Evolution of Drosophila sex comb length illustrates the inextricable interplay between selection and variation

In spite of the diversity of possible biological forms observed in nature, a limited range of morphospace is frequently occupied for a given trait. Several mechanisms have been proposed to explain this bias in the distribution of phenotypes including selection, drift, and developmental constraints. Despite extensive work on phenotypic bias, the underlying developmental mechanisms explaining why particular regions of morphological space remain unoccupied are poorly understood. To address this issue, we studied the sex comb, a group of modified bristles used in courtship that shows marked morphological diversity among Drosophila species. In many Drosophila species including Drosophila melanogaster , the sex comb rotates 90° to a vertical position during development. Here we analyze the effect of changing D. melanogaster sex comb length on the process of rotation. We find that artificial selection changes the number of bristles per comb without a proportional change in the space available for rotation. As a result, when increasing sex comb length, rather than displaying a similar straight vertical shape observed in other Drosophila species, long sex combs bend because rotation is blocked by a neighboring row of bristles. Our results show ways in which morphologies that would be favored by natural selection are apparently impossible to achieve developmentally. These findings highlight the potential role of development in modifying selectable variation in the evolution of Drosophila sex comb length. Significance Not all possible biological shapes are actually seen in nature. Despite much experimental work, the developmental basis explaining the presence or absence of certain biological shapes remains poorly understood. We studied Drosophila melanogaster development using the sex comb, a group of modified bristles exhibiting spectacular morphological diversity among Drosophila species. We provide several lines of evidence suggesting that increasing D. melanogaster sex comb length produces a mechanical blockage, affecting comb shape and position. We infer that simple physical principles acting on tissues can influence the direction of evolution, and comparative studies of other fly species are consistent with this hypothesis. This work highlights the fundamental role of development for understanding biodiversity and evolution.