Mating system theory, based on economics of territorial defense, has been applied to describe the diversity in social systems across taxa. Mating systems play a critical role in genetic, demographic, and social dynamics of populations. Early models explaining mating system diversity emphasized links between resource and mate monopolization. These economic models favored largely extrinsic factors in explaining mating system evolution, but they did not explicitly consider intrinsic genetic factors that drive mating system evolution, nor the likelihood of transitions between mating system states. Mating systems generate strong sexual selection favoring the evolution of genetic alternative strategies, or plastic strategies that depend on social context or individual condition. By influencing space use, genetic mechanisms complement ecological approaches, but they could also shape mating system evolution independent of ecology. Paternal care can shift the advantage to a monogamous system. In addition, parental care can dramatically alter patterns of selection on the newly derived caregiving sex, which has cascading effects on selection for resource allocation in the ancestral caregiving sex. Mate choice and sexual selection involving Fisherian runaway, which genetically couples female choice and male traits, is a key component of the process by which partners choose mates for signals carrying genes for other traits of high quality, some of which might be linked to caregiving behavior. Throughout this review, we highlight the need for experiments of diverse types (genetic, endocrine, signals) to unravel the complex evolutionary dynamics of mating systems.
Emlen and Oring 1977 described how the distribution of resources (including potential mates) in both time and space influences the economics of defense, and hence the potential for polygamy. Orians 1969 predicted that the quality of resources controlled by a male (i.e., territory) would influence his access to mates, with males on higher-quality territories supporting additional females compared to monogamous males on low-quality territories. These early economic models were subsequently expanded by Shuster and Wade 2003, which examined how the opportunity for sexual selection and the evolution of alternative reproductive strategies influence the evolution of mating systems. In addition, game theory approaches and phylogenetic approaches provide theoretical and empirical avenues for studying the transitions among mating systems (see Alternative Reproductive Strategies and Evolutionary Game Theory). Fisherian runaway sexual selection and the handicap principle are fundamental explanations for the evolution of elaborate male traits related to mating success. Lande 1981 mathematically demonstrated the process linking male traits and female preference, while Zahavi 1975 first argued that females prefer certain traits precisely because they impose a high cost on the male’s survival. While initially deemed implausible, Grafen 1990 (cited under Sexual Selection) later demonstrated the feasibility of the handicap principle. Parent-offspring conflict theory was developed by Trivers 1974 to describe the social tension in mating systems due to a variety of emerging ideas of the role of genetics, including those of Hamilton 1964 on inclusive fitness theory. Burley 1986 developed and later tested the differential allocation hypothesis that predicted how differences in attractiveness or quality between parents can influence allocation patterns, intra-pair dynamics, and even lifetime reproductive success.
Burley, N. 1986. Sexual selection for aesthetic traits in species with biparental care. American Naturalist 127:415–445.
The “differential allocation hypothesis” was originally formulated for species exhibiting biparental care, and thus social monogamy, but it has since been extended to polygynous species as well as species with no care.
Emlen, S., and L. Oring. 1977. Ecology, sexual selection, and the evolution of mating systems. Science 197:215–222.
Emlen and Oring reviewed the types of mating systems, including monogamy, polygyny, polyandry, promiscuity, and polygamy, and they argued that mating systems are driven by the accessibility that each sex has to mates, and by the potential for desertion by one mate (or both).
Hamilton, W. D. 1964. The genetical evolution of social behaviour. Journal of Theoretical Biology 7:1–52.
Hamilton derived inclusive fitness theory, which serves as a cornerstone for modern theories of social systems and is at the core of genetic theories of mating systems. He also generalized ideas of kin selection into cooperation arising from genic self-interest referred to as greenbeards (see Genetic Theories).
Lande R. 1981. Models of speciation by sexual selection on polygenic traits. Proceedings of the National Academy of Sciences of the United States of America 78:3721–3725.
Lande, along with M. Kirkpatrick (see Kirkpatrick 1982, cited under Sexual Selection), derived mathematically a profoundly important, seemingly intuitive statement, made by Sir Ronald Fisher (in Fisher 1930, cited under Sexual Selection), regarding “Runaway Sexual Selection” and its propensity to genetically couple male traits and female choice.
Orians, G. H. 1969. On the evolution of mating systems in birds and mammals. American Naturalist 103:589–603.
Orians constructed the polygyny threshold model, an earlier mating system version of the “ideal free distribution,” which shows how females may gain fitness by mating with a male who already has a mate because of economic benefits from the territory compared to mating with other as yet unmated males.
Shuster, S., and M. J. Wade. 2003. Mating systems and strategies. Princeton, NJ: Princeton Univ. Press.
The authors work out in detail the factors promoting the evolution of alternative strategies in mating systems and intensity of selection on mating systems, reviewing diverse mating systems and alternative strategies.
Trivers, R. L. 1974. Parent-offspring conflict. American Zoologist 14:249–264.
Trivers realized that there was strong tension between the sexes and between parents and offspring in the mating system, based on his empirical observations on the sexes in pigeons. In a series of papers, including this one, he laid the groundwork for a modern theory of mating systems.
Zahavi, A. 1975. Mate selection: A selection for a handicap. Journal of Theoretical Biology 53:205–214.
Argued to be unfeasible for more than a decade, Zahavi’s verbal explanation of the handicap principle, along with diverse modern analogues involving direct versus indirect benefits of mate choice, is now a cornerstone of sexual selection theory involving parental care and mate choice.
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