Skeletal morphology of bird wings is determined by thermoregulatory demand for heat dissipation in warmer climates

Abstract

AbstractThe tendency for animals in warmer climates to be longer-limbed (Allen’s Rule) is widely attributed to the demands of thermoregulation. However, the underlying mechanism remains unclear, because variation in limb-length can typically be driven by selection for both efficient heat retention and increased heat dissipation capacity. Using comparative phylogenetic models, we find that occurrence in warmer climates is associated with longer wing bones for 1,520 species of passerine birds. The highly vascularized musculature along these bones is only uncovered during flight, when the wings function as the primary site of heat exchange, cooling the organism by dissipating excess heat generated by muscular activity. Conversely, the musculature along the wing bones is insulated by feathering when at rest, playing a negligible role in heat retention, even in colder climates. Given this asymmetry in thermoregulatory roles, we can identify the positive relationship between temperature and wing bone length as a phenotypic gradient shaped by increased demand for heat dissipation in warmer climates. Our findings provide a clear illustration of the mechanism by which global warming can drive spatial and temporal trends in appendage length, and also highlight the role of heat dissipation in reshaping even the most critical features of vertebrate anatomy.Significance StatementAnimals tend to be longer-limbed in warmer climates, but it remains unclear whether this pattern is driven by selection for cold tolerance at low temperatures or efficient heat dissipation at high temperatures. We show that for 1,520 species of passerines, bird wing bones are relatively longer in warmer climates. The vascularized musculature along these bones primarily functions in heat exchange during flight, when the overwhelming thermoregulatory challenge is dissipating heat, suggesting longer wing-bone length is driven by heat dissipation demands. Our findings reveal the pervasive impacts of thermoregulatory demands on even the most important functional traits.