Bernardo e Loreto 2013

Genetica (2013) 141:471–478 DOI 10.1007/s10709-013-9746-1

hobo-brothers elements and their time and place for horizontal transfer Larissa Paim Bernardo • Elgion L. S. Loreto

Received: 31 July 2013 / Accepted: 18 October 2013 / Published online: 25 October 2013 Ó Springer Science+Business Media Dordrecht 2013

Abstract Transposable elements (TEs) are ubiquitous components of nearly all genomes studied. These elements are highly variable in copy number, molecular structure and transposition strategies. They can move within and between genomes, thus increasing their copy numbers and avoiding being eliminated by stochastic and deterministic processes. hobo is a class II element isolated from Drosophila melanogaster. Previous phylogenetic analyses have shown that the canonical hobo element from D. melanogaster has a sister group formed by sequences found in D. willistoni (called howilli2) and D. mojavensis (called homo1). In the present study, we investigated 36 Drosophilidae species for sequences similar to howilli2 and homo1 using degenerate primers. Additionally, in silico searches were performed in 21 available Drosophila genomes. The obtained sequences formed a monophyletic sister group with the canonical hobo element; we termed these sequences ‘hobo-brothers’ elements. These elements showed a patch distribution and incongruities with the TE and host species phylogenies, suggesting possible cases of horizontal transfer (HT). Species that possess hobo-brothers sequences are from the New World, mainly Neotropical areas. In addition, the estimated divergence of the sequences found showed that these elements are or were Electronic supplementary material The online version of this article (doi:10.1007/s10709-013-9746-1) contains supplementary material, which is available to authorized users. L. P. Bernardo  E. L. S. Loreto PPG Biodiversidade Animal, CCNE, Universidade Federal de Santa Maria, Santa Maria, Brazil E. L. S. Loreto (&) Biology Department, CCNE, Universidade Federal de Santa Maria, Santa Maria, RS 97105 970, Brazil e-mail: [email protected]

recently active; the large number of HT events observed suggests that these elements could be experiencing an expansion process in Neotropical genomes. A comparison of these results with the literature is discussed with regard to the importance of the time and location of horizontal transposon transfer events. Keywords hAT  Transposable elements  Transposon  hobo  Drosophila

Introduction Transposable elements (TEs) are ubiquitous components of essentially all genomes studied to date. These genetic elements are highly variable and can be abundant in certain genomes. There is strong evidence for the important role of TEs in the evolutionary process, as they promote changes in chromosome structure, induce epigenetic modifications and are an origin of allelic diversity, new genes and biological innovations (Feschotte and Pritham 2007; Hua-Van et al. 2011). Transposable elements undergo a ‘‘life cycle’’ during the evolution of genomes. The first step is the invasion of a new genome by horizontal transfer (HT). Additionally, TEs can arise through the recombination of different resident TEs in the genome, which can represent old or relic elements. The second step of the life cycle is the spread of the TEs throughout the host genome, which is typically achieved by a transposition burst, whereby the transposition rate is higher than the loss due to natural selection or genetic drift. The next step is generally accompanied by a mechanism to reduce the deleterious effects associated with the high mutation rate observed in the transposition burst phase.

