. Here we test this hypothesis by performing experimental evolution in Caenorhabditis elegans.ResultsWe show that self-compatible hermaphrodites provide reproductive assurance to a male-female population facing a novel environment where outcrossing is limiting. Invasions of hermaphrodites in male-female populations, and subsequent experimental evolution in the novel environment, led to successful transitions to selfing and adaptation. Adaptation was not due to the loss of males during transitions, as shown by evolution experiments in exclusively hermaphroditic populations and in male-hermaphrodite populations. Instead, adaptation was due to the displacement of females by hermaphrodites. Genotyping of single-nucleotide polymorphisms further indicated that the observed evolution of selfing rates was not due to selection of standing genetic diversity. Finally, numerical modelling and evolution experiments in male-female populations demonstrate that the improvement of male fitness components may diminish the opportunity for reproductive assurance.ConclusionsOur findings support the hypothesis that reproductive assurance can drive the transition from outcrossing to selfing, and further suggest that the success of transitions to selfing hinges on adaptation of obligate outcrossing populations to the environment where outcrossing was once a limiting factor.Electronic supplementary materialThe online version of this article (doi:10.1186/s12915-014-0093-1) contains supplementary material, which is available to authorized users.
Highlights
Evolutionary transitions from outcrossing between individuals to selfing are partly responsible for the great diversity of animal and plant reproduction systems
Despite the considerable efforts trying to demonstrate the hypothesis of reproductive assurance, empirical evidence is mixed [18,19,20,21], and whether individual selection can drive the transition to selfing has not been subject to direct experimental tests; but see [22,23,24]
We have presented comprehensive evidence supporting the hypothesis that individual selection among selfers and outcrossers can drive the transition from dioecy to androdioecy, or to effective monoecy, when there is limited outcrossing in novel environments
Summary
Evolutionary transitions from outcrossing between individuals to selfing are partly responsible for the great diversity of animal and plant reproduction systems. Transitions to selfing have repeatedly occurred during evolution even though this breeding mode usually leads to inbreeding depression [1,7], restricts the generation of potentially adaptive genetic diversity [8,9,10] and may result in Despite the considerable efforts trying to demonstrate the hypothesis of reproductive assurance, empirical evidence is mixed [18,19,20,21], and whether individual selection can drive the transition to selfing has not been subject to direct experimental tests; but see [22,23,24] This is partly because hermaphroditism and selfing occur in multiple forms, not all of which clearly assure population persistence in environments with limited opportunity for outcrossing [17,25,26,27,28]. It is largely unknown how selection of standing genetic diversity specific to breeding mode [41,42], such as the purging of deleterious recessive alleles [43,44,45] or the maintenance of coevolved sets of loci [46,47,48,49], relate to reproductive assurance and may feedback on the evolution of selfing rates
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