Variation in DRD4 gene methylation in wild great tits is associated with behavioural tolerance for human disturbance but not with habitat urbanization

The increasing presence and activities of people in both urban
environments and non-urban areas result in the exposure of many wild
animal populations to persistent human disturbance. As a response,
individuals in disturbed populations often become tolerant towards humans
that can have significant ecological and societal consequences, for
example by affecting ecosystem services and human-wildlife conflicts.
Although several mechanisms have been proposed to explain the emergence
and spread of disturbance tolerance, their biological bases are rarely
investigated in natural populations. In this study, we investigated
behavioural tolerance in great tits (Parus major) along urbanization
gradients of two cities representing different levels of human
disturbances. Specifically, we studied whether variation in disturbance
tolerance is related to epigenetic variation in the DRD4 gene that are
often linked to behavioural plasticity. We did not detect differences in
DNA methylation at 23 CpG sites between wild great tit populations
breeding in differently urbanized areas. However, variation in methylation
at some CpG sites was associated with two proxies of tolerance, the return
latency and the vigilance behaviour of parent birds measured after
standardized disturbance. These findings suggest that epigenetic variation
may be involved in the processes generating behavioural tolerance for
human disturbance. These results have implications for the understanding
of the mechanisms by which animal populations can respond to disturbances
in human-dominated environments.