@article {67734, title = {Distinct genetic architectures underlie divergent thorax, leg, and wing pigmentation between Drosophila elegans and D. gunungcola.}, journal = {Heredity}, volume = {127}, year = {2021}, month = {2021 Nov 01}, pages = {467-74}, abstract = {

Pigmentation divergence between Drosophila species has emerged as a model trait for studying the genetic basis of phenotypic evolution, with genetic changes contributing to pigmentation differences often mapping to genes in the pigment synthesis pathway and their regulators. These studies of Drosophila pigmentation have tended to focus on pigmentation changes in one body part for a particular pair of species, but changes in pigmentation are often observed in multiple body parts between the same pair of species. The similarities and differences of genetic changes responsible for divergent pigmentation in different body parts of the same species thus remain largely unknown. Here we compare the genetic basis of pigmentation divergence between Drosophila elegans and D. gunungcola in the wing, legs, and thorax. Prior work has shown that regions of the genome containing the pigmentation genes yellow and ebony influence the size of divergent male-specific wing spots between these two species. We find that these same two regions of the genome underlie differences in leg and thorax pigmentation; however, divergent alleles in these regions show differences in allelic dominance and epistasis among the three body parts. These complex patterns of inheritance can be explained by a model of evolution involving tissue-specific changes in the expression of Yellow and Ebony between D. elegans and D. gunungcola.

}, issn = {1365-2540}, doi = {10.1038/s41437-021-00467-0}, author = {Massey, Jonathan H and Li, Jun and Stern, David L and Wittkopp, Patricia J} } @article {65585, title = {Co-evolving wing spots and mating displays are genetically separable traits in Drosophila.}, journal = {Evolution}, volume = {74}, year = {2020}, month = {2020 May 03}, pages = {1098-1111}, abstract = {

The evolution of sexual traits often involves correlated changes in morphology and behavior. For example, in Drosophila, divergent mating displays are often accompanied by divergent pigment patterns. To better understand how such traits co-evolve, we investigated the genetic basis of correlated divergence in wing pigmentation and mating display between the sibling species Drosophila elegans and D. gunungcola. Drosophila elegans males have an area of black pigment on their wings known as a wing spot and appear to display this spot to females by extending their wings laterally during courtship. By contrast, D. gunungcola lost both of these traits. Using Multiplexed Shotgun Genotyping (MSG), we identified a \~{}440 kb region on the X chromosome that behaves like a genetic switch controlling the presence or absence of male-specific wing spots. This region includes the candidate gene optomotor-blind (omb), which plays a critical role in patterning the Drosophila wing. The genetic basis of divergent wing display is more complex, with at least two loci on the X chromosome and two loci on autosomes contributing to its evolution. Introgressing the X-linked region affecting wing spot development from D. gunungcola into D. elegans reduced pigmentation in the wing spots but did not affect the wing display, indicating that these are genetically separable traits. Consistent with this observation, broader sampling of wild D. gunungcola populations confirmed the wing spot and wing display are evolving independently: some D. gunungcola males performed wing displays similar to D. elegans despite lacking wing spots. These data suggest that correlated selection pressures rather than physical linkage or pleiotropy are responsible for the coevolution of these morphological and behavioral traits. They also suggest that the change in morphology evolved prior to the change in behavior. This article is protected by copyright. All rights reserved.

}, issn = {1558-5646}, doi = {10.1111/evo.13990}, author = {Massey, Jonathan H and Rice, Gavin R and Firdaus, Anggun and Chen, Chi-Yang and Yeh, Shu-Dan and Stern, David L and Wittkopp, Patricia J} } @article {64944, title = {Pleiotropic effects of ebony and tan on pigmentation and cuticular hydrocarbon composition in Drosophila melanogaster.}, journal = {Frontiers in Physiology}, volume = {10}, year = {2019}, month = {05/2019}, pages = {518}, abstract = {

Pleiotropic genes are genes that affect more than one trait. For example, many genes required for pigmentation in the fruit fly also affect traits such as circadian rhythms, vision, and mating behavior. Here, we present evidence that two pigmentation genes, and , which encode enzymes catalyzing reciprocal reactions in the melanin biosynthesis pathway, also affect cuticular hydrocarbon (CHC) composition in females. More specifically, we report that loss-of-function mutants have a CHC profile that is biased toward long (\>25C) chain CHCs, whereas loss-of-function mutants have a CHC profile that is biased toward short (\<25C) chain CHCs. Moreover, pharmacological inhibition of dopamine synthesis, a key step in the melanin synthesis pathway, reversed the changes in CHC composition seen in mutants, making the CHC profiles similar to those seen in mutants. These observations suggest that genetic variation affecting and/or activity might cause correlated changes in pigmentation and CHC composition in natural populations. We tested this possibility using the Genetic Reference Panel (DGRP) and found that CHC composition covaried with pigmentation as well as levels of and expression in newly eclosed adults in a manner consistent with the and mutant phenotypes. These data suggest that the pleiotropic effects of and might contribute to covariation of pigmentation and CHC profiles in .

