Conserved gene content and unique phylogenetic history characterize the ‘bloopergene’ underlyingTriturus’balanced lethal system

Abstract

In a balanced lethal system, half of the reproductive output always succumbs. A clear example is observed in Triturus newts, which contain two distinct versions of chromosome 1. Developmental arrest occurs in Triturus embryos with two copies of the same chromosome 1 version, but not in those that possess two different versions, suggesting that each version carries something uniquely vital. We use a target capture approach to investigate over 7,000 nuclear DNA markers across the genus Triturus. We sequence the same markers for all the main lineages of the Salamandridae family (to which Triturus belongs) to explore the evolutionary history of chromosome 1 versus other chromosomes. We discover dozens of genes that are completely missing from either one or the other version of chromosome 1. We also show that the gene content of 1A and 1B is remarkably similar across all Triturus species, as both chromosome versions have a unique, but consistent set of deleted genes. This suggests that the balanced lethal system evolved rapidly and reached its current form before the radiation of Triturus. The tree topology of Triturus chromosome 1 distinctly differs from the rest of the genome. We attribute this to pervasive, ancient hybridization between the ancestor of Triturus and other modern European newt lineages. Our findings accentuate the intriguingly complex nature of Triturus chromosome 1: the "bloopergene" driving the evolutionarily enigmatic balanced lethal system.