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Distinct Genetic Architectures Underlie Divergent Thorax, Leg, and Wing Pigmentation

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Distinct Genetic Architectures Underlie Divergent Thorax, Leg, and Wing Pigmentation bioRxiv preprint doi: https://doi.org/10.1101/2020.06.28.176735; this version posted June 29, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 1 Distinct genetic architectures underlie divergent thorax, leg, and wing pigmentation 2 between Drosophila elegans and D. gunungcola 3 Jonathan H. Massey1,2, Jun Li1,3, David L. Stern2, Patricia J. Wittkopp1,4* 4 5 1Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI 6 48109, USA 7 2Janelia Research Campus of the Howard Hughes Medical Institute, Ashburn, VA 20147, USA 8 3Institute of Evolution and Ecology, School of Life Sciences, Central China Normal University, 9 Wuhan 430079, China 10 4Department of Molecular, Cellular, and Developmental Biology, University of Michigan, Ann 11 Arbor, MI 48109, USA 12 13 14 *Corresponding author 15 [email protected] 16 17 Running head: Pigmentation divergence between D. elegans and D. gunungcola 18 Keywords: yellow, ebony, optomotor-blind 19 Word count: 4,553 bioRxiv preprint doi: https://doi.org/10.1101/2020.06.28.176735; this version posted June 29, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 20 Abstract 21 Understanding the genetic basis of species differences is a major goal in evolutionary biology. 22 Pigmentation divergence between Drosophila species often involves genetic changes in 23 pigmentation candidate genes that pattern the body and wings, but it remains unclear how these 24 changes affect pigmentation evolution in multiple body parts between the same diverging 25 species. Drosophila elegans and D. gunungcola show pigmentation differences in the thorax, 26 legs, and wings, with D. elegans exhibiting male-specific wing spots and D. gunungcola lacking 27 wing spots with intensely dark thoraces and legs. Here, we performed QTL mapping to identify 28 the genetic architecture of these differences. We find a large effect QTL on the X chromosome 29 for all three body parts. QTL on Muller Element E were found for thorax pigmentation in both 30 backcrosses but were only marginally significant in one backcross for the legs and wings. 31 Consistent with this observation, we isolated the effects of the Muller Element E QTL by 32 introgressing D. gunungcola alleles into a D. elegans genetic background and found that D. 33 gunungcola alleles linked near the pigmentation candidate gene ebony caused intense darkening 34 of the thorax, minimal darkening of legs, and minimal shrinking of wing spots. D. elegans ebony 35 mutants showed changes in pigmentation consistent with Ebony having different effects on 36 pigmentation in different tissues. Our results suggest that multiple genes have evolved 37 differential effects on pigmentation levels in different body regions. 38 39 40 41 42 bioRxiv preprint doi: https://doi.org/10.1101/2020.06.28.176735; this version posted June 29, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 43 Introduction 44 Pigmentation differences within and between species illustrate some of the most striking 45 examples of phenotypic evolution in nature. In insects, pigmentation intensity in the body, legs, 46 and wings varies widely, often distinguishing sexes, populations, and species (True, 2003; 47 Wittkopp et al., 2003). The genetic and developmental processes determining pigment patterning 48 are well understood, which has facilitated the use of insect pigmentation as a model system to 49 investigate the genetic basis of phenotypic evolution (Wittkopp et al., 2003; Kopp, 2009). 50 Multiple studies have revealed that the same genes have often evolved independently to cause 51 pigmentation variation; that genetic variation within these genes often explains the majority of 52 pigmentation differences; and that mutations affecting the expression of enzymes and 53 transcription factors cause pigmentation to evolve (Massey and Wittkopp, 2016). These results 54 support the hypothesis that the genetic architecture of phenotypic evolution is, at least to some 55 degree, predictable (Stern and Orgogozo, 2008). 56 57 The insect pigmentation synthesis pathway (Figure 1) therefore provides a roadmap for 58 predicting which genes likely contribute to pigmentation differences within and between insect 59 species. Differences in how dopamine is metabolized in this pathway ultimately lead to 60 combinations of black and brown melanins as well as yellow, tan, and colorless sclerotins that 61 diffuse into the developing cuticle in sex-, population-, and species-specific ways (reviewed in 62 True, 2003). The genes yellow, tan, and ebony in this pathway have repeatedly evolved to 63 contribute to these differences. These include both within and between species differences in 64 abdominal, thorax, and wing pigmentation (reviewed in Massey and Wittkopp, 2016). In each bioRxiv preprint doi: https://doi.org/10.1101/2020.06.28.176735; this version posted June 29, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 65 case, mutations in cis-regulatory DNA underlie these phenotypic changes, emphasizing the 66 importance of gene regulatory evolution in generating animal pigmentation diversity. 