Boldness behavior and stress physiology in a novel urban environment suggest rapid correlated evolutionary adaptation

Abstract

Novel or changing environments expose animals to diverse stressors that likely require coordinated hormonal and behavioral adaptations. Predicted adaptations to urban environments include attenuated physiological responses to stressors and bolder exploratory behaviors, but few studies to date have evaluated the impact of urban life on codivergence of these hormonal and behavioral traits in natural systems. Here, we demonstrate rapid adaptive shifts in both stress physiology and correlated boldness behaviors in a songbird, the dark-eyed junco, following its colonization of a novel urban environment. We compared elevation in corticosterone (CORT) in response to handling and flight initiation distances in birds from a recently established urban population in San Diego, California to birds from a nearby wildland population in the species' ancestral montane breeding range. We also measured CORT and exploratory behavior in birds raised from early life in a captive common garden study. We found persistent population differences for both reduced CORT responses and bolder exploratory behavior in birds from the colonist population, as well as significant negative covariation between maximum CORT and exploratory behavior. Although early developmental effects cannot be ruled out, these results suggest contemporary adaptive evolution of correlated hormonal and behavioral traits associated with colonization of an urban habitat.

Mechanisms Associated with an Advance in the Timing of Seasonal Reproduction in an Urban Songbird

“…We compared circulating corticosterone and gonadal GR and MR transcript abundance in sedentary urban and migrant juncos in our common garden study. Both in the field and a common garden, sedentary urban juncos, and migrant juncos that breed close-by had similar baseline levels of corticosterone during the breeding season (Atwell et al, 2012). Similar to these observations, our data collected during the period preceding the breeding season found no differences in baseline levels of corticosterone; sedentary urban and migrant juncos had similar levels of corticosterone over our 4-week captive study in early spring ( Figure 5A).…”

“…A previous study (Atwell et al, 2012) conducted during the breeding season, found higher stress-induced corticosterone in a nearby rural breeding population compared to breeders from the urban San Diego population. We did not measure stress-induced corticosterone in this study, so we cannot say whether differences in stress-induced corticosterone levels might have delayed reproductive development in migrant juncos in San Diego.…”

“…In the current study, we compared specific neuroendocrine mechanisms predicted to underlie reproductive timing differences between a recently established (∼35 years) urban population of juncos vs. heteropatric ancestral migrant juncos, under both free-living (field) and common-garden (captive) conditions. This study focused on a population of dark-eyed juncos (J. hyemalis thurberi) that became established in urban San Diego CA USA in the early 1980s, likely as a result of overwintering migratory birds remaining to breed (Rasner et al, 2004;Yeh, 2004;Atwell et al, 2012Atwell et al, , 2014. Since then, an isolated sedentary urban breeding population has persisted with limited subsequent immigration despite a sympatric distribution with migratory juncos between October and April Unitt, 2005).…”

Seasonal and urban effects on the endocrinology of a wild passerine

“…2009; Atwell et al. 2012). These responses to the urban environment are mediated by the organism's endocrine system (Bonier 2012).…”

“…2011; Atwell et al. 2012). However, changes in endocrine patterns due to urban influences in general were not consistent between species, sexes, and life‐history stages (Bonier 2012).…”