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Logo of gbeAboutAuthor GuidelinesEditorial BoardGenome Biology and Evolution
Genome Biol Evol. 2010; 2: 656–664.
Published online 2010 August 6. doi:  10.1093/gbe/evq050
PMCID: PMC2997563

Pervasive Horizontal Transfer of Rolling-Circle Transposons among Animals


Horizontal transfer (HT) of genes is known to be an important mechanism of genetic innovation, especially in prokaryotes. The impact of HT of transposable elements (TEs), however, has only recently begun to receive widespread attention and may be significant due to their mutagenic potential, inherent mobility, and abundance. Helitrons, also known as rolling-circle transposons, are a distinctive subclass of TE with a unique transposition mechanism. Here, we describe the first evidence for the repeated HT of four different families of Helitrons in an unprecedented array of organisms, including mammals, reptiles, fish, invertebrates, and insect viruses. The Helitrons present in these species have a patchy distribution and are closely related (80–98% sequence identity), despite the deep divergence times among hosts. Multiple lines of evidence indicate the extreme conservation of sequence identity is not due to selection, including the highly fragmented nature of the Helitrons identified and the lack of any signatures of selection at the nucleotide level. The presence of horizontally transferred Helitrons in insect viruses, in particular, suggests that this may represent a potential mechanism of transfer in some taxa. Unlike genes, Helitrons that have horizontally transferred into new host genomes can amplify, in some cases reaching up to several hundred copies and representing a substantial fraction of the genome. Because Helitrons are known to frequently capture and amplify gene fragments, HT of this unique group of DNA transposons could lead to horizontal gene transfer and incur dramatic shifts in the trajectory of genome evolution.

Keywords: Helitrons, insect viruses, transposable elements, lateral transfer


The movement of genetic material between reproductively isolated species, known as horizontal transfer (HT), is known to be an important process in genome evolution. In eukaryotes, this has been shown in the case of genes (for review, see Anderson 2005; Keeling and Palmer 2008) and, more recently, with transposable elements (TEs) (e.g., Silva et al. 2004; Casse et al. 2006; Diao et al. 2006; de Boer et al. 2007; Loreto et al. 2008; Pace et al. 2008; Bartolome et al. 2009; Roulin et al. 2009). TEs are mobile, parasitic pieces of genetic material that can mobilize and replicate within the host genome. Their inherent ability to replicate and integrate into the genome is likely to make them prone to HT (Kidwell 1992). HT has been proposed as an essential part of the lifecycle of some types of TEs in order to avoid co-evolved host suppression mechanisms aimed at limiting their mobility within lineages (Hartl et al. 1997; Silva et al. 2004). It has also been proposed that the propensity for HT could be related to the mechanism of transposition used (see Schaack, Gilbert and Feschotte 2010 for review). TEs are classified based on whether they move via an RNA intermediate (Class 1) or a DNA intermediate (Class 2), with further divisions based on the mechanism of integration (Wicker et al. 2007).

A unique group of rolling-circle (RC) DNA transposons called Helitrons (with atypical structural characteristics including 5′ TC and 3′ CTRR termini and a 16 to 20-nt palindrome upstream of the 3′ end [Feschotte and Wessler 2001; Kapitonov and Jurka 2001]) have been described in a wide array of eukaryotes including fungi (Poulter et al. 2003; Cultrone et al. 2007), plants (Kapitonov and Jurka 2001; Lal et al. 2003; Rensing et al. 2008; Yang and Bennetzen 2009a), insects (Kapitonov and Jurka 2001; Poulter et al. 2003; Langdon et al. 2009; Yang and Bennetzen 2009a; The International Aphid Genomics Consortium 2010), nematodes (Kapitonov and Jurka 2001), and vertebrates (Poulter et al. 2003; Zhou et al. 2006; Pritham and Feschotte 2007). In some cases, Helitrons constitute a significant portion of the genomes (e.g.,Caenorhabiditis elegans, Arabidopsis thaliana, Myotis lucifugus). Helitrons, unlike most other DNA transposons that use transposase, putatively encode a protein with a rolling circle initiator motif and PIF1-like DNA helicase domains and are categorized in their own subclass (Kapitonov and Jurka 2001; Wicker et al. 2007). Homology of the Helitron-encoded protein to bacterial RC transposons (IS91, IS1294, IS801), which are well known for their propensity to shuttle antibiotic resistance genes between distinct bacterial species (Toleman et al. 2006), reveals a distant relationship (Kapitonov and Jurka 2001). Like their bacterial cousins, some Helitrons function as “exon shuffling machines” (Feschotte and Wessler 2001). This ability is particularly pronounced in maize where it is estimated that at least 20,000 gene fragments have been picked up and shuffled by Helitrons (Du et al. 2009; Feschotte and Pritham 2009; Yang and Bennetzen 2009b). The ability to seize and recombine exons from multiple genes to create novel genetic units (Brunner et al. 2005; Gupta et al. 2005; Lal and Hannah 2005; Morgante et al. 2005; Xu and Messing 2006; Pritham and Feschotte 2007; Jameson et al. 2008; Langdon et al. 2009) makes HT of Helitrons especially intriguing because they can shuttle gene fragments between genomes.

