How thermal challenges change gene regulation in the songbird brain and gonad: implications for sexual selection in our changing world

In a rapidly warming world, exposure to high temperatures may impact fitness, but the gene regulatory mechanisms that link sublethal heat to sexually selected traits are not well understood, particularly in endothermic animals. Our experiment used zebra finches (Taeniopygia guttata), songbirds that experience extreme temperature fluctuations in their native Australia. We exposed captive males to an acute thermal challenge (43°C) compared with thermoneutral (35°C) and lower (27°C) temperatures. We found significantly more heat dissipation behaviors at 43°C and heat retention behaviors at 27°C, temperatures previously shown to reduce song production and fertility. Next, we characterized gene expression in tissues important for mating effort – the posterior telencephalon, for its role in song production, and the testis, for its role in fertility and hormone production. Differential expression of hundreds of genes in the testes, but few in the brain, suggest the brain is more buffered from extreme temperatures. Nevertheless, dopaminergic signaling in the brain co-varied with heat dissipation behaviors, providing a mechanism by which temporary thermal challenges may alter motivational circuits for song production. In both brain and testis, we also observed quantitative continuous variation between thermally sensitive gene networks and individual differences in thermoregulatory behavior, indicating that mechanisms of thermal-behavioral tolerance have microevolutionary potential. Taken together, these results suggest that selection for thermal tolerance could impact performance of sexually selected traits, and in turn, sexual selection in a warming world could influence how thermal tolerance evolves. 2 tissues (posterior telencephalon and testis) were collected from 24 male zebra finches exposed to temperatures above (Ta = 43°C), within (Ta = 35°C), or below their thermoneutral zone (Ta = 27°C); total RNA was extracted and run on a Nextseq platform.