* Graduate School of Bioscience and Biotechnology, Tokyo Institute of Technology, Yokohama, Japan
Department of Cell Biology, National Institute for Basic Biology, Myodaiji, Okazaki, Japan
Tropical Biosphere Research Center, University of the Ryukyus, Nishihara, Okinawa, Japan
Correspondence: E-mail: nokada{at}bio.titech.ac.jp.
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Abstract |
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Key Words: tortoise turtle phylogeny SINE retroposon
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Introduction |
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Studies on phylogenetic relationships among members of Bataguridae have thus far been conducted from two viewpoints, namely morphology (McDowell 1964; Bramble 1974; Hirayama 1984; Gaffney and Meylan 1988; Yasukawa, Hirayama, and Hikida 2001) and molecular systematics (Sites et al. 1984; Wu, Zhou, and Yang 1999; McCord et al. 2000; Honda et al. 2002). McDowell (1964) defined the following four subgroups within Bataguridae primarily on the basis of cranial characteristics: the "Hardella complex" (Hardella, Morenia, and Geoclemys), the "Batagur complex" (Batagur, Callagur, Chinemys, Hieremys, Kachuga, Malayemys, and Ocadia), the "Orlitia complex" (Orlitia and Siebenrockiella), and the "Geoemyda complex" (Cuora, Cyclemys, Geoemyda, Heosemys, Mauremys, Melanochelys, Notochelys, Pyxidea, Sacalia, and Rhinoclemmys). Later, however, a morphological analysis suggested that the Hardella complex constitutes a polyphyletic group (Hirayama 1984). This study also suggested that Chinemys and Malayemys are sister genera within the Batagur complex. Gaffney and Meylan (1988) proposed the two subfamilies Batagurinae and Geoemydinae in Bataguridae, the former consisting of species of the Hardella, Batagur, and Orlitia complexes, and the latter corresponding to the Geoemyda complex. However, recent molecular phylogenetic analyses have suggested that a few genera of the subfamily Batagurinae are rather closely related to species in Geoemydinae (McCord et al. 2000; Honda, Yasukawa, and Ota 2002; Honda et al. 2002). McCord et al. (2000) suggested a close relationship between Siebenrockiella (Orlitia complex) and Melanochelys (Geoemyda complex) as well as between Chinemys (Batagur complex) and Mauremys (Geoemyda complex), based on a preliminary analysis of mitochondrial cytochrome b gene sequences. The latter relationship was further supported by an analysis of partial sequences of the mitochondrial 12S and 16S rRNA genes (Honda, Yasukawa, and Ota 2002; Honda et al. 2002). Thus, as with the phylogenetic position of the family Bataguridae, the proposed relationships among its members have also been a subject of vigorous discussion.
Over nearly a decade, the SINE (short interspersed element) method (Cook and Tristem 1997; Miyamoto 1999; Shedlock, Milinkovitch, and Okada 2000; Shedlock and Okada 2000; Rokas and Holland 2000; Graur and Li 2000; Nei and Kumar 2000) has been employed in a number of phylogenetic analyses (e.g., Murata et al. 1993; Shimamura et al. 1997; Takahashi et al. 2001; Nikaido et al. 2001a) as a powerful tool for identifying monophyletic groups. SINEs are retroposons that propagate in the genome by retroposition (Singer 1982; Weiner, Deininger, and Efstratiadis 1986; Okada 1991a, 1991b). Integration of a SINE sequence at a site in the genome is irreversible, and its target site is chosen almost at random (Okada et al. 1997). The latter characteristic of SINE retroposition indicates that we can actually exclude the possibility of parallel and independent insertion of such a sequence in distant phylogenetic lineages. Thus, when a SINE sequence is found at an orthologous locus in two or more lineages, it can be regarded as evidence for synapomorphy.
A SINE family sometimes consists of multiple subgroups that each contain different combinations of diagnostic nucleotides (e.g., Ohshima et al. 1993; Kido et al. 1994; Shimamura et al. 1999; Nikaido et al. 2001b; Nishihara, Terai, and Okada 2002; Takahashi and Okada 2002). Different SINE subgroups often show different relative frequencies of retroposition during the course of evolution. Therefore, when using the SINE method it is necessary to choose a certain subgroup (within the lineage to be tested) that appears to be specifically active (Kido et al. 1991; Shimamura et al. 1997). Otherwise, a large portion of the loci that are analyzed may appear to be phylogenetically uninformative because they might contain a significant number of SINE sequences that became inserted prior to the divergence of the lineage.
