Chapter 12 Summary

Sexual reproduction requires conspecific males and females to attract and find each other and then to successfully court and mate. Because females by definition invest more in gametes than males do (anisogamy), the sexes have different optimal reproductive strategies. Males produce large numbers of small, mobile sperm at relatively low cost, and therefore have a shorter reproductive cycle than females, which produce fewer, large, costly ova at a slower rate. The greater the difference in gametic investment, the more strongly skewed the operational sex ratio of receptive adults becomes in favor of males. Male fitness is thus limited by the availability of females. Males compete among themselves for access to mates by employing various male mating strategies. Females usually have a wide choice of males, and benefit by selecting high-quality mates. These differences are the basis for the traditional reproductive sex roles, with males being the competitive and actively courting sex and females being coy and choosy. Which sex searches while the other gives the long-distance attraction signal depends strongly on a species’ male mating strategy.
Sexual selection is the evolutionary process that arises from competition among members of one sex for access to mates of the opposite sex. In contrast to natural selection, which maximizes fecundity and survivorship, sexual selection maximizes mating success. It typically leads to sexual dimorphism, differences between male and female phenotypes within a species. Intersexual selection leads to the coevolution of male mate attraction signals, female preferences for those traits, and viability consequences of both male traits and female preferences. This coevolution is best described using a multivariate quantitative genetics process. Different models of intersexual selection emphasize interactions between different components of that process. All models require that there be heritable variance in female preference behavior, so that mating biases can evolve. These processes are not exclusive.
The Fisherian runaway model is driven by indirect selection on female preferences caused by a positive genetic covariance between the male trait and the female mating bias for the trait. Females indirectly benefit from preferring males with highly attractive heritable traits, because their sons may inherit these traits and in turn be highly attractive to females—the “sexy sons” effect. Some evidence for the Fisherian model in natural systems exists, but it is often accompanied by effects of one or more of the other models.
The good genes model proposes that females produce fitter offspring by preferring males with traits that indicate their heritable viability or health. There is indirect selection on the female preference caused by a positive genetic covariance between female mating bias and heritable male viability. The male trait must be a costly, condition-dependent display signal that reliably indicates his viability. Male viability must be heritable, and the process will be accelerated if the display trait is also heritable. There is growing evidence in support of this model in natural systems.
The direct benefits model describes the situation in which females develop preferences for male characteristics that provide them with material benefits. There is direct selection on female preferences because of the immediate benefits. No covariance terms are required, and the male trait does not need to be heritable. Environmentally determined variation in males’ ability to provide benefits is sufficient, as long as females have some cue or signal of this variation. Empirical support is most abundant for this model; however that may reflect the fact that it is the easiest of the alternatives to test.
The sensory bias model proposes that males evolve traits that exploit pre-existing sensory biases in females for relevant environmental cues involved in detection of food or predators. In this case, there is indirect selection for female mating preferences arising from pleiotropic genes that affect mating biases and other behaviors. A few good examples in support of this model exist, but it is believed to serve primarily as a mechanism to initiate male display traits and is likely to be displaced by one or more of the other model processes.
The sexual conflict, or chase-away, model envisions a sexual arms race in which males evolve traits that manipulate females to their detriment and females then evolve counter-adaptations. Sexual conflict is characterized by direct antagonistic selection between the sexes, such that traits that enhance the fitness of one sex reduce the fitness of the other. This model can lead to a stable solution, in which the costs and benefits to the sexes are in balance, or to cycles of male escalation and female counteradaptation. Evidence for this model is increasing as more studies look for it.
Persistent female preference for more extreme male trait values causes trait expression to be costly and thus strongly dependent on male condition. Condition is affected by many loci and thus presents a large target for mutations. According to the genic capture hypothesis, trait expression should reveal a male’s overall genetic quality and viability. Many kinds of mate attraction signals show heightened condition-dependent trait expression and provide direct and indirect benefits to females that base their mate choice on such traits. Selection on males then favors increased isolation of the different physiological pathways needed for trait development, a process that results in developmental modularity.
All modalities have been exploited for sexually selected signals. Color patches are a common target of sexual selection because their expression is often condition dependent. Carotenoid-based color patches are generally more dependent on health and environmental conditions than melanin-based color patches, which tend to reflect stress resistance, immunocompetence, and aggressiveness. The brightness of structural color patches, including iridescent and white patches, is readily disrupted by poor condition. The immaculateness of the borders between contrasting color patterns can also reflect overall quality. Whereas tail elaboration is usually a reliable indicator of health and quality in birds, it is too often exploited to exaggerate body size in fish to be a useful mate criterion. The performance quality of vigorous behavioral displays using various combinations of modalities provides one of the best male trait targets for female preference because is it strongly tied to physiological condition, health, and viability, and is difficult to modularize. Chemical blends can directly reveal immunocompetence and current levels of infection. Fluctuating asymmetry is not a good indicator of overall quality.
Good-genes traits provide heritable additive genetic benefits to all females, but choosy females can also select males that have compatible genes with respect to their own genotype, a process based on nonheritable nonadditive genetic variation. A widespread benefit is optimization of heterozygosity at the MHC loci, which improves immunocompetence and offspring survival. Identification of suitably dissimilar mates is achieved via olfactory cues or via cryptic female choice after copulation, which is accomplished by differential sperm selection. Similar mechanisms can also be used to avoid inbreeding and achieve optimal outbreeding.
Females may benefit by attending to signals and cues for additional criteria. One is male age; older males have proven their ability to survive, and show their age in various cues or signals. Another criterion is parental ability; males that provide females with food or other resources demonstrate their ability to provide for offspring. A third criterion is dominance; females may prefer dominant males and respond to signals that have evolved for the purpose of resolving male–male conflicts and status in selecting dominant mates. They may also eavesdrop on the outcomes of male–male contests or incite male competition.
Courtship facilitates successful copulation and consists of an exchange of signals between the sexes. If sex roles are traditional, male displays primarily serve to persuade and stimulate females, while females remain coy to further assess male suitability. Male displays are associated with female behavioral freedom to choose. Male courtship display is more elaborate in species in which the females search for mates while males defend resources and in arena display mating systems. Sufficiently realistic models depicting the battle of the sexes over mating find that a broad range of conditions favor coyness by females and honest signals of fidelity and helpfulness by males. Specific displays may provide information on species and sex identification and sexual receptivity. Synchronization signals coordinate the immediate act of gamete release and fertilization. In some species, males evolve mechanisms to stimulate and manipulate (or coerce) females to mate. In other species, males must cautiously interact with females using negotiation strategies. Partial and complete sex role reversal occurs in species with very high male reproductive investment and strong competition among females for resources, breeding opportunities, or mates. Appropriate mating signals are suitably reversed as well.