The Evolution of Selfing Is Accompanied by Reduced Efficacy of Selection and Purging of Deleterious Mutations

The transition from outcrossing to selfing is predicted to reduce the genome-wide efficacy of selection because of the lower effective population size (N_e) that accompanies this change in mating system. However, strongly recessive deleterious mutations exposed in the homozygous backgrounds of selfers should be under strong purifying selection. Here, we examine estimates of the distribution of fitness effects (DFE) and changes in the magnitude of effective selection coefficients (N_es) acting on mutations during the transition from outcrossing to selfing. Using forward simulations, we investigated the ability of a DFE inference approach to detect the joint influence of mating system and the dominance of deleterious mutations on selection efficacy. We investigated predictions from our simulations in the annual plant Eichhornia paniculata, in which selfing has evolved from outcrossing on multiple occasions. We used range-wide sampling to generate population genomic datasets and identified nonsynonymous and synonymous polymorphisms segregating in outcrossing and selfing populations. We found that the transition to selfing was accompanied by a change in the DFE, with a larger fraction of effectively neutral sites (N_es < 1), a result consistent with the effects of reduced N_e in selfers. Moreover, an increased proportion of sites in selfers were under strong purifying selection (N_es > 100), and simulations suggest that this is due to the exposure of recessive deleterious mutations. We conclude that the transition to selfing has been accompanied by the genome-wide influences of reduced N_e and strong purifying selection against deleterious recessive mutations, an example of purging at the molecular level.     

Heterosis and inbreeding depression in bottlenecked populations: a test in the hermaphroditic freshwater snail Lymnaea stagnalis

Small population size is expected to induce heterosis, due to the random fixation and accumulation of mildly deleterious mutations, whereas within‐population inbreeding depression should decrease due to increased homozygosity. Population bottlenecks, although less effective, may have similar consequences. We tested this hypothesis in the self‐fertile freshwater snail Lymnaea stagnalis, by subjecting experimental populations to a single bottleneck of varied magnitude. Although patterns were not strong, heterosis was significant in the most severely bottlenecked populations, under stressful conditions. This was mainly due to hatching rate, suggesting that early acting and highly deleterious alleles were involved. Although L. stagnalis is a preferential outcrosser, inbreeding depression was very low and showed no clear relationship with bottleneck size. In the less reduced populations, inbreeding depression for hatching success increased under high inbreeding. This may be consistent with the occurence of synergistic epistasis between fitness loci, which may contribute to favour outcrossing in L. stagnalis.     

Dietary stress does not strengthen selection against single deleterious mutations in Drosophila melanogaster

Stress is generally thought to increase the strength of selection, although empirical results are mixed and general conclusions are difficult because data are limited. Here we compare the fitness effects of nine independent recessive mutations in Drosophila melanogaster in a high- and low-dietary-stress environment, estimating the strength of selection on these mutations arising from both a competitive measure of male reproductive success and productivity (female fecundity and the subsequent survival to adulthood of her offspring). The effect of stress on male reproductive success has not been addressed previously for individual loci and is of particular interest with respect to the alignment of natural and sexual selection. Our results do not support the hypothesis that stress increases the efficacy of selection arising from either fitness component. Results concerning the alignment of natural and sexual selection were mixed, although data are limited. In the low-stress environment, selection on mating success and productivity were concordant for five of nine mutations (four out of four when restricted to those with significant or near-significant productivity effects), whereas in the high-stress environment, selection aligned for seven of nine mutations (two out of two when restricted to those having significant productivity effects). General conclusions as to the effects of stress on the strength of selection and the alignment of natural and sexual selection await data from additional mutations, fitness components and stressors.     

HOW ARE DELETERIOUS MUTATIONS PURGED? DRIFT VERSUS NONRANDOM MATING

Accumulation of deleterious mutations has important consequences for the evolution of mating systems and the persistence of small populations. It is well established that consanguineous mating can purge a part of the mutation load and that lethal mutations can also be purged in small populations. However, the efficiency of purging in natural populations, due to either consanguineous mating or to reduced population size, has been questioned. Consequences of consanguineous mating systems and small population size are often equated under \"inbreeding\" because both increase homozygosity, and selection is though to be more efficient against homozygous deleterious alleles. I show that two processes of purging that I call \"purging by drift\" and \"purging by nonrandom mating\" have to be distinguished. Conditions under which the two ways of purging are effective are derived. Nonrandom mating can purge deleterious mutations regardless of their dominance level, whereas only highly recessive mutations can be purged by drift. Both types of purging are limited by population size, and sharp thresholds separate domains where purging is either effective or not. The limitations derived here on the efficiency of purging are compatible with some experimental studies. Implications of these results for conservation and evolution of mating systems are discussed.     

