Abstract
BackgroundSpeculation regarding the importance of changes in gene regulation in determining major phylogenetic patterns continues to accrue, despite a lack of broad-scale comparative studies examining how patterns of gene expression vary during development. Comparative transcriptional profiling of adult interspecific hybrids and their parental species has uncovered widespread divergence of the mechanisms controlling gene regulation, revealing incompatibilities that are masked in comparisons between the pure species. However, this has prompted the suggestion that misexpression in adult hybrids results from the downstream cascading effects of a subset of genes improperly regulated in early development.ResultsWe sought to determine how gene expression diverges over development, as well as test the cascade hypothesis, by profiling expression in males of Drosophila melanogaster, D. sechellia, and D. simulans, as well as the D. simulans (♀) × D. sechellia (♂) male F1 hybrids, at four different developmental time points (3rd instar larval, early pupal, late pupal, and newly-emerged adult). Contrary to the cascade model of misexpression, we find that there is considerable stage-specific autonomy of regulatory breakdown in hybrids, with the larval and adult stages showing significantly more hybrid misexpression as compared to the pupal stage. However, comparisons between pure species indicate that genes expressed during earlier stages of development tend to be more conserved in terms of their level of expression than those expressed during later stages, suggesting that while Von Baer's famous law applies at both the level of nucleotide sequence and expression, it may not apply necessarily to the underlying overall regulatory network, which appears to diverge over the course of ontogeny and which can only be ascertained by combining divergent genomes in species hybrids.ConclusionOur results suggest that complex integration of regulatory circuits during morphogenesis may lead to it being more refractory to divergence of underlying gene regulatory mechanisms - more than that suggested by the conservation of gene expression levels between species during earlier stages. This provides support for a 'developmental hourglass' model of divergence of gene expression in Drosophila resulting in a highly conserved pupal stage.
Highlights
Speculation regarding the importance of changes in gene regulation in determining major phylogenetic patterns continues to accrue, despite a lack of broad-scale comparative studies examining how patterns of gene expression vary during development
Restricting our comparison to the 2,006 genes that were detectibly expressed at all four time points in the three species and the hybrids, we found that 64.2% (1,287), 82.2% (1,649), 62.2% (1,247) and 57.9% (1,162) of genes varied significantly in the expression level over the course of the sampled developmental interval in D. melanogaster, D. sechellia, D. simulans and the hybrids, respectively (Additional File 1 contains supplementary methods and analysis, and tables containing raw data and the results of statistical analyses are found in Additional File 2)
A reduced level of intraspecific polymorphism in expression level could lead to reduced estimates of between-replicate variability on the Between species divergence in the context of ontogeny Focusing only on the pure species, we compared the number of genes that were differentially expressed at each of the four sampled time points in pairwise comparisons among those genes detectibly expressed at all stages in all three species (2,253 genes; Figure 1)
Summary
Speculation regarding the importance of changes in gene regulation in determining major phylogenetic patterns continues to accrue, despite a lack of broad-scale comparative studies examining how patterns of gene expression vary during development. A number of researchers have used interspecific hybrids in order to study patterns of gene expression divergence at the level of the transcriptome, typically with the intent of elucidating the incompatible divergence of regulatory factors responsible for post-zygotic reproductive isolation leading to speciation (reviewed in [6]) Such hybrids offer us the chance to reveal incompatible divergence between regulatory elements that are masked by stabilizing selection acting to maintain similar expression levels in the parental species [7]. Hybrids are often characterized by the breakdown of various developmental systems, such as atrophied or absent germlines or heterosis of particular tissues/organs [8,9] Such observations have led to the suggestion that widespread misexpression of genes in adults may not reflect the widespread incompatible divergence of regulatory elements during this stage. Irrespective its ultimate cause, we shall refer to this hypothesis as the ‘cascade model’ of hybrid misexpression
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