Constraint and turnover in sex-biased gene expression in the genus Drosophila

Laboratory of Cellular and Developmental Biology, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Department of Health and Human Services, Bethesda, Maryland 20892, USA.
Nature (Impact Factor: 42.35). 12/2007; 450(7167):233-7. DOI: 10.1038/nature06323
Source: PubMed

ABSTRACT Both genome content and deployment contribute to phenotypic differences between species. Sex is the most important difference between individuals in a species and has long been posited to be rapidly evolving. Indeed, in the Drosophila genus, traits such as sperm length, genitalia, and gonad size are the most obvious differences between species. Comparative analysis of sex-biased expression should deepen our understanding of the relationship between genome content and deployment during evolution. Using existing and newly assembled genomes, we designed species-specific microarrays to examine sex-biased expression of orthologues and species-restricted genes in D. melanogaster, D. simulans, D. yakuba, D. ananassae, D. pseudoobscura, D. virilis and D. mojavensis. We show that averaged sex-biased expression changes accumulate monotonically over time within the genus. However, different genes contribute to expression variance within species groups compared to between groups. We observed greater turnover of species-restricted genes with male-biased expression, indicating that gene formation and extinction may play a significant part in species differences. Genes with male-biased expression also show the greatest expression and DNA sequence divergence. This higher divergence and turnover of genes with male-biased expression may be due to high transcription rates in the male germline, greater functional pleiotropy of genes expressed in females, and/or sexual competition.

Download full-text


Available from: Michael Parisi, Jun 29, 2015
  • Source
    [Show abstract] [Hide abstract]
    ABSTRACT: Primary sex-determination ''switches'' evolve ra-pidly, but Doublesex (DSX)-related transcription fac-tors (DMRTs) act downstream of these switches to control sexual development in most animal species. Drosophila dsx encodes female-and male-specific isoforms (DSX F and DSX M), but little is known about how dsx controls sexual development, whether DSX F and DSX M bind different targets, or how DSX proteins direct different outcomes in diverse tissues. We undertook genome-wide analyses to identify DSX targets using in vivo occupancy, binding site predic-tion, and evolutionary conservation. We find that DSX F and DSX M bind thousands of the same targets in multiple tissues in both sexes, yet these targets have sex-and tissue-specific functions. Interestingly, DSX targets show considerable overlap with targets identified for mouse DMRT1. DSX targets include transcription factors and signaling pathway compo-nents providing for direct and indirect regulation of sex-biased expression. INTRODUCTION
    Developmental Cell 12/2014; 31(6):761-773. DOI:10.1016/j.devcel.2014.11.021 · 10.37 Impact Factor
  • Source
    [Show abstract] [Hide abstract]
    ABSTRACT: The castes of social insects provide outstanding opportunities to address the causes and consequences of evolution of discrete phenotypes, i.e., polymorphisms. Here we focus on recently described patterns of a positive association between the degree of caste-specific gene expression and the rate of sequence evolution. We outline how neutral and adaptive evolution can cause genes that are morph-biased in their expression profiles to exhibit historical signatures of faster or slower sequence evolution compared to unbiased genes. We conclude that evaluation of different hypotheses will benefit from (i) reconstruction of the phylogenetic origin of biased expression and changes in rates of sequence evolution, and (ii) replicated data on gene expression variation within versus between morphs. Although the data are limited at present, we suggest that the observed phylogenetic and intra-population variation in gene expression lends support to the hypothesis that the association between caste-biased expression and rate of sequence evolution largely is a result of neutral processes.
    Frontiers in Genetics 08/2014; 5:297. DOI:10.3389/fgene.2014.00297
  • Source
    [Show abstract] [Hide abstract]
    ABSTRACT: Vitellogenin, a storage protein, has been extensively studied for its egg-yolk precursor role, and it has been suggested to be fundamentally involved in caste differences in social insects. More than one vitellogenin copy has been reported in several oviparous species, including ants. However, the number and function of different vitellogenins, their phylogenetic relatedness and their role in reproductive queens and non-reproductive workers has been studied in few species only. We studied caste biased expression of vitellogenins in seven Formica ant species. Only one copy of conventional vitellogenin was identified in Formica species, and three vitellogenin homologues, derived from ancient duplications, which represent yet undiscovered vitellogenin-like genes. We show that each of these vitellogenin-like genes is present in all studied Hymenoptera and some of them in other insects as well. We show that after each major duplication event at least one of the vitellogenin-like genes has experienced a period of positive selection. This, combined with the observation that the vitellogenin-like genes have acquired or lost specific protein domains suggests sub- or neofunctionalization between vitellogenin and the duplicated genes. In contrast to earlier studies, vitellogenin was not consistently queen biased in its expression, and the caste bias of the three vitellogenin-like genes was highly variable among species. Furthermore, a truncated and Hymenoptera-specific vitellogenin-like gene, Vg-like-C, was consistently worker biased. Multispecies comparisons are essential for vitellogenin expression studies, and for gene expression studies in general, as we show that expression and also, putative functions cannot be generalized even among closely related species.
    Molecular Biology and Evolution 06/2014; 31(8). DOI:10.1093/molbev/msu171 · 14.31 Impact Factor