Abstract
BackgroundThe age of unisexual salamanders of the genus Ambystoma is contentious. Recent and ancient evolutionary histories of unisexual Ambystoma were proposed by a few separate studies that constructed phylogenies using mitochondrial DNA markers (cytochrome b gene vs. non-coding region). In contrast to other studies showing that unisexual Ambystoma represent the most ancient unisexual vertebrates, a recent study by Robertson et al. suggests that this lineage has a very recent origin of less than 25,000 years ago.ResultsWe re-examined the phylogenetic relationship of the unisexuals to A. barbouri from various populations using both mitochondrial markers as well as the complete mitochondrial genomes of A. barbouri and a unisexual individual from Kentucky. Lineage dating was conducted using BEAST and MultiDivTime on a complete mitochondrial genome phylogeny. Our results support a monophyletic lineage for unisexual Ambystoma that shares its most recent common ancestor with an A. barbouri lineage from western Kentucky. In contrast to the Robertson et al.'s study, no A. barbouri individual shared an identical or almost identical cytochrome b haplotype with any unisexual. Molecular dating supports an early Pliocene origin for the unisexual linage (~5 million years ago). We propose that a unisexual-like cytochrome b numt (or pseudogene) exists in the controversial A. barbouri individuals from Kentucky, which was likely the cause of an erroneous phylogeny and time estimate in Robertson et al.'s study.ConclusionWe reject a recent origin of unisexual Ambystoma and provide strong evidence that unisexual Ambystoma are the most ancient unisexual vertebrates known to exist. The likely presence of an ancient cytochrome b numt in some Kentucky A. barbouri represents a molecular "fossil" reinforcing the hypothesis that these individuals are some of the closest extant relatives to unisexual Ambystoma.
Highlights
The age of unisexual salamanders of the genus Ambystoma is contentious
Using multiple sets of empirical evidence and rigorous statistical methodologies, we reject the conclusion of a recent origin of unisexual Ambystoma and support the hypothesis that unisexual Ambystoma is the most ancient lineage in unisexual vertebrates known to exist
The amplification of unisexual-like cyt-b sequence in a few Kentucky A. barbouri individuals is the possible cause of the erroneous phylogeny and time estimate determined by Robertson et al [19]
Summary
The age of unisexual salamanders of the genus Ambystoma is contentious. Recent and ancient evolutionary histories of unisexual Ambystoma were proposed by a few separate studies that constructed phylogenies using mitochondrial DNA markers (cytochrome b gene vs. non-coding region). Ancient unisexuals and asexuals that persist millions of years have been discovered in various taxa among plants, fungi and animals [2]. With recent advances in molecular genetics and phylogenetics, our knowledge of reproductive systems and evolutionary histories of many unisexual and asexual lineages has been quickly improved. Unisexuality in vertebrates has been discovered in about 90 lineages of fresh water fish, amphibians and reptiles [11], most of which are recently spun off from sexual relatives via interspecific hybridization [7,12]. Unisexual Ambystoma persist as a “parasitic entity” by stealing and incorporating sperm from sympatric sexual species via a complex reproductive mode, kleptogenesis, to generate nearly 30 genomic combinations or biotypes, with ploidy levels ranging from diploid to pentaploid [5,15]. Recent studies using genomic in situ hybridization (GISH) demonstrate complex intergenomic exchanges in unisexual populations [4,16,17,18]
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