Journal of Heredity Advance Access published online on July 19, 2007
Journal of Heredity, doi:10.1093/jhered/esm038
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Evidence for Multiple Retroposition Events and Gene Evolution in the ADP/ATP Translocase Gene Family in Ranid Frogs
From the Ecological Genetics Research Unit, Department of Biological and Environmental Sciences, PO Box 65 (Biocenter 3, Viikinkaari 1), FI-00014 University of Helsinki, Finland (Matsuba, Palo, and Merilä); and the Institute of Ecology and Evolution, Russian Academy of Sciences, Leninsky Prospect, 33, Moscow, 119071, Russia (Kuzmin)
Address correspondence to Chikako Matsuba at the address above, or e-mail: chikako.matsuba{at}helsinki.fi.
Analysis of partial ADP/ATP Translocase gene (Aat) sequences from 11 species of Ranid frogs (Amphibia: Ranidae) identified multiple Aat gene copies. All frog species examined had at least one of the 2 Aat gene copies differing mainly by presence or absence of an approximately 85-bp intron sequence. The sequence data suggest that the gene variant with intron is the ancestral Aat form, whereas the other variants are retroposed copies. Surprisingly, a phylogenetic analysis suggests that multiple reptroposition events have taken place in the Ranid frogs. An analysis including sequences from Drosophila, zebra fish, Xenopus, mouse, and human indicated that all the frog Aat sequences form a monophyletic group with mammalian X-chromosomal Ant2 as a sister unit. Furthermore, the selection test suggested that different variants of the Aat gene appear to have evolved under different modes of evolution (viz., neutral, purifying, and positive selection), and the evolutionary history of different AAT variants appears to differ even among different species.
In general, duplication by unequal crossing over and duplication of a chromosome or an entire genome (polyploidization) are considered to be the most important mechanisms for generating new genes (Ohno 1970; Kimura and Ohta 1974). As information from model organisms has increased, retroposition has also been found to have a role as a general genomic process creating new genes (Brosius 2003; Long et al. 2003). In nonviral retroposition, segments of mRNA are converted to DNA and subsequently inserted in the genome (Weiner et al. 1986). This can occur with the aid of original viral enzymes, such as RNA polymerase, reverse transcriptase, and transposase (Lodish et al. 1995). Although the exact mechanism is still unknown, a nonviral retroposed sequence in eukaryotes is identifiable by its intronless structure, and by the presence of a polyadenylation signal and of a poly-A sequence downstream of 3'-terminal (Weiner et al. 1986; Weiner 2002).
The fate of the retroposed element originating from a processed mRNA is largely determined by the position of insertion. Genomic analyses of retroposed genes, for example jingwei (Long and Langley 1993) and Sphinx (Wang et al. 2002) in Drosophila and phosphoglycerate mutase (PGAM)3 in primates (Betan et al. 2002), suggest that these retroposed elements have shared a regulatory region with the recipient gene that has enabled expression in the new position. This is most likely a rare event, but when found, these young genes provide good models for studying the evolution of new gene functions (Long and Langley 1993).
The ADP/ATP translocase (AAT), also known as the adenine nucleotide translocase (ANT) or ADP/ATP carrier, has an important role in the ADP and ATP transport on the inner mitochondrial membrane and in forming the mitochondrial permeability transition pore (Kokoszka et al. 2004). Thus, the structure is very conserved and most likely present in all eukaryotes (Santamaria et al. 2004). However, the Aat gene is known to exist as multiple copies in most species; in mammals, humans have 3 isoforms Ant1, Ant2, and Ant3, whereas only 2 isoforms have been characterized in rodents (Ant1, Ant2) and bovids (Ant1, Ant3). Sequence lengths of human Ant1, Ant2, and Ant3 are 4.2, 5.9, and 5.9 kb, respectively (Cozens et al. 1989; Schiebel et al. 1993), all comprising of 4 exons. Mammalian Ant1 and Aat2/Ant3 genes are known to have spread on autosomal and X chromosome by gene duplication but have retained similar gene structure at the intron site (Cozens et al. 1989; Schiebel et al. 1993; Dietzel et al. 1999). In amphibians, only cDNA sequences are described from 3 species, Xenopus laevis (in GenBank, AF231347), Rana sylvatica (Cai et al. 1997), and Rana rugosa (Miura et al. 1998), but gene structure or isoform information has not yet been described. All these Aat isoforms cluster together with the mammalian Ant2/Ant3 complex (Santamaria et al. 2004).
