Gene Dictates Male Mating Morphs in Ruff Sandpipers

Male ruff sandpipers engaging in the act of mating typically fall into one of three groups, with variations in how aggressive they are and how showy their plumage is, among other factors. Now, a new study reports a single gene – HSD17B2 – drives these dramatic differences among male ruff sandpiper morphs. The findings show how evolutionary changes in a single gene's structure, sequence, and regulation can drive significant diversity within a single species. The androgen testosterone plays a key role in male reproductive development. It influences a range of physical traits, such as body size and ornamentation. It also influences social behaviors, including those related to courtship. Testosterone levels vary considerably between individuals, and a portion of this variation is thought to be genetic. However, more work is needed to characterize how genetic variants are linked to testosterone concentrations and different reproductive phenotypes. Jasmine Loveland and colleagues investigated testosterone production and metabolism in the ruff (Calidris pugnax), a shorebird renowned for its striking variation in male physical traits and reproductive behaviors. Ruffs exhibit three distinct male mating morphs. "Independent" males exhibit elaborate plumage and aggressively defend display territories to attract mates. "Satellite" males are less ornate and less aggressive, displaying alongside dominant independents to opportunistically secure mates. In contrast, "Faeder" males resemble females in size and appearance, lacking the showy plumage of other morphs, which enables them to blend in, avoid male aggression, and mate covertly. Independents have high circulating testosterone levels but low levels of androstenedione, a less potent androgen. The nonaggressive satellite and faeder males show the reverse pattern. Prior studies linked these morphs to a supergene containing around 100 genes. Loveland et al. focused on HSD17B2, a gene within the supergene, and discovered that evolutionary changes in this gene lead to increased production of highly active enzymes in low-testosterone ruff morphs. These enzymes convert testosterone to androstenedione at a faster rate, lowering testosterone levels in the bloodstream. The tissue-specific activity of HSD17B2 allows these morphs to keep testosterone levels high in the testes for reproduction while limiting its effects elsewhere, supporting ruffs' unique mating behaviors and traits. "The findings of Loveland et al. point to what may be an emerging "rule of life" for hormone-mediated traits or possibly all complex traits – in evolution, each problem has many possible solutions," writes Kimberly Rosvall in a related Perspective.