Unbalanced segmental duplication of W chromosomes in Australian Ridge-tailed goannas

Abstract

Sex chromosomes are mostly conserved, but in some cases are variable within species. Varanids are known for conserved sex chromosomes, but there are differences in the size of the W chromosome among species representing varying stages of sex chromosome evolution. We tested for homology of the ZW sex chromosome system in varanids with size differences among four species from two lineages in Australia, the dwarf lineage Odatria and the sand goanna lineage Gouldii, with a combined genomic and cytogenetic approach. We found that while DNA sequences of the sex chromosomes are conserved, a mutation on an enlarged autosomal microchromosome is homologous with the W in some isolated populations of V. acanthurus and V. citrinus from the Odatria lineage. The enlarged microchromosome was unpaired in all individuals tested and is likely an unbalanced segmental duplication translocated from the W to another microchromosome. We also found evidence of an ancient balanced duplication that is also homologous to the W and to the telomeric region of chromosome 2. We conclude the most parsimonious explanation is that the duplicated region likely originated on chromosome 2. We also demonstrated that genes and related DNA sequences have likely originated on an autosome, translocated to the W, accumulated repeats and amplified on the W and then duplicated and translocated to another autosomal microchromosome. Given the role of these duplications as important evolutionary drivers of speciation in other taxa, our findings provide broader insight into the evolutionary pathway leading to rapid chromosomal and genic divergence of species.