Hormonal, Behavioral, and Life-History Traits Exhibit Correlated Shifts in Relation to Population Establishment in a Novel Environment

Abstract

Climate change, habitat alteration, range expansions, and biological invasions are all predicted to require rapid shifts in multiple traits including behavior and life history, both for initial population establishment and subsequent adaptation. Hormonal mechanisms likely play a key role in facilitating or constraining plastic and genetic responses for suites of traits, but few studies have evaluated their role in shaping contemporary adaptation or diversification. We examined multiple phenotypic adjustments and associated hormonal changes following a recent (early 1980s) colonization event, in which a temperate-breeding songbird, the dark-eyed junco (Junco hyemalis), became established in the Mediterranean climate of San Diego, California. The milder climate has led to an extended breeding season and year-round residency, and we document shifts in multiple sexually selected behaviors and plumage traits. Testosterone titers in San Diego were elevated for longer but with a lower peak value compared to a nearby native-range population, and correlations between testosterone and related traits were similar within and among populations. A common garden study indicated that changes in testosterone likely represent plastic responses to the less seasonal environment of the city, providing the context against which subsequent genetic changes in morphology likely occurred. We argue that correlated shifts in multiple traits, organized by underlying physiology, may be a generally important element of many successful adjustments to changing environments.

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

“…Seasonal fluctuations in climate and resource availability are often reduced in urban environments, which can lead to longer breeding seasons and year-round occupancy by formerly migratory lineages (Adriaensen and Dhondt, 1990;Partecke and Gwinner, 2007;Chamberlain et al, 2009;Atwell et al, 2014). If the physiological processes that lead to differences between urban and rural populations in reproductive timing and other seasonal traits become fixed over time, then gene flow and interbreeding could be limited (Evans et al, 2010;Fudickar et al, 2016a).…”

“…To date, there is limited evidence from studies that have compared the endocrine axes of urban vs. nearby rural populations in both field and common garden settings to support the importance of both plasticity and genetics in modulating earlier reproduction and HPG activation in urban habitats (Partecke et al, 2004(Partecke et al, , 2006Schoech, 2009;Atwell et al, 2014;Davies et al, 2015). While these studies highlight the importance of differential HPG activity in facilitating earlier and extended breeding in urban habitats, much remains to be learned about the generality of those results, as well as the specific mechanistic sources of variation across the many "levels" of the HPG axis.…”

“…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).…”

“…The colonization event and current heteropatric distribution thus provides a unique opportunity to examine mechanisms associated with contemporary adaptation to an urban environment. Although the precise breeding location of the migrants is not known, previous studies have shown that first egg laying dates in the San Diego population are ∼2.5 months earlier than the closest non-urban populations Atwell et al, 2014). A recent study, in which juncos from San Diego and the closest non-urban breeding population (∼50 km) were captured on their respective breeding grounds as juveniles and observed in a commongarden experiment, found that population differences in the seasonal timing of mean peak HPG activity (plasma testosterone and post Gonadotropin-Releasing Hormone (GnRH) challenge testosterone) observed in the wild did not persist in the common garden (Atwell et al, 2014), which suggests a degree of flexibility in reproductive timing in both populations.…”

“…While Atwell et al (2014) compared the duration and peak timing of HPG activity of sedentary urban juncos from San Diego with that of the closest non-urban population, in the current study we focused on a comparison of sedentary urban breeders with migrants that are sympatric during winter and early spring. Based on previous reports indicating that winter flocks of juncos consist of migrants from a range of breeding populations (Fudickar et al, 2016a; J. Atwell personal observations), we expected that migrant juncos in San Diego would originate from multiple breeding populations.…”