Extreme genetic divergence indicated by chromosome rearrangements

Abstract

Chromosomal rearrangements are often associated with local adaptation and speciation because they suppress recombination, and as a result, rearrangements have been implicated in disrupting geneflow. Although there is strong evidence to suggest that chromosome rearrangements are a factor in genetic isolation of divergent populations, the underlying mechanism remains elusive. Here we applied an integrative cytogenetics and genomics approach testing whether chromosomal rearrangements are the initial process, or a consequence, of population divergence in the dwarf goanna, Varanus acanthurus. Specifically, we tested whether chromosome rearrangements are indicators of genetic barriers that can be used to identify divergent populations by looking at geneflow within and between populations with rearrangements. We found that geneflow was present between individuals with chromosome rearrangements within populations, but there was no geneflow between populations that had similar chromosome rearrangements. Moreover, we identified a correlation between reduced genetic variation in populations with a higher frequency of homozygous submetacentric individuals. These findings suggest that chromosomal rearrangements were widespread prior to divergence and because we found populations with higher frequencies of submetacentric chromosomes were associated with lower genetic diversity, this could indicate that polymorphisms within populations are early indicators of genetic drift.

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

“…In V. citrinus we identi ed one female had an enlarged W chromosome that was partially homologous with the enlarged unpaired microchromosome (Fig. 2), and this was mistaken as an enlarged pair in a previous study (Dobry et al 2022) and the other two females had homomorphic sex chromosomes where the W chromosome was similar in size to the Z (Fig. 2a).…”

“…FISH experiments with our chromosome-speci c probes were required to differentiate the sex chromosomes in individuals with cryptic sex chromosomes and to identify the Z chromosome from other microchromosomes. In one individual V. citrinus female, the W chromosomes and the enlarged microchromosome were considered to be an enlarged pair of autosomal microchromosomes because all other females in that population had cryptic sex chromosomes that were indistinguishable from the Z and other microchromosomes (Dobry et al 2022).…”

“…The Varanidae have been proposed to have the oldest conserved ZW sex chromosomes of all vertebrates known to date (Iannucci et al 2019;. Despite this, there are size differences of the W chromosome among closely related species and recently identi ed within a newly described species V. citrinus (formerly V. acanthurus (Pavón-vázquez et al 2022)) where the sex chromosomes are cryptic (Dobry et al 2022). These size differences are likely a result of different rates of evolution of the independent expansion of transposable elements during sex chromosome evolution, and the involved repeat sequences within the sex chromosomes not being conserved between species (Matsubara et al 2014;Pokorná et al 2016).…”

“…citrinus, but it has not been observed in any other goanna species. It was rst reported by Matsubara and colleagues (2014) from a captive bred lineage, but was not identi ed in wild populations until recently(Dobry et al 2022). During our initial cytogenetic analysis, this enlarged microchromosome was mistaken for a W chromosome in individuals that upon dissection were determined to be a males.…”