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Basic models of mating-system evolution predict that hermaphroditic organisms should mostly either cross-fertilize, or self-fertilize, due to self-reinforcing coevolution of inbreeding depression and outcrossing rates. However transitions between mating systems occur. A plausible scenario for such transitions assumes that a decrease in pollinator or mate availability temporarily constrains outcrossing populations to self-fertilize as a reproductive assurance strategy. This should trigger a purge of inbreeding depression, which in turn encourages individuals to self-fertilize more often and finally to reduce male allocation. We tested the predictions of this scenario using the freshwater snail Physa acuta, a self-compatible hermaphrodite that preferentially outcrosses and exhibits high inbreeding depression in natural populations. From an outbred population, we built two types of experimental evolution lines, controls (outcrossing every generation) and constrained lines (in which mates were often unavailable, forcing individuals to self-fertilize). After ca. 20 generations, individuals from constrained lines initiated self-fertilization earlier in life and had purged most of their inbreeding depression compared to controls. However, their male allocation remained unchanged. Our study suggests that the mating system can rapidly evolve as a response to reduced mating opportunities, supporting the reproductive assurance scenario of transitions from outcrossing to selfing.

Sex allocation theory predicts that simultaneous hermaphrodites evolve to an evolutionary stable resource allocation, whereby any increase in investment to male reproduction leads to a disproportionate cost on female reproduction and vice versa. However, empirical evidence for sexual trade-offs in hermaphroditic animals is still limited. Here, we tested how male and female reproductive traits evolved under conditions of reduced selection on either male or female reproduction for 40 generations in a hermaphroditic snail. This selection favors a reinvestment of resources from the sex function under relaxed selection toward the other function. We found no such evolutionary response. Instead, juvenile survival and male reproductive success significantly decreased in lines where selection on the male function (i.e., sexual selection) was relaxed, while relaxing selection on the female function had no effect. Our results suggest that most polymorphisms under selection in these lines were not sex-antagonistic. Rather, they were deleterious mutations affecting juvenile survival (thus reducing both male and female fitness) with strong pleiotropic effects on male success in a sexual selection context. These mutations accumulated when sexual selection was relaxed, which supports the idea that sexual selection in hermaphrodites contributes to purge the mutation load from the genome as in separate-sex organisms.

Theory and empirical data showed that two processes can boost selection against deleterious mutations, thus facilitating the purging of the mutation load: inbreeding, by exposing recessive deleterious alleles to selection in homozygous form, and sexual selection, by enhancing the relative reproductive success of males with small mutation loads. These processes tend to be mutually exclusive because sexual selection is reduced under mating systems that promote inbreeding, such as self‐fertilization in hermaphrodites. We estimated the relative efficiency of inbreeding and sexual selection at purging the genetic load, using 50 generations of experimental evolution, in a hermaphroditic snail (Physa acuta). To this end, we generated lines that were exposed to various intensities of inbreeding, sexual selection (on the male function), and nonsexual selection (on the female function). We measured how these regimes affected the mutation load, quantified through the survival of outcrossed and selfed juveniles. We found that juvenile survival strongly decreased in outbred lines with reduced male selection, but not when female selection was relaxed, showing that male‐specific sexual selection does purge deleterious mutations. However, in lines exposed to inbreeding, where sexual selection was also relaxed, survival did not decrease, and even increased for self‐fertilized juveniles, showing that purging through inbreeding can compensate for the absence of sexual selection. Our results point to the further question of whether a mixed strategy combining the advantages of both mechanisms of genetic purging could be evolutionary stable. Fil: Noël, Elsa. Institut National de la Recherche Agronomique; Francia. Centre National de la Recherche Scientifique; Francia Fil: Fruitet, Elise. University of Amsterdam; Países Bajos. Max Planck Institute for Chemical Ecology; Alemania. Centre National de la Recherche Scientifique; Francia Fil: Lelaurin, Dennyss. Centre National de la Recherche Scientifique; Francia Fil: Bonel, Nicolás. Universidad Nacional del Sur; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Centre National de la Recherche Scientifique; Francia Fil: Ségard, Adeline. Centre National de la Recherche Scientifique; Francia Fil: Sarda, Violette. Centre National de la Recherche Scientifique; Francia Fil: Jarne, Philippe. Centre National de la Recherche Scientifique; Francia Fil: David, Patrice. Centre National de la Recherche Scientifique; Francia

International audience; Self-fertilization is widely believed to be an ''evolu-tionary 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. We applied 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 out-crossing populations maintain their response 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, pheno-typic 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.

Basic models of mating-system evolution predict that hermaphroditic organisms should mostly either cross-fertilize, or self-fertilize, due to self-reinforcing coevolution of inbreeding depression and outcrossing rates. However transitions between mating systems occur. A plausible scenario for such transitions assumes that a decrease in pollinator or mate availability temporarily constrains outcrossing populations to self-fertilize as a reproductive assurance strategy. This should trigger a purge of inbreeding depression, which in turn encourages individuals to self-fertilize more often and finally to reduce male allocation. We tested the predictions of this scenario using the freshwater snail Physa acuta, a self-compatible hermaphrodite that preferentially outcrosses and exhibits high inbreeding depression in natural populations. From an outbred population, we built two types of experimental evolution lines, controls (outcrossing every generation) and constrained lines (in which mates were often unavailable, forcing individuals to self-fertilize). After ca. 20 generations, individuals from constrained lines initiated self-fertilization earlier in life and had purged most of their inbreeding depression compared to controls. However, their male allocation remained unchanged. Our study suggests that the mating system can rapidly evolve as a response to reduced mating opportunities, supporting the reproductive assurance scenario of transitions from outcrossing to selfing.