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Article

Revealing Landscapes of Transposable Elements in Apis Species by Meta-Analysis

by
Kakeru Yokoi
1,*,
Kiyoshi Kimura
2 and
Hidemasa Bono
3,4
1
Insect Design Technology Group, Division of Insect Advanced Technology, Institute of Agrobiological Sciences, National Agriculture and Food Research Organization (NARO), 1-2 Owashi, Tsukuba, Ibaraki 305-8634, Japan
2
Smart Livestock Facilities Group, Division of Advanced Feeding Technology Research, National Institute of Livestock and Grassland Science (NILGS), National Agriculture and Food Research Organization (NARO), Tsukuba, 2 Ikenodai, Tsukuba, Ibaraki 305-0901, Japan
3
Laboratory of BioDX, Genome Editing Innovation Center, Hiroshima University, 3-10-23 Kagamiyama, Higashi-Hiroshima City, Hiroshima 739-0046, Japan
4
Laboratory of Genome Informatics, Graduate School of Integrated Sciences for Life, Hiroshima University, 3-10-23 Kagamiyama, Higashi-Hiroshima City, Hiroshima 739-0046, Japan
*
Author to whom correspondence should be addressed.
Insects 2022, 13(8), 698; https://doi.org/10.3390/insects13080698
Submission received: 20 June 2022 / Revised: 29 July 2022 / Accepted: 1 August 2022 / Published: 3 August 2022
(This article belongs to the Section Insect Molecular Biology and Genomics)
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Abstract

:

Simple Summary

Studies on the detection of transposable elements and their annotations have posed several challenges. For example, simple comparisons of transposable elements in different species using different methods can lead to misinterpretations. Thus, assembling data for transposable elements analyzed by unified methods is important for comparison purposes. Therefore, we performed a meta-analysis of transposable elements identified using genome datasets from five Apis species (11 sets of genome data) and specific software to detect the transposable elements, which revealed the landscapes of transposable elements. We examined the types and locations of transposable elements in the Apis genomes. The landscapes of transposable elements showed that four to seven transposable element families among 13 and 15 families of TEs detected in classes I and II, respectively, consisted mainly of Apis-associated transposable elements. These families include DNA/TcMar-Mariner and DNA/CMC-EnSpm. In addition, more DNA/TcMar-Mariner consensus sequences and copies were detected in Apis mellifera than in other Apis species. These data suggest that TcMar-Mariner might exert A. mellifera-specific effects in the host A. mellifera species. Our landscape data provide new insights into Apis transposable elements; furthermore, detailed analyses of our data could pave the way for new biological insights in this field.

Abstract

Transposable elements (TEs) are grouped into several families with diverse sequences. Owing to their diversity, studies involving the detection, classification, and annotation of TEs are difficult tasks. Moreover, simple comparisons of TEs among different species with different methods can lead to misinterpretations. The genome data of several honey bee (Apis) species are available in public databases. Therefore, we conducted a meta-analysis of TEs, using 11 sets of genome data for Apis species, in order to establish data of “landscape of TEs”. Consensus TE sequences were constructed and their distributions in the Apis genomes were determined. Our results showed that TEs belonged to four to seven TE families among 13 and 15 families of TEs detected in classes I and II respectively mainly consisted of Apis TEs and that more DNA/TcMar-Mariner consensus sequences and copies were present in all Apis genomes tested. In addition, more consensus sequences and copy numbers of DNA/TcMar-Mariner were detected in Apis mellifera than in other Apis species. These results suggest that TcMar-Mariner might exert A. mellifera-specific effects on the host A. mellifera species. In conclusion, our unified approach enabled comparison of Apis genome sequences to determine the TE landscape, which provide novel evolutionary insights into Apis species.