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The main mechanisms to silence TEs are, either transcriptionally by DNA methylation or changes in chromatin structure, or post-trancriptionally through RNAi. Also, TEs can be inactivated by targeted mutations (Hua-Van et al. 2011). A way by which TEs can escape silence and extinction is via horizontal transfer (Lohe et al. 1995). In fact, analyses of Drosophila genomes have shown that approximately one-third of TE families are recent acquisitions by HT (Bartolome´ et al. 2009). As an alternative but not mutually exclusive model, TEs can also be maintained for long evolutionary times if they are able to find ‘‘safe havens’’, i.e. genome’s places with either reduced fitness costs to the host or from which they cannot be removed (Werren 2011). As example, the R1 and R2 elements inserts into ribosomal RNA genes and, by this way, are subject to strong selective constraint that prevents their removal (Eickbush and Eickbush 2007). Although HT is thought to be a rare event in eukaryotes (Kidwell 1993; Andersson 2005), current evidence shows that, for transposable elements, this process is frequent and widespread in all branches of eukaryotes phylogeny. The particular type of HT, related to TEs, is referred to as horizontal transposon transfer (HTT) (Schaack et al. 2010). The genus Drosophila exhibits the highest number of reported cases of HTT, which most likely is indicative of sampling bias, as this taxon is a model for studies of transposable elements and also for evolution (Wallau et al. 2012). Additionally, dissimilar HTT rates have been reported for different types of TEs. For example, Class II (TEs that transpose using a DNA intermediate) are described as being involved in more described HTT cases than Class I elements (those that utilize a RNA intermediate), though the LTR (long terminal repeat) elements of the latter group are more likely to undergo HTT than nonLTR elements (Silva et al. 2004; Wallau et al. 2012). hobo, an active Class II element isolated from D. melanogaster (McGinnis et al. 1983; Streck et al. 1986), has been well characterized with regard to its molecular, functional and population characteristics, including its ability to function as a vector for genetic transformation (Blackman and Gelbart 1989; Daniels et al. 1990a; Ladeve`ze et al. 2012). Additionally, hobo was one of the first TEs reported to be involved in HTT (Simmons 1992). hobo has short terminal inverted repeats (TIRs) of 12 bp and an open reading frame (ORF) of 1982 bp, which encodes the transposase. This element belongs to the hAT superfamily, which is widespread in plants, fungi and animals and includes various well-studied and active elements (Arensburger et al. 2011). According to Arensburger et al. (2011), this superfamily can be divided into at least two families, Ac and Buster; in this classification, hobo belongs to the Ac family.

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Ortiz and Loreto (2009) performed an in silico search for hAT elements in the twelve Drosophila genomes available at the time, using Blastn and, as query, 12 different hAT elements previously described. Thirty-seven new hAT elements were found scattered throughout the genomes of 10 species. Using the criteria proposed by Wicker et al. (2007), these 37 different sequences were classified into four families, and 15 of these elements showed structural characteristics that indicated them to be active elements. The phylogenetic analyses performed by Ortiz and Loreto (2009) showed that the canonical hobo element from D. melanogaster has a sister group formed by sequences found in D. willistoni (called howilli2) and D. mojavensis (homo1). The sequences found in these species are putatively active and remarkably similar (proportion of nucleotide differences p = 0.17) for species belonging to different subgenera. In the present study, we examined 36 Drosophilidae species for sequences similar to howilli2 and homo1 using degenerate primers. Additionally, in silico searches were performed in nine Drosophila genomes now available, adding to the results of Ortiz and Loreto (2009). We found sequences that formed a monophyletic sister group with the canonical hobo, herein called hobo-brothers elements. These elements showed a patchy distribution in the phylogeny of the host species, and some elements harbored by distantly related species are very similar, sometimes identical in the region analyzed. These results suggest that these elements were recently involved in HTT. All species that possess hobo-brothers sequences are from the New World, mainly Neotropical regions. Our results are compared with those in the literature, and the importance of the time and location where HTT occurred is discussed.

Materials and methods Fly stocks A total of 36 Drosophilidae species were used for the molecular analysis: 25 from the Drosophila subgenus and nine from the Sophophora subgenus. Zaprionus indianus and Zygothrica vittimaculosa were also investigated (supplementary Table 1). Some strains were maintained in the laboratory by mass crossing and cultivated on a corn flour culture medium in a controlled chamber (17 ± 1 °C, 60 % r.h.). Others strains were collected directly from the wild, identified and used for genomic DNA isolation. Additionally, nine available Drosophila genomes were searched by an in silico analysis for hobo-brothers sequences (supplementary Table 1) as an addition to the 12 genomes previously studied (Ortiz and Loreto 2009). Of these 21 species,

