Abstract
How natural diversity is maintained is an evolutionary puzzle. Genetic variation can be eroded by drift and directional selection but some polymorphisms persist for long time periods, implicating a role for balancing selection. Here, we investigate the maintenance of a chromosomal inversion polymorphism in the seaweed fly Coelopa frigida. Using experimental evolution and quantifying fitness, we show that the inversion underlies a life-history trade-off, whereby each haplotype has opposing effects on larval survival and adult reproduction. Numerical simulations confirm that such antagonistic pleiotropy can maintain polymorphism. Our results also highlight the importance of sex-specific effects, dominance and environmental heterogeneity, whose interaction enhances the maintenance of polymorphism through antagonistic pleiotropy. Overall, our findings directly demonstrate how overdominance and sexual antagonism can emerge from a life-history trade-off, inviting reconsideration of antagonistic pleiotropy as a key part of multi-headed balancing selection processes that enable the persistence of genetic variation.
Highlights
How natural diversity is maintained is an evolutionary puzzle
While the phenotypic effect on females is moderate, αα males can be up to three times larger than ββ males, but αα males can take up twice as long to develop than ββ males[26,38]. This pattern suggests a trade-off between adult size and egg-to-adult development, which may result in a trade-off between fertility and survival. These findings make the inversion polymorphism in C. frigida a relevant empirical case to investigate the role of antagonistic pleiotropy in promoting polymorphism and to test interactions with other mechanisms favouring the maintenance of variation, such as sex-specific effect, overdominance and spatially varying selection
Results from the experimental evolution trial coupled with simulations show that the inversion dynamics in C. frigida can be largely explained by an antagonistic relationship between viability and fecundity
Summary
How natural diversity is maintained is an evolutionary puzzle. Genetic variation can be eroded by drift and directional selection but some polymorphisms persist for long time periods, implicating a role for balancing selection. Recent models suggest that the role of antagonistic pleiotropy has been underestimated[19,20,21,22] by showing that several factors, realistic in natural populations, can promote polymorphism persistence These factors include trait-specific dominance (i.e. when the level of dominance varies between fitness components22,23), sex-specific selection (i.e. selection strength on each fitness component differs between sexes19) and spatially and temporally varying selection[20,21]. This pattern suggests a trade-off between adult size and egg-to-adult development, which may result in a trade-off between fertility and survival These findings make the inversion polymorphism in C. frigida a relevant empirical case to investigate the role of antagonistic pleiotropy in promoting polymorphism and to test interactions with other mechanisms favouring the maintenance of variation, such as sex-specific effect, overdominance and spatially varying selection
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