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.

Figure 1

FID (means ± standard error of the mean) were shorter in field studies of both foraging birds (GLM, P < 0.001) and incubating females (GLM, P = 0.003) in colonist (San Diego) versus ancestral range (Mt Laguna) populations.

Figure 2

Initial (baseline) and stress-induced plasma corticosterone (CORT; means 6 standard error of the mean) in colonist (San Diego) and ancestral range populations are shown from (a) field study of freeliving nesting females and (b) a captive common garden study of birds raised from early life under identical aviary conditions. We found significant population differences in both maximum CORT and CORT responsiveness (area) in both field and common garden studies, and there were also sex differences in the common garden (see RESULTS).

Figure 3

Exploratory behavior (PC1, means 6 standard error of the mean) scores from a common garden study are shown by population of origin and sex. The effects of both population (GLM, P = 0.001) and sex (GLM, P = 0.009) were significant.

Figure 4

Individual variation for maximum CORT and exploratory behavior from the common garden study. Max CORT predicted individual exploratory behavior scores (P = 0.021) in a GLM model the also included significant effects of population (P = 0.015) and sex (P = 0.049).