Sex a plus monogamy

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Genetic monogamy is rare—at least at the level of a species—and monogamy can exist in the absence of sexual fidelity.

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These features of social monogamy in mammals are supported by patterns of hormonal function originating in the neurobiology of maternity, including oxytocin, as well Sex a plus monogamy a more primitive vasopressin pathway. Another key feature of social monogamy is reduced sexual dimorphism. Processes associated with sexual differentiation offer clues to the mysteries surrounding the evolution of monogamy.

Although there is consistency in the necessary ingredients, it is likely that there is no single recipe for social monogamy. As reviewed here, genes for steroids and peptides and their receptors are variable and are subject to epigenetic regulation across the lifespan permitting individual, gender and species variations and providing substrates for evolution.

Reduced sensitivity to gonadal androgens, and a concurrent increased reliance on vasopressin for selective defense and oxytocin for selective affiliation may have offered pathways to the emergence of social monogamy. Paradoxical statements may seem completely self-contradictory, but they can be used to reveal deeper truths. Social interactions are linked to the ability to mate, survive, and thrive within an always changing environment. For these reasons, explanations for species and individual variations in social behavior were initially discussed in terms of evolution, fitness, and reproduction Kleiman, ; Dewsbury, ; Komers and Brotherton, ; Lukas and Clutton-Brock, ; Klug, In attempts to create order in the description of socio-sexual behavior across species as well as among human cultures it became common to cluster patterns of pd sexual behavior, and label these as mating systems including polygyny, polygamy, polyandry, or monogamy.

Among these, monogamy seemed particularly difficult to understand. Having a single mate, especially in males, was not easily Sex a plus monogamy by theories based on reproductive fitness Barash and Lipton, If monogamy was not primarily about sexual exclusivity, then what was it? Perhaps monogamy was better understood as a social system, and one that offered the advantages of shared parenting, protection of resources, and social support Wilson, ; Gowaty, Here we offer a brief personal of the events that led us to emphasize the importance of viewing monogamy as a social system, and a system that could be understood in terms of its' neuroendocrinology.

Social systems are inherently variable. However, the specific neural substrates upon which hormones act differ between and among species, and can be compared in socially monogamous vs. This work began in the genus Microtusbut as more comparative studies have appeared variations in the effects of hormones, often due to differences in target receptors are becoming more apparent. Keeping this variation in mind, we have attempted to uncover patterns of hormone action that may help to explain the phenotype and origins of the traits of social monogamy Table 1.

From rodent data, discussed in depth throughout this review, it appears that socially monogamous traits emerge during the course of development, in part through the combined actions of steroids and peptides Choleris et al. Table 1. Hypotheses for the roles of steroids and peptides in the emergence of social monogamy.

Among the several unsolved mysteries associated with social monogamy is the apparently independent emergence of a set of shared traits in unrelated mammals ranging from rodents to canids to New World monkeys Kleiman, ; Lukas and Clutton-Brock, ; French et al. The repeated appearance of the cluster of behavioral and anatomical features that have been termed social monogamy raises an important basic question.

What are the mechanisms through which these traits have emerged on over 60 occasions in unrelated mammalian species? Has social monogamy emerged primarily through parallel or convergent evolutionary mechanisms, or some combination of the two?

Did a shared physiology permit the evolution across species of social monogamy? Or are there several pathways to social monogamy? Here we examine the hypothesis that the neurobiology of sexual differentiation and masculinization offers a template for understanding the origins of social monogamy.

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Research in prairie voles has repeatedly indicated that voles are insensitive to androgens. It is possible that a comparative lack of functional availability of androgens during development, for example, through changes in either the androgen receptor or based on inhibitory effects of other molecules, such as glucocorticoids and oxytocin, may help to explain some of the unique traits that have emerged in socially monogamous mammals. We further propose that alterations in mechanisms underlying the behavioral and anatomical traits of social monogamy, shifting from a reliance on androgens to a dependence on peptides would be adaptive, and also would permit the emergence of the prosocial traits of social monogamy.

For example, the components of behavior prominent in males of non-monogamous species, including non-selective aggression, which rely in part on direct actions of androgens may be specifically downregulated in social monogamy.

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Confusion concerning monogamy has arisen across disciplines in part because of different uses of the word. Biologists later borrowed the term monogamy, and alternatives to monogamy, such as polygamy, as a means for categorizing mating systems and social relationships, usually between males and females. In both common usage and within the field of biology the term monogamy often infers sexual exclusivity either across the life-span or at a given point in time.

Definitions of monogamy were applied to a single pair of partners or sometimes even to one individual within a pair. Among the estimated 4, or more different species of mammals for which behavioral data are available, it was estimated that between 3 and 5 percent of species, including apparently unrelated taxa, exhibited the traits of monogamy Kleiman, As is discussed in depth later in this review, there is also a great deal of intraspecies variation in displays of monogamy behaviors in both mammalian and avian species.

Most early behavioral studies in mammals or birds did not differentiate between mating and social systems, assuming homogeneity between these. Sexual preferences were assumed to be the sine qua non of monogamous species. This assumption has repeatedly been shown to be incorrect. As it became clear that in both avian and mammalian species living in long-term pairs might not always be sexually exclusive, it became increasing common in biology to narrow definitions of monogamy to describe what is now called social monogamy Carter et al.

