Heat alters diverse thermal tolerance mechanisms: an organismal framework for studying climate change effects in a wild bird

The ability to cope with heat is likely to influence species success
amidst climate change. However, heat coping mechanisms are poorly
understood in wild endotherms, which are increasingly pushed to their
thermoregulatory limits. We take an organismal approach to this problem,
unveiling how behavioral and physiological responses may allow success in
the face of sublethal heat. We experimentally elevated nest temperatures
for four hours to mimic a future climate scenario (+4.5°C) during a
critical period of post-natal development in tree swallows (Tachycineta
bicolor). Heat-exposed nestlings exhibited marked changes in behavior,
including movement to cooler microclimates in the nest. They panted more
and weighed less than controls at the end of the four-hour heat challenge,
suggesting panting-induced water loss. Physiologically, heat induced high
levels of heat shock protein (HSP) gene expression in the blood, alongside
widespread transcriptional differences related to antioxidant defenses,
inflammation, and apoptosis.  Critically, all nestlings survived
the heat challenge, and those exposed to milder heat were more likely to
recruit into the breeding population. Early-life but sub-lethal heat may
therefore act as a selective event, with the potential to shape population
trajectories. Within the population, individuals varied in their
physiological response to heat, namely in HSP gene expression, which
exhibited higher mean and higher variance in heat-exposed nestlings than
in controls. Heat-induced HSP levels were unrelated to individual body
mass, or among-nest differences in brood size, temperature, and behavioral
thermoregulation. Nest identity explained a significant amount of HSP
variation, yet siblings in the same nest differed by an average of
~4-fold, and individuals in the population differed by as much as
~100-fold in their HSP response. This massive variation extends previous
laboratory work in model organisms showing that heat shock proteins may
harbor cryptic phenotypic variation. These results shed light on
oft-ignored elements of thermotolerance in wild birds at a critical stage
of post-natal development. By highlighting the scope of heat-induced HSP
gene expression and coupling it with a suite of organismal traits, we
provide a framework for future testing of the mechanisms that shape
species success in the face of change.