On the Origin and Evolution of Drosophila New Genes during Spermatogenesis.

Qianwei Su,Qi Zhou,Huangyi He

doi:10.3390/genes12111796

Abstract

The origin of functional new genes is a basic biological process that has significant contribution to organismal diversity. Previous studies in both Drosophila and mammals showed that new genes tend to be expressed in testes and avoid the X chromosome, presumably because of meiotic sex chromosome inactivation (MSCI). Here, we analyze the published single-cell transcriptome data of Drosophila adult testis and find an enrichment of male germline mitotic genes, but an underrepresentation of meiotic genes on the X chromosome. This can be attributed to an excess of autosomal meiotic genes that were derived from their X-linked mitotic progenitors, which provides direct cell-level evidence for MSCI in Drosophila. We reveal that new genes, particularly those produced by retrotransposition, tend to exhibit an expression shift toward late spermatogenesis compared with their parental copies, probably due to the more intensive sperm competition or sexual conflict. Our results dissect the complex factors including age, the origination mechanisms and the chromosomal locations that influence the new gene origination and evolution in testes, and identify new gene cases that show divergent cell-level expression patterns from their progenitors for future functional studies.

Highlights

The origination mechanisms were divided into DNA-based duplication, RNA-based duplication, or de novo evolution [1,29], based on their possibly different patterns emerging from later expression comparison between parental vs. new genes
New genes produced by retrotransposition or located on a different chromosome compared with the parental genes are more likely to share different cis-regulatory elements with those of their parental genes and evolved novel expression patterns
De novo genes have been recently analyzed with the Drosophila adult testis scRNA-seq dataset and are not the focus of this study, nor they help to clarify the role of meiotic sex chromosome inactivation (MSCI) during new gene evolution [26]

Summary

Introduction

Testes, compared with other organs, seem to play a more important role in permitting the nascent new genes to originate, and to subsequently adopt novel functions in other tissues by evolutionary time (the ‘out of the testis’ hypothesis) [5]. New genes, especially those of young ages (e.g., species-specific new genes) are more likely to have a testis-biased expression pattern than the other ‘older’

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