Future directions in urban endocrinology – The effects of endocrine plasticity on urban tolerance

The integration of behavioural, environmental, and evolutionary endocrinology with urban ecology has happened somewhat organically, with researchers of diverse perspectives and interests contributing their discoveries to form a rich and expanding literature. Two decades have passed since the publication of the first studies to investigate endocrine traits in an urban context (Bonier et al., 2007a; Partecke et al., 2006; Schoech and Bowman, 2003; Schoech et al., 2004), which seems like an opportune time to assess progress in the field and consider strong routes forward. Endocrine research could play an important role in urban ecology and evolution, particularly in our search for an understanding of the mechanistic basis of the variation we see in the abilities of individuals, populations, and species to cope with urban challenges (hereafter described as their urban tolerance).

Urban tolerance characterizes the ability of an organism to survive and reproduce in cities (Callaghan et al., 2021a; Fanelli et al., 2022). An individual or species with high urban tolerance can maintain similar, or even higher, fitness in urban compared to natural habitats, whereas an individual with low tolerance has reduced fitness in cities. Most animals seem to have relatively low urban tolerance – that is, they suffer fitness costs when confronted with urban challenges, or they avoid urban habitat altogether (Chamberlain et al., 2009; McKinney, 2006). As such, expanding cities present a serious threat to biodiversity across the globe (McKinney, 2006; Seto et al., 2012). Yet, some species appear to tolerate urban challenges, and a few even thrive in cities (Fanelli et al., 2022; Zuñiga-Palacios et al., 2021).

We don't fully understand why species, populations, or individuals vary in their urban tolerance, but several ecological, behavioural, life history, and physiological traits, including endocrine traits, could influence success in cities (Bonier et al., 2007a, 2007b; Callaghan et al., 2019; Kark et al., 2007; Martin and Bonier, 2018; Sinclair et al., 2022). Past efforts to characterize variation in urban tolerance have focused primarily on differences among species, often grouping them into different categories (e.g., urban avoiders, adapters, and exploiters; Blair 1996, 2001) based on how their abundance varies in urban areas relative to natural habitat. However, urban tolerance can vary more continuously (Callaghan et al., 2019; Fanelli et al., 2022) and might differ not only among species, but also among populations and individuals (Callaghan et al., 2023), and even within individuals across life history stages (Callaghan et al., 2021a). Recent efforts to develop more refined quantitative estimates of urban tolerance have generated advances in our ability to evaluate causes of its variation (Callaghan et al., 2019, 2021b; Fanelli et al., 2022).

Much of the urban endocrine literature to date has focused on using measures of hormones to document possible costs of city living (often estimated with measures of concentrations of glucocorticoids; e.g., Bonier et al., 2007a; Brunton et al., 2020; French et al., 2008; Shimamoto et al., 2020; Zhang et al., 2011) or plastic responses to various aspects of urban environments (e.g., differences in artificial light, noise, or food availability; Dominoni et al., 2013; Injaian et al., 2018; Schoech et al., 2004), rather than directly assessing the role of endocrine traits in determining the degree to which an individual or a species can tolerate urban challenges (but see, Sinclair et al., 2022). Instead, in seeking to understand causes of variation in urban tolerance, many past studies have focused on ecological, behavioural, and life history traits that might contribute to or constrain success in cities (e.g., Bonier et al., 2007b; Callaghan et al., 2019; Carrete and Tella, 2011; Evans et al., 2011; Kark et al., 2007; Martin and Bonier, 2018). Given that most of these traits are proximately regulated by endocrine signals, a logical next step in our field is to directly investigate the role of endocrine phenotypes in influencing urban tolerance.

Here, after a very brief overview of past urban endocrinology research, I propose an exciting route forward for the field, involving studies of the role of endocrine plasticity in determining urban tolerance. I suggest study designs to achieve this research goal, and discuss important considerations about the causes of variation in endocrine plasticity, which could inform predictions about the potential for ongoing evolution of urban tolerance in organisms confronted by an increasingly urbanized world.

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