Monogamy and the Prairie Vole Studies of the prairie vole—a secretive, mouselike animal—have revealed hormones that may be responsible for monogamous behavior by C. Sue Carter and Lowell L. Getz bservation of the mating and females of monogamous species tend from studies of prairie voles was the pup-rearing habits of nonde- to be about the same in size and ap- observation that social cues regulate Oscript, brown rodents that live pearance. Mated pairs will defend the the reproductive physiology of this spe- under weeds and grasses might not nest and territory from intruders, and cies. Even to enter estrus (sexual heat), seem an obvious way to improve knowl- both parents care for the young. Monog- a female prairie vole must sniÝ a male. edge of monogamy. After all, most hu- amous mammals may form complex Indeed, Milo E. Richmond, now at Cor- mans can attest to the complexity of social groups that include an extended nell University, found that female prai- male-female relationships. Yet studies family and oÝspring of various ages. rie voles do not have the ovarian cycles of the prairie vole (Microtus ochrogas- Incest is avoided within these families; that are typical of nonmonogamous ter), a common pest throughout the adult young usually do not reproduce mammals. In monogamous voles, a fe- midwestern U.S., have led us on a fasci- as long as they live with related family male must have a male partner to in- nating scientiÞc journey from our start- members. Finally, we should point out duce estrus. ing point in ecology to the exploration that although common in birds, monog- Furthermore, not just any male can of the neuroendocrinology of social amy is rare in mammals. In an exhaus- bring a female into heat. Fathers and bonds. Unlike most rodents, prairie tive survey, Devra G. Kleiman of the Na- brothers do not seem capable of elicit- voles form long-lasting pair bonds, and tional Zoological Park in Washington, ing sniÛng. This may be an adaptive both parents share in raising their D.C., found that only about 3 percent mechanism designed to prevent incest. young. Our studies have provided a new of mammals are monogamous. In fact, both males and females will es- understanding of the importance of two Sexual exclusivity, however, is not a sentially remain prepubescent as long hormones, oxytocin and vasopressin, feature of monogamy. Studies of the as they stay with their families. which are well known for their respec- prairie vole as well as those of other tive roles in reproduction and body wa- mammals and birds have indicated that y sniÛng an appropriate male, ter regulation. Work with voles now sug- absolute sexual monogamy is not nec- the female picks up a chemical gests that these hormones are involved essarily associated with social monog- B signal called a pheromone. Phero- in the development of monogamy. amy. In fact, DNA Þngerprinting tests mones in turn trigger the hormonal The chief criterion that deÞnes mo- have shown that oÝspring of female events needed to activate the ovaries nogamy is a lifelong association be- prairie voles are not always fathered by and to induce heat. A small chemical tween a male and a female. Within this the cohabiting males. In some cases, a sense organ, known as the vomerona- broad deÞnition lie several characteris- litter may have mixed paternity. sal organ, helps to mediate the eÝects tics that are easily observed. Males and Because prairie voles incorporate the of pheromones. John J. Lepri, now at the deÞning features of monogamy, they University of North Carolina at Greens- make excellent subjects for the explo- boro, and Charles J. Wysocki of the Mo- ration of the biological foundations of nell Chemical Senses Center in Philadel- C. SUE CARTER and LOWELL L. GETZ monogamy, at least as it exists among phia found that removal of the vomero- have collaborated on their respective studies of behavioral endocrinology and nonhumans. Prairie voles are also small, nasal organ in the female prevented the Þeldwork to investigate the biology of weighing only a few ounces, and are eas- start of heat. A similar eÝect occurs monogamy. Both are fellows of the Amer- ily reared in the laboratory. But of par- when the olfactory bulb is detached. By ican Association for the Advancement of ticular importance for understanding removing the bulb, Jessie R. Williams, Science. Carter received her Ph.D. from the biology of monogamy is the fact Brian Kirkpatrick and Burton Slotnick, the University of Arkansas at Fayette- that not all voles are monogamous. The working in our University of Maryland ville. Before taking on her current posi- meadow vole (M. pennsylvanicus) and laboratory, disrupted the sexual and tion as professor of zoology at the Uni- the montane vole (M. montanus) show social behaviors of the prairie voles. versity of Maryland, she was professor of psychology and ecology, ethology and no indications of monogamy. Voles of In our laboratory, Dean E. Dluzen evolution at the University of Illinois. these