Nonapeptides and the evolution of social group sizes in birds

Abstract

Species-typical patterns of grouping have profound impacts on many aspects of physiology and behavior. However, prior to our recent studies in estrildid finches, neural mechanisms that titrate species-typical group-size preferences, independent of other aspects of social organization (e.g., mating system and parental care), have been wholly unexplored, likely because species-typical group size is typically confounded with other aspects of behavior and biology. An additional complication is that components of social organization are evolutionarily labile and prone to repeated divergence and convergence. Hence, we cannot assume that convergence in social structure has been produced by convergent modifications to the same neural characters, and thus any comparative approach to grouping must include not only species that differ in their species-typical group sizes, but also species that exhibit convergent evolution in this aspect of social organization. Using five estrildid finch species that differ selectively in grouping (all biparental and monogamous) we have demonstrated that neural motivational systems evolve in predictable ways in relation to species-typical group sizes, including convergence in two highly gregarious species and convergence in two relatively asocial, territorial species. These systems include nonapeptide (vasotocin and mesotocin) circuits that encode the valence of social stimuli (positive-negative), titrate group-size preferences, and modulate anxiety-like behaviors. Nonapeptide systems exhibit functional and anatomical properties that are biased toward gregarious species, and experimental reductions of nonapeptide signaling by receptor antagonism and antisense oligonucleotides significantly decrease preferred group sizes in the gregarious zebra finch. Combined, these findings suggest that selection on species-typical group size may reliably target the same neural motivation systems when a given social structure evolves independently.

Keywords: aggression; bird; evolution; mesotocin; oxytocin; sociality; vasopressin; vasotocin.

Figure 1

An evolutionarily conserved suite of brain regions that regulate vertebrate social behavior. (A) The core components of the social behavior network include numerous areas of the basal forebrain – the medial extended amygdala (medial amygdala, MeA, or taenial amygdala, TnA, plus the medial bed nucleus of the stria terminalis, BSTm), medial preoptic area (mPOA), anterior hypothalamus (AH), ventromedial hypothalamus (VMH), and lateral septum (LS), as well as areas of the midbrain, most notably the central gray (CG; or periaqueductal gray, PAG) and the ventral tegmental area (VTA). Modified from Newman (1999) and Maney et al. (2008). (B) A photomontage of a female zebra finch brain at the level of the anterior commissure (AC). Immunocytochemical triple-labeling for vasoactive intestinal polypeptide (VIP), neuropeptide Y (NPY), and tyrosine hydroxylase (TH) shows the location of the AH and multiple zones of the LS, BST, and VMH. The topography shown here is very similar across vertebrate groups, particularly among amniotes. Scale bar = 200 μm. Modified from Goodson, . Other abbreviations: BSTl, lateral bed nucleus of the stria terminalis; Hp, hippocampus; LH, lateral hypothalamus; LSc, caudal division of the lateral septum (dorsal, ventrolateral, and ventral zones denoted as LSc.d, LSc.vl, 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; v, lateral ventricle.

Figure 2

Valence sensitivity of vasotocin (VT) neurons in the medial bed nucleus of the stria terminalis (BSTm), as demonstrated by socially induced changes in the immunocytochemical colocalization of VT and the proxy activity marker Fos. (A) Representative colocalization of VT (green) and Fos (red) in the BSTm of a male zebra finch following a courtship interaction. Note that most VT neurons express Fos. Scale bar = 20 μm. (B) In the zebra finch, which is a highly gregarious species, isolation in a quiet room followed by exposure to a same-sex conspecific through a wire barrier produces a robust increase in VT neuronal activity in both males and females. Total n = 10. (C) This same manipulation produces a significant decrease in VT–Fos colocalization in the territorial violet-eared waxbill, a species that does not naturally exhibit same-sex affiliation, but exposure to the subject's pairbond partner (a presumably positive stimulus), produces a robust increase in neuronal activity. Sexes are shown pooled. Total n = 16. (D) VT–Fos colocalization increases in zebra finches following competition with a same-sex individual for courtship access to an opposite-sex bird, but not if the subject is paired with a highly aggressive partner and intensely subjugated. Subjugated animals were aggressively displaced or attacked 71–210 times during a 10-min interaction, demonstrating that social arousal alone does not increase VT–Fos colocalization in the BSTm. Sexes are shown pooled. Total n = 15. (A) is modified from Goodson et al. (2009b); (B–D) are modified from Goodson and Wang (2006).