Cai et al. (1997) found that Aat had differential expression patterns in liver tissue under freezing stress in the wood frog, suggesting a role in adaptation to suboptimal temperatures (see also Roussel et al. 2000). In fact, the expression and function of Aat in many organisms are altered by stressful conditions (e.g., Yan and Sohal 1998; De Santis et al. 1999; Zhang et al. 1999; Talbot et al. 2004).
In this paper, we report multiple gene copies of Aat from several frog species, some of them apparently functional, and consider the possibility of the retroposal origin of these variants. A phylogenetic analysis was conducted on partial Aat sequences from 11 species of Ranid frogs to estimate the number and time of the duplication events. To further study the evolution of these genes after the multiplication events, we analyzed the numbers of synonymous and nonsynonymous nucleotide substitutions in the total sequence, and at each amino acid site.
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Materials and Methods |
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Frog Samples and DNA Extraction
Thirteen individuals from 11 Ranid frog species were analyzed (Table 1). Five species (Rana grylio, Rana palustris, Rana pipiens, Rana septentrionalis, and R. sylvatica) originated from North America. Rana nigromaculata came from Japan, Rana amurensis and Rana dybowskii from the continental Far East, Rana arvalis and Rana dalmatina were collected from Western Europe. Two Rana temporaria individuals originated from Eastern Europe and one from Western Europe. DNA was extracted by salt extraction method (e.g., Bruford et al. 1992) from a muscle or toe tissue that was treated overnight at 60 °C in the extraction buffer (0.18 mM ethylenediaminetetraacetic acid, 0.9 mM Tris–HCl, 36 mM NaCl, 1.8% sodium dodecyl sulfate) containing 0.4 mg/µl Proteinase K. After purification with 6 M NaCl and isopropanol precipitation, DNA was suspended in water.
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PCR Amplification and Sequencing
The Aat was PCR amplified using primers AAT-F1 (5'-GACTGCGTTGTCCGTATCCC-3') and AAT-R4 (5'-ACGACGGACTGTGTCAAATGGG-3'). These universal primers were designed based on the Aat cDNA sequences of R. sylvatica (U44832) and R. rugosa (AB008456, AB008461, AB008462, AB008457, AB008459, AB008458) deposited in the GenBank. PCR reactions (35 cycles) were performed in a total volume of 20 µl, with approximately 20 ng of template DNA, 5 pmol each primer, 0.25 U BioTaq DNA polymerase (BIOLINE, London, UK), 1x reaction buffer (BIOLINE), 1.5 mM MgCl2, and 250 µM of each nucleotide (Amersham Biosciences, Sunnyvale, CA). Each cycle consisted of a denaturing step at 94 °C for 1 min, an annealing step at 53 °C for 30 s, and an extension step at 72 °C for 1 min. For R. sylvatica, R. nigromaculata, and R. amurensis an annealing temperature of 50 °C was used. Amplified fragments were cloned to pGEM-T Easy vector (Promega, Madison, WI) according to the manufacturer's instructions. Inserts were amplified using T7 and SP6 primers, and the lengths of the amplified inserts were checked on EtBr-stained 1% agarose gels. The amplified fragments were then sequenced from both ends with the T7 and SP6 primers using BigDye chemistry (Perkin-Elmer Applied Biosystems, Foster City, CA). The sequences were resolved on ABI377 automatic sequencer (Perkin-Elmer Applied Biosystems). In order to minimize polymerase errors, multiple clones (
3) were sequenced from each individual. The sequences were edited using Sequencher 4.1 software (Gene Codes Corporation, Ann Arbor, MI).
Phylogenetic Analysis
Aat sequences from vertebrates (human, mouse, zebra fish, and frogs) and Drosophila were aligned using CLUSTALW program (Thomopson et al.1994). The sequences were compared with the intron sequences by eye and by the BLASTN program, and the open reading frames were translated into amino acid sequences using program MEGA version 2.1 (Kumar et al. 2001; http://www.megasoftware.net/). Based on the presence/absence of the intron sequence and an open reading frame, the observed haplotypes were classified into 3 different groups, 2 of which comprised of protein coding and 1 group of pseudogene sequences (see Results).
