Dads matter, too: The behavioural and neurogenomic effects of receiving paternal care

Offspring are often influenced by the care they receive from their parents. However, we know little about the underlying neurogenomic mechanisms. Using a half-sib design, threespine stickleback fish were either raised by their fathers or hand-reared (“orphaned”). As offspring developed, they were tested in one of three behavioural assays: an open field assay with a simulated predator attack, a social behaviour assay with a simulated predator attack, and a scototaxis assay. Offspring that received parental care were bolder, more social, and less anxious. Fish in the open field assay had their brains sampled one hour following the simulated attack; brains were sampled at the same time from full-sib controls. These brains were processed for gene expression (via Tag-seq) and chromatin accessibility (via ATAC-seq). Experiencing paternal care affected brain gene expression, but sex was also a major factor, despite the fish being reproductively immature. The predator attack in the open field assay affected expression of fewer genes. Sex, and to lesser extent, paternal care, also influenced chromatin accessibility at a whole genome scale. Our findings further our understanding of the mechanistic basis for offspring response to variation in the care they receive from their parents. Using a half-sib design, threespine stickleback fish were either raised by their wild-caught fathers (from Putah Creek, CA = Day 10) or hand-reared (“orphaned” = Day 0). Prior to sexual maturity, when these offspring were 6-8 months old, a subset were individually introduced to an open field assay (= open-field) and allowed to explore for 10 minutes. At 10 minutes, a model sculpin was moved through the pool in one complete circuit simulating a predatory attack. The subsequent behaviour of the juvenile fish was observed for an additional 10 minutes. Following this observation, the fish was left in the open field assay without any more disturbance. Sixty minutes after the attack, the juvenile fish was gently captured, euthanized via decapitation and its brain quickly dissected. Half of the brain was placed in RNAlater for subsequent RNA extraction for 3'TagSeq and the other half was placed in cold PBS and Roche cOmplete Mini Protease Inhibitor Cocktail (PIC) for processing for ATAC-seq. Each fish that went through the open field assay was paired with a full-sibling who was gently removed from its home tank and acted as a ‘baseline control’ (= baseline). This fish did not go into the pool, but had its brain dissected within 30 minutes of the fish with which it was paired. Fish were sexed with a DNA marker.