Opposing behavioral roles for a single gene in a species with a supergene polymorphism

Behavioral trade-offs, such as between territorial aggression and parental care, require coordination among neural and genetic mechanisms that influence opposing phenotypes. In some systems, including the white-throated sparrow, this coordination has been proposed to be mediated in part by chromosomal inversions that bind together multiple genes associated with alternative strategies. Here, we demonstrate that opposing components of a life-history trade-off can be linked, via alternative alleles inside a chromosomal rearrangement, to a single pleiotropic gene. In white-throated sparrows, a species with polymorphic aggressive and parental behavior, the gene encoding the neuromodulator vasoactive intestinal peptide (VIP) lies within an inversion-based supergene. Working with a free-living population, we found that VIP expression in a pro-aggression cell population in the anterior hypothalamus positively predicted territorial singing, whereas expression in a pro-parental cell population in the infundibular nucleus positively predicted parental provisioning. Expression in these two regions was negatively correlated, consistent with opposing behavioral roles. Allele-specific analyses revealed stronger expression bias toward the supergene-associated allele in the anterior hypothalamus than in the infundibular nucleus. These findings suggest that chromosomal inversions can support opposing behavioral phenotypes not only by linking multiple genes, but also by driving regulatory divergence of individual genes that organize behavioral trade-offs.