Two genomic regions together cause dark abdominal pigmentation in Drosophila tenebrosa

Abstract

Pigmentation is a rapidly evolving trait that is under both natural and sexual selection in many organisms. In the quinaria group of Drosophila, nearly all of the 30 species have an abdomen that is light in color with distinct markings; D. tenebrosa is the exception in that it has a completely melanic abdomen with no visible markings. In this study, we use a combination of quantitative genetic and candidate gene approaches to investigate the genetic basis of abdominal pigmentation in D. tenebrosa. We find that abdominal pigmentation is invariant across wild-caught lines of D. tenebrosa and is not sexually dimorphic. Quantitative genetic mapping utilizing crosses between D. tenebrosa and the light-colored D. suboccidentalis indicates that two genomic regions together underlie abdominal pigmentation, including the X-chromosome and an autosome (Muller Element C/E). Further support for their central importance in pigmentation is that experimental introgression of one phenotype into the other species, in either direction, results in introgression of these two genomic regions. Finally, the expression of the X-linked gene yellow in the pupae exactly foreshadows the adult melanization pattern in the abdomen of both species, suggesting that changes in the regulation of yellow are important for the phenotypic divergence of D. tenebrosa from the rest of the quinaria group. These results contribute to a body of work that demonstrates how changes in expression of highly conserved genes can cause substantial phenotypic differences even between closely related species.

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

“…1a, b). D. guttifera belongs to the quinaria species group, whose members display highly diverse abdominal pigmentation patterns 7,8 . While D. guttifera shows the most complex pattern of this group, most other quinaria group species lack at least one of the four sub-patterns, illustrating the pattern modularity among species.…”

“…While D. guttifera shows the most complex pattern of this group, most other quinaria group species lack at least one of the four sub-patterns, illustrating the pattern modularity among species. Interestingly, the stripe patterns of certain species often separate into spots 7,8 . In this study, we show that the abdominal pigment patterns of quinaria group members may be formed by a combination of localized spot induction and partial stripe repression.…”

“…We focused on the regulation of the yellow ( y ) gene, which is required for the formation of black melanin in insects 8-14 . Several y gene CRMs have been identified in various Drosophila species, and changes in these CRMs and/or in the deployment of trans -factors that regulate y gene expression have been implicated in the diversification of wing and body pigment patterns 12,15-19 .…”

A Pathway Analysis of Melanin Patterning in a Hemimetabolous Insect

“…However, currently the functional roles of most of the yellow family genes are yet to be determined. Even for the yellow gene itself, despite the fact that it is known to be required for melanization in Drosophila and Tribolium (Wright 1987;Wittkopp et al 2002a, b;Jeong et al 2008;Tomoyasu et al 2009;Arakane et al 2010;Bray et al 2014), its enzymatic activity has not yet been established. In terms of the position of yellow in the melanin pathway, two different hypotheses have been proposed ( Figure 1): it may be essential for the production of either DOPA melanin (Wright 1987;Walter et al 1996) or dopamine melanin (Wittkopp et al 2002b(Wittkopp et al , 2003.…”

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

“…D. melanogaster has a relatively simple abdominal pigmentation pattern, as compared to other Drosophila species. The quinaria group, an adaptive radiation of non-model fruit flies, displays a great variety of abdominal and wing pigmentation patterns (Bray et al, 2014; Werner et al, 2018). This abundant morphological diversity and the recent divergence of the lineage (20 million years ago (Scott Chialvo et al, 2019)) allows for the identification of molecular mechanisms underlying differences in species morphology.…”