Evolving nonapeptide mechanisms of gregariousness and social diversity in birds

Abstract

Of the major vertebrate taxa, Class Aves is the most extensively studied in relation to the evolution of social systems and behavior, largely because birds exhibit an incomparable balance of tractability, diversity, and cognitive complexity. In addition, like humans, most bird species are socially monogamous, exhibit biparental care, and conduct most of their social interactions through auditory and visual modalities. These qualities make birds attractive as research subjects, and also make them valuable for comparative studies of neuroendocrine mechanisms. This value has become increasingly apparent as more and more evidence shows that social behavior circuits of the basal forebrain and midbrain are deeply conserved (from an evolutionary perspective), and particularly similar in birds and mammals. Among the strongest similarities are the basic structures and functions of avian and mammalian nonapeptide systems, which include mesotocin (MT) and arginine vasotocin (VT) systems in birds, and the homologous oxytocin (OT) and vasopressin (VP) systems, respectively, in mammals. We here summarize these basic properties, and then describe a research program that has leveraged the social diversity of estrildid finches to gain insights into the nonapeptide mechanisms of grouping, a behavioral dimension that is not experimentally tractable in most other taxa. These studies have used five monogamous, biparental finch species that exhibit group sizes ranging from territorial male-female pairs to large flocks containing hundreds or thousands of birds. The results provide novel insights into the history of nonapeptide functions in amniote vertebrates, and yield remarkable clarity on the nonapeptide biology of dinosaurs and ancient mammals.

An evolutionary framework for studying mechanisms of social behavior

“…Likewise, the demographic and kin composition of a population can affect decision-making in juveniles (Box 2) [59][60][61]. The costs and benefits of living in groups can affect the evolution of neural pathways underlying aggressive and cooperative behaviors, which in turn might affect group composition and persistence, and ultimately population structure (e.g., estrildid finches [62]). …”

“…For example, neuroanatomical differences in the volume of a particular brain region can be related to the relative behavioral demands on that region [74][75][76]. At the cellular level, the release of neurochemicals such as biogenic amines [43] and neuropeptides [62] into specific brain regions can directly result in specific behavioral profiles. Although the expression patterns of neurochemical genes, particularly those encoding receptors, are remarkably conserved [77], quantitative variation in receptor density and/or levels of neurochemicals in specific network nodes is strongly associated with diversity in social behavioral attributes between individuals and across species [68,78].…”

“…Work in seasonally social meadow voles as well as in colonial South American rodents has suggested parallel and potentially convergent pathways by which oxytocin receptor density is involved in natural variation in affiliative behavior and group living outside the context of monogamy [78]. In estrildid finches, homologous peptide receptors modulate group size pre ferences and are differentially distributed in species that exhibit year round territoriality or flocking, and the peptide neurons that supply these receptors respond selectively to positive social stimuli [62]. These species share ecological and other aspects of social organiza tion (e.g., all are monogamous and biparental), thus a major question is how the mechanisms of pair bonding, gregariousness, and territoriality evolve in other taxa where the ecological, social, and functional contexts can be different.…”

Effects of Increased Levels of Prenatal Mesotocin on Postnatal Individual Recognition and Stress Responsiveness in Northern bobwhite quail (Colinus Virginianus)

“…If the injected MT is not stable enough to last in the system once injected, it may be that the MT is no longer present at a critical time when it could have effects on areas of the brain that are involved in social behavior. For example, we know that centrally released MT from the PVN to areas of the amygdala and forebrain are main pathway by which social behavior is affected (Goodson et al, 2012). We also know that approximately embryonic day 8 in chicks is the peak time of neuron formation in the forebrain (Rogers, 1995).…”

“…We did not find any significant results on our individual recognition task. This could suggest that MT is not affecting this behavior due to its' lack of presence during a critical time for development of pathways in the brain associated with social behavior (Goodson et al, 2012). Further studies should work to elucidate the role of MT in prenatal development on postnatal behaviors associated with developmental and psychiatric disorders by developing new techniques to inject hormones not of maternal origin and by implementing behavioral paradigms to assess the behavioral components associated with these disorders.…”