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Abstract:
Chromosomal inversions play an important role in environmental adaptation, reproductive isolation, and sex determination in many organisms. However, there has been little evidence for their presence in large vertebrate adaptive radiations. Here we queried the genomes of 1,379 samples from the Malawi cichlid adaptive radiation for the presence of genomic regions with recombination-suppressed haplotypes. We discovered five such regions, each more than half a chromosome in length containing hundreds of genes. Different methods including cytogenetics, long reads (ONT), Hi-C, and linked reads (haplotagging) confirm the presence of chromosomal inversions in four of these regions. Inversion breakpoints are located within the long tracts of transposable elements. Inversion regions show distinct phylogenetic patterns and differ from the rest of the genome by the mode of selection, apparently contributing to species divergence. Inversion haplotypes originated early in the benthic Malawi cichlid radiation and persisted (evading loss/fixation) in different lineages with some instances of haplotype transfer between ecologically similar but genetically divergent groups. We present evidence that at least three of these inversions contribute to sex determination in some extant species, while other species have fixed one or the other haplotype, indicating repeated turnover of sex determination. We suggest that widespread presence of otherwise deleterious inversion is driven by the evolutionary requirement to maintain co-evolving loci (supergenes) in a species flock extremely prone to gene flow retention.