A concurrent set of behavioral, anatomical, and physiological characteristics— beyond the selection of sexual partners —emerged that was found in most, Sex a plus monogamy not all, apparently monogamous species Kleiman, ; Carter et al. Of particular value to identifying the biology of social monogamy were within-genera comparisons of apparently monogamous species to closely related non-monogamous relatives.

The broader use of the term social monogamy involved descriptions of animals cohabitating in male-female pairs, remaining together after mating, and tly defending resources. Thus, the formation of selective and lasting pair bonds between two opposite sex individuals is the most consistent feature of social monogamy. Paternal or alloparental care is sometimes, but not always, observed Kleiman, ; Komers and Brotherton, In addition, incest avoidance and reproductive suppression of non-breeding animals are common Carter et al.

In some cases, extended families formed, usually around the original male-female pair. Under these conditions members of a group might forego the opportunity to reproduce directly, remaining as philopatric helpers or alloparents in the natal family. The capacity to experience reproductive and juvenile growth suppression is not limited to socially monogamous species, but may be especially apparent in species that carry the traits of social monogamy.

Components of this pattern also are described as cooperative breeding in which non-parents, both related and unrelated, play a major role in the care of offspring Carter and Roberts, ; Solomon and French, ; Hrdy, In cooperative breeding groups one or more breeding females may exist with other members of the group supporting the breeders. Under some environmental conditions, social monogamy can morph into cooperative breeding and colonies, but, at least in rodents, at the core of these it is common to find one primary breeding pair Solomon and French, As described in more detail below, an important clue to the origins of social monogamy is a relative absence of sex differences in anatomical traits including body size Sex a plus monogamy external genitalia.

The same processes that have been implicated in mammalian sexual differentiation and masculinization Arnold, are plausible substrates for differential expression of monogamous vs. As detailed below, variations in the sensitivity of androgen receptors or the production of androgens are among several likely sources of the sexual dimorphism seen in monogamy.

Other steroids, and especially estrogen, also regulate the behavioral effects of neuropeptides Carter, Conversely, peptides, such as oxytocin and vasopressin, may affect behavior in part through interactions with steroids or their receptors, especially during development Carter et al. It was the desire to understand proximate mechanisms supporting lasting social attachments and parenting, that motivated one of us CSC to study monogamy from a neuroendocrine perspective Carter et al.

The history of that ongoing journey is summarized below. Over the last four decades the Sex a plus monogamy vole has become a favored model for studying the neurobiology of social monogamy. However, before we began our work with this species, both voles and lemmings, were widely studied as ecological models for understanding population dynamics Getz, In prairie voles Microtus ochrogasterthere was evidence of extreme and rapid variation in population density.

This led Lowell Getz, a mammologist and my colleague at the University of Illinois, to conduct field and semi-natural studies, some of which continued over a period of more than 25 years Carter and Getz, ; Getz and Carter, Booms and crashes in populations were not easily explained by environmental factors such as food, water, climate or predation.

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Emerging from those studies was evidence that prairie voles were sharing nests in long term pairs, generally remaining together for life. Families built around these pairs sometimes grew into communal groups, or cooperative breeders where young prairie voles help to care for new siblings, usually but not always with only one breeding female. In fact, about 70 percent of young prairie voles of both sexes that remained in the nest did not reproduce Getz and Carter, In parallel studies, meadow voles Microtus pennsylvanicusoften studied in the same fields, did not show these traits Carter and Getz, In the s when I began to collaborate with Getz, monogamy was generally used to refer to a mating system, and discussed in terms of reproductive fitness.

At that time almost no one believed that a small rodent, such as the prairie vole, was capable of any kind of monogamy. We brought prairie voles, as well as the apparently non-monogamous meadow voles, into our laboratory. Assuming that sexual preferences would be of particular relevance to pair bonds, we repeatedly attempted to study mating preference as an index of social bonds; those attempts were unsuccessful. Both female and male Sex a plus monogamy voles failed to show sexual preferences for familiar partners vs. Methods for DNA fingerprinting were first described in the mids Jeffreys et al.

The addition of DNA fingerprints increased the body of evidence indicating that social and sexual monogamy are not always coherent. Using DNA fingerprints from the offspring, we observed in prairie voles that a female given a choice voluntarily mated with and could produce mixed litters sired by both a familiar and an unfamiliar male Carter et al. These early laboratory data, and later field studies in voles done by others Solomon and Jacquot, ; Solomon et al. However, despite the absence of a reliable sexual preference, careful observations of the behavior of established pairs of prairie voles revealed that even when mating preferences were not shown, prosocial contact behaviors were reliably more likely to be directed toward a familiar partner Carter and Getz, Although sexually promiscuous, female and male prairie voles showed a high level of partner specificity for non-sexual contactand after mating showed aggression toward intruders of both sexes presumably to guard the mate or other resources Gavish et al.

At this same time, controversies were arising from many sources around the concept of monogamy. Other species, including birds, were beginning to be described as socially monogamous, but again evidence for genetic monogamy was rare Wickler and Seibt, ; Gowaty, Sexual monogamy as a unitary concept, especially at the species level, was becoming increasingly less useful. Sex a plus monogamyI gave birth to my first son. I was infused with oxytocin during the birth.

This transforming experience left me obsessed by the possible behavioral effects of the hormones of motherhood, and especially oxytocin, for both parents and babies. Although with the exception of one study of maternal behavior in rats which had just appeared Pedersen and Prange,there was at that time virtually no experimental data available to support this notion.

Sex a plus monogamy

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