The tortoise polIII/SINE was reported to exist uniquely in the genomes of hidden-necked turtles (Endoh and Okada 1986; Endoh, Nagahashi, and Okada 1990; Ohshima et al. 1996). In the present study, we isolated tortoise polIII/SINEs from representative species of eight families of cryptodiran turtles, and subjected them to a comprehensive analysis via the SINE method to reveal their subgroup structure. On the basis of this information, we tested the applicability of the SINE method to deduce the phylogeny of these turtles, focusing especially on Bataguridae and related families within Testudinoidea. This study constitutes the first application of the SINE method to infer reptilian phylogeny.
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Materials and Methods |
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Genomic library screening was performed for two different purposes, namely to characterize the tortoise polIII/SINEs sequences themselves and to perform a phylogenetic analysis of Testudinoidea using the SINE method. For the former purpose, we screened genomic libraries of nine species from eight families (table 1) using the oligonucleotide probe TEF1 (5'-GGGAGGGATAGCTCAGTGGT-3'; Ohshima et al. 1996) corresponding to positions 120 of the Cry I consensus (cons) sequence (fig. 1). TEF1 is compatible among all the tortoise polIII/SINE subgroups. For the Testudinoidea phylogenetic analysis, we designed the probe Cry1tC (5'-GGGGCAAAAATTGGTCCTGC-3'), which corresponds to positions 86105 of the CryIC cons sequence (fig. 1), to selectively isolate the SINE type IC from the genomic libraries of Kachuga smithii and Mauremys mutica kami (table 1). Each genomic library was screened with the above probes that were labeled with [-32P] dATP. Hybridization was performed at 42°C overnight in a solution of 6x SSC, 1% SDS, 2x Denhardt's solution, and 100 µg/ml herring sperm DNA in a final volume of 50 ml. Washing was performed at 35°C for 20 min in a solution of 2x SSC and 1% SDS. The inserts of positive clones that appeared to contain these SINE sequences were sequenced by the dideoxy chain termination method (Sanger, Nicklen, and Coulson 1977). Purified plasmid DNAs were sequenced using the BigDye terminator cycle sequencing kit (Applied Biosystems) performed with 25 cycles consisting of denaturation at 96°C for 30 s, annealing at 50°C for 15 s, and extension at 60°C for 1 min in a total volume of 10 µl. The reaction contained 4 µl BigDye terminator premix, 50 ng sequencing primer, and 2 µl template DNA. Sequences were determined with an automated sequencer (3100 Applied Biosystems). The nucleotide sequence data have been deposited in GenBank (AB125391AB125574).
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Alignment of the Tortoise PolIII/SINE Sequences
A total of 382 tortoise polIII/SINEs sequences (for representative sequences, see table 1 of the Supplementary Material online) obtained by screening genomic libraries and by PCR amplification were initially aligned using the ATGC version 3.00 software (Genetyx Corporation). The alignment was inspected by eye using the Genetix version 6.1.1 software.
Amplification of Orthologous Loci by PCR to Test the Presence/Absence of SINE Sequences
To examine the presence or absence of a SINE unit at orthologous loci in various species, we designed and synthesized a pair of primers that flanked the unit based on the sequences obtained from the isolated clones. Polymerase chain reaction amplification was carried out in 50 µl containing 200 ng genomic DNA, 100 ng of each primer, 0.2 mM dNTPs, 5µl ExTaq buffer (Takara, Japan), and 1 U of TaKaRa ExTaq DNA polymerase. Polymerase chain reaction was performed over 30 cycles of denaturation at 94°C for 1 min, annealing at 50°55°C for 1 min, and extension at 72°C for 1 min. The PCR products were electrophoresed in a 1.5% gel of Agarose L03 (Takara, Japan). DNA bands were stained with ethidium bromide and visualized under UV irradiation. When necessary, PCR products were ligated into pGEM-T (Promega) and used as a template for sequencing (see table 2 of the Supplementary Material online). The nucleotide sequence data have been deposited in GenBank (AB125703AB125739).
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Results |
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Phylogenetic Analysis of SINE Insertions in Testudinoidea
Based on the frequencies of the subgroups/types presented above, it was reasonable to assume that tortoise polIII/SINE types IB and IC exhibited higher rates of retroposition during the evolution of Bataguridae and its closely related families compared to other types. Hence, focusing on types IB and IC during the analysis increased the chance of obtaining loci that were informative with regard to elucidating the phylogenetic relationships among the turtle species within these groups. Thus, we investigated loci into which either type IB or IC had inserted. Such loci were either screened with the probe Cry1tC (specific to a type IC sequence) or isolated incidentally during genomic library screening with the general probe TEF1 (see Materials and Methods for details).
