Abstract
Gene duplication is thought to allow for the origin of novel gene functions. However, how duplication influences gene function is difficult to determine, as new adaptations may subsume previous traits and the ancestral state is often unknown. One solution is to investigate the functions of a gene that exists as a single and duplicated state in different species. Here, we leverage a system for which functions have been well-characterized in the duplicates – the oxytocin/vasopressin system in vertebrates – and that exists as a single copy – inotocin - in insects. To answer the question of how functions of a single copy are partitioned prior to gene duplication, we experimentally tested the relationship between inotocin gene expression and the known social and non-social functions of oxytocin/vasopressin in a subsocial beetle that expresses complex parental care. We found that inotocin was strongly related to water balance in both males and females, corroborating other evidence that water balance is an ancestral function. Moreover, we found that inotocin was associated with male, but not female, parental care states, influencing the expression of care behavior towards offspring in males. Lastly, using immunohistochemistry, we show that inotocin is broadly distributed in the brains of both female and male parents. These results suggest that the ancestral social function of the vasopressin system may have been to moderate flexibility in male, rather than female behavior, and the role of oxytocin/vasopressin in female-offspring interactions is more recent.
Significance Statement Oxytocin/vasopressin are amongst the most studied neuropeptides in vertebrates, influencing water balance, mating interactions, and most notably, social bonding. This gene pair evolved from a duplication in the vertebrate lineage of an ancestral vasopressin-like gene. Are the multiple social effects in vertebrates due to this duplication, or are social influences also ancestral? Here, we demonstrate that, in a biparental social beetle with a single copy, inotocin influences social interactions between fathers and offspring as well as having the ancestral function of water balance in both males and females. In vertebrates, influences on social interactions with males is associated with both oxytocin and vasopressin. This may indicate that gene duplication allowed for the evolution of new behavioral functions in females.
Competing Interest Statement
The authors have declared no competing interest.
