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Physiological Substrates of Mammalian Monogamy: the Prairie Vole Model

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Physiological Substrates of Mammalian Monogamy: the Prairie Vole Model Neuroscienceand BiobchavioralReviews, Vol. 19, No. 2, pp. 303-314, 1995 Copyright© 1995 ElsevierScience Lid Pergamon Printed in the USA. All rightsreserved 0149-7634/95 $9.50 + .00 0149-7634(94)00070-0 Physiological Substrates of Mammalian Monogamy: The Prairie Vole Model C. SUE CARTER, .1 A. COURTNEY DEVRIES,* AND LOWELL L. GETZt *DeFartment of Zoology, University of Maryland, College Park, MD 20742, and tDepartment of Ecology, Ethology, and Evolution, University of Illinois, Urbana, IL 61801 CARTER, C. S., A. C. DEVRIES AND L. L. GETZ. Physiological substrates of mammalian monogamy: The prairie vole model. NEUROSCI BIOBEHAV REV 19(2) 303-314, 1995.-Prairie voles (Microtus ochrogaster) are described here as a model system in which it is possible to examine, within the context of natural history, the proximate processes regulating the social and reproductive behaviors that characterize a monogamous social system. Neuropeptides, including oxytocin and vasopressin, and tihe adrenal glucocorticoid, corticosterone, have been implicated in the neural regulation of partner prefer- ences, and in the male, vasopressin has been implicated in the induction of selective aggression toward strangers. We hypothesize here that interactions among oxytocin, vasopressin and glucocorticoids could provide substrates for dynamic changes in social and agonistic behaviors, including those required in the development and expression of monogamy. Results from research with voles suggest that the behaviors characteristics of monogamy, including social attachments and biparental care, may be modified by hormones during development and may be regulated by different mechanisms in males and females. Prairie voles Social behavior Attachment Monogamy Oxytocin Vasopressin Adrenal steroids Corticosterone Sex differences MONOGAMY IN MAMMALS viduals within a family group (that remain with the family as "helpers"). In the present paper we will use the term monog- MONOGAMY has fascinated behavioral researchers for over amy to refer to a social system in which animals exhibit all or a century. However, the concept of monogamy is complex and most of the features described above. monogamy has been defined in sometimes contradictory terms Monogamy is uncommon in mammals, with an estimated (reviewed 33). Most definitions of monogamy, including those occurrence of only three percent. The appearance of monoga- found in dictionaries (105), include reference to the impor- mous mating or social systems does not follow any obvious tance of sexual or mating exclusivity. By such definitions mo- taxonomic or phylogenetic pattern. For example, tamarins, nogamy is a mating system. Monogamy also has been defined marmosets (1,86,90), titi monkeys (70), aardwolves (82), ele- as a social system. These definitions tend to emphasize the phant shrews (81), California mice (49), prairie voles and pine importance of long term associations or pair bonds between voles (14,33) share many of the characteristics of monogamy. one male and one female, and the importance of biparental Social organization and the ultimate or evolutionary causes care. New methods for determining paternity have indicated for monogamy have been discussed by several sources (re- that sexual exclusivity is comparatively rare. However, obser- viewed 6,65,72,106). It has been suggested that monogamous vations of mammalian species that have been described as males increase their reproductive fitness by maintaining their either socially or sexually monogamous have revealed a cluster association with a single female. In contrast, nonmonogamous of unusual behavioral and reproductive features that taken males may abandon their mate to seek out additional sexual together define monogamy (31,57). Among the traits that have partners. Additionally, environments in which single parents been used to characterize monogamy are the following: (a) are incapable of rearing the young may favor monogamy. In male and female cohabitation and long-term selective associa- many species monogamy also involves paternal investment in tion or pair bonds throughout breeding and nonbreeding sea- the defense of or care of offspring from a single female part- sons; (b) selective aggression directed toward unfamiliar con- ner (94). specifics; (c) biparental care, including high levels of paternal In contrast, little is known regarding the proximate or behavior, and alloparenting; (d) socially regulated reproduc- physiological mechanisms underlying the expression of mo- tive processes such as estrus induction and ovulation; and (e) nogamy. In general, it has not been widely recognized that the incest avoidance and reproductive suppression of adult indi- characteristics of either a mating system or social system might i To whom requests for reprints should be addressed. 