The homogeneity of base frequencies across taxa was tested using PAUP*4b10 (Swofford 2002). Maximum likelihood (ML) tree was searched for the protein coding sequences (introns removed) obtained from the Ranid frogs, both for total data (501 bp) and for third position sites (166 bp). Xenopus Ant1 sequence was included as an out-group. Heuristic tree searches were performed using PAUP*4b10, with the taxon input order randomized 50 times. In order to assess different a priori phylogenetic hypotheses, especially the number of the putative transposition events, likelihood scores under alternative constrained tree topologies were evaluated using the likelihood ratio test (LRT).
In addition, a separate ML tree was searched for a data set including Aat sequence from one frog species (R. arvalis) as well as from Drosophila (498 bp), zebra fish, human, and mouse. Both Ant1 and Ant2 sequences observed in the mammals were included. In all ML analyses, substitution models suggested by hierarchical LRTs implemented in the program MODELTEST 3.06 (Posada and Crandall 1998) were assumed. Branch support was obtained by bootstrapping (100 replicates).
Statistical Analysis
The number of synonymous and nonsynonymous substitutions (Nei 1987) was estimated on different Aat sequence groups by program DNASP version 3.99 (Rozas J and Rozas R 1999; http://www.ub.es/dnasp/). The nucleotide diversities for 498-bp coding sequences were analyzed with a 30-bp window sliding forward each 5 bp (Figure 3). To test for the positive or negative selection at single amino acid sites over the sequence, the Suzuki and Gojobori (1999) method as implemented in the DATAMONKEY program (Kosakovsky-Pond and Frost 2004; http://www.datamonkey.org) was used.
Pairwise sequence comparisons of A and B types (see Results) within species for potentially synonymous and nonsynonymous distances, pS and pN, respectively, and the differences (Dp = pS – pN; Figure 4) were estimated in the program MEGA 2.1 using the modified Nei and Gojobori method (1986) with observed transition/transversion rate (ti/tv) (R = 2.0). Standard errors were obtained by bootstrapping (500 replications). Possibility of selection for different genes within species was tested using Fisher's exact tests on pairwise comparisons among sequences (Zhang et al. 1997).
In addition, a ML estimation of 
(dN/dS) ratios was performed for lineages suggested to be under positive selection by the pairwise comparisons by CODEML program of PAML (Yang 1997; http://abacus.gene.ucl.ac.uk/software/paml.html). Two-codon substitution models (Goldman and Yang 1997) were implemented: one ratio model (assuming the same for all branches) and free ratio model (allowing variable value among branches; supplementary material). In the latter analysis, an ancestral sequence is reconstructed for each node of the phylogenetic tree; the value is then estimated for each branch between the assumed ancestral and the given sequence. The performance of these 2 models was compared using the LRT, with N degrees of freedom (df) (N = number of branches on phylogeny).
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Haplotyping
From the 13 individuals representing 11 frog species, 48 Aat haplotypes were found. These Aat sequences have been deposited in GenBank with accession numbers AY947763–AY947811 (Table 1).
The sequences were classified into 3 types (Figure 1) on the basis of their sequence characteristics: 1) sequences containing an open reading frame with an intron (Aat-A, n = 14), 2) intronless sequences having an open reading frame (Aat-B, n = 13), and 3) pseudogene sequences containing a stop codon or a frameshift (Aat-C, n = 21). Because it was impossible to deduce whether the differing intraspecific sequences of one type were alleles of the same gene or copies from another locus, those sequences were given distinct names (e.g., A1 and A2 in R. palustris, or B1 and B2 in R. pipiens) and were treated separately in the subsequent analyses (Table 1).
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The Aat-A type sequences had a 79- to 89-bp intron region at the same position as that of the other vertebrates included, and were encountered in every species assessed (Table 1). Two sequences, differing by 2 synonymous substitutions, were encountered from R. palustris. The deduced Ranid Aat-A amino acid sequences were on the average 78.4%, 93.1%, and 89.9% similar to the published Drosophila, zebra fish, and mammal sequences, respectively.