67 68 Most studies identifying the genetic basis of divergent pigmentation have focused on the 69 divergence of one particular element of the pigment pattern within each species pair. It thus 70 remains unclear how often the same genes and/or mutations are responsible for divergent 71 pigmentation seen in multiple body parts. In some instances, closely related species show 72 striking pigmentation differences across most body regions. Pigmentation divergence between 73 Drosophila americana and D. novamexicana, for example, involves differences in thorax and 74 abdominal pigmentation intensity that are partly explained by evolution of the ebony gene (Lamb 75 et al., 2020). Divergence in pupal case coloration between D. americana and D. virilis, however, 76 is caused by evolution at the dopamine N-acetyltransferase (Dat) gene (Ahmed-Braimah and 77 Sweigart, 2015). In other instances, species differ not only in the pigmentation intensity across 78 multiple body parts but also in pigmentation patterning. Pigmentation evolution in redheaded 79 pine sawfly larvae, for example, involves changes in body coloration and spot patterning that is 80 partially explained by overlapping quantitative trait loci (QTL) (Linnen et al., 2018). 81 82 Species differences between D. elegans and D. gunungcola involve dramatic changes in 83 pigmentation intensity across multiple body parts, although body pigmentation is also 84 polymorphic in D. elegans (Bock and Wheeler, 1972; Hirai and Kimura, 1997). Populations of 85 D. elegans from Hong Kong and Indonesia have light brown thoraxes and legs, and males 86 possess dark black spots at the tips of their wings (Hirai and Kimura, 1997; Figure 2). In Japan 87 and Taiwan, populations have dark black thoraxes while still possessing male-specific wing bioRxiv preprint doi: https://doi.org/10.1101/2020.06.28.176735; this version posted June 29, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 88 spots (Hirai and Kimura, 1997). In D. gunungcola, pigmentation is less variable than in D. 89 elegans (Sultana et al., 1999; Massey et al., 2020). Males and females have dark black thoraxes 90 like the D. elegans Japanese and Taiwanese populations but also show dark black-pigmented 91 legs, and males do not have wing spots (Yeh et al., 2006; Massey et al., 2020; Figure 2). 92 Although these two species diverged 2-2.8 million years ago (Prud'Homme et al., 2006), they 93 can produce fertile, female F1 hybrids in the laboratory (Yeh et al., 2006), allowing us to 94 investigate the genetic basis of pigmentation evolution across multiple body regions in the same 95 mapping population. 96 97 Here, we use quantitative trait locus (QTL) mapping in two backcross populations between the 98 light D. elegans morph from Hong Kong (HK) and D. gunungcola from Sukarami, Indonesia 99 (SK) to identify gene regions associated with thorax, leg, and wing pigmentation divergence. For 100 all three traits, we identified a major effect QTL on the X chromosome, where pigmentation 101 candidate genes omb and yellow are located. We also find evidence for QTL linked to Muller 102 Element E for all three traits, but these effects depend on genetic background. We attempted to 103 isolate these effects by crossing D. gunungcola alleles into a D. elegans genetic background and 104 by introgressing a ~1.5 Mb region containing the ebony locus, which is found on Muller Element 105 E. We find that homozygous D. gunungcola alleles linked to this introgression darkened thorax 106 pigmentation intensity to D. gunungcola levels, but only minimally affected leg and wing 107 pigmentation, consistent with the differences observed in QTL mapping data for the three traits. 108 These data suggest that during the evolution of pigmentation across multiple body parts, epistasis 109 influences the extent to which individual pigmentation loci affect pigmentation divergence in 110 each tissue. In the case of D. elegans and D. gunungcola, evolution of at least two loci is bioRxiv preprint doi: https://doi.org/10.1101/2020.06.28.176735; this version posted June 29, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 111 necessary to cause species differences in leg and wing pigmentation, but evolution at a single 112 locus is sufficient for divergence in thorax pigmentation. 113 114 115 Materials and Methods 116 Fly stocks 117 Drosophila elegans HK (Hong Kong) and D.
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