Asymmetric evolutionary responses to sex‐specific selection in a hermaphrodite

Bonel, Nicolás; Noël, Elsa; Janicke, Tim; Sartori, Kevin; Chapuis, Élodie; Ségard, Adeline; Meconcelli, Stefania; Pélissié, Benjamin; Sarda, Violette; David, Patrice

doi:10.1111/evo.13565

Cited by 11 publications

(12 citation statements)

References 72 publications

(188 reference statements)

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“…This result is in line with our finding of a trend for a higher genetic variance in male reproductive success. Moreover, in an experimental evolution experiment of P. acuta, Bonel et al (2018) found that sexual selection on males prevents the accumulation of male-detrimental alleles but has no effect on female reproductive success, which corresponds to the lack of strong, either positive or negative, cross-sex genetic correlation found in our study. However, reproductive success measures only one component of overall fitness.…”

Section: Implications and Limitationssupporting

confidence: 50%

“…Therefore, male and female lifetime reproductive success of simultaneous hermaphrodites might be inherently positively linked despite constraints arising from sex allocation loci, which are likely to show sexually antagonistic effects. Interestingly, the above‐mentioned experimental evolution study in P. acuta found that lines evolving in the presence of selection on male reproductive success showed a higher juvenile survival compared to lines where this selection had been suppressed, leaving only the female function under selection (Bonel et al., 2018; Noel et al., 2019). In this study, we did not detect any significant genetic variation in juvenile survival (data not shown) and it was therefore excluded from the presented analyses.…”

Section: Discussionmentioning

confidence: 99%

“…Therefore, hermaphroditic organisms are potentially more prone to exert sexually antagonistic genetic variation of fitness components compared to separate‐sexed organisms (Abbott, 2011; Schärer et al., 2015) and such larger genetic constrains may impede their potential to adapt to novel environments. On the other hand, hermaphroditism may also promote positive genetic correlation between male and female fitness components simply because all genes are expressed in one and the same individual also meaning that every allele that promotes resource acquisition and/or survival is likely to be beneficial to both sex functions (Bonel et al., 2018; Noel et al., 2019). Both assertions are very speculative simply because we still know almost nothing about the genetic architecture of male and female reproduction in simultaneous hermaphrodites.…”

Section: Introductionmentioning

confidence: 99%

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Environmental effects on the genetic architecture of fitness components in a simultaneous hermaphrodite

Janicke

Chapuis

Meconcelli

et al. 2021

Journal of Animal Ecology

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1. Understanding how environmental change affects genetic variances and covariances of reproductive traits is key to formulate firm predictions on evolutionary responses. This is particularly true for sex-specific variance in reproductive success, which has been argued to affect how populations can adapt to environmental change.2. Our current knowledge on the impact of environmental stress on sex-specific genetic architecture of fitness components is still limited and restricted to separatesexed organisms. However, hermaphroditism is widespread across animals and may entail interesting peculiarities with respect to genetic constraints imposed on the evolution of male and female reproduction.3. We explored how food restriction affects the genetic variance-covariance (G) matrix of body size and reproductive success of the simultaneously hermaphroditic freshwater snail Physa acuta. 4. Our results provide strong evidence that the imposed environmental stress elevated the opportunity for selection in both sex functions. However, the G-matrix remained largely stable across the tested food treatments. Importantly, our results provide no support for cross-sex genetic correlations suggesting no strong evolutionary coupling of male and female reproductive traits. 5. We discuss potential implications for the adaptation to changing environments and highlight the need for more quantitative genetic studies on male and female fitness components in simultaneous hermaphrodites.

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Section: Implications and Limitationssupporting

confidence: 50%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Environmental effects on the genetic architecture of fitness components in a simultaneous hermaphrodite

Janicke

Chapuis

Meconcelli

et al. 2021

Journal of Animal Ecology

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“…2010; Bonel et al. 2018) with genotyping across multiple generations (e.g., Turner et al. 2011; Long et al.…”

Section: Moving Forwardmentioning

confidence: 99%

The search for sexually antagonistic genes: Practical insights from studies of local adaptation and statistical genomics

et al. 2020

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Sexually antagonistic (SA) genetic variation-in which alleles favored in one sex are disfavored in the other-is predicted to be common and has been documented in several animal and plant populations, yet we currently know little about its pervasiveness among species or its population genetic basis. Recent applications of genomics in studies of SA genetic variation have highlighted considerable methodological challenges to the identification and characterization of SA genes, raising questions about the feasibility of genomic approaches for inferring SA selection. The related fields of local adaptation and statistical genomics have previously dealt with similar challenges, and lessons from these disciplines can therefore help overcome current difficulties in applying genomics to study SA genetic variation. Here, we integrate theoretical and analytical concepts from local adaptation and statistical genomics research-including F ST and F IS statistics, genome-wide association studies, pedigree analyses, reciprocal transplant studies, and evolve-and-resequence experiments-to evaluate methods for identifying SA genes and genome-wide signals of SA genetic variation. We begin by developing theoretical models for between-sex F ST and F IS , including explicit null distributions for each statistic, and using them to critically evaluate putative multilocus signals of sex-specific selection in previously published datasets. We then highlight new statistics that address some of the limitations of F ST and F IS , along with applications of more direct approaches for characterizing SA genetic variation, which incorporate explicit fitness measurements. We finish by presenting practical guidelines for the validation and evolutionary analysis of candidate SA genes and discussing promising empirical systems for future work.

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“…We did not come up with a clear explanation for this observation—a recent study on the adult traits of the same lines suggests no difference between M and C lines with respect to fecundity and mating behavior (Bonel et al. ). However, our results overall show that the contribution of female reproduction to purging deleterious alleles acting on juvenile survival is much smaller than that of male reproduction.…”

Section: Discussionmentioning

confidence: 70%

Sexual selection and inbreeding: Two efficient ways to limit the accumulation of deleterious mutations

et al. 2019

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Theory and empirical data showed that two processes can boost selection against deleterious mutations, thus facilitating the purging of the mutation load: inbreeding, by exposing recessive deleterious alleles to selection in homozygous form, and sexual selection, by enhancing the relative reproductive success of males with small mutation loads. These processes tend to be mutually exclusive because sexual selection is reduced under mating systems that promote inbreeding, such as self‐fertilization in hermaphrodites. We estimated the relative efficiency of inbreeding and sexual selection at purging the genetic load, using 50 generations of experimental evolution, in a hermaphroditic snail (Physa acuta). To this end, we generated lines that were exposed to various intensities of inbreeding, sexual selection (on the male function), and nonsexual selection (on the female function). We measured how these regimes affected the mutation load, quantified through the survival of outcrossed and selfed juveniles. We found that juvenile survival strongly decreased in outbred lines with reduced male selection, but not when female selection was relaxed, showing that male‐specific sexual selection does purge deleterious mutations. However, in lines exposed to inbreeding, where sexual selection was also relaxed, survival did not decrease, and even increased for self‐fertilized juveniles, showing that purging through inbreeding can compensate for the absence of sexual selection. Our results point to the further question of whether a mixed strategy combining the advantages of both mechanisms of genetic purging could be evolutionary stable.

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Asymmetric evolutionary responses to sex‐specific selection in a hermaphrodite

Cited by 11 publications

References 72 publications

Environmental effects on the genetic architecture of fitness components in a simultaneous hermaphrodite

Environmental effects on the genetic architecture of fitness components in a simultaneous hermaphrodite

The search for sexually antagonistic genes: Practical insights from studies of local adaptation and statistical genomics

Sexual selection and inbreeding: Two efficient ways to limit the accumulation of deleterious mutations

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