Chromosomal inversion determines male morphs in the ruff

Ruff male of the morph Independent. Photo: Daniel Pettersson Photography

The ruff is a wading bird where the male becomes especially spectacular during mating season with its colorful and variable breeding plumage. Two papers published together in Nature Genetics in November have now identified the genetic source of the large variation of male plumage in a small region of the ruff’s genome.

Males of this species can be divided into three different morphs that both look and behave very different from each other: Independents have colorful plumage with both collar and head tuft. This morph vary greatly in color and they defend their territories violently at leks. Satellites are non-territorial while carrying white ruffs and head tuft. They are slightly smaller than Independents and display submissive behavior. Faeder is a recently discovered, rare morph (Jukema and Piersma 2006), where the males are small, inconspicuous and avoid fighting Independents by mimicking females.

The different morphs in the ruff. Figure from Farrell et al. (2013).
The different morphs in the ruff. Figure from Farrell et al. (2013).

Lamichhaney and colleagues sequenced the genome of several ruffs and located an inversion on a small region of chromosome 11. They estimated that the inversion that results in the male morph Faeder emerged about 3.8 million years ago, before a new structural change occurred half a million years ago giving rise to the third male morph, Satellite. This means that ruff males most likely initially only consisted of Independents, and that the white, submissive morph is relatively new.

Inversion in the Ruff genome
High Fst in the inversion (Lamichhaney et al. 2016)

The inversion was found to contain 90 genes, several of them interesting candidates coding for traits such as feather color and hormones. It is possible that differences in expression and behavior of these genes between the morphs result in the large variation in plumage and behavior we see in the ruff males today.

References

Lamichhaney et al. (2016) Structural genomic changes underlie alternative reproductive strategies in the ruff (Philomachus pugnax). Nature Genetics. doi: 10.1038/ng.3430

Küpper et al. (2016) A supergene determines highly divergent male reproductive morphs in the ruff. Nature Genetics 48, 79–83. doi: 10.1038/ng.3443

Jukema and Piersma (2006) Permanent female mimics in a lekking shorebird. Biology Letters. doi: 10.1098/rsbl.2005.0416

Farrell et al. (2013) Genetic mapping of the female mimic morph locus in the ruff. BMC Geneticsdoi: 10.1186/1471-2156-14-109

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