Characterization of sex chromosomes in three deeply diverged species of Pseudocrenilabrinae (Teleostei: Cichlidae)

The African cichlid radiations have created thousands of new cichlid species with a wide diversity of trophic morphologies, behaviors, sensory systems, and pigment patterns. In addition, recent research has uncovered a surprising number of young sex chromosome systems within African cichlids. Here, we refine methods to describe the differentiation of young sex chromosomes from whole genome comparisons. We identified a novel XY sex chromosome system on linkage group 14 in Oreochromis mossambicus, confirmed a linkage group 1 XY system in Coptodon zillii, and also defined the limits of our methodology by examining a ZW system on linkage group 3 in Pelmatolapia mariae. These data further demonstrate that cichlids are an excellent model system for understanding the early stages of sex chromosome evolution.

     

Structure and decay of a proto-Y region in Tilapia,Oreochromis niloticus

Background

Sex-determination genes drive the evolution of adjacent chromosomal regions. Sexually antagonistic selection favors the accumulation of inversions that reduce recombination in regions adjacent to the sex-determination gene. Once established, the clonal inheritance of sex-linked inversions leads to the accumulation of deleterious alleles, repetitive elements and a gradual decay of sex-linked genes. This in turn creates selective pressures for the evolution of mechanisms that compensate for the unequal dosage of gene expression. Here we use whole genome sequencing to characterize the structure of a young sex chromosome and quantify sex-specific gene expression in the developing gonad.

Results

We found an 8.8 Mb block of strong differentiation between males and females that corresponds to the location of a previously mapped sex-determiner on linkage group 1 of Oreochromis niloticus. Putatively disruptive mutations are found in many of the genes within this region. We also found a significant female-bias in the expression of genes within the block of differentiation compared to those outside the block of differentiation. Eight candidate sex-determination genes were identified within this region.

Conclusions

This study demonstrates a block of differentiation on linkage group 1, suggestive of an 8.8 Mb inversion encompassing the sex-determining locus. The enrichment of female-biased gene expression inside the proposed inversion suggests incomplete dosage compensation. This study helps establish a model for studying the early-to-intermediate stages of sex chromosome evolution.

Electronic supplementary material

The online version of this article (doi:10.1186/1471-2164-15-975) contains supplementary material, which is available to authorized users.