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.

Download full-text


Available from: Ke Bi,
  • Source
    • "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]. "
    [Show abstract] [Hide abstract]
    ABSTRACT: Polyploid animals have independently evolved from diploids in diverse taxa across the tree of life. We review a few polyploid animal species or biotypes where recently developed molecular and cytogenetic methods have significantly improved our understanding of their genetics, reproduction and evolution. Mitochondrial sequences that target the maternal ancestor of a polyploid show that polyploids may have single (e.g. unisexual salamanders in the genus Ambystoma) or multiple (e.g. parthenogenetic polyploid lizards in the genus Aspidoscelis) origins. Microsatellites are nuclear markers that can be used to analyze genetic recombinations, reproductive modes (e.g. Ambystoma) and recombination events (e.g. polyploid frogs such as Pelophylax esculentus). Hom(e)ologous chromosomes and rare intergenomic exchanges in allopolyploids have been distinguished by applying genome-specific fluorescent probes to chromosome spreads. Polyploids arise, and are maintained, through perturbations of the 'normal' meiotic program that would include pre-meiotic chromosome replication and genomic integrity of homologs. When possible, asexual, unisexual and bisexual polyploid species or biotypes interact with diploid relatives, and genes are passed from diploid to polyploid gene pools, which increase genetic diversity and ultimately evolutionary flexibility in the polyploid. When diploid relatives do not exist, polyploids can interact with another polyploid (e.g. species of African Clawed Frogs in the genus Xenopus). Some polyploid fish (e.g. salmonids) and frogs (Xenopus) represent independent lineages whose ancestors experienced whole genome duplication events. Some tetraploid frogs (P. esculentus) and fish (Squaliusalburnoides) may be in the process of becoming independent species, but diploid and triploid forms of these 'species' continue to genetically interact with the comparatively few tetraploid populations. Genetic and genomic interaction between polyploids and diploids is a complex and dynamic process that likely plays a crucial role for the evolution and persistence of polyploid animals. See also other articles in this themed issue.
    Cytogenetic and Genome Research 06/2013; 140(2-4). DOI:10.1159/000351593 · 1.56 Impact Factor
  • Source
    • "However, most of unisexual vertebrates, such as kleptogenetic Ambystoma salamanders (Bi and Bogart, 2010; Spolsky et al., 1992), hybridogenetic Poeciliopsis fish (Quattro et al., 1992), gynogenetic Amazon molly (Lampert and Schartl, 2008; Schartl et al., 1995), Phoxinus eosneogaeus hybrids (Angers and Schlosser, 2007), and gynogenetic Cobitis (Janko et al., 2003), have been revealed to have long history and large ranges of geographical distribution (Avise, 2008). And, high genetic diversity has been extensively observed in gynogenetic or hybridogenetic fish (Angers and Schlosser, 2007; Cunha et al., 2011; Schmidt et al., 2011; Stöck et al., 2012), kleptogenetic amphibians (Bi and Bogart, 2010) and parthenogenetic reptiles (Fujita et al., 2007; Kupriyanova, 2009). "
    [Show abstract] [Hide abstract]
    ABSTRACT: Carassius auratus complex is believed to originate from East Eurasia and consist of diploid and triploid forms. Diploid form reproduces sexually, whereas triploid form possesses mixture modes of unisexual gynogenesis and sexual reproduction, which makes it a unique case to study evolutionary issues among vertebrates. In this study, we identified 337 triploid individuals from 386 specimens of Carassius auratus complex sampled from 4 different sites of Xingkai Lake and Suifen River on the northeast Asia transboundary areas of Russia and China, and found that triploids were ubiquitous, whereas diploids existed only in SII site of Suifen River. Triploid males were detected in all surveyed sites, and an unusually high triploid male incidence (23%) was found in the Chinese reach of Suifen River. Then, nuclear and cytoplasmic markers were used to analyze their genetic diversity and phylogenetic relationship. A total of 61 distinct tf alleles and 35 mtDNA CR haplotypes were revealed. Higher genetic diversity and divergence were confirmed in triploids than in diploids, and identical genetic background between triploid males and females was demonstrated. Moreover, evolutionary implications and roles of triploid males were suggested in population proliferation and diversity creation of the triploid form.
    Molecular Phylogenetics and Evolution 10/2012; 66(1). DOI:10.1016/j.ympev.2012.10.006 · 3.92 Impact Factor
  • Source
    • "Thereby, the novel clone A+ was created by originally sexual mating between clone D female and clone A male, and rapidly multiplied up to several hundred millions by subsequent 7 generations of unisexual gynogenesis[8]. Here, we summarize formation process of the novel clone strain and attempt to identify the genetic organization and background by nuclear and cytoplasmic markers including chromosome number count, Cot-1 DNA fluorescent banding karyotype analysis, microsatellite electrophoretic pattern, AFLP profile, transferrin allele identification and mitochondrial genome sequence comparison, because most of them had been proven to be particularly valuable for clone discrimination, diversity evaluation and genealogical relationship analysis in several unisexual vertebrates, such as gynogenetic Amazon molly Poecilia formosa[23,24], gynogenetic Phoxinus eos-neogaeus[25], hybridogenetic Poeciliopsis[26-28], hybridogenetic water frog Rana esculenta [29], kleptogenetic salamanders[30-35], parthenogenetic lizards[36], and the gynogenetic gibel carp[19-22,37]. Based on these studies, we explore and discuss the significant implication for clonal diversity contribution. "
    [Show abstract] [Hide abstract]
    ABSTRACT: Unisexual vertebrates have been demonstrated to reproduce by gynogenesis, hybridogenesis, parthenogenesis, or kleptogenesis, however, it is uncertain how the reproduction mode contributes to the clonal diversity. Recently, polyploid gibel carp has been revealed to possess coexisting dual modes of unisexual gynogenesis and sexual reproduction and to have numerous various clones. Using sexual reproduction mating between clone D female and clone A male and subsequent 7 generation multiplying of unisexual gynogenesis, we have created a novel clone strain with more than several hundred millions of individuals. Here, we attempt to identify genetic background of the novel clone and to explore the significant implication for clonal diversity contribution. Several nuclear genome markers and one cytoplasmic marker, the mitochondrial genome sequence, were used to identify the genetic organization of the randomly sampled individuals from different generations of the novel clone. Chromosome number, Cot-1 repetitive DNA banded karyotype, microsatellite patterns, AFLP profiles and transferrin alleles uniformly indicated that nuclear genome of the novel clone is identical to that of clone A, and significantly different from that of clone D. However, the cytoplasmic marker, its complete mtDNA genome sequence, is same to that of clone D, and different from that of clone A. The present data indicate that the novel clone is a nucleo-cytoplasmic hybrid between the known clones A and D, because it originates from the offspring of gonochoristic sexual reproduction mating between clone D female and clone A male, and contains an entire nuclear genome from the paternal clone A and a mtDNA genome (cytoplasm) from the maternal clone D. It is suggested to arise via androgenesis by a mechanism of ploidy doubling of clone A sperm in clone D ooplasm through inhibiting the first mitotic division. Significantly, the selected nucleo-cytoplasmic hybrid female still maintains its gynogenetic ability. Based on the present and previous findings, we discuss the association of rapid genetic changes and high genetic diversity with various ploidy levels and multiple reproduction modes in several unisexual and sexual complexes of vertebrates and even other invertebrates.
    BMC Research Notes 03/2011; 4(1):82. DOI:10.1186/1756-0500-4-82
Show more