2017

Social and ecological challenges often elicit behavioural and physiological responses that are adaptive and subject to selection. The varying behavioural states and traits of animals are a direct output of the nervous system and underlying molecular substrates. Changes in gene expression in response to a variety of contexts such as mate choice, aggression and developmental experience can alter a number of cellular and neural pathways that lead to changes in behaviour. A common framework has emerged to understand the role of the transcriptome in animal behaviour. Behavioural plasticity describes both an individual’s ability to modify behavioural states and correlated suites of behaviour in populations, which may constrain variance across contexts. By integrating the study of behavioural plasticity with genome scale, bioinformatics and candidate gene analyses, we are rapidly expanding our understanding of this kind of organismal flexibility, its relationship with the genome and its evolutionary implications.

In response to a territory intrusion, neighboring males of the African cichlid fish Astatotilapia burtoni engage in aggressive joint territory defense in a manner that depends on their social role. Here, we examine the possible function of several neuroendocrine and neuromodulator pathways previously implicated in the regulation of complex social behavior. We find that the neuromolecular regulation of aggression during joint territory defense is very much dependent on an individual’s role in this context. In neighbors but not in residents, aggression is correlated to gene expression in the medial part of the dorsal telencephalon (area Dm), the putative homolog to the mammalian basolateral amygdala. This correlation is strikingly high for expression of the serotonin receptor 5-HT2c, suggesting the serotonin system is important in regulating context-dependent behavior. Furthermore, by examining candidate gene expression co-variance patterns in area Dm and in the lateral part of the dorsal telencephalon (area Dl), the putative homolog to the mammalian hippocampus, we identify two main patterns: gene expression is co-regulated within, but not across, brain regions, and co-regulation is synergistic rather than antagonistic. Our results highlight the critical effect of social context on both behavior and its neuromolecular basis.

Nervous systems are among the most spectacular products of evolution. Their provenance and evolution have been of interest and often the subjects of intense debate since the late nineteenth century. The genomics era has provided researchers with a new set of tools with which to study the early evolution of neurons, and recent progress on the molecular evolution of the first neurons has been both exciting and frustrating. It has become increasingly obvious that genomic data are often insufficient to reconstruct complex phenotypes in deep evolutionary time because too little is known about how gene function evolves over deep time. Therefore, additional functional data across the animal tree are a prerequisite to a fuller understanding of cell evolution. To this end, we review the functional modules of neurons and the evolution of their molecular components, and we introduce the idea of hierarchical molecular evolution.

Nonapeptides play a fundamental role in the regulation of social behavior, among numerous other functions. In particular, arginine vasopressin and its non-mammalian homolog, arginine vasotocin (AVT), have been implicated in regulating affiliative, reproductive, and aggressive behavior in many vertebrate species. Where these nonapeptides are synthesized in the brain has been studied extensively in most vertebrate lineages. While several hypothalamic and forebrain populations of vasopressinergic neurons have been described in amniotes, the consensus suggests that the expression of AVT in the brain of teleost fish is limited to the hypothalamus, specifically the preoptic area (POA) and the anterior tuberal nucleus (putative homolog of the mammalian ventromedial hypothalamus). However, as most studies in teleosts have focused on the POA, there may be an ascertainment bias. Here, we revisit the distribution of AVT preprohormone mRNA across the dorsal and ventral telencephalon of a highly social African cichlid fish. We first use in situ hybridization to map the distribution of AVT preprohormone mRNA across the telencephalon. We then use quantitative real-time polymerase chain reaction to assay AVT expression in the dorsomedial telencephalon, the putative homolog of the mammalian basolateral amygdala. We find evidence for AVT preprohormone mRNA in regions previously not associated with the expression of this nonapeptide, including the putative homologs of the mammalian extended amygdala, hippocampus, striatum, and septum. In addition, AVT preprohormone mRNA expression within the basolateral amygdala homolog differs across social contexts, suggesting a possible role in behavioral regulation. We conclude that the surprising presence of AVT preprohormone mRNA within dorsal and medial telencephalic regions warrants a closer examination of possible AVT synthesis locations in teleost fish, and that these may be more similar to what is observed in mammals and birds.

