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

Here we explore the regulatory mechanisms underlying breeding stage specific endocrine phenotypes and their response to both acute and chronic extreme weather in male Lapland longspurs (Calcarius lapponicus). In the chronically extreme cold spring of 2013, birds were collected following a delayed arrival on their Alaskan breeding grounds. Whereas in 2016 during typical weather conditions, birds were collected at their arrival on their breeding grounds and during incubation - either in the presence or absence of a snowstorm. We quantified hypothalamic and gonadal gene expression, steroid hormones, and testicular volume to characterize both activatory and inhibitory signaling pathways across breeding stages. Network co-expression was strongly structured during arrival, with pronounced functional segregation of hypothalamic, testes inhibition and testes activation signaling modules. Functional segregation weakened during incubation and was absent during the extreme cold arrival, reflecting increased cross-module integration. Transitions across stages, particularly from arrival to incubation, were characterized by substantial edge level co-expression reorganization, suggesting restructuring of hormone and gene connectivity. Under typical conditions the transition from arrival to incubation was associated with declines in hypothalamic gonadotropin-inhibitory hormone (GnIH) and aromatase, gonadal lutropin receptor, steroidogenic enzymes, and circulating testosterone, while testicular corticosteroid signaling genes remained stable. Chronic cold during arrival elevated hypothalamic type 2 deiodinase and estrogen receptor, and gonadal mineralocorticoid receptor, and reduced hypothalamic GnIH, testicular volume, and plasma testosterone. Snowstorms during incubation caused elevations in hypothalamic TSHβ and aromatase without detectable testicular changes. Our study provides insight into how weather extremes shape endocrine phenotypes of wild organisms.