1. Introduction

Transposable elements (TEs) are mobile DNA sequences that undergo a change in their positions within a genome [1]. TEs occur in diverse forms and are found in the genomes of many species. Numerous effects of TEs on the host species have been reported. To mention some specific effects of TEs, they can serve as a source of mutations, lead to host-genome rearrangements, and change gene expression at the level of transcription. TEs can be divided into two classes: class I and class II (sometimes referred to as retrotransposons and DNA transposons, respectively) [1,2,3]. Class I TEs use an RNA intermediate and a “copy-and-paste” mechanism [1]. Class I TEs are further divided into subclasses (referred to as “order” in [3]), namely long terminal repeats (LTRs), Dictyostelium intermediate repeat sequence (DIRS), and non-LTRs. LTRs are divided into several superfamilies (e.g., Copia, Gypsy, and ERV) while non-LTRs are divided into other several superfamilies (e.g., long interspersed nuclear elements (LINEs), short interspersed nuclear elements (SINEs) and Penelope), several superfamilies of which some are divided into several families. Class II TEs move using a “cut-and-paste” mechanism through a DNA intermediate [1,3,4,5]; however, the Helitron type moves in a “peel-and-paste” manner [6]. Class II TEs are divided into subclasses (orders): terminal inverted repeat (TIR) (possessing transposase in its coding region), Crypton, Helitron, and Marverick. Each category is further classified into subfamilies, of which some are divided into several families [1,3]. For example, Tc1/Mariner is one of the subfamilies belonging to the TIR subclass, and Tc1/Mariner is further classified into Tc1 or Mariner. The TE distributions of each species have specific features. Thus, performing a comparative analysis of the distributions of TEs among several species can potentially uncover some new insights into these species related to their TEs.
Honey bees, which belong to the Hymenoptera; Apidae, are important insects for honey production. They also pollinate wild plants and crops [7] and have been used as models of social insect species. Because of its widespread occurrence, the whole genome sequencing of a representative honey bee species, the western honey bee (Apis mellifera [Am]), was completed at a very early phase among insect species [8]. This led to whole-genome sequencing of other honey bee species, including several Am and A. cerana subspecies. Genome data are currently available in public databases for the following honey bees: A. cerana japonica (Acj) [9], A. cerana Korean native (Ack) [10], A. cerana China native (Acc) [11], A. dorsata (Ad) [12], A. florea (Af), A. laboriosa (Al) [13], A. mellifera carnica (Carniolan honey bee) (Amcar), A. mellifera intermissa (Ami) [14], A. mellifera caucasica (Caucasian honey bee) (Amcau), and A. mellifera (German honey bee) (Amm) (Table 1). Am, A. cerana, Ad, Af are the four major Apis species [7]. Am and Acc genome data were recently updated using the long-read sequencer, and the N50 values have improved dramatically [15,16].
According to these Apis genome reports, Apis genomes contain relatively few TEs, which mainly consist of class II TEs, particularly Mariner-like-elements (MLEs), whereas some other representative insect genomes (e.g., silkworm Bombyx mori [17], yellow fever mosquito Aedes aegypti [18], and red flour beetle Tribolium castaneum [19,20]) contain higher numbers of TEs and MLEs.
Due to their ability to “transpose” within the genome, TEs have increased in number within the genome during evolution. In addition, new TEs enter the genome via horizontal transmission from other species. TE sequences have high diversity, due to the accumulation of mutations, which leads to many variants [1,21]. TE insertion and removal can indirectly cause rearrangements in host-genome sequences, leading to duplications or reshuffling around TEs in the host genome. These events can occur in genes or expression-regulation sites. Moreover, TEs can cause genome structural diversities long after TE could lose the capacity to move. Therefore, accurate TE detection and annotation are difficult to achieve. Although the basal TE status of each genome report is important (e.g., simply showing percentages or numbers of TE families or classes present in the genome), comparisons among multiple species are suboptimal because the TE statuses were constructed using different methods and different software versions. Instead, new knowledge related to TEs could be obtained by studying the landscapes of TEs (the types of TEs and their positions in different Apis genomes), applying a unified TE analysis to the Apis genome data, and comparing the TE status between different species.
Comparing TE composition data among different species is important for genomic and evolutionary research, as indicated above. Recently, one report provided basal TE data for various insect species, suggesting that the content and diversity of TEs and genome sizes are related [22]. Other reports have provided evolutionary insights into pogo and Tc1/mariner by comparing the status data for these TE families in Apoidea genomes [23]. In this study, to obtain landscape data for such comparisons, a meta-analysis was performed using genome data from the 11 Apis genome data (5 Apis species) listed in Table 1, which are available in a public database (Figure 1). Specifically, we first performed de novo TE detection and then constructed consensus sequences for TEs with the same parameters, using RepeatModeler2 with the Apis genome data [24]. RepeatModeler2 runs multiple software packages to search for TEs and repetitive sequences, enabling accurate searches for TEs. To perform a detailed classification of the consensus sequences belonging to the Mariner or MLE family (the most prevalent among TE families in Apis genomes), a phylogenetic analysis of MLE consensus sequences was performed. Finally, the distributions of repetitive elements, including the detected TEs, were investigated in all 11 Apis genomes using RepeatMasker, and the TE landscapes of Apis species were drawn. By comparing the TE statuses of different Apis species and making use of the landscape data, we obtained new insights into TEs in Apis species.

2. Materials and Methods

2.1. Genome Data Used in This Study

All genome data used in this study were downloaded from the NCBI Assembly section (https://www.ncbi.nlm.nih.gov/assembly/, accessed on 2 August 2022). The GenBank assembly accession IDs, genome sizes, N50 values, and abbreviations of each genome data point are presented in Table 1.

2.2. De novo Detection of Transposable Elements Consensus Family Sequences

De novo detection of TE consensus family sequences was performed using Repeat Modeler2 (version DEV) with the default settings and the genome data indicated in Table 1 [24].

2.3. Phylogenetic Analysis

The detected TE sequences of some families were aligned using Clustal Omega (version 1.2.4) [25]. To construct approximately maximum-likelihood phylogenetic trees, aln files and Clustal Omega output files were further analyzed using FastTree (version 2.1.10) [26]. To visualize the phylogenetic trees, the FastTree output files (newick files) were loaded into MEGAX (version 10.1.7) [27].

2.4. Distribution Analysis of Repetitive Elements in Apis Genomes

The distributions of repetitive elements (including the TEs detected with RepeatModeler2) were investigated using the TE sequences as libraries and RepeatMasker (version 4.1.2-p1), with the default settings [28]

3. Results

3.1. Detection of Transposable Elements in Apis Genomes

To determine the types of TEs in the Apis genomes, de novo TE detection was performed, and consensus TE family sequences were constructed with RepeatModeler2 using the Apis genomes shown in Table 1. The detection procedure used with RepeatModeler2 was described in detail previously [24]. Briefly, RepeatModeler2 runs different de novo repeat-detection programs such as RECON [29], RepeatScout [30], LtrHarvest [31], and Ltr_retriever [32]. The constructed family models from each software program are merged, redundancies are removed, and consensus sequences are constructed. The consensus sequences are annotated using RepeatClassifier, which compares the consensus sequences to several databases, including Dfam [24]. The output files from RepeatModeler2 are provided in Supplement data S1. The numbers of consensus sequences for each family are shown in Table 2. More consensus sequences were for class II TEs than for class I TEs. Among the class II TEs, DNA/TcMar-Mariner, that is MLE, DNA/TcMar-Tc1, DNA/hAT-Ac, DNA/CMC-EnSpm, and DNA/CMC-PiggyBac consensus sequences were constructed for all or 10 of the 11 Apis genomes studied, whereas the consensus sequences of other families were constructed in less than three Apis genomes. With class I TEs, the consensus sequences of three LTRs (LTR/Copia, LTR/Gypsy, and LTR/Pao) were constructed in more than 9 of the 11 Apis genomes.
Next, we investigated the differences in the numbers of consensus TE sequences among Apis species.. As shown in the “Total (per species)” row of Table 2, more consensus TE sequences were constructed with the A. mellifera species (Am, Ami, Amm, Amcar, and Amcau: 48, 39, 51, 34, and 38, respectively) than with the other Apis species (Acc, Acj, Ack, Ad, and Af: 34, 17, 24 21, and 35, respectively). Furthermore, more DNA/TcMar-Mariner sequences were detected with the A. mellifera species and Acc, representing the highest numbers of a consensus sequence constructed among the TE families. In addition, relatively high numbers of DNA/TcMar-Tc1 sequences were constructed with the A. mellifera species. These findings indicate that differences in the total number of consensus sequences among the A. mellifera species and other Apis species were mainly due to differences in DNA/TcMar-Mariner and DNA/TcMar-Tc1 consensus sequences.

