Population Genetics and Genome Evolution of Selfing Species

Abstract

The evolution of self‐fertilisation from outcrossing is one of the most frequent evolutionary transitions in hermaphrodite species of plants, animals and fungi. Accordingly, a large body of theoretical and empirical studies has been dedicated to understand the impact of selfing on population genetics and genome evolution. Compared to outcrossing, selfing reduces heterozygosity, effective recombination and migration rate and increases genetic drift. As a consequence, selfing species are expected to show reduced and more structured genetic diversity, genomic degradation and low adaptive potential because they should respond less efficiently to natural selection. Although selfing can have immediate advantages and be selected for, all detrimental genetic effects are thought to drive selfing lineages to extinction on the long run. Human activities (e.g. domestication and breeding, ecosystem alterations) can also induce mating system shifts that could potentially threaten long‐term population viability. Key Concepts The transition from outcrossing to selfing affects fundamental population genetics parameters that influence the evolutionary trajectory of populations and species. Selfing increases homozygosity, which reveals recessive deleterious alleles causing inbreeding depression. Selfing reduces the effective recombination, which increases genome‐wide linkage disequilibrium. Selfing increases genetic structure by reducing gene flow. Selfing reduces the effective population size, making selfing species less diverse and less efficient in responding to selection than outcrossing ones. The outcome of selection in selfing species depends on the interplay among dominance level and selection strength of mutations and the initial conditions (new mutations or preexisting variation). In selfing organisms, sexual conflicts and the spread of selfish genetic elements are attenuated. Overall, the genome of selfing species is prone to the accumulation of deleterious mutations and to low rates of fixation of beneficial mutations, which should make selfing an evolutionary ‘dead‐end’ strategy. The genetic consequences induced by self‐fertilisation have practical implications for human activities linked to the conservation and management of natural and cultivated resources.

Molecular Systematics of Valerianella Mill. (Caprifoliaceae): Challenging the Taxonomic Value of Genetically Controlled Carpological Traits

“…pumila group, where outcrossing can occur randomly in nature [ 8 ]. In contrast, genetic structure is high among populations (70.13%), as previously described for Valerianella [ 34 ] and expected for self-pollinated plants [ 56 , 57 , 58 ], where selfing increases the genetic structure between populations due to the absence of gene flow [ 59 ]. The probable existence of a mixed mating system (selfing, crossbreeding) in the Valerianella species pairs [ 8 ] would explain the balance between the moderate values of genetic diversity and the high genetic structuring of their populations, since complete selfing is extremely rare in nature [ 60 ].…”

Polygenic selection to a changing optimum under self–fertilisation

“…(2014)). Self–fertilisation incurs several genetic effects (Burgarella and Glémin 2017; Glémin et al . 2019); most notably, the resulting inbreeding increases homozygosity and hence also the effects of genetic drift, which manifests itself as a reduction in N e thus weakening the efficacy of selection (Pollak 1987; Charlesworth 1992; Caballero and Hill 1992; Nordborg and Donnelly 1997).…”

“…The transition to self-fertilisation is widely observed in nature but tends to occur at the tips of species' trees, indicating that they are short-lived (reviewed by Wright et al (2013); Barrett et al (2014)). Selffertilisation incurs several genetic effects (Burgarella and Glémin 2017;Glémin et al 2019); most notably, the resulting inbreeding increases homozygosity and hence also the effects of genetic drift, which manifests itself as a reduction in N e thus weakening the efficacy of selection (Pollak 1987;Charlesworth 1992;Caballero and Hill 1992;Nordborg and Donnelly 1997). The resulting homozygosity also reduces effective recombination rates and, hence, the creation of new genetic combinations (Nordborg et al 1996;Nordborg 2000).…”

How and When Does Outcrossing Occur in the Predominantly Selfing Species Medicago truncatula?

“…Yet, once a sufficiently large selfing rate has been reached, the fitness advantages of increasing the selfing rate might become negligible, which would result in a weaker selection gradient. Moreover, the effective population size is expected to be extremely small at high selfing rates ( Glémin, 2007 ), which could further decrease the efficiency of selection ( Burgarella and Glémin, 2017 ). In light of these arguments, residual outcrossing could just be a prolonged transient state toward complete selfing.…”