Sexual monogamy as a unitary concept, especially at the species level, was becoming increasingly less useful. Did a shared physiology permit the evolution across species of social monogamy? This differs from factors regulating paternal behavior in P. campbelli, in which paternal care does not appear to rely on estradiol, and provides additional evidence for species differences in how variation in sociality arises. High levels of testosterone, some of which is aromatized locally to an estrogen, may contribute to low levels of paternal behavior and lead to non-selective social behavior and mating. 23, 673–685. Sci. Among the estimated 4,000 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, 1977). In rodents declines in testosterone often coincide with a decrease in infanticidal aggression, presumably preparing the male to support, or at least not attack, his offspring (Elwood, 1977; Brown, 1986; Perrigo et al., 1991). Perkeybile, A. M., Carter, C. S., Wroblewski, K. L., Puglia, M. H., Kenkel, W. M., Lillard, T. S., et al. doi: 10.1016/S0306-4530(98)00055-9, Carter, C. S. (2007). Early nurture epigenetically tunes the oxytocin receptor. doi: 10.1521/pdps.2017.45.4.499, Carter, C. S., Boone, E. M., Pournajafi-Nazarloo, H., and Bales, K. L. (2009). Young: When a monogamous prairie vole mates, vasopressin is released and it activates receptors in certain areas of the brain that are involved in pleasure and reward. (2013). When the AVP V1a receptor was overexpressed in the lateral septum in non-monogamous rats, using viral vector gene transfer of the prairie vole AVP V1a receptor, social recognition, and social interactions were increased beyond what is typically seen in this species; thus, increasing vasopressin receptor in specific brain regions in rats induced more “prairie vole-like” behavior (Landgraf et al., 2003). %%EOF Effects of neonatal castration and testosterone on rats pup-killing behavior and activity. Sci. Endogenous variation in the oxytocin system also has been associated with social behavior across a number of species (Beery, 2015). Physiol. 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 presumed sexual behavior, and label these as mating systems including polygyny, polygamy, polyandry, or monogamy. Brain Res. Enhanced partner preference in a promiscuous species by manipulating the expression of a single gene. 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. The regulation of aggression results in part from activity of vasopressin and the AVP V1a receptor in the anterior hypothalamus. Animals will show aggression toward novel animals of the same sex, likely as a form of mate guarding behavior (Kleiman, 1977; Getz et al., 1981; Winslow et al., 1993; Carter et al., 1995). The features used to define social monogamy include both behavioral and anatomical traits typically, but not always, occur together. Neurosci. *Correspondence: C. Sue Carter, firstname.lastname@example.org, Front. Exploration in a dispersal task: effects of early experience and correlation with other behaviors in prairie voles (Microtus ochrogaster).  Such differences in parental contribution could be a result of the male's drive to seek other females in order to increase their reproductive success, which may prevent them from spending extra time helping raise their offspring. I.D. Dev. We hypothesize here that oxytocin may have the capacity to prevent masculinization. Intrinsic ability to aid offspring: the male's ability to exhibit parental care. Definitions of monogamy were applied to a single pair of partners or sometimes even to one individual within a pair. Monogamy: dopamine ties the knot, Nature Neuroscience, 9 (1) 7-8. Physiol. , Comparing to monogamous species, polygynous species tend to display more sexual dimorphism, or difference in body size; it is believed that sexual dimorphism could be an evolutionary consequence to a monogamous mating system. Co-administration of testosterone plus fadrozole, an aromatase inhibitor, reduces paternal behaviors, an effect not seen with co-administration of testosterone and saline or estradiol and fadrozole (Trainor and Marler, 2002). This broad geographic home range is associated with variety in habitat resource availability and also in varying degrees of monogamous behavior. However, the notion that love was “hormonal” was not novel (Klopfer, 1971), especially for someone who came of age in the 1960s. In fact, high levels of testosterone have been measured in prairie voles including during the perinatal period (Lansing et al., 2013). Integr. In addition, vasopressin, facilitated by androgens, is involved in mating- and territory-related aggression in these males. The same hormones necessary for the expression of the features of social monogamy, also are implicated in the development of a nervous system capable of being epigenetically tuned to high levels of sociality. doi: 10.1016/j.tips.2017.08.005, Cho, M. M., Devries, A. C., Williams, J. R., and Carter, C. S. (1999). And if so, what were the features and the origins of what would come to be known as “social monogamy”? The addition of DNA fingerprints increased the body of evidence indicating that social and sexual monogamy are not always coherent. Contemporaneous research by Ferris et al. Acad. 123, 979–991. We propose here that endo- crine factors from the adrenal and gonadal axes regulate the organization and expression of the social and reproductive patterns that characterize monogamy. Oxytocin activity in the nucleus accumbens also is vital in females for partner preference formation. (2015). 0000009341 00000 n  Social monogamy does not describe the sexual interactions or patterns of reproduction between monogamous pairs; rather it strictly refers to the patterns of their living conditions. Findings such as these suggest possible pathways to individual differences in sociality within prairie voles, as well as flexibility in social behavior between species. , Only ~3–5% of all mammalian species are socially monogamous, including some species that mate for life and ones that mate for an extended period of time. Oxytocin also was capable of increasing sociality in both sexes. Trends Pharmacol. Oxytocin: its mechanism of action and receptor signalling in the myometrium. Proc. premature loss of her infant will result in the female going into. 0000009364 00000 n Not just skin deep: Neurons detect pleasurable touch, The amygdala: a full brain integrator in the face of fear. Natl. Sci. (1989). A unique characteristic of monogamy is that unlike in polygamous species, parents share parenting tasks. Where an individual or a species falls on that behavioral continuum is controlled at least in part by peptide and steroid systems and the interactions among these. doi: 10.1073/pnas.93.21.11980. Vasopressin receptor blockade in the anterior hypothalamus suppresses aggression in hamsters. The editor and reviewers' affiliations are the latest provided on their Loop research profiles and may not reflect their situation at the time of review. Why monogamy? Both oxytocin and vasopressin may influence alloparental behavior in male prairie voles. Thus, a given hormone, such as estrogen, might promote selective socially in some cases and aggression in others. Thus, the regulation of the features of social monogamy represents a compromise between quickly adapting behavioral changes, such as those necessary for parenting and pair bonding, and more conserved traits, such as sex differences in body size or genital morphology or the distribution of receptors for both steroids and peptides. Much of the early research on the neurobiology of social monogamy was conducted in voles of the genus Microtus, comparing closely-related species that are either non-monogamous or socially monogamous. Choleris, E., Devidze, N., Kavaliers, M., and Pfaff, D. W. (2008). Although both males and females synthesize oxytocin and vasopressin, there are often differences in the roles these molecules play in behavioral regulation in males vs. females (Bales et al., 2007a; Albers, 2015; Caldwell, 2017).
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