Abstract
BackgroundSexually dimorphic phenotypes are generally associated with differential gene expression between the sexes. The study of molecular evolution and genomic location of these differentially expressed, or sex-biased, genes is important for understanding inter-sexual divergence under sex-specific selection pressures. Teleost fish provide a unique opportunity to examine this divergence in the presence of variable sex-determination mechanisms of recent origin. The guppy, Poecilia reticulata, displays sexual dimorphism in size, ornaments, and behavior, traits shaped by natural and sexual selection in the wild.ResultsTo gain insight into molecular mechanisms underlying the guppy’s sexual dimorphism, we assembled a reference transcriptome combining genome-independent as well as genome-guided assemblies and analyzed sex-biased gene expression between different tissues of adult male and female guppies. We found tissue-associated sex-biased expression of genes related to pigmentation, signal transduction, and spermatogenesis in males; and growth, cell-division, extra-cellular matrix organization, nutrient transport, and folliculogenesis in females. While most sex-biased genes were randomly distributed across linkage groups, we observed accumulation of ovary-biased genes on the sex linkage group, LG12. Both testis-biased and ovary-biased genes showed a significantly higher rate of non-synonymous to synonymous substitutions (dN/dS) compared to unbiased genes. However, in somatic tissues only female-biased genes, including those co-expressed in multiple tissues, showed elevated ratios of non-synonymous substitutions.ConclusionsOur work identifies a set of annotated gene products that are candidate factors affecting sexual dimorphism in guppies. The differential genomic distribution of gonad-biased genes provides evidence for sex-specific selection pressures acting on the nascent sex chromosomes of the guppy. The elevated rates of evolution of testis-biased and female-biased genes indicate differing evolution under distinct selection pressures on the reproductive versus non-reproductive tissues.Electronic supplementary materialThe online version of this article (doi:10.1186/1471-2164-15-400) contains supplementary material, which is available to authorized users.
Highlights
Dimorphic phenotypes are generally associated with differential gene expression between the sexes
For a second set complementary DNA (cDNA) libraries were prepared from brain, tail, and gonads with individual barcodes for each tissue from six different individuals to allow quantitative comparisons (Additional file 1: Table S1, Figure 2)
The stacked bars show the number of orthologs common between GGA and guided assembly (GIA), unique to GGA and unique to GIA; (C) Inset rectangle summarizes the steps for merging predicted coding sequences (CDS) from both assemblies and functional annotation of the guppy reference transcriptome (GRT)
Summary
Dimorphic phenotypes are generally associated with differential gene expression between the sexes. The study of molecular evolution and genomic location of these differentially expressed, or sex-biased, genes is important for understanding inter-sexual divergence under sex-specific selection pressures. Research on evolutionary properties of sex-biased genes has shown accelerated rates of coding sequence changes in reproduction-related male-biased genes [16,17]. This is primarily attributed to greater sexual selection on males than females. Elevated nucleotide substitution rates of sex-biased genes expressed in somatic and reproductive tissues may occur due to relaxed selection on nonpleiotropic tissue-specific genes [18,19]. Sex-biased genes show non-random genomic distribution with X- or Z-linkage [20,21] that can arise due to differential selection on the hemizygous sex chromosome [6,7]
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