Phenotypic architecture of sociality and its associated genetic polymorphisms in zebrafish

Sociality is often seen as a single phenotypic trait, but it relies on motivational and cognitive components implemented by specific causal mechanisms. Hence, these components may have evolved independently, or may have been linked by phenotypic correlations driven by a shared selective pressure for increased social competence. Furthermore, these components may be domain-specific or of general domain across social and non-social contexts. Here we have characterized the phenotypic architecture of sociality in zebrafish, which has been increasingly used as a model organism in social neuroscience. For this purpose, we have behaviorally phenotyped zebrafish from different wild type lines in four tests: social tendency, social and non-social recognition, and open-field test. Our results indicate that: (1) sociality has two main components that are independent from each other (social tendency and social recognition), hence not supporting the occurrence of a sociality syndrome; (2) both social traits are phenotypically linked to non-social traits (non-social exploration and non-social memory, respectively), forming two general behavioral modules, general inspection and general recognition, and suggesting that sociality traits have been co-opted from general-domain motivational and cognitive traits. Moreover, the study of the association between genetic polymorphisms (i.e. single nucleotide polymorphisms, SNPs) and each behavioral module further supports this view, since several SNPs from a list of candidate “social” genes, are statistically associated with the general inspection (motivational), but not with a general recognition (cognitive), behavioral module. The SNPs associated with general inspection are widespread across different chromosomes and include neurotransmitters, neuromodulators, and synaptic plasticity genes, suggesting that this behavioral module is regulated by multiple genes, each of them with small effects. Together, these results support the occurrence of general domain motivational and cognitive behavioral modules in zebrafish, which have been co-opted for the social domain. Author summary Social living has been considered one of the major transitions in evolution and it has been considered to act as a major selective force shaping the evolution of brain and behavior in animals. Sociality relies on two basic behavioral mechanisms: (1) the willingness to approach and be near others (aka social tendency); and (2) the ability to distinguish between others (aka social recognition) in order to adjust the behavior expressed during social interactions according to the identity of the interactant. There is an ongoing debate on to what extent these social abilities have specifically evolved in response to social living and are domain specific, or if they were selected as a broad response to cognitive demands and are of general domain. Here, we used zebrafish to test the domain-specific vs. general domain hypotheses and to assess the association of social tendency and social recognition with a set of candidate “social” genes (i.e. genes that have been linked to social behavior in other studies with different vertebrate species). We found that both social traits are not correlated to each other and are of general domain, and that only social tendency is associated with candidate “social” genes, suggesting that social tendency and social recognition are independent behavioral modules that rely on separate genetic architectures and that can evolve separately.