Abstract
To better characterize how variation in regulatory sequences drives divergence in gene expression, we undertook a systematic study of transcription factor binding and gene expression in blastoderm embryos of four species, which sample much of the diversity in the 40 million-year old genus Drosophila: D. melanogaster, D. yakuba, D. pseudoobscura and D. virilis. We compared gene expression, measured by mRNA-seq, to the genome-wide binding, measured by ChIP-seq, of four transcription factors involved in early anterior-posterior patterning. We found that mRNA levels are much better conserved than individual transcription factor binding events, and that changes in a gene's expression were poorly explained by changes in adjacent transcription factor binding. However, highly bound sites, sites in regions bound by multiple factors and sites near genes are conserved more frequently than other binding, suggesting that a considerable amount of transcription factor binding is weakly or non-functional and not subject to purifying selection.
Highlights
In the pursuit of the genetic basis of phenotypic evolution, researchers have favored divergence of gene expression as a major source of diversity [1,2]
Inter-species differences in gene expression during development are a major source of phenotypic diversity, yet the molecular origins of such differences are poorly understood
We were surprised at the extent of variation we observed, especially as we found far less variation in gene expression between these same species’ embryos
Summary
In the pursuit of the genetic basis of phenotypic evolution, researchers have favored divergence of gene expression as a major source of diversity [1,2]. One limitation of many of these studies is that significant changes in DNA sequence are often accompanied by extensive changes in morphology or physiology, complicating direct comparison of molecular phenotypes like transcription factor binding and gene expression. This is not, the case in Drosophila embryogenesis, which is highly conserved across the 40 million-year old Drosophila genus despite accumulating sequence changes equivalent to those separating different classes of amniotes [19]
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