This study expands our understanding of HT of TEs in several ways. First, we provide the first evidence for widespread, repeated HT of Helitrons, a distinctive group of transposons with a unique mechanism of replication. Second, in contrast to previous reports of widespread HT which have involved only hAT superfamily elements distributed largely among vertebrates (Pace et al. 2008; Gilbert et al. 2010), we show horizontally transferred Helitrons are frequently found in insect genomes. However, we have also identified cases of Helitron HT in vertebrates (bat, lizard, and jawless fish), a patchy distribution that indicates that certain host genomes are especially vulnerable to invasion. Third, this is the first report of Helitron HT in insect viruses, which could act as shuttle systems for the delivery of DNA between species (Loreto et al. 2008). Although HT has occasionally been invoked to explain discordant distributions in isolated cases (Kapitonov and Jurka 2003; Lal et al. 2009), our discovery of horizontally transferred Helitrons in viruses, insects, and vertebrates demonstrates the widest range of extensive HT among animals and possible vectors so far.

Materials and Methods

Helitrons identified in Myotis lucifugus (the little brown bat) were used as an initial query (BlastN using default parameters (BlastN… [Altschul et al.1990]) to find Helitrons in other genomes available at the National Center for Biotechnology Information, including the whole genome shotgun, nucleotide collection (nr/nt), genome survey sequences, high throughput genomic sequences, and expressed sequence tag databases. Hits that were ≥65% identical to the query over >300 bp were examined and, when possible, full-length Helitrons were manually extracted. These elements were used as queries to find additional related Helitrons; the resulting hits were examined, and full-length Helitrons were extracted to generate a library of Helitrons for each species (details on all methods are in supplementary Materials and Methods, Supplementary Material online). Helitrons were then classified into families based on the following criteria according to Yang and Bennetzen (2009a, 2009b). We established conservative criteria to identify cases of HT that could be fully analyzed, including >80% identity at the 3′ end, a >400 bp portion of the internal region that is >80% identical, and divergence estimates among species that exclude the possibility of vertical inheritance (supplementary materials and methods, Supplementary Material online). Helitrons that share high levels of identity (>80%) from the same family in multiple species were aligned using MUSCLE (Edgar 2004) and analyzed as a group (including calculations of pairwise divergence [MEGA 4.0.2; Tamura et al. 2007], abundance [RepeatMasker version 3.2.7; A. F. A. Smit, R. Hubley, and P. Green,], and, when possible, calculations of amplification date estimates [as in Pritham and Feschotte 2007; Pace et al. 2008]).