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three are from the Drosophila subgenus and 18 from the Sophophora subgenus. Molecular procedures Total DNA from the Drosophilidae species was isolated following the method described by Oliveira et al. (2009). Primers, designed using Oligo 4.1 software, were based on the homo1 and howilli2 sequences described by Ortiz and Loreto (2009) available in REPBASE. The primer sequences are as follows: forward, 50 CAWCACYGGYT CAGCAAATCAT, and reverse, 50 GCCGACAATCYT GAACYACCCA. These degenerate primers amplify a fragment approximately 600 bp long, which corresponds to the 50 UTR sequences and roughly 300 bp of the transposase ORF (Fig. 1). A non-coding sequence region was chosen, as this part is expected to be more variable, and so, phylogenetically more informative. The DNA quality was tested using primers for the hunchback gene, as described by Mota et al. (2008), and only the DNA samples that showed amplification of hunchback were used for searching hAT sequences. The PCR assays were performed using approximately 20 ng of genomic DNA, 1 U Taq DNA polymerase (Invitrogen), 19 Reaction Buffer, 2.5 mM MgCl2 and 20 pmol each primer. The following thermocycler amplification process was used: 94 °C for 5 min, 30 cycles at 94 °C for 45 s, 57 °C for 30 s and 72 °C for 60 s, followed by a final extension cycle at 72 °C for 5 min. DNA sequencing of the amplified fragments cloned into plasmids was performed with M13 forward and reverse primers using a MegaBace 500 automatic sequencer. The dideoxy chain-termination reaction was performed using the DYEnamicET kit (GE Healthcare). Both DNA chains

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were sequenced and assembled using GAP 4 software from the Staden Package (Staden 1996). Six to eight clones were sequenced for each species. The sequenced elements were deposited in GenBank (Accession numbers: KF430378 to KF430430). Those species generating amplicons of the expected size with sequences not corresponding to hAT elements and also species showing no amplification were screened by Southern Blotting. The rationale was to verify whether hAT sequences are actually absent or merely not represented in the sequenced samples for the former and, for the latter, to verify whether the result was due poor amplification, resulting in no visible bands by ethidium bromide staining. The PCR products were separated on an 0.8 % agarose gel and transferred to a nylon membrane (Hybond N?/GE Healthcare). The hybridization and detection steps followed the Gene Images AlkPhos Direct Labeling and Detection System protocol (GE Healthcare). The membranes were washed twice with 0.2X SSC and 0.5 % SDS (w/v) for 15 min at 65 °C. A plasmid containing the homo 1 sequence was used as the probe. In silico searches Searches for hobo-brothers elements were conducted in nine available genomes (Fig. 2) using the Blast tool. Blastn was used in these searches with default parameters. The criteria used to retrieve sequences for analyses was homology score [100, as available in Flybase (http:// flybase.bio.indiana.edu/blast/). As a query, we used the homo1 and howilli2 sequences described by Ortiz and Loreto (2009) (http://www.girinst.org/repbase). Additionally, searches were performed using Trace Archive Nucleotide Blast (NCBI). All retrieved sequences were also used as queries until no new sequences were obtained. Evolutionary analyses

Fig. 1 a Schematic representation of the full-length homo1 element, which is 2,817 bp long. Shown are the size of the target site duplication (TSD), terminal inverted repeats (TIRs) and the 50 and 30 untranslated regions (UTRs). The open reading frame (ORF) is shown in gray. The rectangle below represents the region amplified by the degenerated primers and the primer annealing position in the sequence. b The full-length howilli2 element is 2,847 bp long

The nucleotide sequences were aligned using ClustalW 2.0.10 software (Thompson et al. 1994) according to the program default parameters. The phylogenetic relationship between the TE sequences was estimated using two methods: (1) maximum likelihood implemented in Mega 5 software (Tamura et al. 2011), with 1,000 bootstrap replications, and (2) Bayesian analysis implemented in MrBayes 3.2 software (Ronquist and Huelsenbeck 2003), with at least 1,000,000 generations and a burn-in region of 1,000 trees. For both analyses, the model used was the (HKY?G) model with gamma distribution, as suggested by the MrModel Test 2.3 program (Posada and Crandall 1998). For the divergence analyses, the sequences were clustered for species to perform a p-distance analysis using the Mega 5 program (Tamura et al. 2011).

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distribution) of a TE across a group of species (for a review, see Silva et al. 2004; Loreto et al. 2008).

