Using Ancestral Reconstruction of Chromosome Expression States (ARChES) to Understand the Evolution of Dosage Compensation

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2020

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Ramesh, Balan
Demuth, Jeff

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Ohno (1967) originally proposed that the sex difference in X-linked gene dose caused by the decay of Y-linked genes may impose a “peril of hemizygosity” and that regulatory mechanisms must compensate to make X=XX=AA at the level of expression. Recent evidence suggests that Ohno’s paradigm is not universal, but our understanding remains unclear because estimating the ancestral expression of X-linked genes is difficult or impossible in many systems. Many studies assess dosage compensation (DC) by comparing X: Autosome expression ratios, thereby implicitly assuming that current average autosomal gene expression (AA) is a good proxy for the average ancestral expression of X-linked genes. A more appropriate test would be whether X=XX=Ancestral expression, where “Ancestral” is the inferred expression level of each X- linked gene before becoming X-linked. The few studies that have attempted to compare X (or Z) linked gene expression to corresponding ancestral levels have relied on distantly related taxa that include changes in chromosome number and sex-determination system. Here, we study the evolution of dosage compensation by comparing expression of neo-X chromosome genes in Tribolium confusum to their inferred ancestral, autosomal expression state. The ancestral expression is estimated by analyzing RNA-Seq data across a time-calibrated phylogeny that includes four additional closely related species that all share an ancestral karyotype where the neo-X genes of T. confusum remain autosomal. We find that the neo-X in T. confusum is dosage balanced (X=XX) and dosage compensated (X=Ancestral), suggesting a chromosome-wide dosage compensation mechanism as envisioned by Ohno. Further, we observe that DC in T. castaneum, which was previously contentious, is fully balanced and compensated (X=XX=Ancestral). The computational approach to analyzing DC evolution via Ancestral Reconstruction of Chromosome Expression States (ARChES) was developed using TACC and is publicly available. ARChES workflow is computationally scalable and can be expanded to analyze DC in any species.

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