303 304 CARTER, DEVRIES AND GETZ have a physiological basis. However, the collective features of Based on field data from prairie habitats in Illinois (45,67) monogamy are reproductive and social behaviors which, in it was found that about 70 percent of juvenile prairie voles do many species, have been shown to be modified by various not disperse, but in fact remain with their family to form hormones and neurochemicals. We propose here that endo- philopatric communal groups. However, juvenile mortality is crine factors from the adrenal and gonadal axes regulate the high (85-90070) and communal groups typically only occur in organization and expression of the social and reproductive late autumn and winter when predation on young is low. patterns that characterize monogamy. Snakes are the major summer predators of young voles; ani- In the present paper, prairie voles are described as a model mals that have reached adulthood are less likely to be affected system for which evidence of monogamy exists under both by predation. field and laboratory conditions. Using this model we will de- During the warmer months in central Illinois, most of the scribe a variety of endocrine factors capable of influencing the social groups identified are either male-female pairs, single expression of specific components of monogamy, including females (known to be survivors of a pair), or small communal pair bonding, male parental care, alloparenting and reproduc- groups (with an average size of three individuals). In late au- tive suppression, and we propose mechanisms through which tumn and winter larger communal groups become common, ontogenetic interactions among the adrenal and gonadal axes and may included 10-12 adults. These communal groups usu- could regulate the development of the characteristics of mo- ally consist of an established breeding pair and in some cases nogamy. Concurrently, we will use these observations to sug- there is evidence of breeding by philopatric offspring. gest several hypotheses regarding the neurochemical control A substantial pool of "wandering" unpaired males exist of social behavior. To date research on the behavioral endocri- within natural populations (45°7o of the adult males). Inbreed- nology of monogamy has focused on the effects of steroids ing is apparently rare. However, at high population densities, from the gonads and adrenal glands and the neuropeptides, resident males may not be able to exclude all intruders, and oxytocin and vasopressin. philopatric females living within communal groups may be- come pregnant. (Reproductively active philopatric females VOLES AS A MODEL SYSTEM FOR THE ANALYSIS most likely mate with nonresident wandering males.) In the OF THE BIOLOGY OF MONOGAMY spring surviving members of communal groups typically break Monogamy has been most clearly demonstrated in mam- up into male-female pairs. Only 207o of the newly formed mals that are not readily available for laboratory study. The spring breeding pairs involve related animals. Within family identification of several monogamous rodents opens the possi- groups about three-fourths of the adult pairs remain together bility of physiological investigations of mammalian monog- until one member dies. In less than 10070 of cases there is amy. At present the best studied of these rodents are prairie evidence that the male has abandoned his female partner. voles (Microtus ochrogaster). Several closely related species, After the death of one member of a pair fewer than 20o7o of including both monogamous and nonmonogamous voles, are the survivors eventually acquire a new mate. available for coordinated field and laboratory investigation. Prairie voles are believed to have evolved in tallgrass prai- Voles are found in diverse habitats. They show dramatic and ries, which are very low food resource habitats. Prairie vole rapid fluctuations in density, and have long been a favored population densities in this habitat remain relatively low and subject for ecological studies of mammalian population dy- females are widely dispersed. The social organization and mat- namics (39,45,67,92). Voles show remarkable species diversity ing system of prairie voles may have evolved as an adaptation in social organization and mating systems, which range from to a low food resource habitat (45,67). According to this hy- monogamous prairie and pine (Microtus pinetorum) voles, to pothesis, under low population densities selective pressure more polygynous species, such as meadow (Microtus pennsyi- would favor monogamous male-female pairs, and in some vanicus) and montane (Microtus montanus) voles (33). cases permit communal groups, which include nonreproduc- Voles have not undergone domestication, and can be stud- five
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