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.
Highlights
Evolution and Diversity in Social Phenotypes Vertebrate animals affiliate in multiple contexts, but sexual behavior is likely the only context of affiliation that is nearly ubiquitous across vertebrate species
Using five finch species that are all socially monogamous and biparental, we have shown that (1) receptor distributions for multiple neuropeptide systems (VT/MT, vasoactive intestinal polypeptide (VIP), and CRF) exhibit divergent and convergent evolution in relation to species-typical group size, within the lateral septum (LS), (2) VT cells in the BSTm exhibit an exquisite sensitivity to the valence of social stimuli, thereby www.frontiersin.org
creating differences between gregarious and territorial species in the response of their BSTm VT neurons to same-sex conspecifics, (3) endogenous nonapeptide signaling via V1a- and OT-like receptors in the LS promotes preferences for larger groups in zebra finches without effects on social contact time, and (4) in male zebra finches, antisense knockdown of VT production in the BSTm profoundly reduces gregariousness
Summary
Evolution and Diversity in Social Phenotypes Vertebrate animals affiliate in multiple contexts, but sexual behavior is likely the only context of affiliation that is nearly ubiquitous across vertebrate species. Territorial birds exhibit significantly greater IEG responses in the medial extended amygdala (especially the BSTm), ventrolateral LS, AH, lateral VMH, and CG (and adjacent “intercollicular” territory that is known to be homologous to the dorsal and dorsolateral CG of mammals; Goodson et al, 2005a; Kingsbury et al, 2011) This pattern is virtually identical to a pattern associated with aversive social stimulation in rodents (Sheehan et al, 2001; providing a good example of deep functional conservation in the social behavior circuits of vertebrate brains), but possible mechanisms of gregariousness were not evident at this level of analysis. OT antagonist administrations (peripheral, intraventricular, and intraseptal; zebra finches)
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