Mating increases male's interest in other females: A cognitive study in socially monogamous prairie voles (Microtus ochrogaster)

Abstract

To determine whether socio-sexual interactions with females influence the male prairie vole's cognitive processing, three groups of males were simultaneously exposed to sensory stimuli of a control and a focal female then tested for their behavioral and neuronal responsiveness to the female cues. From the control female, all males received distal cues. From the focal female, the Unmated males received distal cues, the Unmated-Contact males received all cues but did not mate with her, and the Mated-Contact males received all cues and mated with her. Males were tested for their attentiveness to enclosures holding each female and for their memory of the females’ previous location. Males’ brains were then examined to localize activated regions following exposure to the odor of familiar versus unfamiliar focal females. The Mated-Contact males spent more time in the cage of the control female attending to her enclosure than in the cage of the focal female. Exposure to odors of unfamiliar focal females activated the cingulate cortex of Unmated-Contact males. There was a negative correlation between the level of neuronal activation in the retrosplenial cortex of males that were exposed to the odors of a familiar focal female and their attentiveness to the enclosure of the control female. The data suggest that the effect of socio-sexual interactions with a female on males’ cognition depends on the type of sensory signals males receive from females and how individual males perceive those signals.

Introduction

Arvicoline rodents in the genus Microtus that are commonly known as voles show a range of mating systems from monogamy to polygamy (FitzGerald and Madison, 1983, Gruder-Adams and Getz, 1985, Shapiro and Dewsbury, 1990). Of all the vole species, prairie voles have attracted the most attention since the 1980s when they were found to exhibit social behaviors similar to human and non-human primates (Getz and Hoffman, 1986, Carter and Getz, 1993). Field and laboratory studies have shown that prairie voles have a monogamous mating system. The male and female form pair bonds and jointly care for young (Gavish et al., 1981, Getz and Carter, 1996, Pizzuto and Getz, 1998). Depending on the population density, the monogamous pair lives alone or lives in complex social units (Getz and McGuire, 1997, Cochran and Solomon, 2000). These social units consist of the pair-bonded mates, multiple generations of their litters, and a few unfamiliar adults that join the group (Getz et al., 1990, Getz et al., 1993).

Although the mating system of prairie voles is identified as monogamous, the population is not homogenous. Semi-natural studies have shown that most males form stable pair bonds, but a significant percentage of them remain unpaired and are non-territorial (Solomon and Jacquot, 2002, Ophir et al., 2008a, McGuire and Getz, 2010). The paired animals occupy a smaller home range, have a tendency to defend their exclusive territory, and are less likely to intrude on the territory of their neighbors than unpaired animals (Ophir et al., 2008b, Phelps et al., 2010). Furthermore, there is evidence that even some pair-bonded males and females engage in extra-pair fertilization (Solomon et al., 2009, Ophir et al., 2008a). Laboratory studies have confirmed that prairie voles are socially monogamous by showing that a mated male will choose to visit with females other than his mate, but he prefers to remain in physical contact with his original mate and displays signs of anxiety when he is separated from her (Winslow et al., 1993, Grippo et al., 2007). Together, these data indicate that male prairie voles may vary in how they process reproductively-relevant social information. However, the factors that might influence their cognitive processing are unknown.

It has been speculated that individual differences in capacity for spatial memory of prairie voles leads some males to form a pair bond and guard their territory while other males engage in extra-pair fertilizations or remain unpaired and non-territorial (Ophir et al., 2008b, Phelps et al., 2010). According to this hypothesis, those males that have a greater ability to remember their aggressive interactions with other males avoid intruding in other territories, and are thus less likely to encounter sexually-receptive females and engage in extra-pair fertilization (Ophir et al., 2008b). Although this is a plausible hypothesis, it is also conceivable that interaction with a female alters how a male processes information from other females. Males may differ in how they remember their personal interactions with females and how attentive they are to female cues. Some males may respond to their mate's cues by shifting their attention from other females and focusing on guarding their own territory, whereas other males may ignore those cues and continue to search for other sexually-receptive females.

There is ample evidence that female cues during and after mating play an important role in shaping the male prairie vole's social behavior and neurophysiology. In sexually-naïve male and female prairie voles, mating does not occur until the pair has been in contact with each other for more than two days (Witt et al., 1988). Continuous exposure to the female's sensory stimuli during this lengthy courtship period increases the male's level of: (1) paternal responsiveness towards unrelated infants, (2) aggression towards unfamiliar conspecifics,(4) fearlessness, (5) neuronal activity in specific brain regions, (6) synthesis and release of central vasopressin (Winslow et al., 1993, Wang et al., 1994, Bamshad et al., 1994, Insel et al., 1995, Cushing et al., 2003, Terleph et al., 2004, Simoncelli et al., 2010). In addition, partner preference tests have shown that mating or cohabitation with a female change the male's tendency to affiliate with his mate. Accordingly, when a mated male is given a choice to spend time in one of two cages where his mate and an unfamiliar sexually-receptive female are tethered, he spends more time in side-by-side contact with his mate than with the unfamiliar female (Insel et al., 1995). Collectively, these results suggest that interaction with a female during mating modifies how the male brain processes his mate's information such that he forms a preference for her, guards her, and intensifies his parental responsiveness.

To further investigate this hypothesis, we tested male prairie voles to determine whether the experience of mating and physical contact with a female would change the male prairie vole's attentiveness to her cues, his memory of her location and his neuronal responses to her odors. To do so, we designed an experiment in which the male was tested for his responses towards two females with which he was familiar, but had different levels of contact. We predicted that mated males in physical contact with the female would be more likely to search and remember her location than Unmated males in physical contact with the female or Unmated males physically separated from the female. We also predicted that the neuronal activity measured by the expression of Fos protein in memory centers of the brain would be heightened in response to the female's odors only in males that mated and remained in physical contact with her. In addition, we examined the correlation between Fos protein expression in the male's brain and his behavior to determine if there were individual differences in males’ responses to female cues.