Abstract
Introduction: A central question about the evolution of social behavior is how extensive diversity can arise when behaviors depend on shared neural, molecular, and hormonal mechanisms. Comparing close relatives can offer insights into which components of shared mechanisms are most evolvable. Methods: We discriminate between two nonexclusive hypotheses by which conserved neural mechanisms might evolve to generate differences in social behavior: changes in the number or activity of neurons. We test these hypotheses in two recently diverged ecotypes of threespine stickleback (Gasterosteus aculeatus); the common ecotype provides parental care, while the white ecotype does not. We used double-label fluorescent immunohistochemistry with pS6, a marker of transcriptionally active neurons, to quantify the number and activity of two preoptic neuropeptidergic cell types that affect parental care across vertebrates: galanin (Gal) and oxytocin (OXT). Results: Ecotypes did not differ in the overall activity of the preoptic area or the number of Gal and OXT neurons but did differ in the activity of Gal and OXT neurons. The activity of these neurons changed across reproductive stages in the common but not the white ecotype. Activity peaked after mating in commons when males began to care for their offspring, suggesting that changes in the activity of these specific preoptic neurons are required to transition from courtship to parenting. Conclusion: Overall, our study suggests that rapid behavioral evolution occurred via changes in the activity but not the number of specific preoptic neuropeptidergic neurons.
Plain Language Summary
Animals demonstrate an amazing diversity of social behaviors like cooperation, aggression, and parenting. An outstanding question in animal behavior is how this extensive diversity can arise when behaviors often rely on shared brain regions and hormones. One way to address this question is by comparing closely related populations that differ in social behavior. In this study, we discriminate between two possible ways conserved mechanisms might evolve to generate differences in social behavior: changes in the number or activity of specific types of brain cells (neurons). To do this, we measured the number and activity of two types of neurons known to promote care behavior in many animals (galanin and oxytocin) in two closely related populations of threespine stickleback fish (Gasterosteus aculeatus) that do and do not provide parental care. We found that the two populations did not differ in the number of these neurons but did differ in the activity of these neurons. The activity of galanin and oxytocin neurons changed over time in the caring stickleback as they transitioned from nest building to mating to caring for offspring. The activity of these neurons did not change in the non-caring population, suggesting that dynamic activation may be necessary for care behavior. Overall, our experiments suggest that changes in the timing of activity of specific neurons in the brain may have driven the evolution of care and its loss in stickleback.
