Elsevier

Hormones and Behavior

Volume 53, Issue 1, January 2008, Pages 200-207
Hormones and Behavior

Paternal aggression in a biparental mouse: Parallels with maternal aggression

https://doi.org/10.1016/j.yhbeh.2007.09.017Get rights and content

Abstract

Environmental and social factors have important effects on aggressive behaviors. We examined the effect of reproductive experience on aggression in a biparental species of mouse, Peromyscus californicus. Estrogens are important in mediating aggressive behavior so we also examined estrogen receptor expression and c-fos for insights into possible mechanisms of regulation. Parental males were significantly more aggressive than virgin males, but no significant differences in estrogen receptor alpha or beta expression were detected. Patterns of c-fos following aggression tests suggested possible parallels with maternal aggression. Parental males had more c-fos positive cells in the medial amygdala, and medial preoptic area relative to virgin males. The medial preoptic area is generally considered to be relatively less important for male-male aggression in rodents, but is known to have increased activity in the context of maternal aggression. We also demonstrated through habituation–dishabituation tests that parental males show exaggerated investigation responses to chemical cues from a male intruder, suggesting that heightened sensory responses may contribute to increased parental aggression. These data suggest that, in biparental species, reproductive experience leads to the onset of paternal aggression that may be analogous to maternal aggression.

Introduction

Aggressive behavior is often considered to be a unitary process, but recent studies suggest that different physiological processes regulate aggression in different contexts (Nelson and Trainor, 2007). In humans, a distinction has been drawn between impulsive aggression and instrumental aggression (Vitiello and Stoff, 1997). Impulsive aggression is considered more spontaneous, and mediated by reduced serotonergic function (Blair, 2004, Manuck et al., 2006). In contrast, instrumental aggression is thought to be more premeditated and more closely resemble motivated behaviors (Berkowitz, 1993, Barratt et al., 1999), suggesting a role for dopaminergic function. In female mammals, reproductive context has substantial effects on aggressive behavior. In most mammalian species, females are less aggressive than males, but will become very aggressive after giving birth (Lonstein and Gammie, 2002). This increased parental aggression is directed primarily at male intruders that could be infanticidal. In rodents, this heightened aggression is maintained with tactile stimulation from pups (Svare et al., 1980, Stern and Kolunie, 1993). Patterns of neuronal activity (as inferred by measuring immediate early gene expression) following maternal aggression tests differ from those observed in resident–intruder aggression tests in males (Gammie, 2005), suggesting that there are differences in the neurobiological mechanisms regulating aggression in these contexts. In a few biparental mammalian species, males provide high levels of parental care to their offspring. Whether males of these species display increased aggression as parents has not been examined in detail.

In rats, estradiol facilitates the onset of maternal aggression (Gandelman, 1980, Mayer and Rosenblatt, 1987), but in mice estradiol inhibits the onset of maternal aggression (Ghiraldi et al., 1993). These species differences parallel findings of variable effects of estrogens on male aggression. In some species estrogens increase male aggression, whereas estrogens inhibit male aggression in other species (Trainor et al., 2006b). Estrogens can affect aggression in males because circulating androgens can be converted to estrogens by aromatase present in the brain. One possible mechanism for this intraspecies variability could be differential activation of estrogen receptor subtypes. Mammals have two estrogen receptor subtypes, estrogen receptor α (ERα) and estrogen receptor β (ERβ). In knock-out mouse studies, selective deletion of ERα decreases male-male aggression (Ogawa et al., 1997, Scordalakes and Rissman, 2003), whereas deletion of ERβ is usually associated with increased male-male aggression (Ogawa et al., 1999, Nomura et al., 2006). Another possible mechanism is that the environment can regulate the molecular actions of estrogen receptors. In Peromyscus polionotus, estrogens act rapidly to increase aggression when males are housed in winter-like short days (Trainor et al., 2007a), apparently via non-genomic processes. When males are housed in summer-like long days, estrogens act over a longer time frame to decrease aggression (apparently via genomic action).

We examined the effects of reproductive experience on aggressive behavior in California mice (P. californicus). Field studies show that individuals of this species form monogamous pairs (Ribble, 1991) and laboratory studies show that males provide a high level of parental care to their pups (Gubernick and Alberts, 1987, Bester-Meredith et al., 1999). We tested virgin and parental males in resident–intruder aggression tests to determine the presence of heightened aggression analogous to maternal aggression in male parents. Because estrogens are known to facilitate the onset of maternal aggression, we examined ERα and ERβ immunoreactivity in virgin males and parents. A previous study reported increased ERα in the MPOA of maternal rats (Champagne et al., 2003), but no study has examined whether ERα or ERβ expression changes with parental experience in a biparental species. We also stained for c-fos, an indirect marker of neuronal activity, following aggression tests. To examine whether parents and virgin males differed in their behavioral responses to intruders (independent of aggressive behavior), we assessed responsiveness to intruder odors with a habituation–dishabituation test.

Section snippets

Animals

We used California mice (P. californicus) obtained from Dr. Catherine Marler (University of Wisconsin, Madison, WI, USA). Males were individually-housed and provided with filtered tap water and Harlan Teklad 8640 food (Madison, WI) ad libitum. All experimental procedures were approved by the Ohio State University Institutional Animal Care and Use Committee and animals were maintained in accordance with the recommendations of the National Institutes of Health Guide for the Care and Use of

Results

Parental males bit intruders more frequently than virgin males (Fig. 1, t10 = 3.33, p < 0.01) and had significantly shorter attack latencies (Fig. 1, Mann–Whitney U = 45, p < 0.02). There were no significant differences in ERα expression in the LS, BNST, PVN, VMH, or pdMEA (Fig. 2, all ps > 0.1). In the MPOA, parental males had fewer ERα positive cells than virgins but this difference was not significant (t10 = 1.8, p = 0.1). There were no significant differences in the number of ERβ positive cells in the

Discussion

Many studies have demonstrated that female aggression toward males (maternal aggression) is increased following the birth of offspring. In biparental California mice, we demonstrated that parental males substantially increased aggressive behavior compared to virgin males. Increased aggression was not associated with changes in ERα or ERβ expression in the brain, suggesting that changes in the nuclear expression of these receptors in the hypothalamus and limbic system do not mediate this

Acknowledgments

The authors thank Patience Gallagher for technical assistance. This work was supported by an SBS Undergraduate Research Award to M.S.F., NIH MH076313 to B.C.T., and NIH MH57535 to R.J.N.

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