Quantifying Glucocorticoid Plasticity Using Reaction Norm Approaches: There Still is So Much to Discover!

Abstract

Synopsis Hormones are highly responsive internal signals that help organisms adjust their phenotype to fluctuations in environmental and internal conditions. Our knowledge of the causes and consequences of variation in circulating hormone concentrations has improved greatly in the past. However, this knowledge often comes from population-level studies, which generally tend to make the flawed assumption that all individuals respond in the same way to environmental changes. Here, we advocate that we can vastly expand our understanding of the ecology and evolution of hormonal traits once we acknowledge the existence of individual differences by quantifying hormonal plasticity at the individual level, where selection acts. In this review, we use glucocorticoid (GC) hormones as examples of highly plastic endocrine traits that interact intimately with energy metabolism but also with other organismal traits like behavior and physiology. First, we highlight the insights gained by repeatedly assessing an individual's GC concentrations along a gradient of environmental or internal conditions using a “reaction norm approach.” This study design should be followed by a hierarchical statistical partitioning of the total endocrine variance into the among-individual component (individual differences in average hormone concentrations, i.e., in the intercept of the reaction norm) and the residual (within-individual) component. The latter is ideally further partitioned by estimating more precisely hormonal plasticity (i.e., the slope of the reaction norm), which allows to test whether individuals differ in the degree of hormonal change along the gradient. Second, we critically review the published evidence for GC variation, focusing mostly on among- and within-individual levels, finding only a good handful of studies that used repeated-measures designs and random regression statistics to investigate GC plasticity. These studies indicate that individuals can differ in both the intercept and the slope of their GC reaction norm to a known gradient. Third, we suggest rewarding avenues for future work on hormonal reaction norms, for example to uncover potential costs and trade-offs associated with GC plasticity, to test whether GC plasticity varies when an individual's reaction norm is repeatedly assessed along the same gradient, whether reaction norms in GCs covary with those in other traits like behavior and fitness (generating multivariate plasticity), or to quantify GC reaction norms along multiple external and internal gradients that act simultaneously (leading to multidimensional plasticity). Throughout this review, we emphasize the power that reaction norm approaches offer for resolving unanswered questions in ecological and evolutionary endocrinology.

Genetic integration of behavioural and endocrine components of the stress response

“…In addition, by adopting a reaction norm approach to modelling stress physiology, as recently advocated by ourselves ( Houslay et al, 2019 ) and others (e.g. Fürtbauer et al, 2015 ; Hau and Goymann, 2015 ; Taff and Vitousek, 2016 ; Guindre-Parker, 2020 ; Malkoc et al, 2021 ), we detect GxE reflecting genetic differences in the extent of habituation to the stressor over repeated exposures. This result is potentially important because poor habituation of the hypothalamic-pituitary-adrenal/interrenal (HPA/I) response to repeated or ongoing stressors can lead to well documented health problems in human and animal populations ( Segerstrom and Miller, 2004 ; Koolhaas, 2008 ; Romero et al, 2009 ; Mason, 2010 ).…”

Integrating theoretical and empirical approaches for a robust understanding of endocrine flexibility

“…Thus, it is likely that both mechanistic and evolutionary forces play a role in the causes of variation in endocrine flexibility. Recent reviews have addressed the environmental conditions that might favor endocrine flexibility and some mechanisms that could contribute to variation in endocrine flexibility (Guindre-Parker, 2020; Hau et al, 2016;Malkoc et al, 2021;Taff and Vitousek, 2016;Wada and Sewall, 2014).…”

“…Individuals may also exhibit endocrine flexibility in either their baseline or induced hormone levels across environmental contexts (Guindre-Parker, 2020). Endocrine flexibility might be quantified by calculating endocrine scope and speed or by using reaction norms (see Glossary; Guindre-Parker, 2020; Malkoc et al, 2021). Using the reaction norm approach, endocrine flexibility is derived from the intercept and slope of hormone concentrations measured across contexts.…”

Great tits differ in glucocorticoid plasticity in response to spring temperature

“…Individuals can differ in how strongly they respond to variation in ambient temperature, for instance in metabolic rate (Briga & Verhulst, 2017;Careau et al, 2014;Kar et al, 2021), foraging activity (Hall & Chalfoun, 2019), or incubation behavior (Cones et al, 2021). Since glucocorticoids support the regulation of such traits (Romero & Wingfield, 2016), quantifying the extent of glucocorticoid plasticity within and among individuals of wild vertebrate populations is crucial for evaluating the potential of these mechanisms to evolve (e.g., Angelier & Wingfield, 2013;Guindre-Parker, 2020;Hau et al, 2016;Malkoc, Mentesana, et al, 2021;Taff & Vitousek, 2016;Wada & Sewall, 2014). Individual differences are the raw material of selection, and for evolution to occur these individual differences have to harbor a heritable component.…”

“…Recent reports suggested that individual differences in glucocorticoid reaction norm elevations and slopes exist in wild vertebrate populations (summaries: Guindre-Parker, 2020; Malkoc, Mentesana, et al, 2021;Taff & Vitousek, 2016). However, some of these studies determined glucocorticoid metabolites from excrements (feces: Guindre-Parker et al, 2019;urine: Sonnweber et al, 2018), which can be additionally influenced by individual differences in dietary, metabolic, digestive and other processes (reviews in: Dantzer et al, 2014;Gormally & Romero, 2020;Goymann, 2012).…”