Identification, Classification, and Characterization of Helitrons

In a previous study, Helitrons were reported only in the little brown bat, M. lucifugus, among the 44+ publicly available mammalian genome sequences (Pritham and Feschotte 2007) that suggested the acquisition of these elements via HT. Because M. lucifugus is a good candidate for investigating possible HT, a deeper survey of Helitrons was performed, a previously uncharacterized family (HeligloriaB_Ml) was identified, and was used as a starting point for a series of Blast searches. These searches led to the subsequent identification of Helitrons from animals and animal viruses which were then classified into families based on their identity at the 3′ end (for family designation) and 5′ end (for subfamily designation), as in Yang and Bennetzen (2009a, 2009b; see Materials and Methods): the families were named Heligloria, Helisimi,Heliminu, and Helianu. Cases of recent HT were identified and analyzed when Helitrons of the same family that exhibited >80% identity at the 3′ end and contained a >400 bp portion of the internal region with >80% identity (see Materials and Methods) were found in diverged species (>35 million years ago [Ma]). Helitrons demonstrating high levels of identity that were inconsistent with vertical descent were found in many taxa, including insect viruses, many invertebrates (e.g., insects, nematodes, annelids, molluscs, and planaria), and vertebrates (e.g., salamanders, lizards, snakes, jawless fish, and bat; see supplementary table S1, Supplementary Material online). Those cases for which there were sufficient data to fully analyze the evidence for HT include the little brown bat (M. lucifugus; Chiroptera, Mammalia), sea lamprey (Petromyzon marinus; Petromyzontiformes, Cephalaspidomorphi), green anole (Anolis carolinensis; Squamata, Reptilia), triatomine bug and aphid (Rhodnius prolixus, Acyrthosiphon pisum; Hemiptera, Insecta), fruit flies (Drosophila ananassae, D. willistoni, D. yakuba; Diptera, Insecta), silkworm moth (Bombyx mori; Lepidoptera, Insecta), and two polydnaviruses which are symbiotically associated with hymenopteran wasps (Hymenoptera, Insecta), Cotesia sesamiae Mombasa Bracovirus (CsMBV) and Cotesia plutella Bracovirus (CpBV; see table 1).

Table 1
Distribution and Characterization of Four Helitron Families Including Evidence for HT Across Taxa

Among the four families of Helitrons, Heligloria (which contains two subfamilies based on divergence at the 5′ end, HeligloriaA and HeligloriaB [fig. 1a]) is the most widely distributed across taxa. Furthermore, the subfamily HeligloriaA includes two exemplars (HeligloriaAi and HeligloriaAii) based on the presence of two unique internal regions. A putative autonomous representative (HeligloriaAi) was found in six different insect species (D. yakuba, D. ananassae, D. willistoni, A. pisum, R. prolixus, and B. mori) with levels of sequence identity ≥90% (over 768–3,927 bp) based on pairwise comparisons of the internal region (see supplementary Dataset S1, table S3.1, fig 1b, Supplementary Material online). HeligloriaAii is present in B. mori and two polydnaviruses (CpBV and CsMBV), which have a segmented genome in viral particles and an integrated form (provirus) in the genome of parasitic hymenopteran wasps in which they reside, C. plutella and C. sesamiae (Dupuy et al. 2006; see Discussion). These two polydnaviruses are associated with the braconid wasps, C. plutella and C. sesamiae, and both contain short, nonautonomous copies of HeligloriaAii. Because the Cotesia genus is 10 My old (Dupuy et al. 2006), we included only one of the two species in our analysis of HT (table 1). The subfamily HeligloriaB is present in M. lucifugus, A. carolinensis, R. prolixus, and P. marinus. It has a unique 5′ end and internal region compared with HeligloriaAi and HeligloriaAii. HeligloriaB is 88% identical over 579 bp between these four species (see alignment, supplementary fig. S1, Supplementary Material online). Fragments of HeligloriaB with high sequence identity (84–96%) are also present in mole salamanders, snakes, and in nematodes (see supplementary table S1, Supplementary Material online).

Fig. 1.
(a) Alignment of 5' and 3' ends (30 bp) of Heligloria (Hg) elements from species into which the element has horizontally transferred (for criteria, see Materials and Methods and supplementary table S1, Supplementary Material online for additional species ...

The second family of Helitrons, called Helisimi, was identified in D. ananassae, D. willistoni, A. pisum, R. prolixus, B. mori, and CsMBV. On average, these elements are 87% identical over 463 bp across species that diverged >300 Ma (fig. 2). Pairwise comparisons of individual elements reveal high sequence identity (81–96%) over 469–4,548 bp (supplementary Dataset S1, Supplementary Material online). Although there are no subfamilies within this family, there are two clusters, each of which are 98% identical (supplementary table S3.2, Supplementary Material online), with 81–83% identity between groups. Two copies of Helitrons were found in the C. sesamiae Mombasa bracovirus genome, one copy is intact with a 5′ and 3′ end but has captured host genomic sequence and the other copy is truncated at the 5′ end. The Helitron copy with the intact ends was also found at the orthologous position in the Kitale strain of the virus (supplementary fig. S5 and table S2, Supplementary Material online). Fragments of Helisimi were identified in several other Drosophilids as well; however, the short divergence times between these species prevent us from ruling out the possibility of vertical inheritance, and thus they were excluded from this analysis (see supplementary table S1, Supplementary Material online).