3.2. Sequence Analysis of TcMar-Mariner Consensus Sequences

As indicated in the previous section, the highest numbers of consensus sequences were constructed for the TcMar-Mariner family, among the TE families detected with RepeatModeler2. To obtain a more detailed classification, multiple sequence alignments were performed using the TcMar-Mariner consensus sequences (Supplemental Data S3), Ammar1–6 (which were previously reported as A. mellifera MLEs [7]), and MLE consensus sequences of other species (mentioned in an MLE-related report [20]; Supplemental Data S4), where the subfamilies have been annotated. Based on the alignment results, a phylogenetic tree was constructed (Figure 2 and Supplemental Data S5 contain the raw data and related files). As shown in Figure 2 several clusters formed in the phylogenetic tree. MLEs annotated as a subfamily were expected to be located in a cluster; however, the phylogenetic tree showed that no MLEs belonging to a single subfamily were located in a single cluster. These results showed that the classifications of the MLE subfamilies, which are based on the amino acid sequences of transposase in MLEs, conflicted with the results of the nucleotide sequence-based analyses we performed. All-inclusive count result data are available in Supplemental Data S2.

3.3. Distribution Analysis of Transposable Elements in Apis Genome

To determine the distributions of the TEs detected with RepeatModeler2 in Apis genomes (Section 3.1), we ran RepeatMasker with the Apis reference genome as the input data (Table 1) and the consensus TE sequence data as libraries using Repeat Modeler2 (Supplemental Data S1). RepeatMasker was used to screen the TE sequences (registered in Dfam or Repbase) or the consensus sequences as input data (mainly from RepeatModeler2) and simple repeat sequences as genomic query data (for greater detail, see [28]). Because of these software features, high numbers of short TE sequences were detected. The output files are provided in Supplemental Data S6. The percentages of repetitive elements, including TEs, present in the Apis genomes are shown in Table 3. Our findings indicate that repetitive elements comprised approximately 7 to 12% of the Apis genome regions. The A. mellifera genomes (except for Ami) had higher percentages than the other Apis genomes. The percentages in the Apis genomes were lower than those reported for other insect species. (e.g., approximately 46.8% for B. mori [17], 20% for T. castaneum [20], 65% for A. aegypti [16], and 20% for D. melanogaster [20]).
The RepeatMasker results are summarized in tbl files (RepeatMasker output files) and are available in Supplemental Data S6. Because the summary files did not show the number of copies in the individual TE families, we counted them using. out files and other RepeatMasker output files (Supplemental Data S6). The number of copies belonging to the TE families that were clearly annotated as a TE family member (e.g., DNA and SINE?) plus other repetitive elements (e.g., Simple repeat) in all Apis genomes are given in Supplemental Data S7. The total copy numbers of class II and class I TE families in all Apis genomes are shown in Table 4 and Table 5, respectively. Overall, several TE families had multiple copies. Among these TE families, the TEs of class II had many more copies than those of class I. With regard to class II, more total number of copies (except for Ami) were observed in A. mellifera genomes than in the other Apis genomes (Table 4). In contrast, among the class I TEs, Acj, Ack, and Ami showed lower copy numbers, whereas Am had a higher copy number than the other Apis species (Table 5).
Among the class II TE families, copies of DNA/CMC-EnSpm, DNA/TcMar-Mariner, and DNA/hAT-Ac were detected in all Apis genomes tested (Table 4). Over 1000 copies of DNA/TcMar-Mariner were detected in all A. mellifera species and in Acc and Al. In addition, 1000 DNA/CMC-EnSpm copies were detected in all Apis species tested, except for Ad, Al and Ami, whereas 1000 copies of DNA/hAT-Ac were detected in Am and Amcau genomes. In the case of DNA/TcMar-Tc1, over 1000 copies were detected in all A. mellifera species, but no copies were detected in Ad. Over 400 DNA/PiggyBac copies were detected in some Apis genomes, but no copies were detected in the Acj genome. Among the class I TE families, copies of LTR-Copia were detected in all Apis genomes tested, and copies of LTR-Gypsy and LTR/Pao were detected in 10 and 9 Apis species, respectively.
As shown above, abundant copies of DNA/TcMar-Mariner and DNA/CMC-EnSpm were detected in all Apis genomes tested. To investigate this phenomenon in greater detail, the copy numbers of both TE families in each of the Apis genomes are shown in graphically in Figure 3. In the case of DNA/TcMar-Mariner, A. mellifera species (especially Amm, Amcar, and Amcau) had higher copy numbers than other Apis species (Figure 3A). In the case of DNA/CMC-EnSpm, Am and Amm had higher copy numbers than other Apis species, whereas Ad, Af, Al, and Ami had fewer copies (Figure 3B). We further investigated which consensus TcMar-Mariner sequences, in particular, had many copies (Table 2). As shown in Figure 2, consensus sequences with more than 200 copies (indicated with red circles) were scattered over the trees, and several sequences with red circles were located in a single clade (represented with the green semicircular object). This clade contained the sequences of all Apis species tested, except for Af.

