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

Abstract

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.

Figure 1

Genome-wide scan for population differentiation. Genome-wide statistics for (a) F_ST, (b) Fisher’s Exact Test and (c) intermediate frequency SNPs in males that are fixed or nearly fixed in females.

Figure 2

Population differentiation on linkage group 1. Differentiation statistics for linkage group 1. (a) F_ST, (b) Fisher’s Exact Test and (c) intermediate frequency SNPs in males that are fixed or nearly fixed in females.

Figure 3

Mapping of sex-determination locus on linkage group 1. Previous studies identifying sex-linked markers on LG1. (a) Lee et al., [24] used a bulked segregant analysis. The green rectangle surrounds markers that were significantly sex-associated. The red rectangle encompasses the region with the highest significance. (b) Ezaz et al., [26] identified three Y-specific AFLPs. OniY425 was assigned through BLAST to scaffold UNK43. It was placed on LG1 according to Lee et al., [25], which used BAC contigs to place it within 100 kb of UNH995. (c) Cnaani et al., [21], also used a bulked segregant analysis. The markers within the red rectangles indicate markers that were significantly associated with sex. (d) Palaiokostas et al., 2013, identified sex-linked RAD-Seq markers. The green rectangle encompasses the markers with a LOD score greater than 15, while the red rectangle encloses the markers flanking the marker with the highest LOD score (Oni23063 with a LOD score of 18.5). (e) Proposed inversion in green with the eight candidate genes discussed in this paper.