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Distinct genetic architectures underlie divergent thorax, leg, and wing pigmentation between Drosophila elegans and D. gunungcola

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.

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Fig. 1: Insect sclerotization and pigmentation synthesis pathway and pigmentation differences between Drosophila elegans HK and D. gunungcola SK.
Fig. 2: Quantitative trait locus (QTL) mapping of thorax, leg, and wing pigmentation divergence.
Fig. 3: Genetic interactions among QTL on the X chromosome and Muller element E differ among body parts.
Fig. 4: D. gunungcola SK alleles linked to ebony on Muller element E have varied effects on thorax, leg, and wing pigmentation divergence.
Fig. 5: Model of pigmentation divergence connecting genotypes to gene expression to phenotypes.

Data availability

All supporting data can be accessed at University of Michigan Deep Blue (https://deepblue.lib.umich.edu/data/concern/data_sets/j098zb17n?locale=en) and Dryad https://doi.org/10.5061/dryad.gb5mkkwm5.

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Acknowledgements

We thank members of the Wittkopp, Stern, and Rebeiz labs for helpful discussions. For fly strains, we thank J. True (Stony Brook University). For guidance with CRISPR/Cas9 genome editing and embryo injections, we thank Abigail Lamb. For helpful advice on creating F1 hybrids, we thank Shu-Dan Yeh (National Central University). Funding was provided by University of Michigan, Department of Ecology and Evolutionary Biology, Peter Olaus Okkelberg Research Award, National Institutes of Health (NIH) training grant T32GM007544, and Howard Hughes Medical Institute Janelia Graduate Research Fellowship to JHM; NIH R01 GM089736 and 1R35GM118073 to PJW.

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Correspondence to Patricia J. Wittkopp.

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Massey, J.H., Li, J., Stern, D.L. et al. Distinct genetic architectures underlie divergent thorax, leg, and wing pigmentation between Drosophila elegans and D. gunungcola. Heredity (2021). https://doi.org/10.1038/s41437-021-00467-0

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