Molecular population genetics of the Polycomb genes in Drosophila subobscura.

Juan M Calvo-Martín,Carmen Segarra,Montserrat Papaceit

doi:10.1371/journal.pone.0185005

Abstract

Polycomb group (PcG) proteins are important regulatory factors that modulate the chromatin state. They form protein complexes that repress gene expression by the introduction of posttranslational histone modifications. The study of PcG proteins divergence in Drosophila revealed signals of coevolution among them and an acceleration of the nonsynonymous evolutionary rate in the lineage ancestral to the obscura group species, mainly in subunits of the Pcl-PRC2 complex. Herein, we have studied the nucleotide polymorphism of PcG genes in a natural population of D. subobscura to detect whether natural selection has also modulated the evolution of these important regulatory genes in a more recent time scale. Results show that most genes are under the action of purifying selection and present a level and pattern of polymorphism consistent with predictions of the neutral model, the exceptions being Su(z)12 and Pho. MK tests indicate an accumulation of adaptive changes in the SU(Z)12 protein during the divergence of D. subobscura and D. guanche. In contrast, the HKA test shows a deficit of polymorphism at Pho. The most likely explanation for this reduced variation is the location of this gene in the dot-like chromosome and would indicate that this chromosome also has null or very low recombination in D. subobscura, as reported in D. melanogaster.

Highlights

The identification of genes under adaptive selection is a major goal of evolutionary genetics
The low level of nucleotide variation at Pho relative to the other Polycomb group (PcG) gene regions is evident when nucleotide diversity is normalized by nucleotide divergence (K) with D. guanche to correct for differences in the mutation rate across gene regions
Polycomb group (PcG) proteins form different complexes that maintain the repressive state of chromatin

Summary

Introduction

The identification of genes under adaptive selection is a major goal of evolutionary genetics. Several methods and statistical tests have been developed to detect the footprint left by the action of positive selection at the molecular level (reviewed in [1]). These approaches were first applied to single candidate genes with a clear adaptive function. In Drosophila, these studies consistently corroborated that adaptive selection has shaped the evolution of genes involved in processes such as immunity [2], reproduction [3] and stem cell maintenance [4]. Proteins do not act in isolation, but they are members of complex metabolic, regulatory or interaction networks that control biological processes.

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