FIG. 2.
Schematic representation of phylogenetic relationships among animal lineages and estimated divergence times (Ma). Presence of horizontally transferred Helitrons from four different families in each lineage are denoted by rectangles (not placed relative ...

The families Heliminu and Helianu were identified in insects only. Heliminu is 93% identical over a region of 1,378 bp across species (table 1 and supplementary table S3.3, Supplementary Material online). A pairwise comparison of copies from A. pisum and B. mori reveals that elements are 95% identical over 4,000 bp (supplementary Dataset S1, Supplementary Material online). The fourth family, Helianu, was identified in D. willistoni, D. ananassae, and B. mori. Across these three species, Helianu is 97% identical over 1,894 bp (table 1 and supplementary table S3.4, Supplementary Material online) and pairwise comparisons between species extend the region of identity to 2,600 bp (supplementary Dataset S1, Supplementary Material online). Fragments of copies of Heliminu and Helianu (>90% identical) are also present in a variety of other insects, including butterflies, moths, flies, and fleas (see supplementary table S1, Supplementary Material online). Paralogous or orthologous empty sites were identified for at least one member from each family to confirm the mobility of these elements (supplementary fig. S2, Supplementary Material online). The putative autonomous elements encode all the expected motifs and domains consistent with other described animal protein-coding Helitrons (Rep and helicase; supplementary fig. S3a, b, Supplementary Material online).

Species-Specific Proliferation of Helitrons and Timing of Amplification

In the case of all four families, Helitrons have proliferated via amplification of nonautonomous copies. In the case of HeligloriaB, the autonomous partner responsible for the amplification of the non-autonomous elements was not identified in the genome sequences of bat, lizard, and insect. However, we were able to detect autonomous copies of HeligoriaB in the jawless fish genome sequence (supplementary table S2, Supplementary Material online). However, we were able to detect autonomous copies of HeligloriaB in jawless fish in the UCSC genome browser (supplementary table S2, Supplementary Material online). The discovery of autonomous partners for this family was likely hindered by low genome coverage and the older age of the family. It may be that with higher sequencing coverage or examination of additional genomes that the autonomous copies might be discovered.

Copy number varies across species but in some cases is high (up to 677 copies; table 1). Because we used the last 30 bp of the 3′ end, copy number estimates include all subfamilies. To estimate how much of the genome is occupied by each Helitron family, individual genomes were masked by the four families of Helitrons (not only the last 30 bp but with the entire element [table 1]). The apparent discrepancy in the copy number estimation and percent genome occupied is due to the difference in the methods employed. Some Helitrons tend to capture new 3′ ends, retaining the 5′ end and internal region. In those cases, copy number estimate (based on Blast with 3′ end) will be lower than the RepeatMasker estimate (based on the entire element). Helitron families appear to have differentially amplified or been retained in each host species (fig. 3), Helisimi is the most “successful,” having amplified in B. mori to such an extent that it constitutes 0.2% of the genome and contributes almost 0.8 Mb of DNA (table 1). The timing of amplification of HeligloriaB_Ml in bat was estimated based on the average divergence of copies from the consensus sequence (3.8%) to be 14.1 Ma based on the neutral substitution rate as in Pace et al. (2008). In most of the cases, it was not possible to use this method because of difficulty reconstructing a consensus to estimate the ancestral copy and the lack of data on mutation rates. In these cases, the percent divergence between a given Helitron copy (representative of a particular family) and its second-best hit (not with itself) were used as a proxy to estimate the relative timing of amplification (see supplementary table S4, Supplementary Material online). Even though Helitrons appear to be recently active in many genomes (≥99% identity between copies of some families in R. prolixus, A. pisum, and B. mori), there were other cases with no signs of recent activity (as low as 75% identity between copies).

Fig. 3.
Distribution of Helitron families (Heligloria, Helisimi, Heliminu, and Helianu) across species and their contribution (shown in Kbp) toward the host genome.

