Early Experience Affects the Traits of Monogamy in a Sexually Dimorphic Manner Karen L. Bales Department of Psychology University of California Davis 95616 E-mail: klbales@ucdavis.edu Antoniah D. Lewis-Reese Department of Psychiatry and Brain-Body Center University of Illinois at Chicago 1601 W. Taylor St., Chicago, Illinois 60612 Lisa A. Pfeifer Department of Biology University of Maryland 1204 Biology-Psychology Bldg College Park, Maryland 20742 Kristin M. Kramer Department of Biology University of Memphis Memphis, Tennessee 38152 C. Sue Carter Department of Psychiatry and Brain-Body Center University of Illinois at Chicago 1601 W. Taylor St., Chicago, Illinois 60612 ABSTRACT: The goal of this study was to examine the effects of early life experiences on the subsequent expression of traits characteristic of social monogamy in prairie voles (Microtus ochrogaster). During cage changes parents and their offspring were either transferred between cages in a cup (zero manipulation, MAN0) or with a gloved hand (one manipulation, MAN1). Following weaning the offspring were tested for alloparental behavior. In adulthood they were tested for the capacity to form partner preferences, behavior in an elevated plus- maze (EPM), and corticosterone levels. MAN0 males (but not females) showed lower levels of alloparental behavior than MAN1 males. MAN0 females (but not males) were less likely to form pair bonds than MAN1 females. MAN0 animals of both sexes were less exploratory in the EPM than MAN1 counterparts. These experiments support the hypothesis that behaviors used to characterize monogamy are vulnerable in a sex-specific manner to early experience. ß 2007 Wiley Periodicals, Inc. Dev Psychobiol 49: 335–342, 2007. Keywords: early experience; monogamy; oxytocin; vasopressin; prairie vole The effects of early experiences can result in life-long changes in behavior and neurobiology, as well as contributing to later psychopathologies in humans (Plotsky, Sanchez, & Levine, 2001; Sanchez, Ladd, & Plotsky, 2001). Major depression, as well as schizophre- nia and posttraumatic stress disorder, have been linked to stressful early experience and/or trauma (Brown, Cohen, Johnson, & Smailes, 1999; Kaufman, Plotsky, Nemeroff, & Charney, 2000). Animal models of early experience or maternal separation (MS) paradigms have a long history in developmental psychobiology (Levine, 2001). In rats, daily brief separations (15 min a day during postnatal weeks 2 – 3) often produced decreased stress reactivity in offspring, as well as high levels of licking/grooming and arched-back nursing (LG-ABN) in dams and their female offspring. In contrast, daily longer separations (usually 3 hr a day) produced more reactive female offspring with higher levels of corticotrophin-releasing factor (CRF) receptor binding. Following longer periods of MS females also exhibited lower levels of LG/ABN toward their own offspring (Francis, Diorio, Liu, & Meaney, 1999). Handling studies also have often included a group that received no treatment. These animals typically appeared superficially similar to animals that had experienced longer separations, displaying higher stress reactivity, and ‘‘fearfulness’’ [reviews in Levine, 2001, 2002]. Studies of the effects of early experience have almost exclusively concentrated on species in which females are the sole caretakers of offspring. Social ‘‘monogamy’’ is usually characterized by male–female pair bonds and biparental care of offspring, and alloparenting (Kleiman, 1977). Thus in monogamous or cooperatively breeding species, such as prairie voles (Carter, DeVries, & Getz, 1995; Carter & Roberts, 1997) and humans (Fuentes, 1999; Kleiman, 1977), there is not only the potential for Received 4 June 2006; Accepted 22 December 2006 Correspondence to: K. L. Bales Published online in Wiley InterScience (www.interscience.wiley.com). DOI 10.1002/dev.20216 ß 2007 Wiley Periodicals, Inc.