Abstract

Between-individual variation in behavior can emerge through complex interactions between state-related mechanisms, which include internal physiological constraints or feedback derived from the external environment. State-related conditions can be especially influential during early life, when parental effort and exposure to social stress may canalize consistent differences in offspring hormonal profiles and foster specific behavioral strategies. Here, we unravel how relevant state variables, including sex, somatic condition, local population density, and maternal traits, contribute to within-cohort differences in stress, sex, and thyroid hormone axes in dependent Galapagos sea lions with the primary goal of understanding downstream effects on boldness, docility, habitat use, and activity. Pups within denser natal sites had higher levels of cortisol and thyroid T4, a prohormone and proxy for metabolic reserves, likely as an adaptive physiological response after exposure to increased numbers of conspecific interactions. Furthermore, considering maternal effects, mothers in better body condition produced pups with higher testosterone yet downregulated basal cortisol and thyroid T4. This hormonal profile was correlated with increased boldness toward novel objects and attenuated stress responsiveness during capture. Intriguingly, pups with increased thyroid T3, the biologically active form, maintained faster somatic growth and were observed to have increased activity and extensively explored surrounding habitats. Collectively, these findings provide comprehensive evidence for several links to hormone-mediated behavioral strategies, highlighted by variation in socio-environmental and maternally derived input during a foundational life stage.

Highlights

  • The concept that many aspects of behavior are highly variable across individuals within most species is deeply rooted into modern ecological studies (Wolf et al 2007)

  • When the subset of individuals were recaptured as yearlings, we found that salivary CORT and TEST were positively correlated with serum measurements (LMM: mean C­ ORTsal:CORTser association— R2 = 0.44, p = 0.001; mean ­Tsal:Tser association—R2 = 0.40, P = 0.042), indicating that hormonal profiles across both sample types mostly remained stable within individuals during the first year of dependency

  • Considering covariation between endocrine axes, we found negative correlations between ­CORTser and ­TESTser (Pearson’s r = − 0.47, P = 0.014), and separately between thyroid ­TT4ser and ­TT3ser (Pearson’s r = − 0.17, P = 0.020), but no correlations between C­ ORTser or either thyroid hormone (Pearson’s r, P > 0.05)

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Summary

Introduction

The concept that many aspects of behavior are highly variable across individuals within most species is deeply rooted into modern ecological studies (Wolf et al 2007). Behavior can acutely change in response to environmental stimuli, individuals often exhibit consistent differences in average behavioral phenotypes over time or within and across contexts (deemed animal ‘personalities’) (Sih et al 2004) Traits such as boldness (i.e., risk-taking), exploration, or sociability seem functionally distinct but are often linked through correlations known as behavioral syndromes (Réale et al 2007). As GSL show island tameness and are approachable, this species has allowed for a rare glimpse into describing intraspecific variation in personality traits within this taxon (DeRango et al 2019a, b) These studies of dependent pups revealed strong between-individual consistency in boldness (mean repeatability estimate R = 0.70 ± 0.06 SE), and that boldness is linked to variability in stress coping responses (i.e. docility). We hypothesized that pup sex and body condition, socioenvironmental context (i.e. local population density), and maternal state variables (age and body condition) would directly contribute to hormonal profiles of focal pups, leading to downstream effects on behavioral patterns

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