}, issn = {1664-042X}, doi = {10.3389/fphys.2019.00518}, author = {Massey, Jonathan H and Akiyama, Noriyoshi and Bien, Tanja and Dreisewerd, Klaus and Wittkopp, Patricia J and Yew, Joanne Y and Takahashi, Aya} } @article {65229, title = {The yellow gene influences Drosophila male mating success through sex comb melanization.}, journal = {eLife}, volume = {8}, year = {2019}, month = {2019 Oct 15}, abstract = {

males perform a series of courtship behaviors that, when successful, result in copulation with a female. For over a century, mutations in the gene, named for its effects on pigmentation, have been known to reduce male mating success. Prior work has suggested that influences mating behavior through effects on wing extension, song, and/or courtship vigor. Here, we rule out these explanations, as well as effects on the nervous system more generally, and find instead that the effects of on male mating success are mediated by its effects on pigmentation of male-specific leg structures called sex combs. Loss of expression in these modified bristles reduces their melanization, which changes their structure and causes difficulty grasping females prior to copulation. These data illustrate why the mechanical properties of anatomy, not just neural circuitry, must be considered to fully understand the development and evolution of behavior.

}, issn = {2050-084X}, doi = {10.7554/eLife.49388}, author = {Massey, Jonathan H and Chung, Daayun and Siwanowicz, Igor and Stern, David L and Wittkopp, Patricia J} } @article {45740, title = {The function and regulation of Ultrabithorax in the legs of Drosophila melanogaster.}, journal = {Dev Biol}, volume = {308}, year = {2007}, month = {2007 Aug 15}, pages = {621-31}, abstract = {

Alterations in Hox gene expression patterns have been implicated in both large and small-scale morphological evolution. An improved understanding of these changes requires a detailed understanding of Hox gene cis-regulatory function and evolution. cis-regulatory evolution of the Hox gene Ultrabithorax (Ubx) has been shown to contribute to evolution of trichome patterns on the posterior second femur (T2p) of Drosophila species. As a step toward determining how this function of Ubx has evolved, we performed a series of experiments to clarify the role of Ubx in patterning femurs and to identify the cis-regulatory regions of Ubx that drive expression in T2p. We first performed clonal analysis to further define Ubx function in patterning bristle and trichome patterns in the legs. We found that low levels of Ubx expression are sufficient to repress an eighth bristle row on the posterior second and third femurs, whereas higher levels of expression are required to promote the development and migration of other bristles on the third femur and to repress trichomes. We then tested the hypothesis that the evolutionary difference in T2p trichome patterns due to Ubx was caused by a change in the global cis-regulation of Ubx expression. We found no evidence to support this view, suggesting that the evolved difference in Ubx function reflects evolution of a leg-specific enhancer. We then searched for the regulatory regions of the Ubx locus that drive expression in the second and third femur by assaying all existing regulatory mutations of the Ubx locus and new deficiencies in the large intron of Ubx that we generated by P-element-induced male recombination. We found that two enhancer regions previously known to regulate Ubx expression in the legs, abx and pbx, are required for Ubx expression in the third femur, but that they do not contribute to pupal expression of Ubx in the second femur. This analysis allowed us to rule out at least 100 kb of DNA in and around the Ubx locus as containing a T2p-specific enhancer. We then surveyed an additional approximately 30 kb using enhancer constructs. None of these enhancer constructs produced an expression pattern similar to Ubx expression in T2p. Thus, after surveying over 95\% of the Ubx locus, we have not been able to localize a T2p-specific enhancer. While the enhancer could reside within the small regions we have not surveyed, it is also possible that the enhancer is structurally complex and/or acts only within its native genomic context.

}, keywords = {Animals, Base Sequence, Body Patterning, DNA, Drosophila, Drosophila melanogaster, Drosophila Proteins, Enhancer Elements, Genetic, Evolution, Molecular, Extremities, Female, Gene Expression Regulation, Developmental, Genes, Homeobox, Genes, Insect, Genetic Complementation Test, Homeodomain Proteins, Male, Mutation, Recombination, Genetic, Species Specificity, Transcription Factors}, issn = {0012-1606}, doi = {10.1016/j.ydbio.2007.06.002}, author = {Davis, Gregory K and Srinivasan, Dayalan G and Wittkopp, Patricia J and Stern, David L} }