Correlated Evolution of two Sensory Organs via a Single Cis-Regulatory Nucleotide Change

Abstract

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 was not peer-reviewed) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.The copyright holder for this preprint (which .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...

The role of genomic vs. epigenomic variation in shaping patterns of convergent transcriptomic variation across continents in a young species complex

“…For example, cis-variation in a gene promoter can alter the binding site of a regulatory protein and induce newly derived phenotype. This was observed in the morphological evolution of two Drosophila species [73], in the threespine stickleback where genetic variants in the EDA gene are associated with the presence/absence of armour plates [74] or cis-acting regulation between divergent marine-freshwater ecotypes [17], as well as in corals under changing climatic conditions where the frequency of favoured alleles co-vary with gene expression level [75]. Moreover, genes affected by cis-eQTL showed higher gene expression differentiation between limnetic and benthic species than genes with convergent DMRs between limnetic and benthic whitefish, and more so for overexpressed genes in the limnetic species relative to the benthic whitefish.…”

Evolution of assortative mating following selective introgression of pigmentation genes between two Drosophila species

“…santomea is endemic (Cariou et al, 2001; Llopart et al, 2005, 2014; Turissini & Matute, 2017). Leveraging the crossability of the two species, short‐term introgression experiments were used to identify the QTL underlying their morphological differences (Carbone et al, 2005; Coyne et al, 2004; Liu et al, 2019; Nagy et al, 2018; Peluffo et al, 2015) and reproductive isolation (Cande et al, 2012; Moehring et al, 2006a, 2006b). Introgressing dark pigmentation alleles of D .…”

An atlas of transcription factors expressed in theDrosophila melanogasterpupal terminalia

“…We did not observe cad expression in other structures; thus caudal serves as a 327 marker for these tissues at this stage of development. cad, which functions in the anterior- bristles to a cis-regualtory element of the scute gene (Nagy et al 2018). 360 We found that Dichaete (D) is expressed in the hypandrial phragma (i.e.…”

“…It remains unclear whether these patterns are controlled by 525 multiple regulatory elements, or if disparate patterns are generated by the same enhancer 526 region (Small et al 1996). It is possible that the enhancers controlling these patterns also 527 operate in other tissues or at different developmental stages (Noon et al 2018;Sabarís et al 528 2019), as is the case for the posterior lobe enhancer of Pox neuro (Glassford et al 2015) and 529 the hypandrial enhancer of scute (Nagy et al 2018). By finding the regulatory sequences that 530 control these gene expression patterns, we can determine the direct targets of transcription 531 factors in this system.…”