Genetic Correlations between the Sexes

When particular males mate with particular females within a population, the traits within each sex that make these pairings distinctive are likely to become genetically associated. The best-known example of this phenomenon was proposed by R. A. Fisher in 1930, who argued that a self-accelerating evolutionary process known as 'runaway' selection could lead to extreme male and female pheno-types. Fisher noted that when females tend to vary in the strength of their mate preferences, that is, when some females are 'choosier' than others, and when choosy females prefer to mate with males possessing extreme phenotypes, such males will gain disproportionate fitness relative to other males in the population. If male and female traits are heritable, the greater mating success of extreme males leads to an increase in the frequency of extreme male traits, as well as a corresponding increase in the frequency of females with preferences for such males, among the progeny of choosy females. With regard to male traits and female choosiness, mating in such cases is assortative rather than random. Thus, genes for extremes in male and female traits are brought together simply by the act of mating, and they occur in combinations that, directly or indirectly, enhance the fitness of individuals within each sex. Such conditions, Fisher claimed, will cause extremes in male traits and in female preferences for such traits to increase over evolutionary time.

This process is likely to operate for other male and female traits as well. A tendency for receptive females to aggregate, say at food or near shelter, could favor the reproduction of males who are attracted to such female aggregations. A tendency for females to resist matings with just any male could favor reproduction by males who are most persistent in their attempts to mate. A tendency for males to defend progeny from predators could favor the reproduction of females who leave offspring with such males, and a tendency for females to leave offspring with such males could increase mating opportunities for such females, which in turn could favor males who provide more parental care. If female tendencies to prefer particular males are heritable, a genetic correlation between the male and female traits that lead to particular matings will arise among the progeny of these pairs, and as variance in mate number becomes greater due to nonrandom mating by females, increases in the frequencies ofparticular male phenotypes and particular female preferences, as well as increases in the strength of the genetic association between these male and female characteristics, will cause further increases in fitness variance for each sex. The rate of evolution accelerates too because direct selection on male traits causes an indirect response to selection on genetically correlated female traits and vice versa.

But how do such associations get started? Why might females develop a preference for extreme male phenotypes in the first place? One hypothesis suggests that females prefer traits in males that stimulate particular sensory channels. Positive responses to certain visual or auditory cues in their environment may have enhanced food capture or shelter location by females. If such tendencies enhance female fitness, they are likely to become widespread. Males who fortuitously possess traits that resemble these attractive stimuli are likely to encounter females more often, and because they are more readily available than less conspicuous males, a runaway process can ensue between attractive males and attracted females. Another hypothesis suggests that females prefer males possessing traits that enhance the survival of their offspring. That is, females prefer to mate with males who possess so-called good genes. Most good genes scenarios assume that traits associated with fitness are influenced by multiple genetic factors and thus are normally distributed (Figure 1). For many such traits (e.g., birthweight, body height, disease resistance), the average trait value for the population is also somewhat less than the trait value that provides optimum fitness. Individuals in such populations also may exhibit extreme values of these traits, although these individuals often have fitness less than the optimum. These relationships confirm that good genes can exist in this population. The question is, what sort of mate should the average female choose?

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Phenotype Phenotype Phenotype

Figure 1 The distribution of a quantitative trait in a hypothetical population in which females have the option of selecting among males who vary in their expression of this trait; (a) average females selecting males of average phenotype are likely to produce average offspring; (b) average females selecting males of optimal phenotype will produce suboptimal offspring; (c) only average females choosing males with extreme phenotypes will produce offspring of optimal phenotypes, a condition likely to cause runaway selection favoring extreme male phenotypes and female preference for extreme males; red line: female parental phenotype; blue line: male parental phenotype; green line: offspring phenotype. Redrawn from Shuster SM and Wade MJ (2003) Mating Systems and Alternative Mating Strategies. Princeton, NJ: Princeton University Press, Figure 7.1.

If an average female (red line, Figure 1a) chooses a mate with the average trait value (blue line, Figure 1 a), she will produce average offspring (green line, Figure 1a). If she chooses a male with the optimal trait value (blue line, Figure 1b), she will produce offspring with phenotypes above the trait average, but these offspring will still exhibit phenotypes with suboptimal fitness (green line, Figure 1b). It is only when females mate with males possessing extreme phenotypes (blue line, Figure 1c) that their offspring will exhibit the optimal trait phenotype (green line, Figure 1c). Thus, even in this good genes example, it is clear that female mate preferences can rapidly favor extreme male pheno-types, here within a single generation. Such conditions are likely to establish genetic correlations between male traits and female preferences for them that, as the runaway process accelerates, will soon have little relevance to actual offspring fitness. Although natural selection may favor an optimum phenotype, by this mechanism, sexual selection favors phenotypes that exceed the fitness optimum. Furthermore, as explained above, when fitness variance within one sex becomes large due to a sex difference in mate numbers, the contribution of fitness variance by the other sex to total fitness variance can become comparatively small. For these reasons, again paradoxically from a PIT perspective, when sexual selection intensifies, mate choices based on good genes are likely to contribute little to the total response to selection.

See also: Sex Ratio.

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