Evidence for HT

The high sequence identity (80–97%) of the Helitrons is not limited to the 5′ and 3′ ends but is also observed in the internal regions of all families (fig. 1a and b and supplementary table S3, Supplementary Material online). In many cases, the sequence identity of the Helitrons is exceptionally high compared with the divergence of the hosts (fig. 2). For example, there is 88% sequence identity between Helitrons in the mammal, M. lucifugus, and the lizard, which diverged 360 Ma and these diverged from the common ancestor of the jawless fish and the insect R. prolixus >600 and >750 Ma, respectively (fig. 2; Hedges et al. 2006). Similar patterns of sequence identity of Helitrons (86–97%) can be observed among insects of different orders (Lepidoptera, Diptera, Hemiptera) and the polydnaviruses inhabiting the hymenopteran parasitic wasps. The insects belonging to these orders diverged from their common ancestor >200 Ma (in the case of Diptera and Lepidoptera) and up to 350 Ma (in the case of Hemiptera). Previous work on TEs suggests that that these elements are not under host selective constraints (Silva and Kidwell 2000; Pace et al. 2008), and instead, TEs evolve neutrally upon inactivation of their transposition in the host genomes. The highly fragmented nature and lack of intact open reading frames of the Helitrons identified further supports the idea of lack of active transposition. The levels of divergence observed among Helitrons in these species are much lower than what would be expected based on direct estimates of neutral substitutions rates (e.g., 5.8 × 10−8 mutations per site per year in Drosophila [Haag-Liautard et al. 2007]) given the current estimates of their divergence times (Hedges et al. 2006). Thus, HT is the best explanation for the exceedingly high sequence identity displayed by these TEs across widely diverged species. Another line of evidence that can be used to exclude the possibility of vertical transfer is the discontinuous presence of these elements across different species represented in the database. All four families of Helitrons have a patchy distribution with high sequence identity among vertebrates and insects (figs. 2 and and3).3). Although, it should be noted that false negative results might occur in genomes with low sequencing coverage and few copies. However, to attribute the patchy distribution observed here to vertical inheritance would require a nonparsimonious scenario of many cases of independent loss and intense activity in a small subset of lineages.


This is the first report of the HT of Helitrons among a diverse array of animal species. We identified 25 definitive cases of HT involving four families of Helitrons and nine animal species, including vertebrates and invertebrates that diverged, in some cases, more than 700 Ma (fig. 2 and table 1; for additional cases, see supplementary table S1, Supplementary Material online). Very high sequence identity among species (80–97%), in conjunction with the extremely fragmented nature of the Helitrons identified, preclude the possibility of vertical inheritance and selective constraint as an explanation for the similarity observed between elements across species. Our data reveal interesting patterns within the patchy distribution among animals, including the repeated invasion of some genomes by multiple Helitron families (figs. 2 and and3).3). Although some families (Heliminu and Helianu) are restricted to insects, HeligloriaB has invaded mammals, reptiles, and jawless fish, in addition to several insect species (table 1 and supplementary table S1, Supplementary Material online). Remarkably, two of the four Helitron families were also found in polydnaviruses that are involved in facilitating the parasitism of lepidopterans by hymenopteran wasps. We propose that the presence of Helitrons in viruses may reflect their role as vectors for HT between parasitic wasps and their hosts, although other routes of HT also likely exist.

Mechanisms of Transfer

The remarkable breadth of species involved in these cases of HT (including not only bat, lizard, jawless fish but also triatomine bug, silkworm, aphid, drosophilids, and bracoviruses) suggests multiple mechanisms may underlie the horizontal spread of TEs. The identification of Helitrons in bracoviruses (double-stranded DNA viruses; Polydnaviridae family) is of particular interest as a potential vector for the delivery of TEs among species. These viruses have an obligatory relationship with parasitic wasps belonging to the Braconidae family, replicating only in wasp ovary cells and releasing fully formed viral particles during oviposition by the wasp into the lepidopteran larvae. The viral particles encode virulence factors that suppress the immunity of the lepidopteran (e.g., for review, see Webb et al. 2009), facilitating the growth of the wasp larvae. Yoshiyama et al. (2001) suggested that the close association between the parasitoid wasp and moth facilitates the HT of TEs, as in the case of the “mariner” element transferred between the braconid parasitoid wasp, Ascogaster reticulatus, and its moth host, the smaller tea tortrix, Adoxophyes honmai. There have been several reports of TE-like sequences in the genomes of DNA viruses (Miller DW and Miller LK 1982; Fraser et al. 1983; Fraser 1986; Friesen and Nissen 1990; Jehle et al. 1998; Drezen et al. 2006; Piskurek and Okada 2007; Desjardins et al. 2008; Marquez and Pritham 2010). If viruses shuttle TEs from one species to another, we might expect to see biased distributions of horizontally transferred TEs based on host susceptibility to a particular virus group. In fact, our data reveal biased distributions (e.g., Helisimi and Heliminu are only found in insects, whereas HeligloriaB is frequently found in vertebrates); however, the sampling bias of the available databases also influences our ability to detect patterns or identify mechanisms based on distribution.

