Impact of male trait exaggeration on sex-biased gene expression and genome architecture in a water strider

William Toubiana,Abderrahman Khila,Corentin Dechaud,Roberto Arbore,David Armisén

doi:10.1186/s12915-021-01021-4

Abstract

BackgroundExaggerated secondary sexual traits are widespread in nature and often evolve under strong directional sexual selection. Although heavily studied from both theoretical and empirical viewpoints, we have little understanding of how sexual selection influences sex-biased gene regulation during the development of exaggerated secondary sexual phenotypes, and how these changes are reflected in genomic architecture. This is primarily due to the limited availability of representative genomes and associated tissue and sex transcriptomes to study the development of these traits. Here we present the genome and developmental transcriptomes, focused on the legs, of the water strider Microvelia longipes, a species where males exhibit strikingly long third legs compared to females, which they use as weapons.ResultsWe generated a high-quality genome assembly with 90% of the sequence captured in 13 scaffolds. The most exaggerated legs in males were particularly enriched in both sex-biased and leg-biased genes, indicating a specific signature of gene expression in association with trait exaggeration. We also found that male-biased genes showed patterns of fast evolution compared to non-biased and female-biased genes, indicative of directional or relaxed purifying selection. By contrast to male-biased genes, female-biased genes that are expressed in the third legs, but not the other legs, are over-represented in the X chromosome compared to the autosomes. An enrichment analysis for sex-biased genes along the chromosomes revealed also that they arrange in large genomic regions or in small clusters of two to four consecutive genes. The number and expression of these enriched regions were often associated with the exaggerated legs of males, suggesting a pattern of common regulation through genomic proximity in association with trait exaggeration.ConclusionOur findings indicate how directional sexual selection may drive sex-biased gene expression and genome architecture along the path to trait exaggeration and sexual dimorphism.

Highlights

Exaggerated secondary sexual traits are widespread in nature and often evolve under strong directional sexual selection
De novo assembly and automatic annotation of M. longipes genome To study the genetic mechanisms underlying extreme growth of male legs, we generated de novo the genome of M. longipes (Fig. 1a) using lines established from a French Guiana population that were inbred through 15 brother-sister crosses [41]
Trait exaggeration and sex-biased gene expression Comparing the three pairs of legs in M. longipes offers a unique opportunity to understand how gene regulation correlates with phenotypic differences between males and females, as these legs present different types and degrees of sexual dimorphism, including discrete and quantitative phenotypes [40, 41]

Summary

Introduction

Exaggerated secondary sexual traits are widespread in nature and often evolve under strong directional sexual selection. Heavily studied from both theoretical and empirical viewpoints, we have little understanding of how sexual selection influences sex-biased gene regulation during the development of exaggerated secondary sexual phenotypes, and how these changes are reflected in genomic architecture. This is primarily due to the limited availability of representative genomes and associated tissue and sex transcriptomes to study the development of these traits. Phenotypic differences between males and females of the same species, is one of the most common sources of phenotypic variation in nature [1, 2] Understanding how this process is regulated in a sex-specific manner at the genomic level still poses an important challenge [3]. Recent studies have notably shown that sex-biased or sex-specific genes tend to be unevenly distributed between chromosomes (e.g., X chromosome versus autosomes), sometimes even forming gene clusters within chromosomes, highlighting a possible role of sexual selection in driving genome evolution [11, 12]

Objectives

Methods

Results

Discussion

Conclusion