Throughout nature, organisms evolve morphological features that then undergo further diversification among the species. So far, the genetic mechanisms underlying these two distinct evolutionary steps, the emergence of a novel trait followed by its diversification among different species, has not been well defined. But now French researchers have started to work that process out by examining the minute spots of pigment on the wings of male flies from different species of the Drosophila genus.
Different species of flies have specific patterns of pigmented spots on their wings. Prud’homme and Gompel found that the spots mimicked the distribution of the yellow protein, so they screened for transcription factors that regulated expression of the gene yellow.
Surprisingly, the group found that Distalless (Dll), a transcription factor with a well-characterized role in wing patterning, was both necessary and sufficient to control yellow expression. “Given its essential function in wing development, we would have thought that Dll distribution cannot change without messing up wing formation,” said Prud’homme. “Yet…Dll changes expression pattern after its essential function in wing formation is over.”
The researchers found that Dll is expressed as a gradient around the perimeter of the wing in early pupal development in all the species examined. But after 30 hours, when wing patterning is done, Dll expression diverges among the species to drives the expression of yellow and thus the placement of the pigment spot on the wing.
But Prud’homme and Gompel did not believe that just the one protein, yellow, could be solely responsible for the placement of the pigmentation spot on the flies’ wings. They thought it more likely that Dll acted as a master regulator of different enzymes. They found that Dll in fact controls the spatial distribution of a protein called ebony as well as yellow and that other pigmentation genes may also be involved.
“In wing-spotted Drosophila species, Dll has, on top of its other roles, acquired a novel function: to regulate pigmentation genes to make a wing spot. This is showing us the opportunistic nature of the evolutionary process that recombine whichever genetic players are available—here Dll and pigmentation genes—to produce a morphological novelty,” Prud’homme noted.
Along with wing pigmentation patterns, the males of these species have evolved a specific wing display courtship behavior. “We have developed functional tools to manipulate gene activity (gain and loss of function) and wing spot formation in multiple Drosophila species,” said Prud’homme about this most recent work. “This will allow us to investigate in a precise and controlled manner the function of the wing spot in the context of courtship behavior.”
1. Arnoult, L., K. F. Y. Su, D. Manoel, C. Minervino, J. Magriña, N. Gompel, and B. Prud'homme. 2013. Emergence and diversification of fly pigmentation through evolution of a gene regulatory module. Science 339(6126):1423-1426.