Abstract
Early-life experiences can predict the environments experienced later in life, giving individuals an opportunity to develop adaptive behaviour appropriate to a likely future environment. Epigenetic mechanisms such as DNA methylation (DNAm) have been implicated in developmental behavioural plasticity; however, studies investigating this possibility are limited in taxonomic breadth and ecological relevance. We investigated the impact of early-life exposure to predation stress on behaviour and DNAm in the brains of Trinidadian guppies (Poecilia reticulata). We exposed guppies throughout development to either an alarm cue (conspecific skin extract), inducing predation stress, or a control cue (water) for 8 weeks and then raised them to adulthood under identical conditions. Then, we conducted two behavioural assays, an open-field and a grouping test, before performing whole-genome bisulfite sequencing on whole brains. Guppies exposed to the alarm cue during development exhibited increased grouping (shoaling) in adulthood compared to those exposed to the control treatment, but there were no detectable impacts on activity, boldness, or exploratory behaviour. We also identified stable shifts in brain DNAm in response to developmental alarm cue exposure in genes involved in behavioural regulation. Some differentially methylated sites were significantly associated with shoaling propensity in both males and females. Additionally, males and females differed in the magnitude of DNAm responses and the genes impacted, suggesting distinct roles for DNAm between the sexes. This study shows how early-life predation stress can induce behavioural changes in adulthood and that shifts in neural DNAm could be an underlying mechanism responsible for these changes.