Adaptive gene regulation in wild mammals exposed to high predator abundance

Psychological stress induced by exposure to predators has complex effects on the behaviour and physiology of prey species. This includes potential influences on gene expression mediated via stress-responsive physiological pathways such as the sympathetic nervous system and hypothalamus -pituitary-adrenal (HPA) axis. Laboratory studies have documented diverse transcriptional effects of predator-induced fear, but genomic responses to predator exposure in the wild remain poorly understood. Here, we used RNA-sequencing to investigate the leukocyte transcriptome response to chronic predator pressure in a well-studied population of wild yellow-bellied marmots, Marmota flaviventer. We assessed the genomic response to this stressor in three ways by (1) identifying differentially expressed individual genes across the genome, (2) assessing whether differentially expressed genes were statistically over-represented by functional categories and (3) testing for transcription factor activity that may mediate observed gene expression differences. We found 349 individual genes regulated in association with chronic predator presence, including transcripts known to regulate heat shock proteins, metabolism and DNA damage repair. Gene ontology analysis revealed that the majority of these differentially expressed genes were involved with the cellular response to stress, cellular metabolism and protein transport. Transcription factor analysis implicated glucocorticoid signalling in mediating these effects. Our work confirms that the physiological response to predator-induced stress is complex, initiating transcriptional activity in multiple processes and pathways. In addition to the canonical expectations that individuals exposed to predators mobilize HPA signalling and homeostasis pathways, we also detected activity in genes typically associated with human anxiety and cerebral function. This is the first study to demonstrate that leukocyte transcriptomes taken from animals living in a natural environment can reflect the complex ecology of fear. (C) 2019 Published by Elsevier Ltd on behalf of The Association for the Study of Animal Behaviour.