Ruffs, Philomachus pugnax, are shorebirds that wade around in the Palearctic. Males take on three distinctive types (or morphs) and gather in arenas called leks to perform and display for females. Between 80 and 95 percent of them are aggressive "independent" males with elaborate ruffs and head tufts of varying colors; they vigorously fight and defend territories on leks to gain access to females. Between 5 and 20 percent of males are semi-cooperative "satellites" who are smaller and have mostly white ornamental plumage. These males are non-territorial and submissive to independents at leks, mating mostly when independents are otherwise distracted fighting with other independents. About 1 percent of the males are female-mimicking "faeders" (pictured below to the right). Since they resemble females in their size and lack of flashy feathers, they’re disguised from aggressive independents. They have no territories to defend, and they attempt rapid copulations when females are soliciting matings from ornamented, displaying males. Watch a very cool video of wild ruffs here.
Previous work revealed that all three morphs are controlled by a single genetic factor, and that satellite and faeder morphs are controlled by dominant versions of genes. Now, the genetic mechanism underlying the major differences in their mating strategies is described in two new papers published in Nature Genetics.
Two separate teams assembled the genomes of male ruffs to better understand how complex behavioral, as well as visual, differences between male morphs could have such a simple genetic basis. Both teams found that a region on one chromosome was inverted in satellite and faeder males, relative to that of independent males. This region contains about 100 genes, and the inversion is a single “supergene” that’s inherited in a single block.
Furthermore, the team led by University of Edinburgh’s Mark Blaxter, David Lank of Simon Fraser University, and University of Sheffield’s Terry Burke identified genes within the supergene that are involved in hormone signaling, formation of feather arrays, sperm motility, and gonadal expression. These might contribute to differences between the morphs. They also found that the testes of satellites and faeders are larger than those of independents – presumably to increase the efficiency of less frequent or effective copulations. Based on observations in the wild, independents get more copulations per mating bout than satellites, Lank explains to IFLScience, but the larger testes of satellites and faeders may allow them to deliver more sperm. About 70 percent of female ruffs have more than one male represented in their clutches of four eggs, so sperm competition between males is extensive.
Another team, led by Xin Liu of BGI-Shenzhen and Uppsala University’s Leif Andersson, estimate that the inversion first occurred about 3.8 million years ago. Over time, accumulated mutations within the inverted region led to differences between satellites and faeders. Additionally, both groups link the gene MC1R (which codes for the melanocortin 1 receptor) to the white pigmentation of satellite males' ornamental feathers.
"We think that this evolutionary process started with the occurrence of the inversion about 4 million years ago and that the inversion in itself altered the regulation of one or more genes affecting the metabolism of sex hormones," Andersson explains in a statement. "This created a primitive alternative male morph, which has been further improved step-by-step by the accumulation of many genetic changes."
Variation in breeding plumage and strategy of male ruffs, including female mimic, satellite, and territorial morphs, is determined by a chromosomal inversion. Susan McRae
Image in the text: Female mimic ruff. Melissa Hafting
