Urbanization is associated with non‐coding polymorphisms in candidate behavioural genes in the Eurasian coot

Abstract

Extensive transformation of natural land cover into urbanized areas enhances accumulation of phenotypic differences between animals from urban and nonurban populations, but there is little information on whether these changes, especially in terms of animal behaviour and circadian rhythm, have a genetic basis. The aim of this study was to investigate genetic background of behavioural differences between four pairs of urban and nonurban populations of a common waterbird, the Eurasian coot Fulica atra. For this purpose, we quantified polymorphisms in personality‐related candidate genes, previously reported to be associated with avian circadian rhythms and behavioural traits that may be crucial for urban life. We found general associations between landscape urbanization level and polymorphisms in 3′UTR region of CREB1 gene encoding transcriptional factor, which participates in development of cognitive functions and regulation of circadian rhythm. We also found significant differentiation between urban and nonurban populations in the intronic region of CKIɛ gene responsible for regulation of circadian clock. Although we lacked evidence for linkage of this intronic variation with coding polymorphisms, genetic differentiation between urban populations was significantly stronger at CKIɛ intron compared with neutral microsatellite markers, suggesting possible local adaptations of CKIɛ expression regulation to specific urban sites. Our results indicate that behavioural differentiation between urban and nonurban coot populations may be the effect of habitat‐specific selective pressure resulting in genetic adaptations to urban environment and supporting the microevolutionary scenario. These adaptations, however, prevailed in non‐coding regulatory rather than coding gene regions and showed either general or local patterns, revealing high complexity of associations between behaviour and landscape urbanization in birds.

Abstract

In the study, we identified polymorphisms in behavioural genes in four pairs of urban and nonurban populations of the Eurasian coot (a common waterbird) to test for their associations with landscape urbanization level. For the study, we have chosen 10 candidate genes previously reported to be associated with aggression, exploratory behaviour, circadian rhythm, cognition and migration in birds. We showed conspicuous associations between CREB1 3′UTR genotypes and the level of landscape urbanization and also recorded strong differentiation at CKIɛ intronic region among urban populations, either suggesting local adaptations through linkage with polymorphisms in coding regions or adaptations of gene expression regulation to particular urban sites.