The evolution of males and females depends on the environment

Opportunities for adaptation in females and males are mediated by life history and population characteristics that vary widely between species. Combining these factors with environmental heterogeneity can yield surprising evolutionary outcomes that are not always predicted by classic theories that deal with each factor separately.

Tim Connallon, Shefali Sharma and Colin Olito have analysed four simple models of evolution of female and male adaptations in changing environments. They compared the outcomes to classical population genetics models of sex-specific selection in stable environments and found some important differences.

Females and males make roughly equal genetic contributions to offspring. Consequently, the response to natural selection tends to depend equally on the pattern of selection in each sex. Selection does not necessarily increase adaptation of both sexes, but instead favours evolutionary changes in which the gains in adaptation for one sex are sufficient to offset any reductions in adaptation for the other. Such ‘sexually antagonistic’ selection is common and contributes to the maintenance of genetic variation.

Classical population genetics theory predicts that, where there are separate sexes, natural selection will favour genotypes that allow fitness across both males and females to be maximised. While these theories have proved extremely useful they tend to focus on evolution in constant environments – a condition that will be violated in many species.

Tim and his colleagues are interested in the outcomes of sex-specific selection in variable environments and how the life history and demography of a species’ can influence evolutionary dynamics. To this end they developed four mathematical models that vary in the life stage, or the sex, that disperses through a spatially or temporally heterogeneous environment.

In the first model, adults of both sexes disperse from the areas they were born in, with local selection happening before dispersal, and mating and reproduction happening after dispersal. This scenario applies to species with relatively immobile early-life stages, including many vertebrate and insect taxa. The second model considers taxa that have highly mobile early life-stages such as seed dispersal in plants or larval dispersal in many aquatic organisms. In the third example, adults from only one sex disperse from the area they were born in, prior to mating and reproduction. Sex biased migration is common in animals and can be strongly female biased or male biased. Finally, the fourth model deals with sex-specific selection that changes over time but is uniform across space.

When they ran these four different models and compared the outcomes with predictions from the classical population genetics models, they found the details of a species’ life history and demography were critical to determining the evolutionary dynamics of sex-specific adaptations.

For example, the models predict that conspicuous sex-limited colour polymorphisms (the simultaneous occurrence of multiple phenotypes limited to one sex only) should be particularly common in species that have strong sex-biased migration (scenario 3) and species where dispersal occurs early in the life cycle (scenario 2).

This work paves the way for diversifying the range of species that serve as models for studying sex-specific adaptations.

This work has been published in The American Naturalist.

Model outputs demonstrating that environmental variability promotes the maintenance of genetic variation beyond the comparatively restrictive conditions for polymorphism in a constant environment (solid grey versus dotted grey curves). Solid pink and blue lines indicate the likelihood of a beneficial allele becoming fixed for males and females in the different scenarios and over increasing selection pressure. Note that the pink curves overlay the blue curves in Models 1 and 4 and in Model 3 the equivalent results (with sexes reversed) would be obtained if there was female-limited dispersal.