4. Discussion

In this study, we investigated the landscapes of TEs in Apis species using Apis genome data available in public databases; TE consensus sequences were also constructed. Sequence analysis was performed, and phylogenetic trees were constructed to reveal more detailed relationships for the MLEs, the consensus sequences of which are the most diverse among the TE families detected. Consequently, the distributions of repetitive elements, including the constructed consensus TE sequences within the corresponding Apis genomes, were revealed. Our landscapes showed that several limited TE families (from four to seven families among 13 and 15 families detected of classes I and II, respectively, in each Apis genome: see Table 4 and Table 5) are mainly found in Apis genomes.
As described above, detecting TEs in genome sequences is a difficult task because TE sequences have many variants and deletions [21]. Therefore, the results related to TEs can be varied can vary when different methods are adopted. Our meta-analysis was performed using two major software packages that are commonly employed. RepeatModeler2 is commonly used for de novo TE detection with genome data [24]. This software package can also be used to construct consensus sequences. Multiple repeat-searching programs can be run, and merging the results of the program enables accurate detection of TEs (for benchmarking the results, see a previous article that described RepeatModeler2 [24]). RepeatMasker searches for simple repeats and TEs in queried genome data, with consensus sequences serving as the input data [28]. A series of analyses can provide accurate landscape data for TEs in the queried genome. These landscape data can be utilized for further detailed analyses (e.g., comparing the TE status between different species).
The genome assembly level of genome data can affect TE detections. As shown in Table 2, over half of Apis genome data we used from the public database are not “chromosome-level genome assembly data”. TE data in detailed points using scaffold-level genome assembly data and chromosome-level genome assembly data in the same species can be different. However, we think that the genome assembly level can not affect on main features of Apis TEs we showed; for example, limited TE families consisted mainly of TEs and much more copies of DNA/CMC-EnSpm, DNA/TcMar-Mariner in all Apis species genomes, which included various genome assembly levels. It is very interesting to analyze the two levels separately. However, since our goal is to clarify the landscape of TEs in the genus Apis, which is not affected by differences in genome assembly, we did not analyze them separately in this study.
There is adequate and reliable software for de novo TE detection in genome sequences, such as EDTA [33] and REPET [34]). The benchmarking results showed that RepeatModeler2 produced the output file which was similar to the curated libraries using several model species genome data, and showed better status related to the detected family quality and the detected sequences of fragmentation and redundancy than other software tested while these software showed better status related to some cases [24]. Considering these results, we decided to choose RepeatModeler2 for de novo TE detection.
As mentioned in the introduction part, there are more than 10 known species of honey bees, and by examining the four main species (Af, Ad, A. cerana, and Am) and one closely related species (Al) [7] with RepeatModeler2 and RepeatMasker, which were used for de novo TE detections and revealing distributions of the detected TE families respectively, we were able to characterize the TEs common to the genus Apis without using all species, thus providing a “landscape” of the TEs in the genus Apis, which is our goal of this article. Interestingly, although Ad and Al are closely related species, the landscapes showed that there were several different features of TEs between the two species.
With both class II and class I TEs, several families have diverse consensus sequences, whereas the other families had a few consensus sequences in Apis genomes, implying that these TE families might exert several effects on host Apis species through several mechanisms (e.g., gene insertions or alterations at the transcription level) [35,36]. Comparisons of the consensus TE sequences among Apis species revealed that more consensus sequences were constructed for A. mellifera than for the other Apis species, which was mainly due to DNA/Tc-Mariner and DNA/Tc-Tc1 (which have many consensus sequences). These results suggest that some of the TEs could have had effects on A. mellifera species that might not have occurred in other Apis species.
Among the several characteristics of honey bee TEs revealed by the landscape data, it is worth noting the patchy distribution of each TE. Some TEs are identified only in certain Apis species. For example, DNA/MULE-MuDR was only found only in Af and TcMar-Tigger was found only in Acc. Moreover, RC/Heliton was found only in Am and not in any other Am subspecies. This biased and patchy distribution of the TEs is well known in other species [22,23]. The most famous example of such a distribution is the P element, which is present only in certain strains (e.g., P strains) of Drosophila melanogaster [37]. Using this landscape data, we plan to conduct a detailed comparative analysis in the future.
Many Mariner or MLE consensus sequences were constructed for Apis species in this study. As described above, these consensus sequences were constructed using RepeatModeler2, which runs repeat detection programs and annotates the constructed sequences using several databases including Dfam [2,24]. A further detailed classification of these MLEs was performed. This was done by generating alignments and constructing phylogenetic trees using MLE consensus nucleotide sequences that were previously annotated with MLE consensus sequences. Our results revealed that MLE sequences annotated as part of the same MLE subfamily did not form a single clade. MLEs, which have a DD34D catalytic motif in their encoded transposase, are classified into subfamilies based on their transposase amino acid sequences [38,39]. This classification principle must be respected; however, we believe that nucleotide-based classification may also be required. As shown in this study, an enormous number of TE nucleotide sequences can be detected in target genomes because the whole-genome data of many species are available in public databases, and sophisticated TE detection software, such as RepeatModeler2, are now available [24]. Some detected MLEs do not encode transposases of sufficient length because of mutations or deletions in their sequences. Therefore, annotations based on amino acid sequences cannot be used to study such MLE sequences. According to a previous report, annotation methods for studying subfamilies are fraught with problems such as a lack of reproducibility [21]. The development of nucleotide-based annotations of MLE subfamilies is essential for future genome analysis, and our data could lead to future research in this field.
Nucleic acid-based analysis using RepeatModeler2 and RepeatMasker (in this study), and analysis using the consensus amino acid sequence of transposase have yielded several different results [22,23]. However, even if the same genome data are used for nucleic acid-based analysis, the results will differ slightly depending on the method used, and the number of each TE found differs depending on the software used. For example, as mentioned above, we identified many copies of many DNA/TcMar-Tc1 types. However, in a previous analysis using the tblastn method with amino acid sequences against Apoidea genomes, including some Apis genomes [23], these TEs were not found in the Apis genomes. This discrepancy may reflect our method used, which recognizes the Tc1 and Mariner types as different, whereas the previous analysis considered them to be the same type of TEs. Another example is the detection of DNA/CMC-EnSpm in all Apis genomes tested, whereas previous findings indicated that DNA/CMC-EnSpm was absent from the Am genome [40]. This may be because the TEs annotated as DNA/CMC-EnSpm in this study were classified as putative elements, unclassified, or classified Class II TEs. Indeed, Nasonia vitripennis DNA/CMC-EnSpm was registered in Repbase (e.g., EnSpm-2_NVi) [41], and another report showed that CMC TEs were detected in the Am genome [22]. This discrepancy illustrates the difficulty of classifying TEs. However, our landscape was successful in providing a general framework for the TEs of the Apis genus. Further evolutionary studies of TEs will require analysis of the individual TEs found. Recent advances in bioinformatics have made this possible.
RepeatMasker results for the Apis species showed that repetitive elements comprise approximately 7 to 12% of Apis genomes, which is lower than that of many other insect species [20]. However, these percentages are consistent with previous reports [9,10,12,14,15,16], which validate the accuracy of our datasets and the analytical methods used in this study. Comparing the numbers of TEs among Apis species showed that A. mellifera species, with the exception of Ami, have more TEs than other Apis species. Ami showed lower percentages of repetitive elements, perhaps because the N50 value of Ami was much lower than those of other Apis species. Thus, we conclude that A. mellifera species have more repeat regions and TEs than other Apis species.
RepeatMasker detected high numbers of short TEs in Apis genomes. We assume that while some of them are false positives by RepeatMasker, they are TE footprints [39,42], or fragmented sequences of TEs by insertion or deletions. By detailed analysis of such sequences in our landscape data, the dynamics of Apis TEs could be revealed, leading to the biological interpretation of the TEs.
The total number of TE copies in each TE family showed that families with a higher number of consensus sequences had a higher number of elements. In addition, more copies of class II TEs than class I TEs were detected. Furthermore, these results revealed that the TEs of several limited families in both classes (II and I) consisted of Apis TEs. Most of these results have the same tendencies as those of the consensus TE sequences. These results suggest that TEs belonging to limited TE families mostly consist of Apis TEs. A more detailed investigation also revealed more class II TEs in A. mellifera genomes, except for Ami, than in other Apis genomes. TcMar-Mariner/MLEs were identified as a family with a high number of copies in all Apis species tested. The phylogenetic tree revealed that, although several MLE consensus sequences of all Apis species tested (except for Af, which had over 200 copies) were located in a clade, these sequences were scattered in the trees, suggesting that the abundant MLEs may have been copied from many consensus sequences rather than from a very limited number of consensus sequences.
Although clear differences were found in the number and type of TEs between species, it is interesting to note that variation has occurred within species. This may be due to differences in the quality of the genome data. Among the genome data used in this study, the Ami genome data showed a much lower contig N50 number than the other genome data. No significant correlations were found between the contig N50 numbers for the Apis genome data and the numbers and types of TEs. It would be interesting from an evolutionary point of view if the intraspecific variation observed here was not due to differences in the quality of the genome data. Our findings indicate that many TEs increase in number, shift, or propagate horizontally in the genome after subspeciation. Further studies are required to elucidate these differences.
In this study, we performed a meta-analysis of Apis TEs using Apis whole-genome data and TE-detection software. Through this analysis, we determined the landscape data of TEs showing the specific types of TEs and their positions in the Apis genomes. We also showed that several limited TE families exist in Apis genomes and that A. mellifera species have more TEs, mainly due to MLEs. The findings of this study provide several new insights into the genomes of Apis species. The landscape data obtained in this study can be compared to TE data for other species, including Hymenoptera or other insects [20,22,23], leading to findings related to the evolution of TEs between these species. In addition, analyzing our landscape data in greater detail could help elucidate new TE-related biological insights for Apis species.

