Abstract

How pleiotropy influences evolution of protein sequence remains unclear. The male-specific lethal (MSL) complex in Drosophila mediates dosage compensation by 2-fold upregulation of the X chromosome in males. Nevertheless, several MSL proteins also bind autosomes and likely perform functions not related to dosage compensation. Here, we study the evolution of MOF, MSL1, and MSL2 biding sites in Drosophila melanogaster and its close relative Drosophila simulans. We found pervasive expansion of the MSL binding sites in D. melanogaster, particularly on autosomes. The majority of these newly-bound regions are unlikely to function in dosage compensation and associated with an increase in expression divergence between D. melanogaster and D. simulans. While dosage-compensation related sites show clear signatures of adaptive evolution, these signatures are even more marked among autosomal regions. Our study points to an intriguing avenue of investigation of pleiotropy as a mechanism promoting rapid protein sequence evolution.

Highlights

  • The rate and mechanism of protein sequence evolution are central questions in evolutionary biology

  • There was no significant difference for NSC or RSC values between D. melanogaster and D. simulans (t-test, both P > 0.05, Supplementary Table 2), suggesting that the overall qualities of the male-specific lethal (MSL) protein ChIP-seq data are comparable between the two species

  • We studied evolution of dosage compensation complex binding sites in D. melanogaster and D. simulans

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Summary

Introduction

The rate and mechanism of protein sequence evolution are central questions in evolutionary biology. Empirical data have shown that essential genes do not evolve more slowly than nonessential genes (Greenberg et al, 2008; Zhang and Yang, 2015). This supports the view that the rate of protein sequence evolution depends primarily on the level of functional constraint (Zhang and Yang, 2015; Wollenberg Valero, 2020), rather than on the level of functional importance (Karp et al, 2008). To better understand how pleiotropy shapes adaptation driven by rapidly evolving

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