How can we estimate natural selection on endocrine traits? Lessons from evolutionary biology

Abstract

An evolutionary perspective can enrich almost any endeavour in biology, providing a deeper understanding of the variation we see in nature. To this end, evolutionary endocrinologists seek to describe the fitness consequences of variation in endocrine traits. Much of the recent work in our field, however, follows a flawed approach to the study of how selection shapes endocrine traits. Briefly, this approach relies on among-individual correlations between endocrine phenotypes (often circulating hormone levels) and fitness metrics to estimate selection on those endocrine traits. Adaptive plasticity in both endocrine and fitness-related traits can drive these correlations, generating patterns that do not accurately reflect natural selection. We illustrate why this approach to studying selection on endocrine traits is problematic, referring to work from evolutionary biologists who, decades ago, described this problem as it relates to a variety of other plastic traits. We extend these arguments to evolutionary endocrinology, where the likelihood that this flaw generates bias in estimates of selection is unusually high due to the exceptional responsiveness of hormones to environmental conditions, and their function to induce adaptive life-history responses to environmental variation. We end with a review of productive approaches for investigating the fitness consequences of variation in endocrine traits that we expect will generate exciting advances in our understanding of endocrine system evolution.

Heritable variation in circulating glucocorticoids and endocrine flexibility in a free‐living songbird

“…Hallinger, C. Zimmer & D.W. Winkler, in review), but these relationships are by no means ubiquitous (Breuner et al ., ). In contrast, little is known about how selective pressures shape the scope of glucocorticoid flexibility, or the speed of glucocorticoid reaction norms (Bonier & Martin, ; Taff & Vitousek, ).…”

“…Winkler, in review), but these relationships are by no means ubiquitous (Breuner et al, 2008). In contrast, little is known about how selective pressures shape the scope of glucocorticoid flexibility, or the speed of glucocorticoid reaction norms (Bonier & Martin, 2016;Taff & Vitousek, 2016). This study examined variation in glucocorticoids during the late nestling period, shortly prior to fledging.…”

“…Selection on endocrine expression could therefore influence the ability of organisms to cope with environmental variation and to persist in changing environments (Angelier & Wingfield, 2013;Cockrem, 2013a). Yet while selection requires heritable variation on which to act, relatively little is known about whether the often remarkable interindividual variation in hormone levels, or their context-dependent flexibility, are heritable traits (Bonier & Martin, 2016).…”

Rapid effects of elevated stress hormones on male courtship signals suggest a major role for the acute stress response in intra‐ and intersexual selection

“…In this regard, considerable effort has been directed at understanding the fitness consequences associated with variation in neuroendocrine regulation of stress hormones (i.e. glucocorticoids; Bonier & Martin, ; Bonier, Martin, Moore, & Wingfield, ; Breuner, Patterson, & Hahn, ; Crespi, Williams, Jessop, & Delehanty, ; Dantzer, Westrick, & van Kestern, ; Hau, Ricklefs, Wikelski, Lee, & Brawn, ; Ricklefs & Wilkelski, ). Such research has been pivotal in revealing how baseline and/or acute elevations in circulating glucocorticoids affect whole‐animal performance, life‐history traits and behaviours that serve as indirect or direct estimates of fitness.…”

“…In this regard, considerable effort has been directed at understanding the fitness consequences associated with variation in neuroendocrine regulation of stress hormones (i.e. glucocorticoids; Bonier & Martin, 2016;Bonier, Martin, Moore, & Wingfield, 2009;Breuner, Patterson, & Hahn, 2008;Crespi, Williams, Jessop, & Delehanty, 2013;Dantzer, Westrick, & van Kestern, 2016;Hau, Ricklefs, Wikelski, Lee, & Brawn, 2010;Ricklefs & Wilkelski, 2002).…”