species are rarely retrapped with found that once a female is exposed Getz heads the department of ecology, the same partner and do not establish ethology and evolution at the University stable families, and males of these spe- of Illinois. He received his Ph.D. from cies do not usually care for their young. the University of Michigan. The work de- PRAIRIE VOLES (Microtus ochrogaster) Therefore, comparisons of prairie voles engage in prolonged periods of mating, scribed here reßects a 15-year collabora- with their nonmonogamous relatives tion and arose from observations made often past the time that is needed to en- during approximately 35 years of Þeld- can yield insights into the causes of sure pregnancy. These extended bouts work by Getz. monogamy. may help to facilitate the formation of One of the Þrst surprises that came monogamous social bonds. 100 SCIENTIFIC AMERICAN June 1993 Copyright 1993 Scientific American, Inc. to male odors, levels of norepinephrine, vomeronasal system. The stimulation of luteinizing hormone begins a cascade of a neurotransmitter, and luteinizing hor- the olfactory system and the secretion of chemical and neural events that stimu- moneÐreleasing hormone (LHRH) change LHRH cause the pituitary gland to re- lates the ovary to secrete gonadal ste- within minutes. These biochemical lease a surge of luteinizing hormone into roids. Two of the most important ste- events occurred within the area of the ol- the bloodstream. In conjunction with roids secreted are estradiol, a potent factory bulb that receives input from the other endocrine changes, the release of kind of estrogen, and progesterone. Copyright 1993 Scientific American, Inc. SCIENTIFIC AMERICAN June 1993 101 PRAIRIE VOLE (MONOGAMOUS) FEMALE MALE MEADOW VOLE (NONMONOGAMOUS) FEMALE MALE 0 10 20 30 40 50 60 70 80 90 100 TIME IN NEST WITH PUPS (PERCENT) PARENTAL CARE demonstrated by prairie voles far exceeds that shown by nonmonogamous meadow voles. The diÝerence is most apparent with male prairie voles, which are with the pups four times as often as male meadow voles are. Might estrogen and progesterone also gins. This rise in progesterone probably and Syrian hamsters become nonrecep- be involved in monogamous behav- helps to regulate the duration of sexual tive after about 45 minutes of mating. ior? In collaboration with Janice M. activity by bringing these rodents into It is possible that the lengthy sexual Bahr of the University of Illinois, we and out of heat. In contrast, we found interactions of prairie voles help the searched for patterns of gonadal steroid that in prairie voles progesterone lev- sperm enter the uterus and reach the production that varied between estrus els in the blood did not increase until egg. Studies of rats by Norman T. Adler and nonestrus female prairie voles and many hours after coitus began. of the University of Pennsylvania have compared the results with data from The delayed secretion of progester- shown that complex patterns of sexu- nonmonogamous species. Estradiol, a one explains an observation made in al behavior can inßuence the release of hormone known to be essential in in- previous studies: that female prairie hormones and alter the ability of sperm ducing estrus in rodents, was elevat- voles in their Þrst estrus mate for pro- to enter the femaleÕs reproductive tract ed only in female prairie voles in heat. longed periods. In our laboratory, Di- and fertilize an egg. It declined after mating. This pattern ane M. Witt observed that when the fe- Yet improving the chances of fertil- is similar to that displayed by polyga- male was in natural estrus, males and ization is probably not the sole reason mous rodents. Analysis of the patterns females continued to engage in bouts for these extended bouts of mating. of progesterone levels, however, pre- of mating for about 30 to 40 hours. Once mating begins, females ovulate sented an unexpected Þnding. In the This extended mating period contrasts within about 12 hours, and successful nonmonogamous rats and montane sharply to that seen in nonmonoga- pregnancy can occur shortly thereafter. voles, progesterone is released in the mous species. Mating in meadow and Thus, prairie voles in their Þrst heat bloodstream shortly after mating be- montane voles persists for a few hours, continue to copulate for hours after they have met the requirements for 18 pregnancy. We suspect that, like humans and 16 some other primates, prairie voles may copulate to facilitate the formation of 14 monogamous social bonds. Protracted 12 mating would be particularly crucial for prairie voles that are interacting for the 10 Þrst time, because they need to estab- PRAIRIE VOLES lish their lifelong monogamous bond. 8 Indeed, some evidence for this idea comes from observations of females 6 that have previously mated and become 4 MEADOW VOLES NUMBER OF MALE-FEMALE PAIRS 2 CAPTURED PER TRAPPING SESSION MALE-FEMALE PAIRS of prairie voles are caught far more frequently than are such 0 pairs of meadow voles.