Mating Systems and the Efficacy of Selection at the Molecular Level

Institut des Sciences de l'Evolution (UM2-CNRS), Université Montpellier II, 34095 Montpellier Cedex 5, France.
Genetics (Impact Factor: 5.96). 11/2007; 177(2):905-16. DOI: 10.1534/genetics.107.073601
Source: PubMed


Mating systems are thought to play a key role in molecular evolution through their effects on effective population size (N(e)) and effective recombination rate. Because of reduced N(e), selection in self-fertilizing species is supposed to be less efficient, allowing fixation of weakly deleterious alleles or lowering adaptation, which may jeopardize their long-term evolution. Relaxed selection pressures in selfers should be detectable at the molecular level through the analyses of the ratio of nonsynonymous and synonymous divergence, D(n)/D(s), or the ratio of nonsynonymous and synonymous polymorphism, pi(n)/pi(s). On the other hand, selfing reveals recessive alleles to selection (homozygosity effect), which may counterbalance the reduction in N(e). Through population genetics models, this study investigates which process may prevail in natural populations and which conditions are necessary to detect evidence for relaxed selection signature at the molecular level in selfers. Under a wide range of plausible population and mutation parameters, relaxed selection against deleterious mutations should be detectable, but the differences between the two mating systems can be weak. At equilibrium, differences between outcrossers and selfers should be more pronounced using divergence measures (D(n)/D(s) ratio) than using polymorphism data (pi(n)/pi(s) ratio). The difference in adaptive substitution rates between outcrossers and selfers is much less predictable because it critically depends on the dominance levels of new advantageous mutations, which are poorly known. Different ways of testing these predictions are suggested, and implications of these results for the evolution of self-fertilizing species are also discussed.

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Available from: Sylvain Glémin, Feb 04, 2014
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    • "A reduction in N e is expected to lower selection efficacy, whereas increased homozygosity should make selection more efficient by exposing recessive mutations. Glémin (2007) predicted that relaxed selection should be detected under a range of mutation and population size parameters in spite of the countervailing effect of homozygosity. Moreover, he found that divergence-based measures of selection were more likely to reveal differences compared to those based on polymorphism data. "
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    ABSTRACT: The transition from outcrossing to selfing is predicted to reduce the genome-wide efficacy of selection because of the lower effective population size (Ne) 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 (Nes) 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 (Nes<1), a result consistent with the effects of reduced Ne in selfers. Moreover, an increased proportion of sites in selfers were under strong purifying selection (Nes>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 Nes and strong purifying selection against deleterious recessive mutations, an example of purging at the molecular level. Copyright © 2014, The Genetics Society of America.
    Genetics 12/2014; 199(3). DOI:10.1534/genetics.114.172809 · 5.96 Impact Factor
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    • "These effects reduce the efficacy of purifying selection. On the other hand, selfing exposes recessive deleterious mutations in a homozygous state and can thus also enhance purging (Glé min 2007). In selfers with a diploid-dominant life cycle the first effect dominates, thus leading to a net reduction in purifying selection (Slotte et al. 2013; Wright et al. 2013). "
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    ABSTRACT: In diploid organisms, selfing reduces the efficiency of selection in removing deleterious mutations from a population. This need not be the case for all organisms. Some plants, for example, undergo an extreme form of selfing known as intragametophytic selfing, which immediately exposes all recessive deleterious mutations in a parental genome to selective purging. Here, we ask how effectively deleterious mutations are removed from such plants. Specifically, we study the extent to which deleterious mutations accumulate in a predominantly selfing and a predominantly outcrossing pair of moss species, using genome-wide transcriptome data. We find that the selfing species purge significantly more nonsynonymous mutations, as well as a greater proportion of radical amino acid changes which alter physicochemical properties of amino acids. Moreover, their purging of deleterious mutation is especially strong in conserved regions of protein-coding genes. Our observations show that selfing need not impede but can even accelerate the removal of deleterious mutations, and do so on a genome-wide scale.
    Genome Biology and Evolution 05/2014; 6(5):1238-1252. DOI:10.1093/gbe/evu099 · 4.23 Impact Factor
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    • "As stated above, this additional more than two-fold reduction in N e (a(F) < 1) is pivotal to the argument that selection is less efficient in selfers (Gl emin, 2007). Bottlenecks should affect cytoplasmic and nuclear genes similarly, whereas nuclear genes should be more sensitive to hitchhiking effects. "
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    ABSTRACT: Selfing is assumed to reduce selection efficacy, especially purifying selection. This can be tested using molecular data, for example by comparing the Dn/Ds ratio between selfing and outcrossing lineages. So far, little evidence of relaxed selection against weakly deleterious mutations (as inferred by a higher Dn/Ds ratio) in selfers as compared to outcrossers has been found, contrary to the pattern often observed between asexual and sexual lineages. However, few groups have been studied to date. To further test this hypothesis, we compiled and analysed chloroplastic sequence data sets in several plant groups. We found a general trend towards relaxed selection in selfers in our data sets but with weak statistical support. Simulations suggested that the results were compatible with weak-to-moderate Dn/Ds ratio differences in selfing lineages. Simple theoretical predictions also showed that the ability to detect relaxed selection in selfers could strongly depend on the distribution of the effects of deleterious mutations on fitness. Our results are compatible with a recent origin of selfing lineages whereby deleterious mutations potentially have a strong impact on population extinction or with a more ancient origin but without a marked effect of deleterious mutations on the extinction dynamics.
    Journal of Evolutionary Biology 03/2014; 27(7). DOI:10.1111/jeb.12356 · 3.23 Impact Factor
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