Evolutionary genetic consequences of facultative sex and outcrossing

Abstract

This is an invited review by the winner of the 2015 John Maynard Smith prize, awarded annually by the European Society for Evolutionary Biology to an outstanding young evolutionary biologist. Keywords:adaptation; asexuality; genomics; selfing; sexual reproduction. AbstractExplaining the selective forces that underlie different reproductive modes forms a major part of evolution research. Many organisms are facultative sexuals, with the ability to reproduce both sexually and asexually. Reduced sequencing costs means it is now possible to start investigating genome sequences of a wider number of these organisms in depth, but teasing apart the genetic forces underlying the maintenance of facultative sexual reproduction remains a challenge. An analogous problem exists when determining the genetic consequences of a degree of outcrossing (and recombination) in otherwise self-fertilizing organisms. Here, I provide an overview of existing research on the evolutionary basis behind different reproductive modes, with a focus on explaining the population genetic effects favouring low outcrossing rates in either partially selfing or asexual species. I review the outcomes that both self-fertilization and asexuality have on either purging deleterious mutations or fixing beneficial alleles, and what empirical data exist to support these theories. In particular, a greater application of mathematical models to genomic data has provided insight into the numerous effects that transitions to self-fertilization from outcrossing have on genetic architecture. Similar modelling approaches could be used to determine the forces shaping genetic diversity of facultative sexual species. Hence, a further unification of mathematical models with next-generation sequence data will prove important in exploring the genetic influences on reproductive system evolution.

Background Selection in Partially Selfing Populations

“…As illustrated in Figure S1, this regime may be particularly important in highly selfing populations and when the deleterious mutation rate U is high, since N e may be sufficiently reduced to affect the efficiency of selection at an important proportion of selected sites. This is confirmed by empirical observations of higher ratios of nonsynonymous to synonymous polymorphism (p N =p S ) in selfing lineages than in their outcrossing relatives (Glémin and Muyle 2014;Hartfield 2015 and references therein), indicating that a significant fraction of deleterious alleles may increase in frequency due to drift (in which case the assumption that N e s 1 at most loci is not valid). It is thus important to keep in mind that background selection models such as the one presented here overestimate the reduction in N e in such situations, and it would be interesting (although probably challenging) to obtain analytical predictions for neutral diversity in populations undergoing low rates of sex or high selfing rates and in which selection against a high proportion of deleterious mutations is rendered ineffective.…”

“…Analyses based on molecular data show little evidence for increased ratios of nonsynonymous to synonymous substitutions (d N =d S ) in selfing lineages that would indicate a reduced efficiency of purifying selection (Glémin and Muyle 2014;Hartfield 2015 and references therein): this may be due to the recent origin of those lineages or to the low rates of outcrossing maintained by most predominantly selfing species ). However, several recent studies showed elevated ratios of nonsynonymous to synonymous polymorphism (p N =p S ) in various selfing species (compared with their outcrossing relatives), suggesting that deleterious alleles may reach higher frequencies in selfers (e.g., Brandvain et al 2013;Burgarella et al 2015; and other references listed in table 1 of Hartfield 2015).…”

“…Analyses based on molecular data show little evidence for increased ratios of nonsynonymous to synonymous substitutions (d N =d S ) in selfing lineages that would indicate a reduced efficiency of purifying selection (Glémin and Muyle 2014; Hartfield 2015 and references therein): this may be due to the recent origin of those lineages or to the low rates of outcrossing maintained by most predominantly selfing species ). However, several recent studies showed elevated ratios of nonsynonymous to synonymous polymorphism (p N =p S ) in various selfing species (compared with their outcrossing relatives), suggesting that deleterious alleles may reach higher frequencies in selfers (e.g., Brandvain et al 2013;Burgarella et al 2015; and other references listed in table 1 of Hartfield 2015).The lower effective size of selfing populations has been demonstrated empirically using neutral diversity data from a variety of species (e.g., Charlesworth 2003; Glémin et al 2006) and is thought to result from two types of effects. The first type is an automatic increase in the rate of coalescence per generation, since the ancestral lineages of the two homologous copies of a gene in an individual may coalesce in a single generation (with probability 1=2) if this individual has been produced by selfing.…”

Sexual conflict and the evolution of asexuality at low population densities

“…That male behaviour can have a strong effect on the likelihood of observing sexual reproduction becomes arguably more plausible in the case of facultative sex, where the same organism can perform either sexual or asexual life cycles [12]. Which one is employed at any given time can depend on environmental conditions, competition and also-interestingly for our topic-on the availability of males.…”

Stochastic character mapping of state-dependent diversification reveals the tempo of evolutionary decline in self-compatible Onagraceae lineages

“…These consequences include the increased probability of going extinct due to the accumulation of harmful mutations (Lynch et al 1995a,b) and an increased rate of speciation which may be driven by higher among-population differentiation and reproductive assurance that facilitates colonization of new habitats (Baker 1955;Hartfield 2016). The advantages of reproductive assurance may explain why transitions to SC occur repeatedly (Igic et al 2008;Lande and Schemske 1985).…”