Mating system and recombination affect molecular evolution in four Triticeae species

UMR Diversité et Adaptation des Plantes Cultivées, Montpellier SupAgro, Institut National de la Recherche Agronomique-IRD-UMII, 2 Place Pierre Viala, Montpellier Cedex 1, France.
Genetics Research (Impact Factor: 1.47). 03/2008; 90(1):97-109. DOI: 10.1017/S0016672307009032
Source: PubMed


Mating systems and recombination are thought to have a deep impact on the organization and evolution of genomes. Because of the decline in effective population size and the interference between linked loci, the efficacy of selection is expected to be reduced in regions with low recombination rates and in the whole genome of self-fertilizing species. At the molecular level, relaxed selection is expected to result in changes in the rate of protein evolution and the pattern of codon bias. It is increasingly recognized that recombination also affects non-selective processes such as the biased gene conversion towards GC alleles (bGC). Like selection, this kind of meiotic drive in favour of GC over AT alleles is expected to be reduced in weakly recombining regions and genomes. Here, we investigated the effect of mating system and recombination on molecular evolution in four Triticeae species: two outcrossers (Secale cereale and Aegilops speltoides) and two selfers (Triticum urartu and Triticum monococcum). We found that GC content, possibly driven by bGC, is affected by mating system and recombination as theoretically predicted. Selection efficacy, however, is only weakly affected by mating system and recombination. We investigated the possible reasons for this discrepancy. A surprising one is that, in outcrossing lineages, selection efficacy could be reduced because of high substitution rates in favour of GC alleles. Outcrossers, but not selfers, would thus suffer from a 'GC-induced' genetic load. This result sheds new light on the evolution of mating systems.

Download full-text


Available from: Etienne Paux
  • Source
    • "Thus, both demographic and genetic processes in selfing populations can interact to reduce the efficacy of natural selection. Early investigations of the genomic consequences of transitions from outcrossing to selfing based on divergence among related outcrossing and selfing species provided limited support for theoretical predictions of a reduced efficacy of selection in selfing populations [e.g., Arabidopsis (Wright et al. 2002), Mimulus (Sweigart and Willis 2003), Caenorhabditis (Cutter et al. 2006), and Triticeae (Haudry et al. 2008; Escobar et al. 2010)]. More recent findings of elevated levels of deleterious polymorphisms or a greater frequency of unpreferred codons in selfing Arabidopsis (Cao et al. 2011; Qiu et al. 2011), Eichhornia (Ness et al. 2012), Capsella (Qiu et al. 2011; Brandvain et al. 2013; Slotte et al. 2013), Collinsia (Hazzouri et al. 2013), and Neurospora (Gioti et al. 2013) are consistent with the hypothesis of relaxed selection in selfing populations. "
    [Show abstract] [Hide abstract]
    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.
    Full-text · Article · Dec 2014 · Genetics
  • Source
    • "Endosymbionts have long been noted to be responsible in the manipulation of sexual systems, and conceivably in inducing asexual lifestyles (Normark 2003). Though many studies have compared differences between the ratios of nonsynonymous to synonymous substitutions (dN/dS) in selÞng and outcrossing plants and asexual and sexual animals (see Glé min and Muyle 2014 for a review) and several studies have examined differences in dN/dS ratios in nuclear and chloroplast genomes of taxa with selÞng and outcrossing lineages (Wright et al. 2002, Haudry et al. 2008) and nuclear and mitochondrial genomes of taxa with sexual and asexual lineages (Normark 1999, Normark and Moran 2000, Shoemaker et al. 2004, Paland and Lynch 2006, Henry et al. 2012, Ollivier et al. 2012), no study to our knowledge has simultaneously compared differences across host and endosymbiont genomes. Due to the shared method of transmission between mitochondrial and endosymbiont genomes (i.e., vertically transmitted from mother to offspring), we could expect similar dN/dS ratios between these two genomes. "
    [Show abstract] [Hide abstract]
    ABSTRACT: Here we compare rates of molecular evolution in sexual and parthenogenetic lineages of Aspdiotus nerii Bouché (Hemiptera: Diaspididae) using the genealogies of three protein-coding loci from A. nerii (one mitochondrial and two nuclear), and two protein-coding loci from the primary endosymbiont Uzinura diaspidicola Gruwell (Proteobacteria: Gammaproteobacteria). To our knowledge, this is the first study to examine how the loss of sex affects DNA sequence substitution rates across nuclear, mitochondrial, and endosymbiont genomes. We find no differences between ratios of nonsynonymous to synonymous substitutions (dN/dS) in sexual and parthenogenetic lineages for nuclear loci (CAD and EF1α) and endosymbiont loci (rspB and GroEL). We do find, however, for a fragment spanning portions of the mitochondrial genes cytochrome oxidase 1 and 2 (CO1-CO2) that a model including separate dN/dS ratios for the sexual and parthenogenetic lineages is a significantly better fit for the data (P = 0.003) than a model that includes a single dN/dS ratio for both lineages. We find this result striking because for asexual lineages nuclear, mictochondrial, and endosymbiont genomes share a similar mode of transmission (i.e., vertical from mother to offspring), yet our results show that elevated dN/dS ratios were only observed in the mitochondrial genome. This result supports a recent hypothesis that interactions between the endosymbiont and nuclear genomes may limit the accumulation of deleterious mutations in the endosymbiont genome, and suggests that these same interactions may influence mutation rates in the nuclear genomes of asexual organisms as well.
    Full-text · Article · Sep 2014 · Annals of the Entomological Society of America
  • Source
    • "Such studies have been performed on Arabidopsis (Qiu et al. 2011); Capsella (Qiu et al. 2011; Slotte et al. 2013; Brandvain et al. 2013); and Collinsia (Hazzouri et al. 2013). On the other hand, no evidence for relaxed selection was found when comparing divergence rates between species, such as in a separate study of Arabidopsis (Wright et al. 2002), as well as in studies of Triticeae (Haudry et al. 2008; Escobar et al. 2010), with mixed evidence arising in selfing Caenorhabditis species (Cutter et al. 2008). Together, this evidence suggests that selection has been relaxed recently, indicating that selfing is of recent origin and deleterious mutation accumulation is likely to be too weak to be the main cause of their higher extinction rates. "
    [Show abstract] [Hide abstract]
    ABSTRACT: Self-fertilization is generally seen to be disadvantageous in the long term. It increases genetic drift, which subsequently reduces polymorphism and the efficiency of selection, which also challenges adaptation. However, high selfing rates can increase the fixation probability of recessive beneficial mutations, but existing theory has generally not accounted for the effect of linked sites. Here, we analyze a model for the fixation probability of deleterious mutants that hitchhike with selective sweeps in diploid, partially selfing populations. Approximate analytical solutions show that, conditional on the sweep not being lost by drift, higher inbreeding rates increase the fixation probability of the deleterious allele, due to the resulting reduction in polymorphism and effective recombination. When extending the analysis to consider a distribution of deleterious alleles, as well as the average fitness increase after a sweep, we find that beneficial alleles generally need to be more recessive than the previously assumed dominance threshold (h < 1/2) for selfing to be beneficial from one-locus theory. Our results highlight that recombination aiding the efficiency of selection on multiple loci amplifies the fitness benefits of outcrossing over selfing, compared to results obtained from one-locus theory. This effect additionally increases the parameter range under which obligate outcrossing is beneficial over partial selfing.
    Full-text · Article · Nov 2013 · Genetics
Show more