The prevalence of genome replacement in unisexual salamanders of the genus Ambystoma (Amphibia, Caudata) revealed by nuclear gene genealogy.

Abstract

BackgroundUnisexual salamanders of the genus Ambystoma exemplify the most ancient lineage of unisexual vertebrates and demonstrate an extremely flexible reproductive system. Unisexual Ambystoma interact with and incorporate genomes from two to four sexual species (A. laterale, A. jeffersonianum,A. texanum, and A. tigrinum), to generate more than 20 genome compositions or biotypes. Unisexual ploidy levels range from diploid to pentaploid, but all contain at least one A. laterale (L) genome. Replacement of nuclear genomes might be responsible for the evolutionary longevity of unisexual Ambystoma but direct evidence for the prevalence of genome replacement in natural populations is absent. Two major puzzling questions have remained unanswered over the last few decades: 1) is genome replacement a common reproductive method in various unisexual populations and, 2) is there an ancient "L" genome that persists in various unisexual genome compositions.ResultsWe examined 194 unisexual and 89 A. laterale specimens from 97 localities throughout their range and constructed a genealogy of the "L" genomes using a nuclear DNA marker (L-G1C12) to answer the above questions. Six L-G1C12 haplotypes (A-F) were shared by individuals in various A. laterale and unisexual populations. The general geographical distribution of the haplotypes in unisexual populations conformed to those found in A. laterale, indicating that "L" genomes in unisexuals are obtained from sympatric or nearby populations of A. laterale.ConclusionOur data demonstrate that genome replacement frequently occurs in unisexual Ambystoma across their range, and support previous speculations that genome replacement is an important reproductive mechanism that can enhance their evolutionary longevity. Our results show that there is no ancient "L" genome in the unisexual lineages, and no particular "L" genome is favored in any unisexual individual. The presence of an "L" genome in all unisexuals implies that it is important to the maintenance of unisexuals. Nuclear gene genealogy is a powerful tool to examine the historical interaction between sperm-dependent unisexuals and their sexual sperm donors. This methodology could be applicable to many other unisexual lineages to improve our understanding of their reproduction and their ability to persist.