Results Distribution of hobo-brothers sequences (homo1/ howilli2) in the studied species

Fig. 2 Phylogenetic tree of the studied species reconstructed based on the works of Robe et al. (2010). The two subgenera and the radiations are indicated by brackets at right of the phylogeny. The species groups are represented by numbers: 1 guaramunu, 2 cardini, 3 guarani, 4 tripunctata, 5 pallidipennis, 6 immigrans, 7 funebris, 8 mesophragmatica, 9 repleta, 10 dreyfusi, 11 canalinea, 12 flavopilosa, 13 virilis, l4 robusta, 15 griwshawi, 16 melanogaster, 17 obscura, 18 willistoni, 19 saltans. The positive (?) or negative (-) sign indicates whether the species contains or does not contain hobo-brothers sequences. G indicates that the search was performed by in silico analyses, whereas G* indicates that the searches were performed by Ortiz and Loreto (2009)

Divergence times among sequences and horizontal transfer (HT) inferences The divergence times among the sequences were estimated according to the formula T = k/2r (Graur and Li 2000). The r evolutionary rate used was 0.011 changes/base/myr, as proposed as the neutral mutation rate for Drosophila (Tamura et al. 2004). We used the average divergence of the elements that formed the groups to estimate the time of divergence of the groups shown in the phylogeny. Three aspects were considered to infer the occurrence of HTT: (1) high sequence similarity between TEs of distantly related species; (2) incongruence between host and TE phylogenies and (3) discontinuous occurrence (patchy

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PCR screening showed that nineteen (57 %) of the analyzed species showed hobo-brothers amplicons with the expected size of 600 bp. However, the BLASTn searches in the NCBI and REPBASE transposon databases showed that only 14 species (41 %) harbor sequences corresponding to hAT sequences (supplementary Table 1); the others represent spurious sequences, resulting from non-specific amplification, most likely due to the use of degenerate primers. Southern blot analyses revealed that the PCR amplifications for species displaying spurious sequences did not hybridize to the hobo-brothers probes, stressing that the amplification reactions were non-specific. In silico searches showed the presence of hobo-brothers sequences only in D. willistoni and D. mojavensis; importantly, these are New World species. In summary, of the 54 species tested using both molecular and in silico analyses, sixteen (29.6 %) showed hobo-brothers sequences (Fig. 2). These hobo-brothers sequences exhibited a markedly patchy distribution in the studied species (Fig. 2). hobobrothers sequences were found in all studied species of the cardini and saltans groups and in some species of the guarani, mesophragmatica, repleta and willistoni groups though were absent in the canalinea, dreyfusi, flavopilosa, funebris, immigrans, pallidipennis, robusta, tripunctata, virilis and melanogaster groups and in Zygothrica vittimaculosa and Zaprionus indianus. The nucleotide divergence observed was also highly variable: the p-distance among the hobobrothers elements ranged from 0.00 to 0.24. A remarkable result was that many species, including some that are distantly related or belonging to different subgenera, share very similar sequences that were identical in some cases. For example, D. ornatifrons, D. paulistorum and D. gaucha show 100 % identical sequences in the analyzed region. The p-distance found among the hobo-brothers sequences and the canonical hobo element from D. melanogaster ranged from 0.3 to 0.5 (supplementary Spreadsheet 1). Phylogenetic analyses, horizontal transfer and geographical sympatry The phylogenetic analyses performed using the hobobrothers sequences, with the canonical hobo element as an outgroup, revealed the existence of 8 clades (Fig. 3). In general, the relationships among the hobo-brothers

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Fig. 3 Phylogeny of hobo-brothers sequences reconstructed using a Bayesian analysis and the model (HKY?G), with gamma distribution. Canonical hobo from D. melanogaster was used as the outgroup. The posterior probability of each clade is indicated, beside its respective internal branch, outside the parentheses. Bootstraps values for ML are indicated inside the parentheses.The element(s) found in D. equinoxialis are represented as hAT Equin 2, 4, 5 and 6, D. ornatifrons are represented as hAT Ornat 2, 4, 5, 7, 10, 11 and 14, D. paulistorum are represented as hAT Paulist 5, 9, 11, 16, 17, 18, 19 and 23, D. gaucha is represented as hAT Gau 6, D. pavani is represented as hAT Pav 1, D. neocardini are represented as hAT Neo 1 and 2, D.

