Abstract
Animals display remarkable variation in social behaviour. However, outside of rodents, little is known about the neural mechanisms of social variation, and whether they are shared across species and sexes, limiting our understanding of how sociality evolves. Using coral reef butterflyfishes, we examined gene expression correlates of social variation (i.e. pair bonding versus solitary living) within and between species and sexes. In several brain regions, we quantified gene expression of receptors important for social variation in mammals: oxytocin (OTR), arginine vasopressin (V1aR), dopamine (D1R, D2R) and mu-opioid (MOR). We found that social variation across individuals of the oval butterflyfish, Chaetodon lunulatus, is linked to differences in OTR,V1aR, D1R, D2R and MOR gene expression within several forebrain regions in a sexually dimorphic manner. However, this contrasted with social variation among six species representing a single evolutionary transition from pair-bonded to solitary living. Here, OTR expression within the supracommissural part of the ventral telencephalon was higher in pair-bonded than solitary species, specifically in males. These results contribute to the emerging idea that nonapeptide, dopamine and opioid signalling is a central theme to the evolution of sociality across individuals, although the precise mechanism may be flexible across sexes and species.
Highlights
Animals display spectacular diversity in sociality, prompting fundamental questions about how it arises and evolves
Our work suggests that in Chaetodon butterflyfishes, nonapeptide, dopaminergic and mu-opioid receptor gene expression is important for mediating social variation
We found that the transition from pair bonding to solitary living in six species of Chaetodon butterflyfishes was associated with non-concordant MOR, D1R, D2R and V1aR receptor expression patterning
Summary
Animals display spectacular diversity in sociality (i.e. affiliative social behaviour [1]), prompting fundamental questions about how it arises and evolves. 15 MYA divergence time) that represent a single evolutionary transition from pair-bonded (C. vagabundus, C. lunulatus and C. baronessa) to solitary (C. trifascialis, C. rainfordii and C. plebeius) living These differences in sociality do not covary with other major ecological attributes controlling for these potential confounds (figure 1). Nor is it likely to be confounded with parental care, which is a common confound in mammalian male pair-bonding systems that, has not been studied in the focal populations, is reportedly absent in all butterflyfishes studied to date [20,23,24] We leveraged this butterflyfish system (figure 1) to compare brain gene expression associated with social variation (pair-bonded versus solitary living) between sexes and within versus among species. We tested the hypothesis that in butterflyfishes, mechanisms of social variation are similar across sexes, and within versus between species, and that neural patterns observed in butterflyfish are similar to those documented in Microtus voles
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