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


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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    ABSTRACT: Interspecific hybridization, polyploidization and transitions from sexuality to asexuality considerably affect organismal genomes. Especially the last mentioned process has been assumed to play a significant role in the initiation of chromosomal rearrangements, causing increased rates of karyotype evolution. We used cytogenetic analysis and molecular dating of cladogenetic events to compare the rate of changes of chromosome morphology and karyotype in asexually and sexually reproducing counterparts in European spined loach fish (Cobitis). We studied metaphases of three sexually reproducing species and their diploid and polyploid hybrid clones of different age of origin. The material includes artificial F1 hybrid strains, representatives of lineage originated in Holocene epoch, and also individuals of an oldest known age to date (roughly 0.37 MYA). Thereafter we applied GISH technique as a marker to differentiate parental chromosomal sets in hybrids. Although the sexual species accumulated remarkable chromosomal rearrangements after their speciation, we observed no differences in chromosome numbers and/or morphology among karyotypes of asexual hybrids. These hybrids possess chromosome sets originating from respective parental species with no cytogenetically detectable recombinations, suggesting their integrity even in a long term. The switch to asexual reproduction thus did not provoke any significant acceleration of the rate of chromosomal evolution in Cobitis. Asexual animals described in other case studies reproduce ameiotically, while Cobitis hybrids described here produce eggs likely through modified meiosis. Therefore, our findings indicate that the effect of asexuality on the rate of chromosomal change may be context-dependent rather than universal and related to particular type of asexual reproduction.
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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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    • "divergent lineages in the mtDNA gene tree (Shaffer and McKnight, 1996), and all diploid sexual species outside this clade. The Ambystomatidae also contains a complex of unisexual populations with a complicated evolutionary history (Bi and Bogart, 2010), and representatives from this group were not included in this study. To root the Ambystoma tree, 1–2 samples were included from all four extant Dicamptodon species (seven total individuals). "
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    ABSTRACT: The analysis of diverse data sets can yield different phylogenetic estimates that challenge systematists to explain the source of discordance. The mole salamanders (family Ambystomatidae) are a classic example of this phylogenetic conflict. Previous attempts to resolve the ambystomatid species tree using allozymic, morphological, and mitochondrial sequence data have yielded different estimates, making it unclear which data source best approximates ambystomatid phylogeny and which ones yield phylogenetically inaccurate reconstructions. To shed light on this conflict, we present the first multi-locus DNA sequence-based phylogenetic study of the Ambystomatidae. We utilized a range of analyses, including coalescent-based methods of species-tree estimation that account for incomplete lineage sorting within a locus and concordance-based methods that estimate the number of sampled loci that support a particular clade. We repeated these analyses with the removal of individual loci to determine if any a locus has a disproportionate effect on our phylogenetic results. Collectively, these results robustly resolved many deep and relatively shallow clades within Ambystoma, including the placement of A. gracile and A. talpoideum as the sister clade to a clade containing all remaining ambystomatids, and the placement of A. maculatum as the sister lineage to all remaining ambystomatids excluding A. gracile and A. talpoideum. Both Bayesian coalescent and concordance methods produced similar results, highlighting strongly supported branches in the species tree. Furthermore, coalescent-based analyses that excluded loci produced overlapping species-tree posterior distributions, suggesting that no particular locus - including mtDNA - disproportionately contributed to our species-tree estimates. Overall, our phylogenetic estimates have greater similarity with previous allozyme and mitochondrial sequence-based phylogenetic estimates. However, intermediate depths of divergence in the ambystomatid species tree remain unresolved, potentially highlighting a region of rapid species radiation or a hard polytomy, and which limits our ability to comment on previous morphologically-based taxonomic groups.
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