Evolution of Animal Mating Systems

by

Ingrid Ahnesjö, Luc Bussière

• LAST REVIEWED: 21 April 2021
• LAST MODIFIED: 21 April 2021
• DOI: 10.1093/obo/9780199941728-0136

Introduction

Animal mating systems are fascinating and diverse, and their evolution is central to evolutionary biology. A mating system describes patterns and processes of how females and males mate and reproduce successfully, and how this relates to their reproductive ecologies, including demographic and environmental factors. One of the more stimulating challenges in biology is to provide a comprehensive explanation for the evolution of mating adaptations among animals. In the course of sexual reproduction, animals engage in a dizzying array of traits, behaviors, and strategies. Such diversity simultaneously requires and eludes categorization: it is required for a general understanding, but at once confounds any rigorous classification because an almost inexhaustible supply of animal examples disrupt otherwise neatly ordered systems (see Classifications of Animal Mating Systems). Historically, mating with a single partner was thought to be a common mating system among animals. However, increasing observations of multiple mating by both sexes, supported by genomic evidence of mixed parentage within families, has since revealed that strict genetic monogamy is rare. In this bibliography, the selected literature highlights a compelling diversity and flexibility among animal mating systems, and sexual selection emerges both as a contributing cause and consequence of this variation. Sexual selection plays a central role in animal mating system evolution, and key references provide insights into its operation before and after mating, and describe how it leads to the expression of secondary sexual traits and sexual conflicts. Efforts to explain diversity in animal mating systems have often focused on how acquiring mates or matings relates to variance in reproductive success. This variation and diversity can be approached at the level of an individual, among individuals in a population, or between species. However, a preoccupation with the mean or average pattern often leads to generalizations that obscure important diversity crucial to evolutionary understanding. To avoid unnecessary categorization, the presentation here focus`es on variation in mating patterns and contrasts multiple mating with mating with a single partner. Furthermore, it considers the wider effects of animal mating systems, and includes associations with patterns of parental care. The aim with this bibliography is to provide key citations demonstrating that animal mating systems evolve from diverse, interactive, complex and dynamic processes resulting in a variety of adaptive mating strategies in females and males. A grateful acknowledgment is given to C. Kvarnemo and D. Gwynne for insightful comments.

General Overviews

What is known about animal mating systems owes much to the work of naturalists, including Darwin’s many observations and reflections on the reproductive ecologies and mating systems in animals (see Darwin 1871). According to Orians 1969, as well as Emlen and Oring 1977, Darwin was the first to discuss mating systems in evolutionary terms, reflecting considerably on sexual selection, sexual dimorphisms, and mating patterns. Extravagant ornaments and weapons are often a result of sexual selection and collectively are called secondary sexual characteristics, in contrast to the primary sex organs (although the distinction between primary and secondary characters can be unclear; see Secondary Sexual Traits). Many observant naturalists have focused on birds and mammals, and Orians 1969 influentially described animal mating systems as mostly monogamous, but also predicted conditions for polygyny. In 1983 Thornhill and Alcock published an influential book titled The Evolution of Insect Mating Systems. Emlen and Oring 1977 further developed thinking about mating system theory by focusing on the distribution of mates and the environmental potential for polygamy, introducing the concept of operational sex ratio (see Conceptual Background). Arnold and Duvall 1994 substantially advanced the study of mating systems by forging links between mating systems and the statistical measurement of selection on characters, as explained in Arnold and Wade 1984a and Arnold and Wade 1984b (both cited under Premating Sexual Selection). Shuster and Wade 2003 expanded the formal descriptions of mating systems and provided a consistent quantitative framework for describing continuous variation in and among mating systems. This perspective received an update in Shuster 2019, an accessible review. Arthropods, as arguably the most diverse animals in terms of mating systems, have been important in developing mating system theory; Shuker and Simmons 2014 contains chapters from a diverse range of experts studying various aspects of arthropod mating systems. Herridge, et al. 2016 provides a friendly entry point to the literature on animal mating systems, including explanations of terminology.

