Genome-specific histories of divergence and introgression between an allopolyploid unisexual salamander lineage and two sexual species

Abstract Quantifying genetic introgression between sexual species and polyploid lineages traditionally thought to be asexual is an important step in understanding what factors drive the longevity of putatively asexual groups. However, the presence of multiple distinct subgenomes within a single lineage provides a significant logistical challenge to evaluating the origin of genetic variation in most polyploids. Here, we capitalize on three recent innovations—variation generated from ultraconserved elements (UCEs), bioinformatic techniques for assessing variation in polyploids, and model-based methods for evaluating historical gene flow—to measure the extent and tempo of introgression over the evolutionary history of an allopolyploid lineage of all-female salamanders and two ancestral sexual species. We first analyzed variation from more than a thousand UCEs using a reference mapping method developed for polyploids to infer subgenome specific patterns of variation in the all-female lineage. We then used PHRAPL to choose between sets of historical models that reflected different patterns of introgression and divergence between the genomes of the parental species and the same genomes found within the polyploids. Our analyses support a scenario in which the genomes sampled in unisexuals salamanders were present in the lineage ∼3.4 million years ago, followed by an extended period of divergence from their parental species. Recent secondary introgression has occurred at different times between each sexual species and their representative genomes within the unisexuals during the last 500,000 years. Sustained introgression of sexual genomes into the unisexual lineage has been the defining characteristic of their reproductive mode, but this study provides the first evidence that unisexual genomes have also undergone long periods of divergence without introgression. Unlike other unisexual, sperm-dependent taxa in which introgression is rare, the alternating periods of divergence and introgression between unisexual salamanders and their sexual relatives could reveal the scenarios in which the influx of novel genomic material is favored and potentially explain why these salamanders are among the oldest described unisexual animals.