Supplementary Materials

All supplemental data are available in figshare (DOI: 10.6084/m9.figshare.c.5847335). Supplemental Data S1 Output files (fasta file and stk file) of RepeatModeler2. Out files of family consensus files of transposable elements by RepeatMolder2. {abbreviation of Apis species}.fa and {abbreviation of Apis species}.stk contain consensus sequences with metadata describing transposable element families. The nomenclature of them is shown in [2] (DOI: 10.6084/m9.figshare.19189004). Supplemental Data S2 Numbers of transposable element consensus sequences of all families constructed in all the Apis genomes tested by RepeatModeler2 (DOI: 10.6084/m9.figshare.19189127). Supplemental Data S3 Consensus sequences annotated as Mariner in Apis genomes by RepeatModeler2. All sequences were extracted from RepeatModeler2 output fasta files. Abbreviations of Apis species are shown in Table 1 (DOI: 10.6084/m9.figshare.19189055). Supplemental Data S4 Consensus Mariner sequence files from other papers used for phylogenetic tree analysis. Ammar1–6 (Ammar.fa) are listed in the supplemental information of [8]. Other sequences (MLE.otherspecies.fa) are shown in Additional file 1 of [20] and the Genbank ID of each sequence is shown in a description part (DOI: 10.6084/m9.figshare.19189073). Supplemental Data S5 Phylogenetic analysis-related data. MLE_tree_ana.fa is Input data including all MLE consensus sequences plus Ammar and other species shown in (all_Mariner.fa, Ammar.fa and MLE.otherspecies.fa). MLE_tree_ana.aln is Clustal omega output file (aln), and MLE_tree_ana.newick is FastTree output data (newick). Trees.png is a high-resolution phylogenetic tree picture (DOI: 10.6084/m9.figshare.19189181). Supplemental Data S6 Output files of RepeatMasker using TE consensus sequence files by RepeatModeler2 and Apis genome sequences. (DOI: 10.6084/m9.figshare.19189292). Supplemental Data S7 Copy numbers of TEs in Apis genomes. Numbers of TEs are counted using RepeatMasker out files in Supplemental Data S6 (DOI: 10.6084/m9.figshare.19189376).

Author Contributions

Conceptualization, K.Y., K.K. and H.B.; methodology, K.Y., K.K. and H.B.; data validation, K.Y.; formal data analysis, K.Y.; data curation, K.Y., K.K. and H.B.; writing—original draft preparation, K.Y.; writing—review and editing, K.Y., K.K. and H.B.; supervision, K.Y.; project administration, K.Y.; funding acquisition, K.Y. and H.B. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by ROIS-DS-JOINT (026RP2019 and 030RP2018) to KY and by the National Bioscience Database Center of the Japan Science and Technology Agency (JST) and Hiroshima Prefectural Government to HB. This work was also supported by the Center of Innovation for Bio-Digital Transformation (BioDX), an open innovation platform for industry-academia co-creation (COI-NEXT) of JST (COI-NEXT, JPMJPF2010) to K.Y. and H.B., and JSPS KAKENHI Grant Numbers 21H03831 and 21K19126 to K.Y.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

