Turnover of sex chromosomes in the Lake Tanganyika cichlid tribe Tropheini (Teleostei: Cichlidae)

Abstract

Sex chromosome replacement is frequent in many vertebrate clades, including fish, frogs, and lizards. In order to understand the mechanisms responsible for sex chromosome turnover and the early stages of sex chromosome divergence, it is necessary to study lineages with recently evolved sex chromosomes. Here we examine sex chromosome evolution in a group of African cichlid fishes (tribe Tropheini) which began to diverge from one another less than 4 MYA. We have evidence for a previously unknown sex chromosome system, and preliminary indications of several additional systems not previously reported in this group. We find a high frequency of sex chromosome turnover and estimate a minimum of 14 turnovers in this tribe. We date the origin of the most common sex determining system in this tribe (XY-LG5/19) near the base of one of two major sub-clades of this tribe, about 3.4 MY ago. Finally, we observe variation in the size of one sex-determining region that suggests independent evolution of evolutionary strata in species with a shared sex-determination system. Our results illuminate the rapid rate of sex chromosome turnover in the tribe Tropheini and set the stage for further studies of the dynamics of sex chromosome evolution in this group.

Figure 1

Phylogeny of Tropheini with previous sex chromosome calls and proposed sex chromosome systems. Some systems feature chromosomal fusions or multiple sex chromosomes. Cells in blue indicate an XY system, cells in orange indicate a ZW system. Bolded text indicates disagreement between previous call and current call. Black circles indicate loss of sex chromosome common to that clade. Topology adapted from Ronco et al. and approximate time scale is from Singh et al..

Figure 2

Pairwise male x female F_ST and sex specific allele frequency in pool-seq data for Interochromis loocki and Gnathochromis pfefferi. The x-axis is position on the Metriaclima zebra (UMD2a) reference assembly.

Figure 3

Pairwise male x female F_ST and sex specific allele frequency for S. horei, (a) whole genome, (b) LG5. The x-axis is position on the Metriaclima zebra (UMD2a) reference assembly.

Figure 4

Expansion of the XY-LG5/19 sex chromosome on the phylogeny of Clade 2 as estimated from sex-specific SNP density data. Circles indicate expansion of LG5, stars indicate expansion of LG19. For LG5 the dotted pattern indicates what is presumably the original region, as does the plaid pattern for LG19, with any further additions in different patterns representing potential evolutionary strata. Phylogeny adapted from Ronco et al..