Genetic basis of reproductive and plumage polymorphism in the ruff

Individual animals usually exhibit flexibility in their behaviour, but some behaviours are genetically determined. An extreme example of genetically fixed alternative behaviours occurs in a wading bird, the ruff. The ruff has a "lek" mating system in which males invest all their energy into attracting females to mate with them, and none into parental care. Territorial breeding males have spectacular plumes around their neck and head, and vary enormously in colouration, so that each male at the lek is distinguishable. Other nonterritorial "satellite" males, which are distinguishable by their white feathers, concentrate on "stealing" matings from territorial displaying males. Whether a male becomes a territorial or satellite individual is genetically determined. Satellites are essentially parasitic on territorials, though there is evidence that territorials may benefit from the presence of a small number of satellites. A third type of male, which mimics females, was recently discovered. This parasitic male is able to "hide" from the other males at the lek, so avoiding territorial aggression, and also succeeds by stealing matings from the resident males.

The purpose of this study is to use genome sequencing to identify the genes that make the males behave in these three different ways. We want to understand how the three different strategies can coexist in the population, and how they have evolved. We also plan to discover the genetic mechanism to explain why males are so diverse in their plumage. These mechanisms are likely to be the same ones that produce some of the similar variation that we normally only see between species. Finally, we want to discover the mechanism that ensures that the plumage pattern and behaviour are co-inherited.

The objectives will be achieved by collaboration among three research groups. David Lank (Simon Fraser University) has studied the reproductive behaviour of ruffs in a captive population for 18 generations, and will provide tissue samples to Terry Burke and Jon Slate (University of Sheffield) to enable completion of the ruff pedigree and study of gene expression. Mark Blaxter and colleagues (University of Edinburgh) will support the work by providing new-generation sequencing and associated bioinformatic expertise. Specifically, we will use high-density RAD sequencing to search for genetic markers associated with the three genetically determined reproductive strategies and with plumage patterning. We will use low-density RAD screening of the entire available pedigree to map each trait. The ruff genome will be sequenced and assembled so that we can locate the RAD markers. In combination, we expect to identify the causative loci for both reproductive and plumage traits. We will investigate the expression of the identified loci in the brain and feather follicles. We will investigate the mechanism that maintains the association between behaviour and morphology, and also use standard population genetic tools to test for evidence of selection at the identified loci.

RAD sequencing is currently of academic interest but has the potential to make an impact among plant and animal breeders, where it might allow the rapid and efficient isolation of the genetic basis of many commercially important traits. This could aid the development of new strains and their commercial protection. We will therefore interact with this community to showcase the approach and provide specific advice to potential users.

The ruff system has excellent potential for communicating modern whole-organism biology to the wider public, and so we propose to create and display high-class exhibition materials that convey our results.