Evolutionary genetics of fitness and gender

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The two sexes are selected for different functions yet share the same gene pool. This observation has profound implications for how females and males are expected to evolve, and suggests that conflict may be an important part of their evolutionary interaction. If the sexes are in conflict over control of reproduction, arms races that drive rapid evolutionary change may result. This intersexual 'Red Queen' process challenges traditional views of sexual selection, and suggests that conflict over reproduction alone may be enough to drive the formation of new species. Our research in the Drosophila model genetic system shows that the arms race is fast-paced in this species. When we experimentally prevent one sex (females) from evolving with unique genetic tricks that limit gene expression to males, we see that males quickly evolve to take advantage - through behaviour, through biochemical signals and through direct coercion - over mere dozens of generations. If the same gene is expressed in both sexes, but its function is selected divergently, then a 'tug-of-war' may be the outcome. This second form of conflict can be resolved: many genes are only expressed in females or in males, through a variety of genetic mechanisms. However, our work demonstrates that remarkably high levels of unresolved conflict exist. We find that increases in male fitness are accompanied by matching declines in female fitness, and vice versa. The same genes that help a female survive or reproduce have a harming impact on males. Among the many implications are that low fitness genes are common in populations, and potential gains made via mate choice will be limited by the harming effects of sexual conflict. Our work shows that the X chromosome is the major source of this conflict, worsening the problem of mate choice because male-benefit genes on the X always go to daughters. This problem is alleviated if males transmit their X to sons, as occurs in birds or butterflies. This may account for why birds and butterflies have such bright colouration and dramatic courtship displays. Overall, sexual conflict appears to be a key driver of evolutionary change, and may explain why pathologies causing infertility are common in sexual species, including our own.