An evolutionary shift to prioritizing mating over care is associated with consistently high androgen levels in male threespine stickleback

Abstract

Steroid hormones play a role in regulating social behaviors in vertebrates, but how they mediate the evolution of these traits remains an open question. Here, we use liquid chromatography-mass spectrometry (LC-MS/MS) to quantify a panel of steroids in breeding males of two recently diverged populations of threespine stickleback. The common ecotype provides paternal care, while the white ecotype has evolutionarily lost paternal care. Hormone levels were quantified in both ecotypes at three reproductive stages: (1) after completing a nest, (2) soon after mating, when commons start to provide care and whites disperse the embryos, and (3) four days after mating, when commons are performing parental care and no longer courting females while whites are not providing care and are courting females. Androgens declined in the common ecotype as they began providing care but remained elevated in the white ecotype across stages, possibly to maintain the production of "spiggin," the androgen-dependent glue males use to construct nests. Progestogen levels were low in whites and were lowest in commons after mating, suggesting an antagonistic relationship between progestogens and sexual behavior. Both ecotypes showed elevated glucocorticoids after mating, suggesting the stress axis may not have diverged between ecotypes. Altogether, these results provide evidence that the ecotypes regulate steroid levels differently to support the ways they balance mating and parental effort. Our data suggest a variety of mechanisms by which steroid signaling and regulation can change during the early stages of divergence between behaviorally distinct populations.