All data in this study are available in figshare as described in “Supplementary Materials”.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Bourque, G.; Burns, K.H.; Gehring, M.; Gorbunova, V.; Seluanov, A.; Hammell, M.; Imbeault, M.; Izsvák, Z.; Levin, H.L.; Macfarlan, T.S.; et al. Ten Things You Should Know about Transposable Elements. Genome Biol. 2018, 19, 199. [Google Scholar] [CrossRef]
  2. Storer, J.; Hubley, R.; Rosen, J.; Wheeler, T.J.; Smit, A.F. The Dfam Community Resource of Transposable Element Families, Sequence Models, and Genome Annotations. Mob. DNA 2021, 12, 2. [Google Scholar] [CrossRef]
  3. Wicker, T.; Sabot, F.; Hua-Van, A.; Bennetzen, J.L.; Capy, P.; Chalhoub, B.; Flavell, A.; Leroy, P.; Morgante, M.; Panaud, O.; et al. A Unified Classification System for Eukaryotic Transposable Elements. Nat. Rev. Genet. 2007, 8, 973–982. [Google Scholar] [CrossRef]
  4. Greenblatt, I.M.; Alexander Brink, R. Transpositions of Modulator in Maize into Divided and Undivided Chromosome Segments. Nature 1963, 197, 412–413. [Google Scholar] [CrossRef]
  5. Rubin, G.M.; Kidwell, M.G.; Bingham, P.M. The Molecular Basis of P-M Hybrid Dysgenesis: The Nature of Induced Mutations. Cell 1982, 29, 987–994. [Google Scholar] [CrossRef]
  6. Grabundzija, I.; Messing, S.A.; Thomas, J.; Cosby, R.L.; Bilic, I.; Miskey, C.; Gogol-Döring, A.; Kapitonov, V.; Diem, T.; Dalda, A.; et al. A Helitron Transposon Reconstructed from Bats Reveals a Novel Mechanism of Genome Shuffling in Eukaryotes. Nat. Commun. 2016, 7, 10716. [Google Scholar] [CrossRef] [PubMed]
  7. Winston, M. The Biology of the Honey Bee; Harvard University Press: Cambridge, MA, USA, 1991. [Google Scholar]
  8. Weinstock, G.M.; Robinson, G.E.; Gibbs, R.A.; Worley, K.C.; Evans, J.D.; Maleszka, R.; Robertson, H.M.; Weaver, D.B.; Beye, M.; Bork, P. Insights into Social Insects from the Genome of the Honeybee Apis Mellifera. Nature 2006, 443, 931–949. [Google Scholar]
  9. Yokoi, K.; Uchiyama, H.; Wakamiya, T.; Yoshiyama, M.; Takahashi, J.-I.; Nomura, T.; Furukawa, T.; Yajima, S.; Kimura, K. The Draft Genome Sequence of the Japanese Honey Bee, Apis Cerana Japonica (Hymenoptera: Apidae). Eur. J. Entomol. 2018, 115, 650–657. [Google Scholar] [CrossRef]
  10. Park, D.; Jung, J.W.; Choi, B.-S.; Jayakodi, M.; Lee, J.; Lim, J.; Yu, Y.; Choi, Y.-S.; Lee, M.-L.; Park, Y. Uncovering the Novel Characteristics of Asian Honey Bee, Apis Cerana, by Whole Genome Sequencing. BMC Genom. 2015, 16, 1. [Google Scholar] [CrossRef]
  11. Diao, Q.; Sun, L.; Zheng, H.; Zeng, Z.; Wang, S.; Xu, S.; Zheng, H.; Chen, Y.; Shi, Y.; Wang, Y.; et al. Genomic and Transcriptomic Analysis of the Asian Honeybee Apis Cerana Provides Novel Insights into Honeybee Biology. Sci. Rep. 2018, 8, 822. [Google Scholar] [CrossRef] [PubMed]
  12. Oppenheim, S.; Cao, X.; Rueppel, O.; Krongdang, S.; Phokasem, P.; DeSalle, R.; Goodwin, S.; Xing, J.; Chantawannakul, P.; Rosenfeld, J.A. Whole Genome Sequencing and Assembly of the Asian Honey Bee Apis Dorsata. Genome Biol. Evol. 2020, 12, 3677–3683. [Google Scholar] [CrossRef] [PubMed]
  13. Lin, D.; Lan, L.; Zheng, T.; Shi, P.; Xu, J.; Li, J. Comparative Genomics Reveals Recent Adaptive Evolution in Himalayan Giant Honeybee Apis Laboriosa. Genome Biol. Evol. 2021, 13, evab227. [Google Scholar] [CrossRef] [PubMed]
  14. Haddad, N.J.; Loucif-Ayad, W.; Adjlane, N.; Saini, D.; Manchiganti, R.; Krishnamurthy, V.; AlShagoor, B.; Batainh, A.M.; Mugasimangalam, R. Draft Genome Sequence of the Algerian Bee Apis Mellifera Intermissa. Genom. Data 2015, 4, 24–25. [Google Scholar] [CrossRef]
  15. Wallberg, A.; Bunikis, I.; Pettersson, O.V.; Mosbech, M.-B.; Childers, A.K.; Evans, J.D.; Mikheyev, A.S.; Robertson, H.M.; Robinson, G.E.; Webster, M.T. A Hybrid de Novo Genome Assembly of the Honeybee, Apis Mellifera, with Chromosome-Length Scaffolds. BMC Genom. 2019, 20, 275. [Google Scholar] [CrossRef] [PubMed]
  16. Wang, Z.-L.; Zhu, Y.-Q.; Yan, Q.; Yan, W.-Y.; Zheng, H.-J.; Zeng, Z.-J. A Chromosome-Scale Assembly of the Asian Honeybee Apis Cerana Genome. Front. Genet. 2020, 11, 279. [Google Scholar] [CrossRef] [PubMed]
  17. Kawamoto, M.; Jouraku, A.; Toyoda, A.; Yokoi, K.; Minakuchi, Y.; Katsuma, S.; Fujiyama, A.; Kiuchi, T.; Yamamoto, K.; Shimada, T. High-Quality Genome Assembly of the Silkworm, Bombyx Mori. Insect Biochem. Mol. Biol. 2019, 107, 53–62. [Google Scholar] [CrossRef] [PubMed]
  18. Matthews, B.J.; Dudchenko, O.; Kingan, S.B.; Koren, S.; Antoshechkin, I.; Crawford, J.E.; Glassford, W.J.; Herre, M.; Redmond, S.N.; Rose, N.H. Improved Reference Genome of Aedes Aegypti Informs Arbovirus Vector Control. Nature 2018, 563, 501–507. [Google Scholar] [CrossRef] [PubMed]
  19. Tribolium Genome Sequencing Consortium; Richards, S.; Gibbs, R.A.; Weinstock, G.M.; Brown, S.J.; Denell, R.; Beeman, R.W.; Gibbs, R.; Beeman, R.W.; Brown, S.J.; et al. The Genome of the Model Beetle and Pest Tribolium Castaneum. Nature 2008, 452, 949–955. [Google Scholar] [CrossRef]