Intronless Aat-B sequences were found in all Ranid species, excluding R. temporaria and R. dalmatina (Table 1). These sequences contained an open reading frame; the similarity with the previously published Drosophila and vertebrate amino acid sequences was of the same magnitude as with Aat-A (76.7%, 91.1%, 88.5%). Two different Aat-B sequences were encountered in R. pipiens, R. sylvatica, and R. grylio and 3 from R. dybowskii (Table 1). Excluding the sequences from R. grylio (one synonymous substitution), these were highly divergent variants containing 2–19 nucleotide substitutions leading to 2–13 amino acid substitutions within the Aat-B group.
In addition to Aat-A and Aat-B, Aat-C sequences of widely differing lengths were isolated from 10 species (Table 1). The Aat-C sequences were highly divergent, containing numerous deletions and insertions, some of which exceeded 100 bp. Reliable alignment of the Aat-C sequences proved impossible and they were therefore excluded from the phylogenetic analyses.
Phylogenetic Relationships
Assuming the suggested nucleotide substitution model for the frog data set (TrN-
, with shape parameter 
= 0.326; Tamura and Nei 1993), the average sequence divergence within the coding regions of Aat-A and Aat-B haplotypes were 3.05 ± 0.54% and 4.49 ± 0.64%, respectively, and 3.77 ± 0.56% between these haplotype groups. Within each species, the average divergence between Aat-A and Aat-B variants was 1.3%.
There were no significant differences in the base composition between taxa (
2 = 11.257, df = 108, P = 1.00). In the best ML tree (–lnL = 1813.49) the frog Aat-A and Aat-B sequences formed a well-supported monophyletic group with Xenopus Ant1 as a basal unit (Figure 2). This clade appears to be a sister clade to mammalian Ant2 sequences (Figure 2a).
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In each species, the Aat-A and Aat-B sequences cluster together, suggesting that the retrotransposition of Aat-B type sequences has occurred multiple times. This topology is well supported: forcing the Aat-A and Aat-B into 2 monophyletic groups resulted in a significantly worse ML-tree topology (–lnL = 2021.33 vs. –lnL =1813.49, df = 35, P < 0.001). Furthermore, a phylogenetic analysis based on the presumably neutral third position sites (model: HKY85-
, with = 0.556, ti/tv = 2.9678 and nucleotide frequencies A: 0.1902, C: 0.3538, G: 0.1475, T: 3085; Hasegawa et al. 1985) had a congruent topology significantly better than the tree found under monophyly constraint (unconstrained tree –lnL = 874.39 vs. constrained tree –lnL = 1016.58, df = 35, P < 0.001). The ML tree, rooted with Xenopus sequence, revealed geographical structuring of sequence-variation grouping Japanese, North American, and Eurasian Species loosely together (Figure 2b). In this tree, the Japanese and North American species appear as basal to the Eurasian ones (Figure 2b).
Divergence within the Aat-A and Aat-B Groups among Species
The pattern of synonymous substitution rates (
(s)) in sliding window plot was similar within Aat-A and Aat-B groups (Figure 3e,f). However, there were substantial differences in nonsynonymous substitution rates ((n)) between Aat-A and Aat-B sequence groups (Figure 3c,d). Within the Aat-A group, the (n) divergence was zero in 3 areas corresponding to 3 hydrophobic regions (Figure 3a; II–IV) that have been proposed to fold into transmembrane alpha-helices (Saraste and Walker 1982). In contrast, within the Aat-B group, (n) peaks were distributed along the whole sequence, and the average (n) = 0.0221 was 2 times higher than that of within the Aat-A group ((n) = 0.0091; Figure 3c,d).
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Selection at Single Amino Acid Sites within Each Group
Normalized dS–dN values were calculated separately for every amino acid site within each sequence group (cf. A or B type). Nine negatively selected sites were detected among all sequences, 8 in the Aat-A group and 4 in the Aat-B group (Figure 3). Of these, 8 sites conformed to the hydrophobic region, supposedly folded into transmembrane alpha-helices (Saraste and Walker 1982). However, positive selection was not detected in the Aat-A sequence group (P < 0.05 in all cases). In the Aat-B group, one positively selected site was identified at P = 0.05 significance level (Figure 3).