In the case of the BCr06 locus, the longer products that were expected when a SINE sequence existed in the locus were amplified from the genomes of 14 species that represented Testudinidae and Bataguridae (fig. 3A). In contrast, two species belonging to Emydidae yielded shorter products that were expected if the locus did not contain a SINE unit. These results on the presence/absence of SINEs at this locus (table 5) were further confirmed by sequencing the products amplified from the genomes of representative species (see table 2 of the Supplementary Material online). Similar results were obtained for the BCr01 locus (fig. 3B), although no product was obtained from Melanochelys trijuga, most likely because there was a mutation in the primer binding site. These results suggest that Bataguridae species are more closely related to those of Testudinidae than to those of Emydidae, assuming that the SINE inserted into these loci in a common ancestor of the relevant Testudinidae and Bataguridae species after it branched from the ancestor leading to the relevant Emydidae species.
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Data for the BKs36 locus revealed a close relationship among Kachuga smithii, Callagur borneoensis, and Malayemys subtrijuga, as only these species exhibited longer PCR products (fig. 3D). A similar result was obtained for the BKs52 locus (fig. 3E), although Trachemys scripta elegans, for which the BKs11 locus showed only a distant relationship with the above three species, did not yield a product.
Polymerase chain reaction amplification of the BCr61 locus (fig. 3F) yielded longer products for both Chinemys reevesii and Mauremys mutica kami, indicating a close relationship between these species. No PCR product was obtained for Cyclemys sp.
The BMm105 locus results showed a pattern similar to that of BCr61 (fig. 3G). C. reevesii displayed a product that was longer than expected for the incorporation of a single SINE unit. The sequence revealed one SINE unit at this locus as well as an additional 325-bp sequence unrelated to the tortoise polIII/SINE (see table 2 of the Supplementary Material online). Kachuga smithii and Sacalia bealei did not yield a PCR product from this locus; however, K. smithii is not closely related to either C. reevesii or M. mutica kami, based on the relationships suggested by the loci BKs11, BKs36, and BKs52.
Among the species examined, insertions of SINEs into the BKs31 locus appeared to have occurred specifically in Kachuga smithii, because this species was the only one to yield a long PCR product (fig. 3H). Similarly, the BCr04 locus showed a SINE insertion specific to Chinemys reevesii (fig. 3I). The results obtained for loci BMm74 and BMm85 (fig. 3J and 3K, respectively) suggested that the insertion of SINE units into these loci occurred independently and subsequent to the divergence of Mauremys mutica kami from all the other species investigated. This result was supported by data for the BCr61 and BMm105 loci. With regard to the BMm74 locus, the products obtained for K. smithii, C. borneoensis, and M. subtrijuga (fig. 3J, lanes 1, 2, and 3) were slightly shorter than the products for other species, suggesting the absence of a SINE unit at this locus. Sequencing of these three products confirmed a unique 46-bp deletion in the flanking region (see table 2 of the Supplementary Material online). This observation is consistent with the monophyly of these three genera, as suggested by the BKs36 and BKs52 loci, indicating that the above deletion occurred in a common ancestor.
A phylogenetic tree for Bataguridae and other related families was constructed on the basis of the above results obtained from a total of 11 loci (fig. 4).
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Discussion |
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Tail Region Similarities Between the Cry I/II Subgroups and PsCR1 Long Interspersed Element (LINE)
The diagnostic nucleotides that differentiate the two tortoise polIII/SINE subgroups identified in the present study were found only in their 3' regions (fig. 1). In fact, the sequence of this region is homologous to that of the 3'-tail of PsCR1 LINE (long interspersed element) in turtles (Ohshima et al. 1996; Kajikawa, Ohshima, and Okada 1997). The LINEs encode a reverse transcriptase that facilitates their own retroposition, whereas the SINEs do not encode any protein. This fact, together with the discovery of the similarity between the 3'-tails of SINEs and LINEs (Ohshima et al. 1996; Okada et al. 1997), led to the hypothesis that SINE retroposition is dependent on the retropositional enzymatic machinery of LINEs, and that during retroposition of the SINE, its 3'-tail is recognized by a reverse transcriptase encoded by its partner LINE (Ohshima et al. 1996; Okada et al. 1997; Weiner 2000). This hypothesis was recently verified by experiments showing that the 3'-tail of eel UnaSINE1 is actually recognized by the reverse transcriptase encoded by eel UnaL2 LINE (Kajikawa and Okada 2002).
