The ruff has one of the weirdest sexual systems in the world 鈥� all thanks to a large piece of chromosome that was flipped over 3.8 million years ago.
A type of wading sandpiper, ruffs are named after the large showy feathers sported by males around their necks during breeding season.
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But in 2006, : a rare type of male that looks exactly like a female, only slightly larger.
Unlike territorial males, with their coloured ruffs, head tufts and big showy displays to impress females, these female mimics pursue a different mating strategy.
In the frenzy of ruff mating, which can involve many aggressive and displaying males, copulation is a speedy process. When a female has picked a male, she presents her genital opening, or cloaca, to him, but can instead be fertilised by a female mimic, which rushes in first.
鈥淭hey seem to operate by complete subterfuge,鈥� says at the University of Sheffield, UK.
Mating strategies like this have been seen in a range of animals. But Burke鈥檚 team, and a second team led by at Uppsala University in Sweden, have independently found the genetic changes behind the ruff鈥檚 strange system, making it the best understood of its kind.
Bigger testes
The two teams sequenced the ruff鈥檚 genome and found that a large chunk of chromosome 11, containing around 100 genes, is upside-down in the female mimics.
The inversion of this 鈥渟upergene鈥� region would have protected the genes within it from shuffling between each generation. This allowed a suite of gene variants to evolve together, creating males that look like females but have larger testes than ordinary males.
鈥淚t鈥檚 rather like the emergence of a new sex chromosome,鈥� says Burke.
The teams are yet to identify every gene contained within this supergene region, but have so far found a gene involved in colouring, which could explain differences in plumage, as well as genes involved in processing sex hormones.
鈥淭his is the most detailed picture of alternative mating strategies that are due to genetics,鈥� says at North Carolina State University in Raleigh.
The female mimics鈥� strategy works but is costly. Offspring that inherit two copies of the inverted supergene die, thanks to disruption of both copies of a crucial gene. Such a high rate of failed offspring must be outweighed by huge benefits to being a female mimic. They may not get more mating opportunities during a single breeding season, says Andersson, but they must have more reproductive success over their lifetime than territorial males. 鈥淧erhaps [female mimics] are active at an earlier and a later age,鈥� he says.
The third male
The weirdness doesn鈥檛 stop here. There is a third type of male that has the species鈥� characteristic neck feathers, albeit in drabber colours. These males don鈥檛 fight or compete in displays. Instead, they move unhindered between the territorial males.
The territorial males likely put up with these 鈥渟atellite鈥� males because they bulk out their numbers, making their performing gang of males look more enticing to females.
It鈥檚 not clear whether, like the female mimics, these satellites 鈥渟teal鈥� their copulations with females, or whether the females have a choice. 鈥淭he female bows down, and sometimes it鈥檚 a case of which male gets there first. It鈥檚 not necessarily a highly aggressive act,鈥� says Burke.
The success of this strategy seems to depend on how common the males are. Too few impressive territorial males, and the females may not be attracted at all, so the proportion of satellites seems to be maintained at an optimum of around 16 per cent.
This type of male is far more common than the female mimics, and seems to have evolved more recently, some 500,000 years ago, according to work by Andersson鈥檚 team. A rare event allowed the supergene to swap part of its DNA back with the original, un-inverted region, forming this inbetween type of male.
This newer strategy seems to have usurped that of the female mimics, pushing them to only 1 per cent of all males. But because all three types still exist today, each strategy must be successful in the long run 鈥� otherwise female mimics would have been pushed out long ago.
Journal references: Nature Genetics, 10.1038/ng.3430 and 10.1038/ng.3443
Read more: 鈥�Dangerous liaisons: Fatal animal attractions鈥�
Image credit: Winfried Wisniewski/Minden Pictures/Getty
