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Abstract Chromosomal inversions are an important class of genetic variation that link multiple alleles together into a single inherited block that can have important e7ects on fitness. To study the role of large inversions in the massive evolutionary radiation of Lake Malawi cichlids, we used long-read technologies to identify four single and two tandem inversions that span half of each respective chromosome, and which together encompass over 10% of the genome. Each inversion is fixed in one of the two states within the seven major ecogroups, suggesting they played a role in the separation of the major lake lineages into specific lake habitats. One exception is within the benthic sub-radiation, where both inverted and non-inverted alleles continue to segregate within the group. The evolutionary histories of three of the six inversions suggest they transferred from the pelagic Diplotaxodon group into benthic ancestors at the time the benthic sub-radiation was seeded. The remaining three inversions are found in a subset of benthic species living in deep waters. We show that some of these inversions are used as XY sex-determination systems but are also likely limited to a subset of total lake species. Our work suggests that inversions have been under both sexual and natural selection in Lake Malawi cichlids and that they will be important to understanding how this adaptive radiation evolved. 

ABSTRACT Chromosomal inversions are an important class of genetic variation that link multiple alleles together into a single inherited block that can have important effects on fitness. To study the role of large inversions in the massive evolutionary radiation of Lake Malawi cichlids, we used long-read technologies to identify four single and two tandem inversions that span half of each respective chromosome, and which together encompass over 10% of the genome. Each inversion is fixed in one of the two states within the seven major ecogroups, suggesting they played a role in the separation of the major lake lineages into specific lake habitats. One exception is within the benthic sub-radiation, where both inverted and non-inverted alleles continue to segregate within the group. The evolutionary histories of three of the six inversions suggest they transferred from the pelagic Diplotaxodon group into benthic ancestors at the time the benthic sub-radiation was seeded. The remaining three inversions are found in a subset of benthic species living in deep waters. We show that some of these inversions are used as XY sex-determination systems but are also likely limited to a subset of total lake species. Our work suggests that inversions have been under both sexual and natural selection in Lake Malawi cichlids and that they will be important to understanding how this adaptive radiation evolved. 

ABSTRACT 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 generaMetriaclimaandLabeotropheus. 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.