Neuro-evolutionary patterning of sociality

Abstract

Evolutionary shifts in species-typical group size ('sociality') probably reflect natural selection on motivational processes such as social arousal, approach-avoidance, reward, stress/anxiety and dominance. Using four songbird species that differ selectively in sociality (one territorial, one modestly gregarious, and two highly gregarious species), we here examined immediate early gene (IEG) responses of relevant brain regions following exposure to a same-sex conspecific. The paradigm limited behavioural performance, thus species differences should reflect divergence in motivational and/or perceptual processes. Within the extended medial amygdala (which is involved in appetitive approach, social arousal and avoidance), we observed species differences in IEG response that are negatively graded in relation to sociality. In addition, brain areas that are involved in social stress and dominance-related behaviour (ventrolateral septum, anterior hypothalamus and lateral subdivision of the ventromedial hypothalamus) exhibited IEG responses that dichotomously distinguish the territorial species from the three gregarious species. The IEG responses of areas involved in reward (nucleus accumbens and ventral pallidum) and general stress processes (e.g. paraventricular hypothalamus, lateral bed nucleus of the stria terminalis and most areas of the lateral septum) do not correlate with sociality, indicating that social evolution has been accompanied by selection on a relatively discrete suite of motivational systems.

Figure 1

The social behaviour network and its responses to social stimuli in gregarious and territorial songbirds. (a) The network as originally described for mammals (modified from Newman 1999). As indicated, nodes of the network are extensively interconnected. All areas concentrate steroid hormones and are involved in multiple forms of mammalian social behaviour. (b) Schematic representation of the present data, showing responses of the network in gregarious (i) and territorial (ii) songbird species. As indicated by the dashed line, modestly gregarious species exhibit greater responses in the extended medial amygdala than do highly gregarious species, but less than the territorial species.

Figure 2

(Opposite.) Multiple components of the social behaviour network (visualized by chemoarchitecture) and their IEG responses to a same-sex social stimulus. (a) A coronal section of the midline forebrain of a zebra finch at the level of the anterior commissure (AC; modified from Goodson et al. 2004). Shown are multiple network components and associated structures as visualized by triple-label immunocytochemistry for neuropeptide Y (NPY; red), tyrosine hydroxylase (TH; purple) and vasoactive intestinal polypeptide (VIP; green). We have employed NPY and TH antibodies in conjunction with IEG antibodies to allow delineation of the septal nuclei and other areas. Scale bar, 200 μm. (b,c) FOS immunoreactivity (green) in experimental (b) and control (c) male violet-eared waxbills (territorial), showing responses of the experimental animal in the ventrolateral LS, BSTm and AH (structural detail provided by DAPI nuclear stain, pseudocoloured red). Scale bars, 100 μm. (d–m) ZENK (d–g) and FOS (h–m) response indices (experimental cell counts minus mean counts for controls; see § 3b) for components of the social behaviour network in the territorial violet-eared waxbill (VEW), the modestly gregarious Angolan blue waxbill (ABW) and two highly colonial species—the spice finch (SF) and zebra finch (ZF; unlike other subjects, ZF were domestic and in breeding condition). Response indices are shown as the number of immunoreactive nuclei per 100 μm² (means±s.e.m.). Different letters above the error bars indicate significant species differences (Fisher’s PLSD, p<0.05) following significant ANOVA (sex×species; no main effects of sex were observed, thus male and female data are shown pooled). Abbreviations: AC, anterior commissure; AH, anterior hypothalamus; BSTm, medial bed nucleus of the stria terminalis; BSTl, lateral bed nucleus of the stria terminalis; CG, midbrain central grey; ext. MeA, extended medial amygdala; Hp, hippocampus; ICo, nucleus intercollicularis; LSc, caudal division of the lateral septum (dorsal, ventrolateral, lateral and ventral zones denoted as LSc.d, LSc.vl, LSc.l and LSc.v, respectively); LSr, rostral division of the lateral septum; ME, median eminence; MS, medial septum; MSib, internal band of the medial septum; ot, optic tract; OM, occipitomesencephalic tract; PVN, paraventricular nucleus of the hypothalamus; SH, septohippocampal septum; Tn, nucleus taeniae; v, lateral ventricle; VMH, ventromedial hypothalamus.