Figure 3

Species differences in linear ¹²⁵I–V_1a antagonist binding in the lateral septum (LS) reflect evolutionary convergence and divergence in flocking and territoriality. (A–E) Representative ¹²⁵I–V_1a antagonist binding in the LS of the territorial Melba finch [MF; (A)], territorial violet-eared waxbill [VEW; (B)], moderately gregarious Angolan blue waxbill [ABW; (C)], colonial spice finch [SF; (D)], and colonial zebra finch [ZF; (E)]. The scale bar in (E) corresponds to 500 μm in (A–E). (F,G) Representative sections for a male Angolan blue waxbill and male spice finch (colonial), respectively, showing species differences in binding for the nidopallium (N) and other areas of the forebrain. The scale bar in (G) corresponds to 1 mm in (F,G). (H) Linear ¹²⁵I–V_1a antagonist binding in the dorsal (pallial) portion of the LS, shown as decompositions per min/mg (dpm/mg; means ± SEM). Different letters above the error bars denote significant species differences (Fisher's PLSD following significant ANOVA; P < 0.0001). Asterisks denote near-significant species differences (P = 0.06). Modified from Goodson et al. (2006). Abbreviations: E, entopallium; HA, apical part of the hyperpallium; LSc, caudal division of the lateral septum (dorsal, ventrolateral, and ventral zones denoted as LSc.d, LSc.vl, and LSc.v, respectively); LSr, rostral division of the lateral septum; LSt, lateral striatum; MS, medial septum; N, nidopallium; SH, septohippocampal septum; TeO, optic tectum.

Figure 4

Species-specific distributions of oxytocin-like binding sites reflect evolutionary convergence and divergence in flocking and territoriality. (A–C) Representative autoradiograms of ¹²⁵I–OT antagonist binding sites in the caudal LS (LSc) in two sympatric, congeneric finches – the territorial violet-eared waxbill (A) and the gregarious Angolan blue waxbill (B), plus the highly gregarious zebra finch (C). (D) Densities of binding sites in the dorsal (pallial) LSc of two territorial species (Melba finch, MF, and violet-eared waxbill, VEW), a moderately gregarious species (Angolan blue waxbill, ABW), and two highly gregarious species (spice finch, SF, and zebra finch, ZF). No sex differences are observed and sexes were pooled. Total n = 23. Different letters above the boxes denote significant species differences (Mann–Whitney P < 0.05) following significant Kruskal–Wallis. (E) Binding densities tend to reverse in the subpallial LSc (P = 0.06), suggesting that species differences in sociality are most closely associated with the relative densities of binding sites along a dorso-ventral gradient, as confirmed in the bottom (F) using a dorsal:ventral ratio. Abbreviations: Hp, hippocampus; LSc.d, dorsal zone of the LSc; LSc.v,vl, ventral, and ventrolateral zones of the LSc; N, nidopallium; PLH, posterolateral hypothalamus; TeO, optic tectum. Modified from Goodson et al. (2009c).

Figure 5

Endogenous activation of oxytocin-like receptors promotes preferences for larger groups. (A) Choice apparatus design. A 1-m wide testing cage was subdivided into zones by seven perches (thin lines). Subjects were considered to be within close proximity when they were within 6 cm of a stimulus cage (i.e., on the perches closest to the sides of the testing cage). The stimulus cages contained either 2 or 10 same-sex conspecifics. (B–E) Relative to vehicle treatments, subcutaneous (s.c.) or intracerebroventricular (i.c.v.) administrations of the oxytocin antagonist desGly–NH₂, d(CH₂)₅[Tyr(Me)², Thr⁴]OVT (OTA; 250 ng), reduce the amount of time that zebra finches spend in close proximity to the large group (B,C) and increase time in close proximity to the small group (D,E). *P < 0.05, ***P < 0.001, main effect of Treatment; #P < 0.5 Sex*Treatment; n = 12 m, 12 f. Letters above the error bars denote significant within-sex effects. Modified from Goodson et al. (2009c).