• Arnold, S. J., and D. Duvall. 1994. Animal mating systems: A synthesis based on selection theory. American Naturalist 143:317–348.

  DOI: 10.1086/285606

  Influential synthesis that links the study of mating systems to selection on quantitative traits, and clarifies the central place of the Bateman gradient (which the authors confusingly call the “sexual selection gradient”) in mating system evolution. For more on Bateman gradients, see Conceptual Background.

• Darwin, C. 1871. The descent of man, and selection in relation to sex. London: J. Murray.

  DOI: 10.5962/bhl.title.121292

  Classical and foundational; Darwin describes and reflects on the mating behavior of many animals, and introduces the concept of sexual selection to explain the evolution of conspicuous traits and behaviors that do not provide any obvious survival advantage.

• Emlen, S. T., and L. W. Oring. 1977. Ecology, sexual selection, and the evolution of mating systems. Science 197:215–223.

  DOI: 10.1126/science.327542

  Important paper arguing that economically defendable resources shape the evolution of mating systems according to the distribution of fertilizable individuals in space and over time. Authors also introduce the concept of “operational sex ratio” and an ecological classification of mating systems.

• Herridge, E. J., R. L. Murray, D. T. Gwynne, and L. F. Bussière. 2016. Mating and parental sex roles, diversity in. In Encyclopedia of evolutionary biology. Vol. 2. Edited by R. M. Kliman, 453–458. Amsterdam: Academic Press.

  An accessible overview of the diversity of mating and parental care patterns in animals, and underlying sources of selection. This is a good article for students, with a useful glossary to help out with terminology.

• Orians, G. H. 1969. On the evolution of mating systems in birds and mammals. American Naturalist 103:589–603.

  DOI: 10.1086/282628

  A classic paper that brought the study of mating systems in line with evolutionary thinking in terms of individual fitness, and emphasized the relevance of environmental factors. However, Orians’s prediction of common monogamy and rare polyandry among birds was not upheld by the succeeding research and literature, which revealed that multiple mating among female birds is common.

• Shuker, D. M., and L. W. Simmons, eds. 2014. The evolution of insect mating systems. Oxford: Oxford Univ. Press.

  An edited scholarly work, available online by subscription (titled identically to Thornhill and Alcock’s classic from 1983). The Shuker and Simmons book includes many important and well-written chapters, by experts on sexual selection theory, mating systems, genetics, contests and weaponry, mate choice, alternative phenotypes, polyandry, parental care, parasites and pathogens, and finally a chapter by Alcock and Thornhill reflecting on the legacy of their original book. Highly recommended reading.

• Shuster, S. M. 2019. Mating systems. In Encyclopedia of ecology. Vol. 1. 2d ed. Edited by B. Fath, 274–283. Amsterdam: Elsevier.

  This is an easy-to-read chapter that briefly reviews some of the main ideas from Shuster and Wade 2003; the previous work by these authors is updated and generalized with an emphasis on intervening studies. The impressive variation and diversity in mating patterns is once again emphasized.

• Shuster, S. M., and M. J. Wade. 2003. Mating systems and strategies. Monographs in Behavior and Ecology. Princeton, NJ: Princeton Univ. Press.

  DOI: 10.1515/9780691206882

  A tremendously important book (with some technically challenging sections), this covers most aspects of animal mating systems, is taxonomically broad, and addresses alternative mating strategies and many other aspects. Because of the focus on quantifying mating systems, this work is easy to reconcile with continuous variation in mating systems.

• Thornhill, R. J., and J. Alcock. 1983. The evolution of insect mating systems. Cambridge, MA: Harvard Univ. Press.

  Thornhill and Alcock’s classic volume is out of print and sometimes hard to find, perhaps because it is treasured by a generation of behavioral ecologists for whom it was a formative example of how selection on individuals can help explain the extraordinary diversity of mating strategies among insects. Worth reading because it helped shape so much of the insect sexual selection literature in the succeeding decades.