Difference between Synonymous and Nonsynonymous Distance in Pairwise Comparisons
Pairwise comparisons recovered evidence for positive selection on Aat in 3 frog species by the difference between synonymous and nonsynonymous distances (Dp = pS – pN). The overall substitution rate difference (Dp) was negative in pairwise comparison of Aat-A and Aat-B2 in R. pipiens (Dp = –0.008, standard error [SE] = 0.005), Aat-A and Aat-B in R. septentrionalis (Dp = –0.008, SE = 0.005), and Aat-B2 and Aat-B3 in R. dybowskii (Dp = –0.008, SE =0.004). However, in Fisher's exact tests the null hypothesis of neutral evolution could not be rejected for any of these comparisons.
Variation of dN/dS Ratio among Lineages
Two-codon substitution models were implemented in estimating the values from the ML tree. The variable ratio model fitted significantly better with the data set than the one ratio model (–lnL =1008.8445 vs. 1026.971, 2
l = 36.145, df = 16, P < 0.05). Under the one ratio model, = 0.3082 with a likelihood value of –lnL = 1026.971 was obtained. The branch-specific model revealed substantial differences in the values among the branches, however some of the branches contained too few substitutions to be reliable; the estimated values are shown in Figure 4 A-type sequences, with the exception of R. septentrionalis, showed a significantly lower value than the B type when compared with the reconstructed ancestral sequence of the lineage in question. The B2 and B3 sequence of R. dybowskii, B of R. septentrionalis, and B2 of R. pipiens showed a higher nonsysnonymous than synonymous substitution rate from the ancestor sequence of each species.
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= 3.24854). Two numbers beside 
) means dS = 0, |
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Multiple Aat Forms and Multiple Retroposition Events in the Ranid Frogs
The analysis of Aat sequences among 11 Ranid frog species revealed 3 different variants (A, B, and C), with most of the analyzed species harboring at least 2 types in their genome. The Aat-A variants isolated from all 11 species represented most likely the ancestral Aat gene in each species, as suggested by the gene structure and constrained mode of substitution. The Aat-B variants were characterized by precise and complete loss of the intron sequence and this structure is typical for retroposed sequences, where the novel form stems from the transcribed cDNA sequence. The Aat-B sequences thus appear to have arisen from the Aat-A through retrotransposition; this direction of events is further supported by the basal (albeit weakly supported) position of the Aat-A sequences compared with the Aat-B sequences in each species. Also the nonfunctional form (Aat-C) is expected to be a retroposition from Aat-A although the sequences have accumulated numerous substitutions after retroposition. It is worth noting that due to the nature of the PCR method, 3 variants must be considered the minimum number in Ranid frogs.
The most intriguing finding of this analysis was the close relationship between the A and B type within each species. This suggests that several separate retropositions leading to the Aat-B types have occurred in the Ranid frogs (Figure 2). Selection within the lineages most likely does not account for this intraspecific similarity between A and B type as the (presumably) neutral third position sites yielded a congruent paraphyletic topology. The intraspecific divergences through multiple retroposition events appear rather recent. In the total data set, the average divergence between Nearctic (R. grylio, R. palustris, R. pipiens, R. septentrionalis, R sylvatica) and Palearctic (R. nigromaculata, R. amurensis, R. dybowskii, R. temporaria, R. arvalis, R. dalmatina) was 4.3 ± 0.68%. By placing this separations at 7 Mya as suggested by Veith et al. (2003), the average divergence rate in A and B variants would be 0.61%/My (0.52–0.71%/My). Applying this rate on the average intraspecific A and B variant divergence 1.3% would give an estimate of 2.1 My (1.8–2.5 My) for the age of the putative retrotranspositions. This estimate must be considered as a rough approximation, as there are substantial interspecific differences, and some sequences deviate from the assumed neutrality. This age is lower or in the same range than the estimated ages of species divergences in Palearctic brown frogs (Veith et al. 2003), coinciding with the onset of Pleistocene glaciations. No B variant was found in R. temporaria, one of the distal taxons in the brown frog tree in Veith et al. (2003).
