Masculinization of the X-chromosome in aphid soma and gonads

Abstract

SummaryMales and females share essentially the same genome but differ in their optimal values for many phenotypic traits, which can result in intra-locus conflict between the sexes. Aphids display XX/X0 sex chromosomes and combine unusual X chromosome inheritance with cyclical parthenogenesis. Theoretical and empirical works support the hypothesis that the large excess of male-biased genes observed on the aphid X chromosome compared to autosomes has evolved in response to sexual conflicts, by restricting the product of a sexually antagonistic allele to the sex it benefits. However, whether such masculinization of the X affects all tissues (as expected if it evolved in response to sexual conflicts) or reflects tissue specificities (which would contradict the sexual conflict hypothesis) remains an open question. To address it, we measured gene expression in different somatic and gonadic tissues of males, sexual females and parthenogenetic females of the pea aphid. We observed a masculinization of the X at the tissue-level, with male-biased genes being 2.5 to 3.5 more frequent on the X than expected. We also tested the hypothesis that gene duplication can facilitate the attenuation of conflicts by allowing gene copies to neo- or sub-functionalize and reach sex-specific optima. As predicted, X-linked copies of duplicated genes having their other copies on autosomes were more frequently male-biased (40.5% of the genes) than duplicated autosomal genes (6.6%) or X-linked single-copy genes (32.5%). These results highlight a peculiar pattern of expression of X-linked genes in aphids at the tissue level and provides further support for sex-biased expression as a mechanism to attenuate intra-locus sexual conflicts.