Abstract

Climate change is pushing organisms closer to their physiological limits. Animals can reduce heat exposure – and the associated risks of lethal hyperthermia and dehydration – by retreating into thermal refuges. Refuge use nonetheless reduces foraging and reproductive activities, and thereby potentially fitness. Behavioural responses to heat thus define the selection pressures to which individuals are exposed. However, whether and why such behavioural responses vary between individuals remains largely unknown. Here, we tested whether early-life experience generates inter-individual differences in behavioural responses to heat at adulthood. In the arid-adapted zebra finch, parents incubating at high temperatures emit “heat-calls,” which adaptively alter offspring growth. We experimentally manipulated individual early life acoustic and thermal experience. At adulthood, across two summers, we then repeatedly recorded individual panting behaviour, microsite use, activity (N = 2,402 observations for 184 birds), and (for a small subset, N = 23 birds) body temperature, over a gradient of air temperatures (26–38°C), in outdoor aviaries. We found consistent inter-individual variation in behavioural thermoregulation, and show for the first time in endotherms that early-life experience contributes to such variation. Birds exposed prenatally to heat-calls started panting at lower temperatures than controls but panted less at high temperatures. It is possible that this corresponds to a heat-regulation strategy to improve water saving at high temperature extremes, and/or, allow maintaining high activity levels, since heat-call birds were also more active across the temperature gradient. In addition, microsite use varied with the interaction between early acoustic and thermal experiences, control-call birds from cooler nests using the cooler microsite more than their hot-nest counterparts, whereas the opposite pattern was observed in heat-call birds. Overall, our study demonstrates that a prenatal acoustic signal of heat alters how individuals adjust behaviourally to thermal challenges at adulthood. This suggests that there is scope for selection pressures to act differently across individuals, and potentially strengthen the long-term fitness impact of early-life effects.

Highlights

  • Global temperatures are increasing at an unprecedented rate, and heatwaves are becoming more frequent and longer (IPCC, 2014)

  • Individuals differed significantly in the intercept of their panting response but not in the reaction norm slope (Figure 2). This indicates that individuals varied in the temperature threshold at which they started panting, but generally not in how panting increased with temperature past that threshold. This was true in both Ccont (Figure 2A; likelihood ratio tests (LRTs): elevation, χ2 = 7.63, p = 0.006; slope: χ2 = 4.72, p = 0.094) and Cexp (LRTs: elevation, χ2 = 80.50, p < 0.001; slope: χ2 = 1.07, p = 0.586), including when control- and heat-call birds were considered separately: intercepts varied in both playback groups (LRTs: χ2 = 35.51, p < 0.001 and χ2 = 42.69, p < 0.001 respectively) but control-call birds were remarkably consistent in slope (Figure 2B, χ2 = 0.06, p = 0.968) while heat-call birds showed slightly more variation, even though non-significant (Figure 2B; χ2 = 2.57, p = 0.277)

  • We showed for the first time in endotherms that inter-individual variation in behavioural thermoregulation at adulthood can originate from early-life experience

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Summary

Introduction

Global temperatures are increasing at an unprecedented rate, and heatwaves are becoming more frequent and longer (IPCC, 2014). In the short-term, extreme heat exposes organisms to an immediate risk of lethal dehydration and hyperthermia (McKechnie and Wolf, 2010; Albright et al, 2017), which has caused mass-mortality events, including in birds and bats (Welbergen et al, 2008; McKechnie et al, 2012, 2021). In the longer-term, high temperatures can impose important fitness costs through effects on reproduction and body condition (Cunningham et al, 2021; Oswald et al, 2021). Such selection pressures from high temperatures are exacerbated under climate change

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