Pupal development and pigmentation process of a polka-dotted fruit fly, Drosophila guttifera (Insecta, Diptera)

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...

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“…Transgenic experiments were performed as outlined in 32 . Pupal stages were identified according to 33 .…”

Section: Methodsmentioning

confidence: 99%

The regulation of a pigmentation gene in the formation of complex color patterns inDrosophilaabdomens

Raja

Shittu

Nouhan

et al. 2020

Preprint

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“…Pupal developmental stages were determined according to (Bainbridge and Bownes, 1981) and (Fukutomi et al, 2017).…”

Section: Methodsmentioning

confidence: 99%

From simplicity to complexity: The gain or loss of spot rows underlies the morphological diversity of threeDrosophilaspecies

Dion¹,

Shittu²,

Steenwinkel³

et al. 2020

Preprint

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13To understand how novel animal patterning emerged, one needs to ask how the 14 development of color patterns has changed among diverging species. Here we examine 15 three species of fruit flies -Drosophila guttifera (D. guttifera), Drosophila palustris (D. 16 palustris), and Drosophila subpalustris (D. subpalustris) -displaying a varying number 17 of abdominal spot rows that were either gained or lost throughout evolutionary time. 18 Through in situ hybridization, we examine the mRNA expression patterns for the 19 pigmentation genes Dopa decarboxylase (Ddc), tan (t), and yellow (y) during pupal 20 development. Our results show that Ddc, t, and y are co-expressed in identical patterns, 21 each foreshadowing the adult abdominal spots in D. guttifera, D. palustris, and D. 22 subpalustris. 23

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“…Pupae at stage P12 (i) or P12 (ii) were used for two successive transcriptome analyses. These stages are just after the stage when yellow expression and pigmentation process have started [53]. (Fig.…”

Section: Collecting Samples For Transcriptome Analysismentioning

confidence: 99%

Transcriptome analysis reveals evolutionary co-option of neural development and signaling genes for the wing pigmentation pattern of the polka-dotted fruit fly

Fukutomi

Kondo

Toyoda

et al. 2020

Preprint

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How evolutionary novelties have arisen is one of the central questions in evolutionary biology. Pre-existing gene regulatory networks or signaling pathways have been shown to be co-opted for building novel traits in several organisms. However, the structure of entire gene regulatory networks and evolutionary events of gene co-option for emergence of a novel trait are poorly understood. In this study, we used a novel wing pigmentation pattern of the polka-dotted fruit fly, and identified the complete set of genes for pigmentation pattern formation by de novo genome sequencing and transcriptome analyses. In pigmentation areas of wings, 151 genes were positively or negatively regulated by wingless, a master regulator of wing pigmentation. Genes for neural development, Wnt signaling, Dpp signaling, Zinc finger transcription factors, and effectors (such as enzymes) for melanin pigmentation were included among these 151 genes. None of the known regulatory genes that regulate pigmentation pattern formation in other fruit fly species were included. Our results suggest that the novel pigmentation pattern of the polka-dotted fruit fly emerged through multi-step co-options of multiple gene regulatory networks, signaling pathways, and effector genes, rather than recruitment of one large gene circuit.

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Pupal development and pigmentation process of a polka-dotted fruit fly, Drosophila guttifera (Insecta, Diptera)

Cited by 25 publications

References 41 publications

The regulation of a pigmentation gene in the formation of complex color patterns inDrosophilaabdomens

The regulation of a pigmentation gene in the formation of complex color patterns inDrosophilaabdomens

From simplicity to complexity: The gain or loss of spot rows underlies the morphological diversity of threeDrosophilaspecies

Transcriptome analysis reveals evolutionary co-option of neural development and signaling genes for the wing pigmentation pattern of the polka-dotted fruit fly

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