Ruff is a palearctic wader bird with one of the most remarkable mating system in the animal kingdom. Three different males morphs (Independents, Satellites and Faeders) are adapted to unique set of behavior to compete for females. Independents are the majority (80-95%), develop ornamental feathers of diverse color around head and neck and vigorously defend their territory at leks. Satellites constitute 5-20% of males, only develop white colored ornamental feathers and display submissive behavior. Faeder is a rare third morph (< 1%) that mimics females by its female like plumage. Independents attract females by their elaborate performance display, high degree of aggression and strong colored plumage. Satellites allow Independents to dominate them, in exchange for getting closer to females visiting the territories occupied by Independents. Faeders being a female-mimic, get uninterrupted access to mating territories due to this disguise and attempt to mate with females accordingly. Adaptations in each of theses males allow them to take advantage of their unique courtship behavior to reproduce and survive.
We sequenced genomes of 15 Independents, nine Satellites and one Faeder male to explore the genetic basis of such complex phenotypic differences. We identified a large 4.5 MB inversion in Satellites and Faeder that occurred 3.8 million years ago. Further examination of this locus revealed it being recessively lethal as it disrupted CENPN, a critical gene responsible for cell division. There were additional deletions within the inversion around HSD17B2 gene that converts testosterone into less-active keto-forms. These deletions in Satellite and Faeders possibly lead to overexpression of HSD17B2 that causes increased degradation of testosterone leading to submissive behavior in these males. We also identified four missense mutations at highly conserved sites in MC1R gene within the inversion, which is possibly associated with white ornamental feathers in Satellites.