23Changes in cis-regulatory modules (CRMs) that control developmental gene expression 24 patterns have been implicated in the evolution of animal morphology 1-6 . However, the 25 genetic mechanisms underlying complex morphological traits remain largely unknown. 26 Here we investigated the molecular mechanisms that induce the pigmentation gene yellow 27 (y) in a complex spot and shade pattern on the abdomen of the quinaria group species 28 Drosophila guttifera. We show that the y expression pattern is controlled by only one CRM, 29 which contains a stripe-inducing CRM at its core. We identified several developmental 30 genes that may collectively interact with the CRM to orchestrate the patterning in the 31 pupal abdomen of D. guttifera. We further show that the core CRM is conserved among D. 32 guttifera and the closely related quinaria group species Drosophila deflecta, which displays 33 a similarly spotted abdominal pigment pattern. Our data suggest that besides direct 34 activation of patterns in distinct spots, abdominal spot patterns in Drosophila species may 35 have evolved through partial repression of an ancestral stripe pattern, leaving isolated 36 spots behind. Abdominal pigment patterns of extant quinaria group species support the 37 partial repression hypothesis and further emphasize the modularity of the D. guttifera 38 pattern. 39 40 How complex morphological features develop and evolve is a question of foremost importance 41 in biology. To address this question, we identified genes underlying abdominal pigmentation 42 pattern development in Drosophila guttifera (D. guttifera). The abdomen is decorated with six 43 rows of black spots that run along the anterior-posterior axis, divided by a dark dorsal midline 44shade. This color pattern shows four sub-patterns: a dorsal, median, and lateral pair of spot rows, 45 plus the dorsal midline shade (Fig. 1a, b). D. guttifera belongs to the quinaria species group, 46 whose members display highly diverse abdominal pigmentation patterns 7,8 . While D. guttifera 47 dorsal midline (Extended Data Fig. 2c). Similarly, wg foreshadowed all six rows of spots, while 126 dpp expression matched all but the lateral spot rows (Extended Data Fig. 3b, c). In contrast to the 127 D. guttifera results, abd-A, hh, and zen were absent along the dorsal midline, which is in 128 agreement with the lack of pigment in D. deflecta adults (Extended Data Fig. 3d, e, f, g). 129However, abd-A expression was not detectable where the lateral spot rows will form (Extended 130 Data Fig. 3d), suggesting that these particular spots are controlled differently in D. deflecta. We 131 next cloned the 938 bp orthologous def y spot CRM and transformed it into D. guttifera, using 132 the DsRed reporter assay. The def y spot CRM drove faint dorsal spot row and stripe expression, 133 especially along the dorsal spots (Extended Data Fig. 4). We further subdivided the def y spot 134 CRM into 8 sub-fragments and identified a minimal def y core stripe CRM (288 bp) (#7, 135 Extended Data Fig. 4). This...
Changes in the control of developmental gene expression patterns have been implicated in the evolution of animal morphology. However, the genetic mechanisms underlying complex morphological traits remain largely unknown. Here we investigated the molecular mechanisms that induce the pigmentation gene yellow in a complex color pattern on the abdomen of Drosophila guttifera. We show that at least five developmental genes may collectively activate one cis-regulatory module of yellow in distinct spot rows and a dark shade to assemble the complete abdominal pigment pattern of Drosophila guttifera. One of these genes, wingless, may play a conserved role in the early phase of spot pattern development in several species of the quinaria group. Our findings shed light on the evolution of complex animal color patterns through modular changes of gene expression patterns.
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