Groupe Roulin
Evolution and Maintenance of Genetic Colour Polymorphism

The main goal of the first project is to understand the role of natural and sexual selection in the evolution and maintenance of genetic variation at loci coding for melanin-based colour traits by combining disciplines of behavioural ecology, genetics and population genetics. In the second project, our aim is to determine the role of nestling begging and sib-sib communication in the resolution of conflicts between parents and offspring and among siblings. We recently started a project on the evolution of language in animal communication.

In vertebrates melanin-based coloration is often associated with variation in physiological and behavioural traits. We recently proposed that this association stems from pleiotropic effects of the genes regulating the synthesis of brown to black eumelanin. Because melanocortins act through five G-protein-coupled melanocortin receptors (MC1-5R), which have very different functions (i.e. melanin production, sexual behaviour, aggressiveness and exocrine gland activity, HPA stress response, immune function and energy homeostasis), the degree of melanin-based coloration should covary with other phenotypic traits. The finding that regulators of the melanocortin system can pleiotropically affect the expression of suites of correlated phenotypic traits has important implications with regard to the existence of behavioural syndromes. These syndromes are analogous to personality differences with some individuals being bolder or more shy and where individuals consistently differ with respect to many traits across a range of situations and contexts. We proposed that behavioural syndromes might evolve by pleiotropic effects, whereby different strategies are signalled by melanin-based coloration. Indeed, darker eumelanic individuals are usually more aggressive, sexually active, immunocompetent and resistant to stress, traits that can be useful for bold individuals being explorative and taking more risks. Less eumelanic individuals might adopt the opposite strategy to derive the same fitness as dark conspecifics.

The aim of our research is to:
(i) determine the adaptive function of alternative melanin-based colour traits,
(ii) identify how ecological, social and physiological factors jointly influence and maintain inter-individual variation in melanin-based coloration and the other associated phenotypic traits,
(iii) examine whether the level of melanocortins in different tissues correlate with melanin-based coloration,
(iv) identify the mechanism underlying a difference in melanocortin levels between differently coloured individuals (i.e. genetic polymorphism, expression of the POMC mRNA or post-translational modification of the POMC prohormone), and
(v) manipulate melanocortin level to demonstrate that these hormones are responsible for the production of melanin-based coloration and its covariation with other phenotypic traits as observed in natural situations.

Aim, method and originality of the project
To study the evolution, maintenance and genetics of melanin-based coloration, we mainly work with three species: the barn owl, tawny owl and kestrel. These birds display polymorphism in melanin-based coloration which signal different individual attributes. These three species of birds vary in a number of life history traits and ecological aspects, and are therefore suited to perform a thorough study on melanin-based coloration. More specifically, we investigate the following key issues:
(1) The signalling function of melanin-based coloration. To this end, we perform experiments in the field with wild animals, and analyse a long-term database (20 years of data.
(2) Genetics of melanin-based coloration. This part is done in the laboratory using molecular techniques.

This project is original, since the interest in melanin-based colour traits and genetic colour polymorphism has recently grown. Furthermore, we recently proposed a new genetic mechanism to explain why melanin-based colour traits are frequently associated with several individual attributes.

Key papers
Ducrest, A.-L., Keller, L. & Roulin, A. In press. There is more to colour than what you see: the pleiotropic effects of the melanocortin system. Trends in Ecology and Evolution.

Roulin, A. & Altwegg, R. 2007. Breeding rate is associated with pheomelanism in male and with eumelanism in female barn owls. Behavioral Ecology 18: 563-570.

Roulin, A. 2004. Proximate basis of the covariation between a melanin-based female ornament and offspring quality. Oecologia 140, 668-675.

Roulin, A. 2004. The evolution, maintenance and adaptive function of genetic colour polymorphism in birds. Biological Reviews 79, 815-848.

Roulin, A. & Dijkstra, C. 2003. Genetic and environmental components of variation in eumelanin and phaeomelanin sex-traits in the barn owl. Heredity 90, 359-364.

When siblings strongly differ in need, in the absence of parents they signal to each other their willingness to compete for non-divisible food at their parent's return. A needy individual signals to its siblings that it will vigorously contest the impending food resources in order to deter siblings from competing when parents return to the nest, thus ensuring that it will be fed without having to beg too intensely. In contrast, since less needy siblings have little chance of being fed, they may expect little reward from investment in sibling competition. They should refrain from signalling to siblings, therefore indicating that they will retreat from sibling competition. This would allow them to avoid wasting energy in negotiation, competitive behaviour and begging. In sum, sibling negotiation should allow nestlings to optimally invest effort in competitive begging mainly when food resources are non-divisible. The sibling negotiation hypothesis has been demonstrated in the barn owl and recently in spotless starling (Bulmer et al. 2007 Behav. Ecol. 19, 279-284).

Aim, method and originality of the project
In this project, we study the adaptive value of sibling interactions by using an experimental approach with wild barn owl broods. This species is particularly suited because nestlings vocalise all night long even when parents are not at the nest. These vocalisations are directed to siblings and signal food need.

Currently, we have five major aims:
(1) Importance of individual recognition in sib-sib communication, since calls of each individual is distinctive
(2) Importance of begging behaviour and sibling negotiation on within-brood food allocation
(3) Dynamics over time of begging behaviour and sibling negotiation
(4) Role of punishment to reinforce the honesty of nestling calls as a honest signal of need
(5) Evolution of nest-specific signals of need. This project encompasses also the evolution of proto-language

This project is original because the importance of sib-sib communication in the resolution of conflicts between parents and offspring and among siblings has not been considered in detail. This system also allows us to investigate original questions linked to individual recognition, punishment and the evolution of language.

Key papers
Roulin, A., Kölliker, M. & Richner, H. 2000. Barn owl (Tyto alba) siblings vocally negotiate resources. Proceedings of the Royal Society of London B267, 459-463.

Johnstone, R. A. & Roulin, A. 2003. Sibling negotiation. Behavioral Ecology 14, 780-786.

Roulin, A. 2002. The sibling negotiation hypothesis. In The evolution of begging: competition, cooperation and communication (eds. Wright J. & Leonard M.), Dordrecht, Kluwer Academic Press, pp. 107-127.

Roulin, A. 2004. Effects of hatching asynchrony on sibling negotiation, begging, jostling for position and within-brood food allocation in the barn owl Tyto alba. Evolutionary Ecology Research 6, 1083-1098.