Evolutionary computation and neuroevolution seek to create systems of ever increasing sophistication, such that the digitally evolved forms reflect the variety, diversity, and complexity seen within nature in living organisms. In general, most evolutionary computation and neuroevolution techniques do so by encoding the final form without any type of development. This is in contrast to nature, where most complex organisms go through a developmental period. Here we focus on an evolving digital tissues that develop from a single cell and unfold into a complex body plan. It quickly became evident that evolving developing forms is quite challenging. We compare four different techniques that have successfully been employed within evolutionary computation to evolve complex forms and behavior: scaffolding (i.e., gradually increasing the difficulty of the task rewarded by the environment over evolutionary time), stepping stones (i.e., rewarding easier tasks within an environment that can co-opted for the performance of more complex tasks), and island models (i.e., rewarding different fitness functions within different subpopulations with migration). We show the effect of these methods on the evolution of complex forms that develop from a single cell, the rate of adaptation, and different dimensions of robustness and variation among solutions.

Oxytocin (OT) mediates social habituation in rodent model systems, but its role in mediating this effect in other vertebrates is unknown. We used males of the African cichlid fish, Astatotilapia burtoni , to investigate two aspects of isotocin (IT; an OT homolog) signaling in social habituation. First, we examined the expression of IT receptor 2 (ITR2) as well as two immediate early genes in brain regions implicated in social recognition. Next, we examined IT neuron activity using immunohistochemistry. Patterns of gene expression in homologs of the amygdala and hippocampus implicate IT signaling in these regions in social habituation to a territorial neighbor. In the preoptic area, the expression of the ITR2 subtype and IT neuron activity respond to the presence of a male, independent of familiarity. Our results implicate IT in mediating social habituation in a teleost.

Social context often has profound effects on behavior, yet the neural and molecular mechanisms which mediate flexible behavioral responses to different social environments are not well understood. We used the African cichlid fish, Astatotilapia burtoni, to examine aggressive defense behavior across three social contexts representing different motivational states: a reproductive opportunity, a familiar male and a neutral context.To elucidate how differences in behavior across con-texts may be mediated by neural gene expression, we examined gene expression in the preoptic area, a brain region known to control male aggressive and sexual behavior. We show that social context has broad effects on preoptic gene expression. Specifically, we found that the expression of genes encoding nonapeptides and sex steroid receptors are upregulated in the familiar male context. Furthermore, circulating levels of testosterone and cortisol varied markedly depending on social context. We also manipulated the D2 receptor (D2R) ineach social context, given that it has been implicated in mediating context-dependent behavior. We found that a D2R agonist reduced intruder-directed aggression in the reproductive opportunity and familiar male contexts, while a D2R antagonist inhibited intruder-directed aggression in the reproductive opportunity context and increased aggression in the neutral context. Our results demonstrate a critical role for preoptic gene expression, as well as circulating steroid hormone levels, in encoding information from the social environment and in shaping adaptive behavior. In addition, they provide further evidence for a role of D2R in context-dependent behavior.

Cooperative behavior is widespread among animals, yet the neural mechanisms have not been studied in detail. We examined cooperative territory defense behavior and associated neural activity in candidate forebrain regions in the cichlid fish, Astatotilapia burtoni. We find that a territorial male neighbor will engage in territory defense dependent on the perceived threat of the intruder. The resident male, on the other hand, engages in defense based on the size and behavior of his partner, the neighbor. In the neighbor, we find that an index of engagement correlates with neural activity in the putative homolog of the mammalian basolateral amygdala and in the preoptic area, as well as in preoptic dopaminergic neurons. In the resident, neighbor behavior is correlated with neural activity in the homolog of the mammalian hippocampus. Overall, we find distinct neural activity patterns between the neighbor and the resident, suggesting that an individual perceives and processes an intruder challenge differently during cooperative territory defense depending on its own behavioral role.