Evolution of Aat Gene Families in Ranid Frogs
The phylogenetic relationship between A and B variants suggests that they might be a subject of concerted evolution, in which the gene sequences within a gene family are repeatedly homogenized by unequal crossing over and gene duplication. However, the model of concerted evolution originally applies to gene families that are responsible for producing large quantities of the same gene products (Nei and Rooney 2005). Furthermore, because the gene structure of Aat-A variants is different from that of B-variants, any occurrence of gene conversion should be easily detected. Nei and Rooney (2005) mentioned that at the early stages of the gene birth-and-death evolution, a similar pattern is shown between the original and the new gene created by duplication. In our study, the novel Aat variants detected in the Ranid frogs showed signals of 3 distinct evolutionary trajectories, typical for transposed elements: 1) gene inactivation and subsequent relaxation of selective constraints, leading to accumulation of mutations (Aat-C variants), 2) retention of the original gene function under purifying selection (most Aat-B variants), and 3) retention of functionality under positive selection (Aat-B variants in R. pipiens, R. septentrionalis, and R. dybowskii). However, the evidence for positive selection is weak because the used ML method has been known to be liberal (Zhang 2004).
Aat plays a fundamental role in energy metabolism at least in mammals (Klingenberg and Heldt 1982) and the AAT expression is also known to increase under freezing stress in R. sylvatica (Cai et al. 1997). Furthermore, AAT has been associated with stress tolerance in Drosophila (Zhang et al. 1999), cold tolerance in maize (Zea mays; De Santis et al. 1999), duck (Cairina moschata; Roussel et al. 2000), and in the king penguin (Aptenodytes patagonicus; Talbot et al. 2004). Interestingly, the cold adaptation in the king penguins is partly based on the protein amount of AAT, with larger concentrations increasing proton conductance in the mitochondria. The multiple Aat variants (Aat-Bs) in frogs might have been favorable when they were adapting to the newly colonized environments, for instance by allowing increased expression of AAT, that was obtained from a new regulatory system by retroposition, in different stages of development and/or in different tissues. Especially when frogs started to inhabit the Northern latitudes', the shorter summer season might have limited their activity. The boreal R. temporaria appears as an exception in this data set, however. Furthermore, a signal for positive selection in the novel Aat variants was observed only in 3 frog species (R. pipiens, R. septentrionalis, R. dybowskii). Five of the total mutation sites are located on the hydrophobic region that was proposed to be fold transmembrane alpha-helices. Because mutation on alpha-helices leads to change the pore diameter of intercellular channels (Fleishman et al. 2004), this suggests that the function of these genes has changed under positive selection.
The Aat genes appear to serve as a good amphibian model for studying the evolution of redundant genes after gene duplication under different environmental conditions. Although only partial sequences were studied, and the function of these genes remains largely unknown, both type A and B sequences were considered functional because they did not include stop codons and had similarly high GC content in the coding regions (Table 1) as exons of Xenopus genome (Xia et al. 2003). However, even if the DNA sequences have no stop codons, they may be inactive due to absence of functional control elements or they can code for functionally important RNA (ncRNA) genes like Sphinx in Drosophila melanogaster instead of a protein (Wang et al. 2002). We continue to investigate the mRNA sequences and genomic region sequences of Aat gene of R. temporaria, and future analyses of the whole sequence of both Aat genes, its regulatory region, and quantitative analysis of its expression in Ranid frogs could shed more light on the function and evolution of Aat genes in amphibians.
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Supplementary Material |
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Supplementary material can be found at http://www.jhered.oxfordjournals.org/.
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Funding |
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Scandinavia-Japan Sasakawa Fundation (Tokyo, Japan), Centre for International Mobility (Finland), the Academy of Finland, and the University of Helsinki Science Foundation.
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Acknowledgments |
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We thank R. W. Murphy (Royal Ontario Museum, Canada), I. V. Maslova (Russia), S. M. Lyapkov (Russia), Yoko Ichikawa (Hiroshima Women's University, Japan), and T. Knopp (University of Helsinki, Finland) for helping in obtaining DNA samples and A. Aronta and L. Laaksonen for their help with a laboratory work.
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Footnotes |
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Corresponding Editor: William Modi
Received February 8, 2006
Accepted February 27, 2007
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