Do Seasonal Glucocorticoid Changes Depend on Reproductive Investment? A Comparative Approach in Birds

Abstract

Animals go through different life history stages such as reproduction, moult, or migration, of which some are more energy-demanding than others. Baseline concentrations of glucocorticoid hormones increase during moderate, predictable challenges and thus are expected to be higher when seasonal energy demands increase, such as during reproduction. By contrast, stress-induced glucocorticoids prioritize a survival mode that includes reproductive inhibition. Thus, many species down-regulate stress-induced glucocorticoid concentrations during the breeding season. Interspecific variation in glucocorticoid levels during reproduction has been successfully mapped onto reproductive investment, with species investing strongly in current reproduction (fast pace of life) showing higher baseline and lower stress-induced glucocorticoid concentrations than species that prioritize future reproduction over current attempts (slow pace of life). Here we test the "glucocorticoid seasonal plasticity hypothesis", in which we propose that interspecific variation in seasonal changes in glucocorticoid concentrations from the non-breeding to the breeding season will be related to the degree of reproductive investment (and thus pace of life). We extracted population means for baseline (for 54 species) and stress-induced glucocorticoids (for 32 species) for the breeding and the non-breeding seasons from the database "HormoneBase", also calculating seasonal glucocorticoid changes. We focused on birds because this group offered the largest sample size. Using phylogenetic comparative methods, we first showed that species differed consistently in both average glucocorticoid concentrations and their changes between the two seasons, while controlling for sex, latitude, and hemisphere. Second, as predicted seasonal changes in baseline glucocorticoids were explained by clutch size (our proxy for reproductive investment), with species laying larger clutches showing a greater increase during the breeding season-especially in passerine species. In contrast, changes in seasonal stress-induced levels were not explained by clutch size, but sample sizes were more limited. Our findings highlight that seasonal changes in baseline glucocorticoids are associated with a species' reproductive investment, representing an overlooked physiological trait that may underlie the pace of life.

Macroevolutionary Patterning in Glucocorticoids Suggests Different Selective Pressures Shape Baseline and Stress-Induced Levels

“…Be-cause elevated GCs can be particularly costly to reproduction, this pattern could reflect a protective role of GC evolution reducing stress-induced levels more in the sex that tends to invest more in each reproductive attempt. Most previous phylogenetically informed analyses of steroid hormones have either included males only or averaged data from both sexes, but two analyses in birds support this hypothesis (Bókony et al 2009;Casagrande et al 2018). Our finding that sex does not predict baseline GCs across tetrapods is consistent with patterns observed in mammals (Haase et al 2016) but not in birds (Casagrande et al 2018).…”

“…These patterns are broadly consistent with the findings of a previous analysis of birds actively engaged in parental care (Bókony et al 2009), which used a metric of brood value that incorporated both longevity and clutch size. A recent analysis, also in birds, which incorporated data from the breeding and nonbreeding seasons, found that clutch size positively predicted baseline but not stress-induced GC levels (Casagrande et al 2018). The presence of this pattern at larger taxonomic scales, and in a data set that includes many measures from species and sexes that do not engage in parental care, suggests that general reproductive investment may be a particularly important driver of variation in GCs across populations and species.…”

Enzymatic antioxidants but not baseline glucocorticoids mediate the reproduction–survival trade-off in a wild bird

“…R. Soc. B 285: 20182141 challenges, and therefore analysing individual changes (or reaction norms) are perhaps as important as absolute values, or even more important [23,31,[87][88][89][90][91]. The field is now ripe for the development of quantitative predictions for the links between changes in physiology and life-history decisions of individuals.…”

“…However, whether GCs play a role in mediating such trade-offs at low baseline concentrations is less clear, although their involvement has been hypothesized [22]. Baseline GCs are elevated when individuals experience increased energetic demands [11,12,17,18,[22][23][24][25], for example, in the reproductive season when parents provision their offspring [18,[26][27][28][29][30][31]. These findings prompted the hypothesis that baseline GCs may mediate trade-offs, but in an opposite way to stress-induced concentrations: baseline GCs would support investment in current reproduction at the expense of survival [22,32,33].…”

Does variation in glucocorticoid regulation predict fitness? A phylogenetic meta-analysis

“…More surprising was the finding of a consistently negative relationship between baseline GC levels and reproductive success. Although elevated baseline GCs are often seen in individuals facing stressors, baseline GCs are also frequently upregulated in advance of energetically demanding life history stages, and are believed to help organisms mobilize energy to meet these demands (Romero, Reed, & Wingfield, 2000; Bonier et al ., 2009a; Casagrande et al ., 2018; Vitousek et al ., 2019).…”