The vertebrate social behavior network: Evolutionary themes and variations

Abstract

Based on a wide variety of data, it is now clear that the brains of birds and teleost (bony) fish possess a core "social behavior network" within the basal forebrain and midbrain that is homologous to the social behavior network of mammals. The nodes of this network are reciprocally connected, contain receptors for sex steroid hormones, and are involved in multiple forms of social behavior. Other hodological features and neuropeptide distributions are likewise very similar across taxa. This evolutionary conservation represents a boon for experiments on phenotypic behavioral variation, as the extraordinary social diversity of teleost fish and songbirds can now be used to generate broadly relevant insights into issues of brain function that are not particularly tractable in other vertebrate groups. Two such lines of research are presented here, each of which addresses functional variation within the network as it relates to divergent patterns of social behavior. In the first set of experiments, we have used a sexually polymorphic fish to demonstrate that natural selection can operate independently on hypothalamic neuroendocrine functions that are relevant for 1) gonadal regulation and 2) sex-typical behavioral modulation. In the second set of experiments, we have exploited the diversity of avian social organizations and ecologies to isolate species-typical group size as a quasiindependent variable. These experiments have shown that specific areas and peptidergic components of the social behavior network possess functional properties that evolve in parallel with divergence and convergence in sociality. Keywords sociality; aggression; sexual behavior; communication; vocalization; arginine vasopressin; arginine vasotocin; isotocin; mesotocin; oxytocin; fish; bird; bed nucleus of the stria terminalis; amygdala; lateral septum; anterior hypothalamus; ventromedial hypothalamus; preoptic area; periaqueductal gray; nucleus intercollicularis; c-fos; egr-1; ZenkThe research program described below is designed to address two major goals. The first of these goals is to elucidate evolutionary themes in the neuroendocrine, functional, and connectional organization of brain circuits that regulate social behavior. This will provide a phylogenetically broad framework for examining the neural and neuroendocrine mechanisms of behavior, and will allow detailed and meaningful comparisons to be made across the major vertebrate classes. Building upon this foundation, the second primary goal is to capitalize on the extraordinary behavioral diversity of birds and teleost (bony) fish to elucidate the ways that neural and neuroendocrine mechanisms are adjusted over evolutionary time to produce intraspecific and interspecific variation in behavior. If conducted within a well-characterized, comparative framework, these findings obtained in birds and fish should yield solid predictions for other vertebrates as well. Thus, our work addresses evolutionary themes, as described in the first section below, and variations on those themes, as...

Effects of season, testosterone and female exposure on c-fos expression in the preoptic area and amygdala of male green anoles

“…However, as in the present research, in other brain regions including the POA and portions of the AMY, female exposure did not affect c-fos expression (Michael et al, 1999). Similarly, in several avian species (ranging from a highly territorial species to one that is very gregarious), immediate early gene expression in the extended medial AMY is negatively correlated with group size of the species (Goodson, 2005;Goodson et al, 2005a,b).…”

“…The expression of immediate early genes, such as c-fos, has been widely used to identify brain regions involved in the control of sexual behavior, including those composing the "social behavior network" (Goodson, 2005;Newman, 1999). For example, c-fos expression is enhanced in the POA and AMY of male rodents, quail and house sparrows following exposure to a sexual stimulus and/or reproductive behavior (Heeb and Yahr, 1996;Pfaus and Heeb, 1997;Riters et al, 2004;Taziaux et al, 2006).…”

Neuropeptide binding reflects convergent and divergent evolution in species-typical group sizes

“…Species differences in binding are observed for a number of basal forebrain sites that participate in the control of social behavior, reproductive physiology, and stress responses. These include the LS, BSTm, and VMH --areas that may act in concert to coordinate approach-avoidance behaviors and aversion processes (review: Goodson, 2005; also see Sheehan et al, 2001). Given that these brain areas are evolutionarily conserved in their functional and anatomical features, our findings may be relevant for a wide range of vertebrates.…”

“…In contrast, the behavioral and ecological diversity of birds (Konishi et al, 1989) offers at least a few good opportunities for highly controlled, comparative studies of sociality (Goodson et al, 2005c). Given that the neurobehavioral systems of birds are very similar to other vertebrates, including mammals, avian studies on this topic should also be broadly relevant (Ball and Balthazart, 2001;Goodson, 2005).Interestingly, manipulations that influence pair-bonding in monogamous prairie voles (Microtus ochrogaster) also influence non-sexual affiliation (Pitkow et al, 2001). This finding suggests that evolution in sociality and evolution in mating system may involve coordinated modifications of at least some neural mechanisms.…”

“…In contrast, the behavioral and ecological diversity of birds (Konishi et al, 1989) offers at least a few good opportunities for highly controlled, comparative studies of sociality (Goodson et al, 2005c). Given that the neurobehavioral systems of birds are very similar to other vertebrates, including mammals, avian studies on this topic should also be broadly relevant (Ball and Balthazart, 2001;Goodson, 2005).…”