Ancestral chromosome-level assemblies reveal posthybridization genome evolution in the New Mexico whiptail lizard (Aspidoscelis neomexicanus)

Abstract

Unisexual species of whiptail lizards in the genus Aspidoscelis arose by interspecific hybridization. They reproduce clonally through parthenogenesis and are thought to maintain the fixed heterozygosity that resulted from their hybrid origin by avoiding recombination between homeologous chromosomes. In the absence of chromosome-level assemblies for the sexual progenitor species, questions relating to the long-term consequences of clonal reproduction have remained largely unanswered. Here, we present chromosome-level genome assemblies for A. marmoratus and A. arizonae, the parental species of the unisexual A. neomexicanus. Using these references, we have analyzed whole-genome sequencing data from both wild and laboratory-reared A. neomexicanus individuals as well as newly generated F1 hybrids. Our analysis identified population-specific losses of heterozygosity affecting multiple syntenic chromosome pairs, demonstrating that homeologous chromosome pairing and recombination must occur at a low frequency and contribute to genome erosion in these unisexual lineages. The loss of heterozygosity patterns we observed further suggest that the genomes of unisexual lineages diverge over time more quickly than anticipated based on mutation accumulation alone. Our results establish genomic resources for Aspidoscelis and provide new insights into how genome structure can evolve in the absence of sexual reproduction.