Abstract
Cichlids are well known for their propensity to radiate generating arrays of morphologically and ecologically diverse species in short evolutionary time. Following this rapid evolutionary pace, cichlids show high rates of sex chromosome turnover. We here studied the evolution of sex-biased gene (SBG) expression in 14 recently diverged taxa of the Lake Tanganyika Tropheini cichlids, which show different XY sex chromosomes. Across species, sex chromosome sequence divergence predates divergence in expression between the sexes. Only one sex chromosome, the oldest, showed signs of demasculinization in gene expression and potentially contribution to the resolution of sexual conflict. SBGs in general showed high rates of turnovers and evolved mostly under drift. Sexual selection did not shape the rapid evolutionary changes of SBGs. Male-biased genes evolved faster than female-biased genes, which seem to be under more phylogenetic constraint. We found a relationship between the degree of sex bias and sequence evolution driven by sequence differences among the sexes. Consistent with other species, strong sex bias towards sex-limited expression contributes to resolving sexual conflict in cichlids.This article is part of the theme issue ‘Challenging the paradigm in sex chromosome evolution: empirical and theoretical insights with a focus on vertebrates (Part II)’.
Highlights
Males and females of the same species share most of their genome but differ in their fitness optima for morphological, physiological as well as behavioural traits [1,2]
They are major contributors to reaching sexual optima and the resolution of sexual conflict [6]. This is evidenced by an over-representation of sex-biased gene (SBG) on sex chromosomes
To investigate changes in SBGs across the species tree, we reconstructed ancestral sex bias with the ace function in the ape package in R based on categorical information for each gene (i.e. female-biased genes (FBGs), male-biased genes (MBGs) or unbiased derived from differential expression analysis described above), under maximum-likelihood (ML) estimation with an equal-rates model using joint estimation procedures that take into account all the information for each node
Summary
Males and females of the same species share most of their genome but differ in their fitness optima for morphological, physiological as well as behavioural traits [1,2]. Owing to their sex-specific inheritance and selection, sex chromosomes in particular can be subject to feminization or masculinization of gene expression They are major contributors to reaching sexual optima and the resolution of sexual conflict [6]. We here investigated the evolution of SBG expression in 14 closely related fish taxa that experienced recent sex chromosome turnovers or losses These fishes show variation in sexual dimorphism and probably in their degree of sexual selection. We investigated how sex bias in gene expression evolved with respect to changes in sex chromosomes and how this is accompanied by patterns of sequence evolution This dataset allowed us to investigate: (i) how fast sex chromosomes can accumulate SBG expression, (ii) how turnover of sex chromosomes impacts sex bias, and (iii) which selection regimes act on sex chromosomes and SBGs of recently diverged taxa
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