Female social reproductive roles affect central monoamines

Abstract

Central monoamines display a variety of activation patterns in different social groups, and among males and females. We addressed three social conditions for female lizards of the species Anolis carolinensis: Isolated, paired with a mate, and in a group of 5 competing for one mate. Among those in a group, only 1 or 2 females exhibited recrudescing ovaries. Individuals paired with a mate (for one month) exhibited ovarian growth, isolated animals (initial controls) had quiescent ovaries. Reproductively dominant females had significantly greater telencephalic 5-HIAA, and serotonergic activation, as indicated by the ratio of 5-HIAA to 5-HT. Telencephalic HVA as well as the HVA/DA ratio were also significantly greater in dominant females compared to all other groups. In contrast, serotonergic activation in brainstem was elevated in subordinate females only. These results suggest that serotonergic activation in telencephalon, found only in dominant females, not in other reproductively active females, is a function of the unique social role of a dominant female, possibly combining submissive behaviors toward a male with dominance over other females and competition for access to that male. Dopaminergic activation in telencephalon, also found only in dominant females, may be related to aggressive interactions with other females. Activation of serotonin in brainstem, found in this study in subordinate females and previously in males [C.H. Summers and N. Greenberg, Activation of central biogenic amines following aggressive interaction in male lizards, Anolis carolinensis, Brain Behav. Evol., 45 (1995) 339–349], may be associated with subordinate social status. Monoamines, involved in social behaviors, appear to be regionally specialized for dominant and subordinate social roles, in males [C.H. Summers and N. Greenberg, Activation of central biogenic amines following aggressive interaction in male lizards, Anolis carolinensis, Brain Behav. Evol., 45 (1995) 339–349][T.R. Summers, E.T. Larson, A.L. Hunter, K.J. Renner, N. Greenberg and C.H. Summers, Amygdalar serotonin mediates long-term social roles following aggressive interaction, Soc. Neurosci. Abs., 22 (1996) 1147] and females. Dominant females exhibit unique social position, behavior and monoamine profile whereas subordinate females and males have a similar serotonergic response in this species.

Introduction

Gender and reproductive status play important roles in determining social behavior. Differential activation of monoamine systems may mediate behavior that varies with social and reproductive status. Changes in monoaminergic activity have been linked to social status and aggression in both vertebrates [43] and invertebrates [21]. The objective of the research reported here was to investigate the effects of social and reproductive status on monoamine utilization in females.

Dominant and subordinate social roles are mediated neurochemically. An increase in serotonin (5-HT) system activity has been demonstrated in subordinate animals from fish to primates 5, 44, 45 as indicated by either 5-hydroxyindoleacetic acid (5-HIAA), or the ratio of 5-HIAA to 5-HT. In lizards, subordinate male Sceloporus jarrovi in the field also have increased serotonergic activity [28], as do subordinate male Anolis carolinensis (in brainstem, and telencephalon) [36]. Dominant male S. jarrovi actively defending their territory, however, also exhibit telencephalic serotonergic activation immediately following an aggressive display [28]. It would appear that dominant individuals may have a substantial, but short-lived 5-HT system activation which occurs during aggressive encounters and diminishes quickly. In contrast, subordinate males may exhibit chronic activation of the serotonergic system 36, 38. Taken together, these results suggest a component of 5-HT action in dominant individuals related to aggressive encounters, and another component related to conditions of subordinate social status.

There is substantial evidence for a relationship between aggression and serotonergic activation 9, 29, 30 where reduced serotonergic activity is generally associated with aggressiveness. Lesions of the medial and dorsal raphe nuclei resulted in decreased forebrain serotonin content and increased aggressiveness 16, 39, 41. Isolated aggressive male mice have decreased serotonergic activation (as measured by 5-HIAA/5-HT) when compared to non-isolated, non-aggressive controls [40]. Females of this species do not exhibit aggressiveness in isolation, and there is no difference in 5-HIAA/5-HT between isolated and non-isolated females [40]. Aggression in females would appear to include a serotonergic element, however, since aggressive behavior of postpartum female mice toward unfamiliar males can be inhibited by manipulation of brain serotonin levels [22]. In addition, maternal aggression in rats is inhibited by 5-HT agonists [30].

Dopamine (DA) system activation is often associated with dominant individuals. Dominant male fish have increased telencephalic levels of the dopamine catabolite homovanillic acid (HVA) [44], and dominant A. carolinensis males have increased brainstem DA activation as indicated by higher ratios of DOPAC (dopamine catabolite 3,4-dihydroxyphenylacetic acid) to DA (DOPAC/DA) [36]. Territorial male S. jarrovi actively defending their territory also exhibit telencephalic DA system activation [28].

Female A. carolinensis manifest dominant/subordinate relationships characterized by behavior, posture and fighting as in males [2]. Changes in body color in A. carolinensis also reflect stress and social status 2, 17, 18, 37. Subordinate males are darker in color [35]. Dominant and subordinate females are not different in body color when males are absent [2]. However, both groups are significantly darker when a male is present, and dominant females are darker than subordinate females. Dominant female A. carolinensis interact more with males [2] and have enhanced reproductive function [37] when compared with subordinate females. The characteristic response of a female A. carolinensis to male courtship behavior [2] is remarkably similar to the submissive behavior of a subordinate male to a dominant male [17].

The purpose of these experiments was to study monoamine activation in females in relation to aggression within a dominance hierarchy, and in the context of competition for and interactions with a male. We hypothesized that differences found in females with regard to social status, ovarian recrudescence, and body color would be reflected in changes in brain neurochemistry. Dominant female A. carolinensis in the presence of a male, have the unique behavioral profile of submissive/subordinate interactions with the male in combination with aggressive interactions with other females, while ovaries are growing (recrudesce) 2, 11. Although very little is known about the neurochemistry of social dominance among females, we hypothesized that the pattern of neurochemical activity associated with dominant and subordinate status in females would be similar to that measured in males. Specifically, we expected to see elevated 5-HIAA and 5-HIAA/5-HT ratio in brainstem of subordinate females [35]. We also hypothesized that DA utilization would be higher in dominant females [28].