  20. Bouallègue, M.; Filée, J.; Kharrat, I.; Mezghani-Khemakhem, M.; Rouault, J.-D.; Makni, M.; Capy, P. Diversity and Evolution of Mariner-like Elements in Aphid Genomes. BMC Genom. 2017, 18, 494. [Google Scholar] [CrossRef] [PubMed]
  21. Carey, K.M.; Patterson, G.; Wheeler, T.J. Transposable Element Subfamily Annotation Has a Reproducibility Problem. Mob. DNA 2021, 12, 4. [Google Scholar] [CrossRef]
  22. Petersen, M.; Armisén, D.; Gibbs, R.A.; Hering, L.; Khila, A.; Mayer, G.; Richards, S.; Niehuis, O.; Misof, B. Diversity and Evolution of the Transposable Element Repertoire in Arthropods with Particular Reference to Insects. BMC Ecol. Evol. 2019, 19, 11. [Google Scholar] [CrossRef] [PubMed]
  23. Liu, Y.; Zong, W.; Diaby, M.; Lin, Z.; Wang, S.; Gao, B.; Ji, T.; Song, C. Diversity and Evolution of Pogo and Tc1/Mariner Transposons in the Apoidea Genomes. Biology 2021, 10, 940. [Google Scholar] [CrossRef] [PubMed]
  24. Flynn, J.M.; Hubley, R.; Goubert, C.; Rosen, J.; Clark, A.G.; Feschotte, C.; Smit, A.F. RepeatModeler2 for Automated Genomic Discovery of Transposable Element Families. Proc. Natl. Acad. Sci. USA 2020, 117, 9451–9457. [Google Scholar] [CrossRef]
  25. Sievers, F.; Higgins, D.G. The Clustal Omega Multiple Alignment Package. Methods Mol. Biol. 2021, 2231, 3–16. [Google Scholar] [CrossRef]
  26. Price, M.N.; Dehal, P.S.; Arkin, A.P. FastTree: Computing Large Minimum Evolution Trees with Profiles Instead of a Distance Matrix. Mol. Biol. Evol. 2009, 26, 1641–1650. [Google Scholar] [CrossRef] [PubMed]
  27. Kumar, S.; Stecher, G.; Li, M.; Knyaz, C.; Tamura, K. MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms. Mol. Biol. Evol. 2018, 35, 1547–1549. [Google Scholar] [CrossRef] [PubMed]
  28. Smit, A.; Hubley, R.; Green, P. RepeatMasker Open-4.0, 2013–2015. Available online: http://www.repeatmasker.org (accessed on 1 June 2022).
  29. Bao, Z.; Eddy, S.R. Automated de Novo Identification of Repeat Sequence Families in Sequenced Genomes. Genome Res. 2002, 12, 1269–1276. [Google Scholar] [CrossRef]
  30. Price, A.L.; Jones, N.C.; Pevzner, P.A. De Novo Identification of Repeat Families in Large Genomes. Bioinformatics 2005, 21 (Suppl. 1), i351–i358. [Google Scholar] [CrossRef] [PubMed]
  31. Ellinghaus, D.; Kurtz, S.; Willhoeft, U. LTRharvest, an Efficient and Flexible Software for de Novo Detection of LTR Retrotransposons. BMC Bioinform. 2008, 9, 18. [Google Scholar] [CrossRef] [PubMed]
  32. Ou, S.; Jiang, N. LTR_retriever: A Highly Accurate and Sensitive Program for Identification of Long Terminal Repeat Retrotransposons. Plant Physiol. 2018, 176, 1410–1422. [Google Scholar] [CrossRef] [PubMed]
  33. Ou, S.; Su, W.; Liao, Y.; Chougule, K.; Agda, J.R.A.; Hellinga, A.J.; Lugo, C.S.B.; Elliott, T.A.; Ware, D.; Peterson, T.; et al. Benchmarking Transposable Element Annotation Methods for Creation of a Streamlined, Comprehensive Pipeline. Genome Biol. 2019, 20, 275. [Google Scholar] [CrossRef] [PubMed]
  34. Flutre, T.; Duprat, E.; Feuillet, C.; Quesneville, H. Considering Transposable Element Diversification in de Novo Annotation Approaches. PLoS ONE 2011, 6, e16526. [Google Scholar] [CrossRef]
  35. Chuong, E.B.; Elde, N.C.; Feschotte, C. Regulatory Activities of Transposable Elements: From Conflicts to Benefits. Nat. Rev. Genet. 2017, 18, 71–86. [Google Scholar] [CrossRef]
  36. Goerner-Potvin, P.; Bourque, G. Computational Tools to Unmask Transposable Elements. Nat. Rev. Genet. 2018, 19, 688–704. [Google Scholar] [CrossRef]
  37. Ghanim, G.E.; Rio, D.C.; Teixeira, F.K. Mechanism and Regulation of P Element Transposition. Open Biol. 2020, 10, 200244. [Google Scholar] [CrossRef] [PubMed]
  38. Robertson, H.M. The Tcl-Mariner Superfamily of Transposons in Animals. J. Insect Physiol. 1995, 41, 99–105. [Google Scholar] [CrossRef]
  39. Plasterk, R.H.; Izsvák, Z.; Ivics, Z. Resident Aliens: The Tc1/Mariner Superfamily of Transposable Elements. Trends Genet. 1999, 15, 326–332. [Google Scholar] [CrossRef]
  40. Elsik, C.G.; Worley, K.C.; Bennett, A.K.; Beye, M.; Camara, F.; Childers, C.P.; de Graaf, D.C.; Debyser, G.; Deng, J.; Devreese, B.; et al. Finding the Missing Honey Bee Genes: Lessons Learned from a Genome Upgrade. BMC Genom. 2014, 15, 86. [Google Scholar] [CrossRef]
  41. Bao, W.; Kojima, K.K.; Kohany, O. Repbase Update, a Database of Repetitive Elements in Eukaryotic Genomes. Mob. DNA 2015, 6, 11. [Google Scholar] [CrossRef] [PubMed]
  42. Miskey, C.; Izsvák, Z.; Kawakami, K.; Ivics, Z. DNA Transposons in Vertebrate Functional Genomics. Cell. Mol. Life Sci. 2005, 62, 629. [Google Scholar] [CrossRef]
Insects 13 00698 g001 550
Figure 1. Workflow of the data analyses performed in this study. De novo TE detection was performed using 11 Apis genome sequences (Table 1) from NCBI genome database (URL: https://www.ncbi.nlm.nih.gov/genome/ accessed on 1 June 2022) using RepeatModeler2 [24]. Phylogenetic analysis revealed MLE relationships, where the most abundant consensus sequences were detected among the TE families in Apis species. The distributions of repetitive elements, including the TEs detected by RepeatModeler2, were investigated using RepeatMasker. The landscapes of TEs in Apis species were obtained using both sets of results, which led to new insights into TEs in Apis species. The images in Figure 1 were obtained from TogoTV (© 2016 DBCLS TogoTV).