Significance of Population Size on the Fixation of Nonsynonymous Mutations in Genes Under Varying Levels of Selection Pressure

Previous studies observed a higher ratio of divergences at nonsynonymous and synonymous sites (ω = d_N/d_S) in species with a small population size compared to that estimated for those with a large population size. Here we examined the theoretical relationship between ω, effective population size (N_e), and selection coefficient (s). Our analysis revealed that when purifying selection is high, ω of species with small N_e is much higher than that of species with large N_e. However the difference between the two ω reduces with the decline in selection pressure (s → 0). We examined this relationship using primate and rodent genes and found that the ω estimated for highly constrained genes of primates was up to 2.9 times higher than that obtained for their orthologous rodent genes. Conversely, for genes under weak purifying selection the ω of primates was only 17% higher than that of rodents. When tissue specificity was used as a proxy for selection pressure we found that the ω of broadly expressed genes of primates was up to 2.1-fold higher than that of their rodent counterparts and this difference was only 27% for tissue specific genes. Since most of the nonsynonymous mutations in constrained or broadly expressed genes are deleterious, fixation of these mutations is influenced by N_e. This results in a higher ω of these genes in primates compared to those from rodents. Conversely, the majority of nonsynonymous mutations in less-constrained or tissue-specific genes are neutral or nearly neutral and therefore fixation of them is largely independent of N_e, which leads to the similarity of ω in primates and rodents.     

Inbreeding effective population size under some artificial selection schemes

Summary It is well known that truncation selection is the most efficient form of directional selection in terms of changing gene frequency. In this paper we show circumstances where truncation selection followed by a balanced mating generates inbreeding effective population size smaller than that generated by a selection that assigns mating frequencies to individuals according to their breeding values, where both selection schemes give the same expected performance of selected individuals (selection differential). Breeding values of selected individuals and the weight used to determine mating frequencies are assumed to be linearly distributed on a performance scales, x. To assign mating frequencies to the individuals in the weighting system, the selected individuals are grouped using a constant , and ith group in the interval x_i, x_i + . With small number of groups, say 2 or 3, the weighting system in general generates inbreeding effective population size that is larger than that generated by a truncation selection. As the number of the groups increases, truncation selection generates larger effective numbers.     

The effects of cyclic dynamics and mating system on the effective size of an island mouflon population

The Haute Island mouflon (Ovis aries) population is isolated on one small (6.5 km2) island of the remote Kerguelen archipelago. Given a promiscuous mating system, a cyclic demography and a strong female-biased sex ratio after population crashes, we expected a low effective population size (Ne). We estimated Ne using demographic and temporal genetic approaches based on genetic information at 25 microsatellite loci from 62 and 58 mouflons sampled in 1988 and 2003, respectively. Genetic Ne estimates were higher than expected, varying between 104 and 250 depending on the methods used. Both demographic and genetic approaches show the Haute Island Ne is buffered against population crashes. The unexpectedly high Ne likely results from the cyclic winter crashes that allow young males to reproduce, limiting the variance of male reproductive success. Based on individual-based simulations, we suggest that despite a strongly female-biased sex ratio, the effects of the mating system on the effective population size more closely resemble random mating or weak polygyny.     

AN INTEGRATIVE TEST OF THE DEAD‐END HYPOTHESIS OF SELFING EVOLUTION IN TRITICEAE (POACEAE)

Self‐fertilization is hypothesized to be an evolutionary dead end because reversion to outcrossing can rarely happen, and selfing lineages are thought to rapidly become extinct because of limited potential for adaptation and/or accumulation of deleterious mutations. We tested these two assumptions by combining morphological characters and molecular‐evolution analyses in a tribe of hermaphroditic grasses (Triticeae). First, we determined the mating system of the 19 studied species. Then, we sequenced 27 protein‐coding loci and compared base composition and substitution patterns between selfers and outcrossers. We found that the evolution of the mating system is best described by a model including outcrossing‐to‐selfing transitions only. At the molecular level, we showed that regions of low recombination exhibit signatures of relaxed selection. However, we did not detect any evidence of accumulation of nonsynonymous substitutions in selfers compared to outcrossers. Additionally, we tested for the potential deleterious effects of GC‐biased gene conversion in outcrossing species. We found that recombination and not the mating system affected substitution patterns and base composition. We suggest that, in Triticeae, although recombination patterns have remained stable, selfing lineages are of recent origin and inbreeding may have persisted for insufficient time for differences between the two mating systems to evolve.     

Strong effects of heterosis on the evolution of dispersal rates

When dispersal is limited, crosses between different regions may generate progeny of higher fitness than crosses within regions, due to the fact that individuals from the same region are more likely to share the same recessive deleterious alleles. This phenomenon (termed heterosis) generates a selective force favouring dispersal; however, the importance of heterosis on dispersal evolution has been a subject for debate. In this paper, we use computer simulations representing deleterious mutations occurring over a whole genome (of arbitrary map length R) to explore the magnitude of heterosis, and its effect on the evolution of dispersal. These results show that heterosis may have important effects on dispersal when it is in the upper range of values observed in natural populations, which occurs in our simulations when the genomic deleterious mutation rate U is also in the upper range of observed values. Comparing the results with extrapolations from an analytical two‐locus model indicates that the effect of heterosis is mainly driven by pairwise associations between the locus affecting dispersal and selected loci when U is not too high (roughly, U < 0.5), whereas higher order associations become important for higher values of U.