A Chromosome Inversion Creates a Supergene for Sex and Colour in Lake Malawi Cichlids

Cichlid fishes have the highest rates of evolutionary turnover of sex chromosomes among vertebrates. Many large structural polymorphisms in the radiation of cichlids in Lake Malawi are associated with sex chromosomes and may also carry adaptive variation. Here, we investigate the structure and evolutionary history of an inversion polymorphism that includes both a ZW sex locus and an orange-blotch colour polymorphism in the rock-dwelling cichlid fishes of Lake Malawi. We use long-read sequencing to characterise the sequence and breakpoints of the inversion. We quantify allele frequency differences across the inversion in population samples of the genera Metriaclima and Labeotropheus. We also examine expression differences of genes in the inversion. The simple inversion spans 7 Mb and is flanked by CACTA transposons that may have catalysed the rearrangement. The region includes ~600 genes, several of which show large differences in expression. Some of these genes are candidates for the sex and colour phenotypes. This inversion is an accessible model system for studying the role of structural polymorphisms and sex chromosome turnover in the adaptive radiation of cichlids in the lakes of East Africa.