Acute and chronic extreme weather events influence hypothalamic and testicular gene expression in a free-living Arctic breeding songbird, the Lapland longspur

Climate change is creating new global weather patterns which frequently exceed historical records. In 2013, avian migrations were delayed and birds breeding near Toolik Lake, Alaska, endured unseasonably late snowstorms that resulted in high reproductive failure rates. To understand how animals cope with extreme weather events on a mechanistic level we collected tissue and blood samples from male Arctic breeding Lapland longspurs (Calcarius lapponicus) during the extreme spring of 2013 on arrival on their breeding grounds, under benign conditions at arrival in 2016 and during incubation and during a snowstorm that resulted in 90% reproductive failure. Here we investigated gene expression changes across the hypothalamic pituitary gonad (HPG) axis as well as the effects on circulating steroids and the reproductive system. Circulating testosterone and testes mass were highest during arrival, but were suppressed by the extreme spring of 2013. Chronic extreme spring conditions resulted in increased expression of type two deiodinase and 5 alpha-reductase and suppression of gonadotropin inhibitory hormone mRNA in the hypothalamus. The snowstorm resulted in a rapid increase in hypothalamic aromatase and thyroid stimulating hormone beta mRNA in the pituitary gland, whilst in the testes, we observed predictable declines in genes associated with steroidogenesis from arrival to incubation stage. We discovered that the gonadal endocrine phenotype is distinct at each of the measured sub-stages of nesting and provide, for the first time, evidence for mechanistic regulation of the HPG axis at the level of the gene in a free-living songbird following extreme weather events.