Abstract
Self-fertilization is widely believed to be an "evolutionary dead end" [1, 2], increasing the risk of extinction [3] and the accumulation of deleterious mutations in genomes [4]. Strikingly, while the failure to adapt has always been central to the dead-end hypothesis [1, 2], there are no quantitative genetic selection experiments comparing the response to positive selection in selfing versus outcrossing populations. Here we studied the response to selection on a morphological trait in laboratory populations of a hermaphroditic, self-fertile snail under either selfing or outcrossing. Weapplied both treatments to two types of populations: some having undergone frequent selfing and purged a substantial fraction of their mutation load in their recent history [5], and others continuously maintained under outcrossing. Populations with a history of outcrossing respond faster to selection than those that have experienced selfing. In addition, when self-fertilization occurs during selection, the response is initially fast but then rapidly slows, while outcrossing populations maintain theirresponse throughout the experiment. This occurs irrespective of past selfing history, suggesting that high levels of inbreeding depression, contrary to expectation [6], do not set strong limits to the response to selection under inbreeding, at least at the timescale of a few generations. More surprisingly, phenotypic variance is consistently higher under selfing, although it quickly becomes less responsive to selection. This implies an increase in non-heritable variance, hence a breakdown of developmental canalization [7] under selfing. Our findings provide the first empirical support of the short-term positive and long-term negative effects of selfing on adaptive potential.
Highlights
We addressed this central question in the hermaphroditic outcrossing snail Physa acuta via the following questions: (1) Do populations regularly exposed to self-fertilization lose additive genetic variance compared to outcrossing ones? (2) Does self-fertilization during selection affect the population response to selection? (3) Does inbreeding depression strongly limit the ability to respond to selection under self-fertilization? We constructed two types of experimental evolution lines: individuals from C lines always outcrossed, whereas self-fertilization was imposed every other generation in S lines [5]
Some ideas in biology have become classical with surprisingly little empirical evidence, for example that selfing species are less able to cope with changes in selection regimes than outcrossing ones, as suggested by theoretical models [11, 14]
Starting from the same standing genetic variance, populations switching to self-fertilization initially undergo an accelerated response to selection due to homozygosity and the recruitment of dominance and epistatic effects into the heritable variance
Summary
Self-Fertilization Enhances the Response to Selection at First but Compromises It Later In all eight populations (two types 3 two replicates 3 two mating treatments during six generations of selection; 12,000 individuals measured), we observed significant increases in shell roundness over generations (p < 0.001; Table 1; Figure 2A3), while unselected experimental evolution lines (1,200 individuals measured) underwent no significant changes during the same period (Table S1; Figure S1). Both C and S populations responded to selection under outcrossing (Figures 2A2 and 2A3), but the phenotypic change per generation, which reflects the additive genetic variance, was higher in C than in S populations in both the first and second halves of the experiment (‘‘line type 3 generation’’: p = 0.015 and p < 0.001, respectively; the dataset was broken in two halves, as the response was not linear over the entire period).
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