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Regulatory divergence in Drosophila revealed by mRNA-seq
Open accessAbstract
The regulation of gene expression is critical for organismal function and is an important source of phenotypic diversity between species. Understanding the genetic and molecular mechanisms responsible for regulatory divergence is therefore expected to provide insight into evolutionary change. Using deep sequencing, we quantified total and allele-specific mRNA expression levels genome-wide in two closely related Drosophila species (D. melanogaster and D. sechellia) and their F(1) hybrids. We show that 78% of expressed genes have divergent expression between species, and that cis- and trans-regulatory divergence affects 51% and 66% of expressed genes, respectively, with 35% of genes showing evidence of both. This is a relatively larger contribution of trans-regulatory divergence than was expected based on prior studies, and may result from the unique demographic history of D. sechellia. Genes with antagonistic cis- and trans-regulatory changes were more likely to be misexpressed in hybrids, consistent with the idea that such regulatory changes contribute to hybrid incompatibilities. In addition, cis-regulatory differences contributed more to divergent expression of genes that showed additive rather than nonadditive inheritance. A correlation between sequence similarity and the conservation of cis-regulatory activity was also observed that appears to be a general feature of regulatory evolution. Finally, we examined regulatory divergence that may have contributed to the evolution of a specific trait--divergent feeding behavior in D. sechellia. Overall, this study illustrates the power of mRNA sequencing for investigating regulatory evolution, provides novel insight into the evolution of gene expression in Drosophila, and reveals general trends that are likely to extend to other species.
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“These methods discard allelic multireads that map to both parents and fail to account for reads that are simultaneously genomic and allelic multireads.”
From RNA-Seq Alignment to Individualized Genomes Improves Transcript Abundance Estimates in Multiparent Populations (2014) · cites this paper as McManus et al. 2010
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“Therefore, after aligning reads, we excluded differentiating sites with fewer than 20 overlapping reads and used binomial exact tests with a false discovery rate threshold of 0.05 to test each differentiating site for a statistically significant difference in relative allelic abundance [15,27].”
From Sources of bias in measures of allele-specific expression derived from RNA-seq data aligned to a single reference genome (2013) · cites this paper as [15]
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“two alternative strategies for aligning reads have been shown to eliminate the systematic bias in measures of relative ASE favoring the reference allele”
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Wang, Y., Wang, F., Meng, G., López‐Giráldez, F., Dong, C., Wang, Z., & Townsend, J. P. (2025) · Molecular Biology and Evolution · doi:10.1093/molbev/msaf131 · Cited by 3
Ma, X., Zhang, Z., Guo, L., Gou, X., Bian, Y., Zhao, Y., Wang, B., Lang, M., Wang, T., Xie, K., et al. (2022) · Frontiers in Plant Science · doi:10.3389/fpls.2022.887133 · Cited by 3
Ranz, J. M., Yeh, S., Nyberg, K. G., & Machado, C. A. (2013) · Wiley eBooks · doi:10.1002/9781118552872.ch2 · Cited by 4
Metadata
- Authors
- McManus, C. J., Coolon, J. D., Duff, M. O., Eipper-Mains, J., Graveley, B. R., & Wittkopp, P. J.
- Affiliations
- University of Connecticut (US)
- University of Michigan (US)
- Venue
- Genome Research
- Publisher
- Cold Spring Harbor Laboratory
- Published
- 2010-03-30
- Volume
- 20
- Issue
- 6
- Pages
- 816-825
- ISSN
- 1088-9051 (ISSN-L)
- PMC
- PMC2877578
- OpenAlex
- W2121547736
- Cited by
- 381
- References
- 51
- Citations by year
- 2026: 16 · 2025: 16 · 2024: 19 · 2023: 18 · 2022: 33 · 2021: 26 · 2020: 34 · 2019: 18 · 2018: 17 · 2017: 16 · 2016: 26 · 2015: 31 · 2014: 27 · 2013: 24 · 2012: 31
- Type
- posted content
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Genome Research (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- HighWire Press Open Archive (submittedVersion)
- Funders
- Alfred P. Sloan Foundation
- March of Dimes Foundation (5-FY07-181)
- University of Michigan
- National Institutes of Health
- National Institute of General Medical Sciences (R01GM062516)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Chromosomal and Genetic Variations
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
- Keywords
- regulatory divergence, cis-regulatory divergence, gene expression evolution, Drosophila sechellia, Drosophila melanogaster, interspecific hybrids, hybrid incompatibility, allele-specific expression, additive inheritance, phenotypic diversity
- MeSH terms
- Animals, Drosophila, Gene Expression Regulation, RNA, Messenger, Species Specificity, Evolution, Molecular, Gene Expression Profiling
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