Precise paternal ancestry of hybrid unisexual ZW lizards (genus Darevskia: Lacertidae: Squamata) revealed by Z-linked genomic markers

Abstract

We genotyped multiple populations of all seven parthenogenetic species of rock lizards, genus Darevskia, as well as their putative sexual parental populations, using double digest RAD-sequencing genomic markers. Taking advantage of the conserved homology of the ZW/ZZ sex chromosomes among lacertid lizards, we aligned our short sequence reads to a reference Z chromosome assembly of the common wall lizard Podarcis muralis. This provided unique insight into the origin of all-female hybrid populations, which inherited their single Z chromosome exclusively from a paternal ancestor. The mapped Z-linked loci were used to construct a robust time-calibrated phylogeny. In each parent–offspring species pair, the geographically nearest population of the paternal species was identified as the most likely ancestor of the respective parthenogen, mirroring the trend observed previously on the maternal side in mitochondrial DNA. The estimated splits between the sampled paternal sexual ancestors and their daughter species occurred much earlier than suggested previously and during two narrow time periods: (1) the parthenogenetic Darevskia armeniaca, D. dahli, D. uzzelli and D. rostombekowi dated back to ~0.5 or ~0.9 Mya, depending on the calibration point used, while (2) D. bendimahiensis, D. sapphirina and D. unisexualis appear to have diverged ~1 or ~2 Mya.