Article

Time and time again: Unisexual salamanders (genus Ambystoma) are the oldest unisexual vertebrates

Department of Integrative Biology, University of Guelph, Guelph, Ontario, Canada.
BMC Evolutionary Biology (Impact Factor: 3.37). 08/2010; 10(1):238. DOI: 10.1186/1471-2148-10-238
Source: PubMed

ABSTRACT

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). 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.
We 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 (approximately 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.
We 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.

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    • "However, Bi and Bogart[25]described intergenomic recombination blocks on chromosomes of Ambystoma hybrids composed of A. laterale and A. jeffersonianum parental species. Despite authors did not provide divergence time of these species, Robertson et al.[68]showed that their divergence in cyt b (~ 10%) is more than twice as large than between A. laterale and A. texanum (~ 4%), which diversified about 10 MYA[69]. Recombination can therefore occur between genomes of species that are even more diverged than Cobitis under study (~ 7 MYA). "
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    • "For example, LJJ would signify a triploid unisexual salamander that possesses 1 A. laterale and 2 A. jeffersonianum nuclear genomes and would be one 'genomotype' [Lowcock, 1994] of more than 20 [Bogart, 2003; Bogart et al., 2009] diploid, triploid (3n), tetraploid (4n), or even pentaploid (5n) nuclear genomic combinations that have so far been identified. All unisexual genomotypes have at least one L nuclear genome and very similar mitochondrial genomes that distinctly differ from mitochondrial sequences in all 5 species [Hedges et al., 1992; Bogart, 2003; Bi and Bogart, 2010a]. Unisexual salamanders normally outnumber individuals of the sympatric, bisexual species in this complex [Bogart and Klemens, 1997; 2008]. "
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