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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. 

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 African cichlid fishes are known for their high rates of phenotypic evolution. A rapid rate of diversification is apparent also in the diversity of their sex chromosomes. To date, sex determiners have been identified on 18 of 22 chromosomes in the standard karyotype. Here, we use whole-genome sequencing to characterize the sex chromosomes of seven populations of basal haplochromines, focusing on the genus Pseudocrenilabrus. We identify six new sex chromosome systems, including the first report of a cichlid sex–determining system on linkage group 12. We then quantify the rates and patterns of sex chromosome turnover in this clade. Finally, we test whether some autosomes become sex chromosomes in East African cichlids more often than expected by chance. 

Abstract BackgroundAfrican cichlid fishes are well known for their rapid radiations and are a model system for studying evolutionary processes. Here we compare multiple, high-quality, chromosome-scale genome assemblies to elucidate the genetic mechanisms underlying cichlid diversification and study how genome structure evolves in rapidly radiating lineages. ResultsWe re-anchored our recent assembly of the Nile tilapia (Oreochromis niloticus) genome using a new high-density genetic map. We also developed a new de novo genome assembly of the Lake Malawi cichlid, Metriaclima zebra, using high-coverage Pacific Biosciences sequencing, and anchored contigs to linkage groups (LGs) using 4 different genetic maps. These new anchored assemblies allow the first chromosome-scale comparisons of African cichlid genomes. Large intra-chromosomal structural differences (~2–28 megabase pairs) among species are common, while inter-chromosomal differences are rare (<10 megabase pairs total). Placement of the centromeres within the chromosome-scale assemblies identifies large structural differences that explain many of the karyotype differences among species. Structural differences are also associated with unique patterns of recombination on sex chromosomes. Structural differences on LG9, LG11, and LG20 are associated with reduced recombination, indicative of inversions between the rock- and sand-dwelling clades of Lake Malawi cichlids. M. zebra has a larger number of recent transposable element insertions compared with O. niloticus, suggesting that several transposable element families have a higher rate of insertion in the haplochromine cichlid lineage. ConclusionThis study identifies novel structural variation among East African cichlid genomes and provides a new set of genomic resources to support research on the mechanisms driving cichlid adaptation and speciation. 

Abstract Recent studies have revealed an astonishing diversity of sex chromosomes in many vertebrate lineages, prompting questions about the mechanisms of sex chromosome turnover. While there is considerable population genetic theory about the evolutionary forces promoting sex chromosome replacement, this theory has not yet been integrated with our understanding of the molecular and developmental genetics of sex determination. Here, we review recent data to examine four questions about how the structure of gene networks influences the evolution of sex determination. We argue that patterns of epistasis, arising from the structure of genetic networks, may play an important role in regulating the rates and patterns of sex chromosome replacement. 

Abstract African cichlid fishes are a prime model for studying speciation mechanisms. Despite the development of extensive genomic resources, it has been difficult to determine which sources of genetic variation are responsible for cichlid phenotypic variation. One of their most variable phenotypes is visual sensitivity, with some of the largest spectral shifts among vertebrates. These shifts arise primarily from differential expression of seven cone opsin genes. By mapping expression quantitative trait loci (eQTL) in intergeneric crosses of Lake Malawi cichlids, we previously identified four causative genetic variants that correspond to indels in the promoters of either key transcription factors or an opsin gene. In this comprehensive study, we show that these indels are the result of the movement of transposable elements (TEs) that correlate with opsin expression variation across the Malawi flock. In tracking the evolutionary history of these particular indels, we found they are endemic to Lake Malawi, suggesting that these TEs are recently active and are segregating within the Malawi cichlid lineage. However, an independent indel has arisen at a similar genomic location in one locus outside of the Malawi flock. The convergence in TE movement suggests these loci are primed for TE insertion and subsequent deletions. Increased TE mobility may be associated with interspecific hybridization, which disrupts mechanisms of TE suppression. This might provide a link between cichlid hybridization and accelerated regulatory variation. Overall, our study suggests that TEs may be an important driver of key regulatory changes, facilitating rapid phenotypic change and possibly speciation in African cichlids. 

Advances in genome sequencing have greatly accelerated the identification of sex chromosomes in a variety of species. Many of these species have experienced structural rearrangements that reduce recombination between the sex chromosomes, allowing the accumulation of sequence differences over many megabases. Identification of the genes that are responsible for sex determination within these sometimes large regions has proved difficult. Here, we identify an XY sex chromosome system on LG19 in the West African cichlid fishChromidotilapia guntheriin which the region of differentiation extends over less than 400 kb. We develop high-quality male and female genome assemblies for this species, which confirm the absence of structural variants, and which facilitate the annotation of genes in the region. The peak of differentiation lies withinrin3, which has experienced several debilitating mutations on the Y chromosome. We suggest two hypotheses about how these mutations might disrupt endocytosis, leading to Mendelian effects on sexual development.