One Sentence Summary: We identify one nucleotide substitution in a gene regulatory region contributing to evolutionary change of two distinct organs.
SUMMARYDiverse traits often covary between species. The possibility that a single mutation could contribute to the evolution of several characters between species is rarely investigated as relatively few cases are dissected at the nucleotide level. Drosophila santomea has evolved additional sex comb sensory teeth on its legs and has lost two sensory bristles on its genitalia. We found that a single nucleotide substitution in an enhancer of the scute gene contributes to both changes. The mutation alters a binding site for the Hox protein Abdominal-B in the developing genitalia, leading to bristle loss, and for another factor in the developing leg, leading to bristle gain. Our study shows that morphological evolution between species can occur through a single nucleotide change affecting several sexually dimorphic traits. was not peer-reviewed) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.The copyright holder for this preprint (which . http://dx.doi.org/10.1101/313197 doi: bioRxiv preprint first posted online May. 2, 2018;
RESULTS AND DISCUSSION
"Variability is governed by many unknown laws, of which correlated growth is probably the most important."[1]Correlated evolution of traits is widespread among taxa [1,2] and can be due to pleiotropy, where a single locus causally affects several traits [3]. Pleiotropy imposes large constrains on the paths of evolution [4,5], making it crucial to assess the extent of pleiotropy to understand the evolutionary process. Empirical studies suggest that many loci influence multiple traits [3,6,7] and current data cannot reject the idea that all genetic elements have pleiotropic roles [3,8,9]. Several pleiotropic substitutions have been associated with natural variation [10][11][12]: all are coding changes and all underlie intraspecific changes (www.gephebase.org). Nevertheless it remains unclear whether pleiotropic mutations contribute also to interspecific evolution, as experimental evidence suggests that the mutations responsible for interspecies evolution may be less pleiotropic than the mutations underlying intraspecific variation [13].Here we focused on male sexual bristle evolution between Drosophila yakuba and Drosophila santomea, which diverged approximately 0.5-1 million years ago [14] and can produce fertile F1 females in the laboratory [15], facilitating genetic mapping. We found that hypandrial bristles -two prominent mecanosensory bristles located on the ventral part of male genitalia in all D. melanogaster subgroup species -are missing in D. santomea males (Fig. 1). Examination of many inbred stocks and 10 closely related species revealed that the absence of hypandrial bristles is a derived D. santomea-specific trait (Fig. 1, Tables S1-S2). No other genital bristle type was noticeably variable in number between D. yakuba and D. santomea (Fig. S1).We performed whole-ge...