Before the East African radiation: sex chromosome systems in basal haplotilapiine cichlids.

Abstract

Cichlid fishes have undergone an extraordinary diversification in East Africa. They also have a high rate of sex chromosome turnover. This clade provides an opportunity to study the rates and patterns of sex chromosome turnover, and the interactions of sex chromosome turnover with adaptation and speciation. Here we investigate the evolution sex chromosomes in the tribes Tilapiini, Coptodonini, Heterotilapiini, Gobiocichlini, Pelmatolapiini and Oreochromini. We assembled chromosome-scale genomes of male and female Pelmatotilapia mariae. We then mapped pooled sequencing reads for males and females of P. mariae and 12 additional species on several genome assemblies to identify sex chromosomes. Tilapia sparrmanii and Oreochromis aureus share a ZW system on LG3 that overlaps the ZW system identified in P. mariae. Heterotilapia buettikoferi, T. brevimanus and Coptodon bakossiorum share an XY system mapping to another region of LG3. Coptodon zilli, Sarotherodon galilaeus, S. melanotheron and O. niloticus share an XY system on LG1. Finally, O. mossambicus and O. shiranus share an XY system on LG14 and we find evidence of an XY system on LG20 in Danakilia sp. 'shukoray'. The phylogenetic distribution of these sex determination systems suggests a long period of polymorphism for the systems on LG1 and LG3 and a generally lower rate of sex chromosome turnover in these lineages compared to the lacustrine lineages of the East African radiation. Our data is not consistent with the recent suggestion of figla and banf2 as candidate genes for the LG1XY and LG3ZW systems. We suggest a possible role for ubiquitination in the XY systems on LG3.