Hidden genetic variance contributes to increase the short‐term adaptive potential of selfing populations

Abstract

Standing genetic variation is considered a major contributor to the adaptive potential of species. The low heritable genetic variation observed in self‐fertilizing populations has led to the hypothesis that species with this mating system would be less likely to adapt. However, a non‐negligible amount of cryptic genetic variation for polygenic traits, accumulated through negative linkage disequilibrium, could prove to be an important source of standing variation in self‐fertilizing species. To test this hypothesis, we simulated populations under stabilizing selection subjected to an environmental change. We demonstrate that, when the mutation rate is high (but realistic), selfing populations are better able to store genetic variance than outcrossing populations through genetic associations, notably due to the reduced effective recombination rate associated with predominant selfing. Following an environmental shift, this diversity can be partially remobilized, which increases the additive variance and adaptive potential of predominantly (but not completely) selfing populations. In such conditions, despite initially lower observed genetic variance, selfing populations adapt as readily as outcrossing ones within a few generations. For low mutation rates, purifying selection impedes the storage of diversity through genetic associations, in which case, as previously predicted, the lower genetic variance of selfing populations results in lower adaptability compared to their outcrossing counterparts. The population size and the mutation rate are the main parameters to consider, as they are the best predictors of the amount of stored diversity in selfing populations. Our results and their impact on our knowledge of adaptation under high selfing rates are discussed.

Significance of Linkage Disequilibrium and Epistasis on the Genetic Variances in Non-Inbred and Inbred Populations

“…The ratio was minimized in the populations with intermediate LD and average allele frequency of 0.7 (3 to 10%) and high LD and average allele frequency of 0.5 (3 to 8%). Our results also give support to the main conclusions of J Clo, J Ronfort and D Abu Awad [2], who assumed additive model under LD and distinct selfing rates. The differences observed for outcrossing species relies on their assumption of negative LD.…”

“…Further, he also recognized the significance of the linkage phase between genes on the population variance and on the correlation between relatives. The influence of linkage disequilibrium (LD), epistasis, and inbreeding on the genotypic variance continues to be an important area of investigation in genetics and evolution [2][3][4].…”

“…Based on the additive model, J Clo, J Ronfort and D Abu Awad [2] showed that assuming stabilizing selection and high mutation rates, self-pollinated populations are able to accumulate genetic variation through negative LD. Using a meta-analysis of quantitative traits heritability, J Clo, L Gay and J Ronfort [5] confirmed previous theoretical and empirical evidences that selfpollinated populations exhibit lower levels of additive variance for quantitative traits.…”

Genetics of quantitative traits with dominance under stabilizing and directional selection in partially selfing species

“…Following Clo et al. (2020), the life cycle can be summarized by five successive events. First, there is a phenotype‐dependent choice of the first parent (selection), followed by mating‐type choice (selfing versus outcrossing at rates s and [1‐ s ], respectively).…”

“…2017; Clo et al. 2020; Cheptou 2021). A consequence of the focus of theoretical and empirical studies on the additive variance is that little is known about the effect of dominance on the evolutionary potential of populations, or how its interaction with self‐fertilization can modify the effect of inbreeding on evolvability.…”