Of the two subgroups (Cry I and Cry II) identified in the present study, the consensus sequence of the 3'-tail region of Cry II SINEs is 95% identical to that of PsCR1 LINE, as suggested by Ohshima et al. (1996) for the TE3 sequence (fig. 5). Thus, the Cry II SINE subgroup appears to exploit the retropositional machinery of the PsCR1 LINE, the characterization of which was previously reported (Ohshima et al. 1996; Kajikawa, Ohshima, and Okada 1997). In contrast, the 3'-tail region of the consensus sequence of Cry I SINEs shows only 75% identity with that of the PsCR1 LINE. Although this 75% identity constitutes a significant level of homology, the 3'-tail sequence of a SINE is stringently recognized by the reverse transcriptase of its partner LINE (Okada et al. 1997). Thus, the fact that the Cry I SINE subgroup exists may indicate the existence of an as yet unreported PsCR1 LINE subgroup whose 3'-tail sequence is highly similar to that of the Cry I SINEs. This putative PsCR1 LINE subgroup may be directly responsible for retroposition of the Cry I subgroup.
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We also identified three new clades within Bataguridae (fig. 4). SINE insertions at loci BKs36 and BKs52 as well as a 46-bp deletion in BMm74, indicated that three species (Kachuga smithii, Callagur borneoensis, and Malayemys subtrijuga) out of the four we investigated from the Batagur complex (McDowell 1964) form a monophyletic group (clade A). In addition, Chinemys reevesii, another species of the Batagur complex that we investigated, was not included in this clade, although morphological studies suggested it is a sister species of Malayemys subtrijuga (Hirayama 1984; Gaffney and Meylan 1988).
The results obtained from the BKs11 locus suggested monophyly of the clade B (fig. 4), which was also supported by our preliminary analysis of locus BKs85 (unpublished data). This finding is inconsistent with an earlier phylogenetic analysis (McCord et al. 2000) based on the sequence of the mitochondrial cytochrome b gene, which suggested the close relationship between Siebenrockiella and Melanochelys, because the former genus was included in the clade B, but the latter was not a member of the clade in the present study.
The close relationship between Chinemys reevesii and Mauremys mutica kami, as suggested by loci BCr61 and BMm105 (clade C in fig. 4), is in agreement with a preliminary study based on the sequence of the mitochondrial 12S and 16S rRNA genes (Honda, Yasukawa, and Ota 2002; Honda et al. 2002). Sequence analysis of the cytochrome b gene also suggested that these species are closely related (McCord et al. 2000). However, this relationship is in conflict with the accepted taxonomy because Chinemys reevesii belongs to Batagurinae whereas Mauremys mutica kami is included in Geoemydinae (Gaffney and Meylan 1988; Ernst, Altenburg, and Barbour 2000; Yasukawa, Hirayama, and Hikida 2001). Accordingly, the monophyly of the Batagur complex (Callagur, Chinemys, Kachuga, and Malayemys, in terms of the specimens examined in the present study), as suggested by McDowell 1964, is also inconsistent with the present result. Chinemys reevesii shares several morphological traits, such as the broad and triangular fissura ethmoidalis and small foramen palatinum posterius, with other members of Batagurinae (Hirayama 1984; Gaffney and Meylan 1988). This conflict between the molecular systematics and the taxonomy may be due in part to extensive convergence in the morphological evolution of the Bataguridae (see Hirayama [1984] and Yasukawa, Hirayama, and Hikida [2001] for further details), which is largely affected by environmental selective forces, as suggested by Honda et al. (2002).
Applicability of the SINE Method for Inferring Turtle Phylogeny
The present study is the first application of the SINE method to reptilian phylogeny, specifically to that among families and genera of cryptodiran turtles. The phylogenetic tree that includes polIII/SINE insertions of the tortoise Cry I subgroup members (fig. 4) indicates that the individual types within this subgroup show different tendencies with respect to relative retropositional frequencies along the nodes. Indeed, retropositional insertion of the IB type SINE was evident only during the earliest evolutionary period of the turtles we investigated, whereas the retroposition of type IC was detected only during the later period, as shown in the phylogenetic tree. Such differences in relative retropositional frequencies within each evolutionary period or lineage is advantageous for phylogenetic analyses using the SINE method because the choice of the type(s) of the SINEs allows the analysis to focus on a specific relationship of interest. The above information regarding the choice of the types to be investigated will be useful in future detailed phylogenetic analyses within Bataguridae itself, as well as among Bataguridae and its related turtle families of Testudinoidea. In a similar manner, the present SINE methodology may be applied to other families of turtles, such as Chelydridae and Cheloniidae, although other types of tortoise polIII/SINEs (type IIB for these families, for example) must be used for such analyses.
The SINE method may be useful for resolving relationships not only among families or genera but also among species that diverged more recently. The loci BKs31, BCr04, BMm74, and BMm85 (table 5 and fig. 4) contain Cry I insertions within a single taxon. By including additional species and genera, more detailed analyses of SINE insertions at such loci would be informative for the above purpose (see Kido et al. [1991] and Murata et al. [1993] for examples of such analyses). The present study provides the indispensable groundwork for future phylogenetic analyses of cryptodiran turtles using the SINE method.
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Acknowledgements |
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Footnotes |
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