In addition to viruses, some parasitic insects have also been implicated as agents of HT because of their intimate association with their hosts (e.g., Houck et al. 1991). Gilbert et al. (2010) recently found evidence for the HT of four DNA transposon families in R. prolixus and a wide array of tetrapods. Because R. prolixus is a sanguivorous parasite of mammals and vertebrates, transfer of DNA could occur through salivary deposition or blood intake by this species. The presence of closely related Helitrons in R. prolixus and M. lucifugus, a host of R. prolixus, further indicates this bug may be a candidate vector for transferring TEs. Other proposed mechanisms of transfer include endosymbiotic bacteria such as Wolbachia (Hotopp et al. 2007). It is known that Wolbachia infect C. sesamiae wasps (Mochiah et al. 2002), drosophilids, aphids (Jeyaprakash and Hoy 2000; The International Aphid Genomics Consortium 2010), Rhodnius sp. (Espino et al. 2009), and even nematodes (Fenn et al. 2006). In addition to the possibility of HT through Wolbachia, the bacteriophage of Wolbachia is also a potential vector for HT (Gavotte et al. 2007; Loreto et al. 2008). Additional experiments and taxon sampling are necessary to further delineate the role of host–parasite interactions and other intermediates such as bacteria and viruses, in the direction and frequency of HT of TEs and the as of yet unknown mechanisms underlying this process.

Impact on Genome

Diverse mechanisms of HT can lead to recurrent invasions of genomes by Helitrons, thereby increasing the dynamic portion of the genome. The proposed rolling circle-like transposition mechanism could explain the tandem duplicates and arrays generated by Helitrons (supplementary fig. S4, Supplementary Material online, Pritham and Feschotte 2007; Schaack et al. 2010, Choi et al. 2010). The frequent capture of new 3′ and 5′ ends without disrupting their ability to transpose could extend the lifespan of Helitrons in the host genome and generate genetic diversity among elements. Their proposed replication mechanism also likely explains their unique propensity to capture host gene fragments, which could have a tremendous impact on the genome (e.g., Brunner et al. 2005; Gupta et al. 2005; Morgante et al. 2005; Xu and Messing 2006; Jameson et al. 2008; Du et al. 2009; Langdon et al. 2009; Yang and Bennetzen 2009b). Indeed, in M. lucifugus, HelibatN3 has captured the promoter and first exon of the NUBPL (a single copy gene which is highly conserved in mammals) and amplified it to high copy number (>1,000; Pritham and Feschotte 2007). Amplification is thought to closely follow invasion of a naive genome (Pace et al. 2008) and results in opportunities for genetic innovation. Genetic innovation, in turn, leads to diversification within the lineage, a possibility supported by the occurrence of multiple waves of TE invasion in the bat lineage around the time of their rapid diversification, 16–25 Ma (Teeling et al. 2005; Pritham and Feschotte 2007; Ray et al. 2008; Oliver and Greene 2009; Zeh et al. 2009; Gilbert et al. 2010). We conclude that the HT, colonization, and amplification of Helitrons are rampant and widespread across animals and can play a major role in genome evolution.

Supplementary Material

Supplementary dataset, materials and methods, figures S1S5, and tables are available at Genome Biology and Evolution online (


This work was supported by start-up funds from the University of Texas-Arlington to E.J.P. and National Science Foundation award 0805546 to S.S. We would like to acknowledge the genome sequencing consortiums for sequencing the M. lucifugus, A. carolinensis, P. marinus, and R. prolixus and C.sesamiae bracovirus genomes. We would also like to thank Brian Fontenot, Matt Carrigan, and two anonymous reviewers for helpful comments on the manuscript.


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