willistoni are represented as hAT willi 10, 13, 14, 18, 19, 20, 22 and 23, D. sucinea is represented as hAT Suc 1, D. capricorni are represented as hAT Cap 4, 2 and 3, D. sturtevanti are represented as hAT Sturt 2, 3, 4, 5, 11 and 16, D. buzzati are represented as hAT Buz 2, 3, 4, 6, 7, 11, 15 and 18, D. griseolineata is represented as hAT Gris 1, and D. cardinoides are represented as hAT Card 1, 2 and 4. The canonical elements homo1 and howilli2 of D. mojavensis and D. willistoni, respectively. The species groups is indicated by the letters A—H. The eight hobo-brothers clades found are indicated by roman numerals

sequences were incongruent with the host species phylogeny (Fig. 2). Some clades, such as clades 2 and 3, were composed of very similar sequences, as demonstrated by the short lengths of the branches; these clades also contained sequences from distantly related species belonging to different groups or subgenera. For example, in clade 2, a higher p-distance was 0.01 between the D. paulistorum sequence hAT_Dpaulist19 and the sequences from D. neocardini (hAT_Dneo1 and hAT_Dneo1), D. ornatifrons (hAT Ornat10) and D. pavani (hAT Pavani1), whereas the lowest p-distance (0.0) was between species belonging to

different subgenera (D. paulistorum and D. gaucha; see supplementary Spreadsheet 1). Clade 3 was formed by sequences from D. willistoni and D. griseolineata, also members of different subgenera, and the p-distance ranged from 0.006 to 0.014. Clade 4 was composed of species from the willistoni and saltans groups (Sophophora subgenus) and were very similar (p-distances ranging from 0.00 to 0.044). The other clades were formed by sequences arising from only a single species. The phylogenetic incongruences and high similarities observed among the sequences belonging to clades 2, 3 and

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Discussion

Fig. 4 Geographic distribution of hobo-brothers host species: Geographic coordinates of the collection points obtained in TaxoDros (Ba¨chli, 2008) were plotted on maps using Corel Draw 12 software. In the first map is included the species found in cluster II of Fig. 3 (D. ornatifrons, D. neocardini, D. pavani, D. paulistorum and D. gaucha). In the second map is shown the species found in cluster III of Fig. 3 (D. willistoni and D. griseolineata). In the third map is shown the species found in cluster IV of Fig. 3 (D. capricorni, D. sturtevanti, D. sucinea and D. willistoni)

4 are suggestive of horizontal transfer. The divergence times among the sequences were estimated and can be found in Supplementary spreadsheet 1. The divergence time among the sequences from clade 2 ranged from zero to 0.59 MYA. For clade, 3 the divergence time ranged from 0.29 to 0.726 MYA, and these estimation were zero to 1.8 MYA for clade 3. The highest divergence time among the hobo-brothers sequences was estimated at 11.8 MYA, and the estimated divergence time among the hobo-brothers sequences and canonical hobo ranged from 25 to 45 MYA. Additionally, the current geographical distribution of the species involved in these putative horizontal transfer events were investigated. It was found that these species are sympatric in the present time, which is a condition for a recent HT occurrence (Fig. 4).

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As highlighted by Ladeve`ze et al. (2012), ‘‘among the hAT superfamily, hobo is the unique element for which a complete set of data (at genetical, physiological as well as population level) is available’’. hobo has been found exclusively in the melanogaster group of the Drosophila genus, more specifically in the melanogaster and montium subgroups (Daniels et al. 1990a, b). Based on Southern blot analysis, these authors pointed out that hobo have had two independent introduction in the melanogaster group. One is ancient, with elements being maintained by vertical transmission and another one more recent, corresponding to the canonical hobo element, present in the melanogaster subgroup. In those studies, the ancient TEs were called ‘‘relics’’ and characterized for the absence of XhoI restriction sites. Whereas, the canonical hobo elements were characterized by a 3 kb fragment when digested with XhoI restriction enzyme. More recently Ortiz and Loreto (2008) have shown that some ‘‘relic’’ elements are mobilizable and have been residents in the genomes of species of the melanogaster group for long time (Ortiz and Loreto 2008). However, canonical hobo is a recent acquisition in the D. melanogaster genome by HTT (Simmons 1992; Periquet et al. 1994; Boussy and Itoh 2004), showing that both old and new elements can inhabit the same genome. The species that harbor hobo elements are of African origin, whereas D. melanogaster and D. simulans are cosmopolitan. The presence of hobo in others species that are endemic to Africa is indicative that D. melanogaster and D. simulans obtained this TE before dispersing from Africa. The data in the present study indicate that hobo-like sequences are widely distributed in different Drosophila groups of the New World. The elements (hobo-brothers) that inhabit the Drosophila genomes of the New World are a counterpart of the canonical hobo found in African Drosophila. Although it is not known when Drosophila arrived in the New World, Throckmorton (1975) proposed Old World[Holartic[Neotropical as the dispersion route for the species of this genus, and Robe et al. (2010) dated the radiation of Neotropical species in pre-Glacial/Tertiary times during which the major radiations occurred from 22 to 42 MYA. Our estimation for the divergence time among the hobo-brothers sequences and canonical hobo was 23–45 MYA, which is compatible with the hypothesis that the ancestral hobo elements arrived in the New World with the ancestral Drosophila and that the canonical hobo and hobo-brothers sequences evolved separately on both sides of the Atlantic. Alternatively, the hobo-brothers elements could have invaded the genomes of New World Drosophila via HTT from an unknown donor. It should be mentioned that the sequence most similar to canonical hobo is not present in another Drosophila species but in the cabbage

