Male ruffs look and behave differently around females, depending on their version of a 125-gene stretch of DNA.
Common to marshes and wet meadows in northern Europe and Asia, ruffs (Philomachus pugnux) are named after the decorative collars popular in Renaissance Europe. But the birds’ poufy plumage is not the only baroque aspect of their biology. Males gather at mass breeding grounds where they juke, jump and lunge toward other males, in hopes of winning females.
Male ruffs belong to one of three different forms, each with a unique approach to mating. 'Independent' males, with hodgepodge of brown and black neck feathers, are territorial and defend their bit of the breeding ground. White-feathered 'satellite' males, by contrast, invade the turf of independents to steal nearby females. A third, rarer form, called 'faeders' (Old English for father), take advantage of their resemblance to female ruffs to interrupt coital encounters.
“They dash in and jump on the female before the territorial males does,” says Terry Burke, an evolutionary biologist at University of Sheffield, UK. “My colleague describes this as the 'sandwich'. You end up with the territorial male jumping on the back of the mimic.”
Burke was part of a team that, in 1995, found that the different approaches of male ruffs were caused by a single inherited factor3. But it seemed improbable that one gene could trigger such wide-ranging differences in behaviour and appearance.
Instead, a supergene 4.5 million DNA letters long and composed of 125 individual genes seems responsible for the peculiar behaviour of ruffs, report teams led by Burke2 and Leif Andersson1, an evolutionary geneticist at Uppsala University in Sweden, in Nature Genetics.
Ordinarily, a long continuous stretch of DNA would be broken up by the reshuffling of maternal and paternal chromosome segments that occurs in each new generation (known as homologous recombination). But the ruff’s supergene was born when a long stretch of DNA inverted itself some 3.8 million years ago. This inversion prevented genes within it from recombining with corresponding genes on a sister chromosome, and so cemented around 125 adjacent genes together. Some 500,000 years ago, portions of the inverted supergene flipped back to the correct orientation, creating a second version. Faeders possess one copy of the original inverted supergene, satellite males have one copy of the newer switched-back version, and independents lack either version.
Genetic alterations that have accrued within the supergene in the last 3.8 million years may explain why the ruff forms behave and look so differently. Faeders and satellites both harbour mutations near a gene that breaks down testosterone, and Andersson speculates that an overactive version of this gene explains why faeders and satellites are not aggressively territorial. The satellite supergene, however, carries mutations that disrupt the MC1R gene, which is involved in hair and skin colour in many animals. The white tufts of satellite ruffs could be the consequence.
Those are nice stories, but laboratory tests would be needed to determine how variations in genes such as MC1R influence traits, says Chris Jiggins, an evolutionary geneticist at the University of Cambridge, UK.
The supergene concept was first proposed in the early twentieth century to explain why sets of coloration genes seemed to be inherited in an all-or-nothing fashion in some insects — but no supergenes were found. But they are now being identified in particular animals, thanks to cheap genome sequencing4. Researchers have mapped supergenes in butterflies, sparrows, ants and a few other species in recent years, but Jiggins expects that the phenomenon is relatively uncommon.
“It’s nice example of how evolution can throw up spectacular things on very rare occasions,” Burke says.
Lamichhaney, S. et al. Nature Genet. http://dx.doi.org/10.1038/ng.3430 (2015).
Küpper, C. et al. Nature Genet. http://dx.doi.org/10.1038/ng.3443 (2015).
Lank, D. B., Smith, C. M., Hanotte, O., Burke, T. & Cooke, F. Nature 378, 59-62 (1995).
Schwander, T., Libbrecht, R. & Keller, L. Curr. Biol. 24, R288–R294 (2014).
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Callaway, E. 'Supergene’ determines wading birds’ sex strategy. Nature (2015). https://doi.org/10.1038/nature.2015.18802