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 degrees C) compared with thermoneutral (35 degrees C) and lower (27 degrees C) temperatures. We found significantly more heat dissipation behaviours at 43 degrees C, a temperature previously shown to reduce song production and fertility, and more heat retention behaviours at 27 degrees C. Next, we characterized transcriptomic responses 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, suggests the brain is less responsive to extreme temperatures. Nevertheless, gene network analyses revealed that expression related to dopaminergic signalling in the brain covaried with heat dissipation behaviours, providing a mechanism by which temporary thermal challenges may alter motivational circuits for song production. In both brain and testis, we observed correlations between thermally sensitive gene networks and individual differences in thermoregulatory behaviour. Although we cannot directly relate these gene regulatory changes to mating success, our results suggest that individual variation in response to thermal challenges could impact sexually selected traits in a warming world.

Automated summary

This study investigates the impact of high temperatures on sexually selected traits and the underlying gene regulatory mechanisms in zebra finches. The results show that exposure to acute heat challenges leads to heat dissipation behaviors and differential gene expression in the testis. Few genes in the brain show differential expression, suggesting it is less responsive to extreme temperatures. Gene network analyses suggest a correlation between dopaminergic signaling in the brain and heat dissipation behaviors, providing a potential mechanism for the alteration of motivational circuits for song production.