2018

Animals have evolved flexible strategies that allow them to evaluate and respond to their social environment by integrating the salience of external stimuli with internal physiological cues into adaptive behavioral responses. A highly conserved social decision-makingnetwork (SDMN), consisting of interconnected social behavior and mesolimbic reward networks, has been proposed to underlie such adaptive behaviors across all vertebrates, although our understanding of this system in reptiles is very limited. Here we measure neural activation across the SDMN and associated regions in the male brown anole (Anolis sagrei), within both reproductive and agonistic contexts, by quantifying the expression density of the immediate early gene product Fos. We then relate this neural activity measure to social context, behavioral expression, and activation (as measured by colocalization with Fos) of different phenotypes of ‘source’ node neurons that produce neurotransmittersand neuropeptides known to modulate SDMN ‘target’ node activity. Our results demonstrate that measures of neural activation across the SDMN network are generally independent of specific behavioral output, although Fos induction in a few select nodes of the social behavior network component of the SDMN does vary with social environment and behavioral output. Under control conditions, the mesolimbic reward nodes of the SDMN actually correlate little with the social behavior nodes, but the interconnectivity of these SDMN components increases dramatically within a reproductive context. When relating behavioral output to specific source node activation profiles, we found that catecholaminergic activation is associated with the frequency and intensity of reproductive behavior output, as well as with aggression intensity. Finally, in terms of the effects of source node activation on SDMN activity, we found that Ile⁸-oxytocin (mesotocin) populations correlate positively, while Ile³-vasopressin (vasotocin), catecholamine, and serotonin populations correlate negatively with SDMN activity. Taken together, our findings present evidence for a highly dynamic SDMN in reptiles that is responsive to salient cues in a social context-dependent manner.

Understanding how the brain processes social information and generates adaptive behavioural responses is a major goal in neuroscience. We examined behaviour and neural activity patterns in socially relevant brain nuclei of hermaphroditic mangrove rivulus fish (Kryptolebias marmoratus) provided with different types of social stimuli: stationary model opponent, regular mirror, non-reversing mirror and live opponent. We found that: (i) individuals faced with a regular mirror were less willing to interact with, delivered fewer attacks towards and switched their orientation relative to the opponent more frequently than fish exposed to a non-reversing mirror image or live opponent; (ii) fighting with a regular mirror image caused higher expression of immediate-early genes (IEGs: egr-1 and c-Fos) in the teleost homologues of the basolateral amygdala and hippocampus, but lower IEG expression in the preoptic area, than fighting with a non-reversing mirror image or live opponent; (iii) stationary models elicited the least behavioural and IEG responses among the four stimuli; and (iv) the nonreversing mirror image and live opponent drove similar behavioural and neurobiological responses. These results suggest that the various stimuli provide different types of information related to conspecific recognition in the context of aggressive contests, which ultimately drive different neurobiological responses.

The ability to reliably identify individuals over time and across contexts is essential in numerous areas of science. There are a variety of well-established methods for uniquely marking individuals, such as using paint or dye, visible implant elastomer tags, numbers or barcodes glued to the animal, passive integrated transponders, and more. For some species, life history stages, and/or experiments, however, these existing tagging methods are not sufficient. Here, we describe the method we developed for tagging juveniles of the African cichlid fish, Astatotilapia burtoni, which are too small for the methods used to tag adults. We used fishing line threaded through the needle of an insulin syringe to tie a loop of line through the dorsal muscle of juveniles as small as 10 mm standard length. Unique color patterns on the line can be used to distinguish among individuals. The tag is compatible with normal locomotion and social behavior, discernible to the eye and on camera, durable enough to last at least months, and the juvenile can grow with the tag. For A. burtoni, which is a model system in social neuroscience, the lack of an appropriate tagging method for very small juveniles likely contributes to the relative lack of early-life studies, and the same may be true for other small species. We expect this method to be useful in a variety of species and will facilitate the integration of organismal and behavioral development into more research programs.

A central challenge to evolutionary computation is enabling techniques to evolve increasingly complex target end products. Frequently direct approaches that reward only the target end product itself are not successful because the path between the starting conditions and the target end product traverses through a complex fitness landscape, where the directly accessible intermediary states may be require deleterious or even simply neutral mutations. As such, a host of techniques have sprung up to support evolutionary computation techniques taking these paths. One technique is scaffolding where intermediary targets are used to provide a path from the starting state to the end state. While scaffolding can be successful within well-understood domains it also poses the challenge of identifying useful intermediaries. Within this paper we first identify some shortcomings of scaffolding approaches — namely, that poorly selected intermediaries may in fact hurt the evolutionary computation’s chance of producing the desired target end product. We then describe a light-weight approach to selecting intermediate scaffolding states that improve the efficacy of the evolutionary computation.

The diversity of mating systems among animals is astounding. Importantly, similar mating systems have evolved even across distantly related taxa. However, our understanding of the mechanisms underlying these convergently evolved phenotypes is limited. Here, we examine on a genomic scale the neuromolecular basis of social organization in Ectodini cichlids from Lake Tanganyika. Using field collected males and females of four closely related species representing two independent evolutionary transitions from polygyny to monogamy, we take a comparative transcriptomic approach to test the hypothesis that these independent transitions have recruited similar gene sets. Our results demonstrate that while lineage and species exert a strong influence on neural gene expression profiles, social phenotype can also drive gene expression evolution. Specifically, 331 genes (~6% of those assayed) were associated with monogamous mating systems independent of species or sex. Among these genes, we find a strong bias (4:1 ratio) toward genes with increased expression in monogamous individuals. A highly conserved nonapeptide system known to be involved in the regulation of social behavior across animals was not associated with mating system in our analysis. Overall, our findings suggest deep molecular homologies underlying the convergent or parallel evolution of monogamy in different lineages of Ectodini cichlids.