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The Prevalence of Genome Replacement in Unisexual Salamanders of the Genus Ambystoma (Amphibia, Caudata) Revealed by Nuclear Gene Genealogy

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The Prevalence of Genome Replacement in Unisexual Salamanders of the Genus Ambystoma (Amphibia, Caudata) Revealed by Nuclear Gene Genealogy

Ke Bi et al. BMC Evol Biol.

Abstract

Background: Unisexual 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.

Results: We 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.

Conclusion: Our 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.

Figures

Figure 1
Figure 1
Distribution of 97 sampling sites and geographic distribution of L-G1C12 haplotypes in unisexuals and Ambystoma laterale in northeastern North America (see Additional file 1 for description of locations and sample sizes). Numbers represent sampling sites where we collected specimens for this study. The shaded grey area shows the current known range of unisexual Ambystoma. Small map on the top corresponds to the boxed area on the large map. A-F represent six L-G1C12 haplotypes. Blue and green letters indicate populations where we only sampled unisexuals or A. laterale, respectively. Red letters indicate populations where both unisexual and A. laterale were found and they shared the same haplotypes. Multiple letters divided by slashes represent populations where more than one haplotype was found.
Figure 2
Figure 2
The variable sites of sequences of six haplotypes (A-F). Five indels and 14 informative variable nucleotide sites were identified. The deleted sties are highlighted as blue dashes.
Figure 3
Figure 3
Maximum parsimony tree (left) and TCS analysis (right) for six L-G1C12 haplotypes recovered from populations of Ambystoma laterale and unisexuals. For the MP tree, the outgroup species are A. jeffersonianum,A. texanum, and A. tigrinum. Taxa are haplotypes (A-F). Numbers above the branches represents numbers of mutations, and below depicts bootstrap values greater than 50. There is a distinct genetic break between clade I [A, B] and clade II [C, D, E, F]. For the TCS haplotype network, haplotypes A-F are represented by circles whose areas are proportional to the frequencies of the particular haplotype. The relative frequencies of unisexuals vs A. laterale partitioned in each particular haplotype are shown by different colors (green and pink respectively). Small and empty circles represent intermediate haplotypes that are not present in the samples but are necessary to link all observed haplotypes to the network. All haplotypes are separated from the nearest haplotype by one nucleotide difference. A distinct genetic break (13 transitional steps) between [A, B] and [C, D, E, F] is identified by TCS.

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