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Impact of deleterious mutations, sexually antagonistic selection, and mode of recombination suppression on transitions between male and female heterogamety.

ABSTRACT: Deleterious mutations accumulating on non-recombining Y chromosomes can drive XY to XY turnovers, as they allow to replace the old mutation-loaded Y by a new mutation-free one. The same process is thought to prevent XY to ZW turnovers, because the latter requires fixation of the ancestral Y, assuming dominance of the emergent feminizing mutation. Using individual-based simulations, we explored whether and how an epistatically dominant W allele can spread in a young XY system that gradually accumulates deleterious mutations. We also investigated how sexually antagonistic (SA) polymorphism on the ancestral sex chromosomes and the mechanism controlling X-Y recombination suppression affect these transitions. In contrast with XY to XY turnovers, XY to ZW turnovers cannot be favored by Y chromosome mutation load. If the arrest of X-Y recombination depends on genotypic sex, transitions are strongly hindered by deleterious mutations, and totally suppressed by very small SA cost, because deleterious mutations and female-detrimental SA alleles would have to fix with the Y. If, however, the arrest of X-Y recombination depends on phenotypic sex, X and Y recombine in XY ZW females, allowing for the purge of Y-linked deleterious mutations and loss of the SA polymorphism, causing XY to ZW turnovers to occur at the same rate as in the absence of deleterious and sex-antagonistic mutations. We generalize our results to other types of turnovers (e.g., triggered by non-dominant sex-determining mutations) and discuss their empirical relevance.

SUBMITTER: Saunders PA

PROVIDER: S-EPMC6781157 | biostudies-literature | 2019 Sep

REPOSITORIES: biostudies-literature

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Impact of deleterious mutations, sexually antagonistic selection, and mode of recombination suppression on transitions between male and female heterogamety.

Saunders Paul A PA Neuenschwander Samuel S Perrin Nicolas N

Heredity 20190427 3

Deleterious mutations accumulating on non-recombining Y chromosomes can drive XY to XY turnovers, as they allow to replace the old mutation-loaded Y by a new mutation-free one. The same process is thought to prevent XY to ZW turnovers, because the latter requires fixation of the ancestral Y, assuming dominance of the emergent feminizing mutation. Using individual-based simulations, we explored whether and how an epistatically dominant W allele can spread in a young XY system that gradually accum ...[more]

PMID: 31028370

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Project description:BackgroundThere is theoretical and empirical evidence for strong sexual selection in males having positive effects on population viability by serving to purify the genome of its mutation load at a low demographic cost. However, there is also theoretical and empirical evidence for negative effects of sexual selection on female fitness, and therefore population viability, known as the gender load. This can take the form of sexually antagonistic (SA) genetic variation where alleles with a selective advantage in males pose a detriment to female fitness, and vice versa. Here, using seed beetles, we shed light on a previously unexplored manifestation of the gender load: the effect of SA genetic variation on tolerance to inbreeding.ResultsWe found that genotypes encoding high male, but low female fitness exhibited significantly greater rates of extinction upon enforced inbreeding relative to genotypes encoding high female but low male fitness. Also, genotypes encoding low fitness in both sexes exhibited greater rates of extinction relative to generally high-fitness genotypes (though marginally non-significant), an expected finding attributable to variation in mutation load across genotypes. Despite follow-up investigations aiming to identify the mechanism(s) underlying these findings, it remains unclear whether the gender load and the mutation load have independent consequences for tolerance to inbreeding, or whether these two types of genetic architecture interact epistatically to render male-benefit genetic variation relatively intolerant to inbreeding.ConclusionsRegardless of the underlying mechanism(s), our results show that male-benefit/female-detriment SA genetic variation poses a previously unseen detriment to population viability due to its elevated vulnerability to inbreeding/homozygosity. This suggests that sexual selection in the context of SA genetic variance for fitness may enhance the gender load on population viability more than previously appreciated, due to selecting for male-benefit SA genetic variation that engenders lineages to extinction upon inbreeding. We note that our results imply that SA alleles that are sexually selected for in males may be underrepresented or even lacking in panels of inbred lines.

Dataset Information

Impact of deleterious mutations, sexually antagonistic selection, and mode of recombination suppression on transitions between male and female heterogamety.

Publications

Impact of deleterious mutations, sexually antagonistic selection, and mode of recombination suppression on transitions between male and female heterogamety.

Similar Datasets

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