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moth Mamestra brassicae (Torti et al. 2005, Ortiz and Loreto 2009). Three different lines of evidence have been used to implicate HTT: (1) phylogenetic incongruence; (2) patchy distribution in the host species and (3) a high similarity of the sequences (Silva et al. 2004; Loreto et al. 2008). hobobrothers elements show patchy distribution in the host species, a high sequence similarity (indeed, some species belonging to different subgenera share identical sequences) and phylogenetic incongruences have been observed, suggesting that these elements have undergone HTT. Time estimations indicate that much of the HTT events occurred very recently, from 0.2 to 2.0 MYA. Furthermore, for some pairwise comparisons, the estimation is zero, suggesting that horizontal transfer in the recent past. Drosophila has been used as a model for more than a century, and a significant body of knowledge has accumulated with regard to the phylogenetic relationships, geographic distribution and ecology of this genus. The availability of 21 sequenced genomes provides the opportunity to address evolutionary processes through new approaches. Moreover, since the description of the horizontal transfer of P element between D. willistoni and D. melanogaster (Daniels et al. 1990b), this genus has been an important model for the study of HTT (Wallau et al. 2012). Based on the current knowledge, it has recently been possible to reconstruct scenarios that suggest the time and location of HTT events. The first study to describe waves of HTT was Silva and Kidwell (2000), which addressed P element among flies of the saltans and willistoni species groups, occurring from 1.5 to 2.5 MYA in the Neotropics. Other examples have since been reported. Mota et al. (2010) dated an HTT event in the hAT element harrow and also established the geographical distribution overlap of the species involved in these HTT events. Although the species involved were different from the species groups of Silva and Kidwell (2000), coincidentally the time and location found for the harrow HTT waves were similar (Neotropics from 1.5 to 2.5 MYA). Depra´ et al. (2010) studied other hAT element involved in HTT, hosimary, which was related by HTT to flies of the melanogaster group and flies from the Zaprionus genus, occurring in Africa from 1 to 2 MYA. Carareto (2011) has described four other HTT events among species of the melanogaster group and Zaprionus, suggesting that geographical sympatry was an imperative for the occurrence of HTT. In the present study, the use of the Drosophila model allowed us, at least for some TEs, to elucidate an important step for genomic evolution: the location and time of the invasion of these TEs. Our data suggest that the sister clade of hobo element originated in the New World from an ancestor that arrived with the Drosophila strains that colonized this part of the world in the Tertiary. Given that

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some sequences are identical in distantly related species, these elements are putatively experiencing HTT at the present time, or at least these sequences were able to perform HTT in the recent past. Acknowledgments We thank Dr. Lizandra Robe and Gabriel Wallau for suggestions. This study was supported by research grants and fellowships from CAPES (Coordenac¸a˜o de Aperfeic¸oamento de Pessoal de Nı´vel Superio), CNPq-Conselho Nacional de Desenvolvimento Cientı´fico e Tecnolo´gico, PRONEX-FAPERGS (10/00287) and Fapergs (11/0938-0).

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