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The role of sexually antagonistic effects in maintaining genetic variation in natural populations

Final Activity Report Summary - SEXUAL ANTAGONISM (The role of sexually antagonistic effects in maintaining genetic variation in natural populations)

Both theory and experimental data suggest that males and females of the same species may have divergent genetic optima. At fitness-related loci, a given genotype may be selected in opposite directions in the two sexes. Such sexually antagonistic selection will reduce the otherwise-expected positive genetic correlation between male and female fitness. Given the frequency of sexual dimorphisms in morphology, physiology and life histories across numerous taxa, divergent sex-specific selection may therefore play an under-appreciated role in the maintenance of genetic variance for fitness.

We found evidence for sexually antagonistic fitness variation in a natural population, using data from a long-term study of red deer (Cervus elaphus) on the Isle of Rum, Scotland. We showed that male red deer with relatively high fitness fathered, on average, daughters with relatively low fitness. This was due to a negative genetic correlation between estimates of fitness in males and females. In particular, we showed that selection favoured males that carried low breeding values for female fitness. Our results demonstrated sexually antagonistic selection: genes that made a good male did not generally make a good female, and vice versa.

We further showed that red deer had sexually dimorphic bone proportions. Males usually had wider skulls and bulkier bones than females of the same size. We used skull and leg bone proportions to estimate how much an individual deviated from the norm physiognomy of its sex. Females with more male-like skull features were less fecund. This was caused by a negative genetic correlation between female skull proportions and fecundity. This result suggested that bone proportions, reproductive cycles and fecundity were regulated by physiological processes (e.g. hormone regimes) that could be triggered by the same, or closely linked, genes. If males were selected for more male-like physiognomy, their female relatives would carry genes that coded for more male-like bone proportions, but also for lower fecundity. This could be one of the selection trade-offs underlying the antagonistic genetic variation for fitness observed in red deer, and deviations from the norm physiognomy could be used as phenotypic signatures of genetic sexually antagonistic effects in this species.

In summary, our study proved the existence of limits to the evolution of a single genetic optimum for males and females in the wild. Furthermore, we showed selection against males that carried optimal female genotypes, a finding that had important implications on how selection acted on individuals in the wild. It pinpointed the impact of phenotype sex on the adaptive value of genotypes, a fact that called for re-evaluation of many studies on selection in natural populations and of selection and mate choice experiments in the lab, which had mostly ignored intersexual genetic covariances. These results were an important step towards refining a widely known general concept. They demonstrated that the selective advantage of 'good genes' was sex-specific. Good genes for males were not necessarily good genes for females.