Figure 1. Workflow of the data analyses performed in this study. De novo TE detection was performed using 11 Apis genome sequences (Table 1) from NCBI genome database (URL: https://www.ncbi.nlm.nih.gov/genome/ accessed on 1 June 2022) using RepeatModeler2 [24]. Phylogenetic analysis revealed MLE relationships, where the most abundant consensus sequences were detected among the TE families in Apis species. The distributions of repetitive elements, including the TEs detected by RepeatModeler2, were investigated using RepeatMasker. The landscapes of TEs in Apis species were obtained using both sets of results, which led to new insights into TEs in Apis species. The images in Figure 1 were obtained from TogoTV (© 2016 DBCLS TogoTV).
Insects 13 00698 g001
Insects 13 00698 g002 550
Figure 2. Phylogenetic tree of Apis TcMar–Mariner consensus sequences identified in this study. The MLE sequences of other species and A. mellifera were annotated with Mariner subfamilies in previous reports [8,20]. Blue, orange, green, purple, and yellow circles located at end of each node (MLE sequences from the previous reports) indicate the MLE subfamilies. The red circles indicate consensus sequences detected with more than 200 copies. The green semicircular shading encompasses a clade including many sequences with over 200 copies. The numbers at the branches indicate bootstrap values. A high-resolution phylogenetic tree data is available in Supplemental Data S5.
Figure 2. Phylogenetic tree of Apis TcMar–Mariner consensus sequences identified in this study. The MLE sequences of other species and A. mellifera were annotated with Mariner subfamilies in previous reports [8,20]. Blue, orange, green, purple, and yellow circles located at end of each node (MLE sequences from the previous reports) indicate the MLE subfamilies. The red circles indicate consensus sequences detected with more than 200 copies. The green semicircular shading encompasses a clade including many sequences with over 200 copies. The numbers at the branches indicate bootstrap values. A high-resolution phylogenetic tree data is available in Supplemental Data S5.
Insects 13 00698 g002
Insects 13 00698 g003 550
Figure 3. The total numbers of DNA/TcMar-Mariner (A) and DNA/CMC-EnSpm (B) TEs in each Apis genome listed in Table 1. Both TE families were detected using Repeat Modeler 2 and the total numbers of TEs were calculated using. out files from Repeat Masker. Abbreviations of names of Apis species in the figure are shown in Table 1.
Figure 3. The total numbers of DNA/TcMar-Mariner (A) and DNA/CMC-EnSpm (B) TEs in each Apis genome listed in Table 1. Both TE families were detected using Repeat Modeler 2 and the total numbers of TEs were calculated using. out files from Repeat Masker. Abbreviations of names of Apis species in the figure are shown in Table 1.
Insects 13 00698 g003
Table
Table 1. Apis genome assemblies used in this study.
Table 1. Apis genome assemblies used in this study.
Organism Name [Reference]GenBank Assembly Accession IDGenome Size (bp)Contig N50Abbreviation in This Study
A. mellifera [15] *GCA_003254395.2225,250,8845,382,476Am
A. cerana japonica [9] GCA_002217905.1211,200,590179,487Acj
A. cerana Korea native [10]GCA_001442555.1228,331,81243,751Ack
A. cerana China native [16] *GCA_011100585.1215,670,0333,898,192Acc
A. dorsata [12]GCA_009792835.1223,527,74930,868Ad
A. floreaGCA_000184785.2229,015,09024,915Af
A. laboriosa [13]GCF_014066325.1226,078,798303,790Al
A. mellifera intermissa [14]GCA_000819425.1 243,566,977504Ami
A. mellifera (German honey bee) *GCA_003314205.1227,036,4735,131,172Amm
A. mellifera carnica (Carniolan honey bee) *GCA_013841245.1226,044,1792,692,667Amcar
A. mellifera caucasica (Caucasian honey bee) GCA_013841205.1 224,766,6973,303,520Amcau
Asterisks indicate chromosome-level genome assembly data according to NCBI genome assembly statistics in the NCBI dataset database (URL: https://www.ncbi.nlm.nih.gov/datasets/, accessed on 2 August 2022). See discussion section.
Table
Table 2. Total numbers of consensus sequences in the TE families of all Apis species, based on de novo TE detection with RepeatModeler2 [24].
Table 2. Total numbers of consensus sequences in the TE families of all Apis species, based on de novo TE detection with RepeatModeler2 [24].
Family NameAccAcjAckAdAfAlAmAmiAmmAmcarAmcau
DNA/CMC-EnSpm23412171622
DNA/IS3EU00000300100
DNA/MULE-MuDR00001000000
DNA/Maverick00010000101
DNA/Merlin00100000200
DNA/PIF-Harbinger00000011100
DNA/PiggyBac10343522322
DNA/TcMar00000000001
DNA/TcMar-Mariner115646111113141111
DNA/TcMar-Tc12110517111387
DNA/TcMar-Tigger10001000000
DNA/hAT00001100000
DNA/hAT-Ac53444272425
DNA/hAT-Charlie00100200101
RC/Heliton00100030000
LINE/Dong-R400001000000
LINE/I00000100000
LINE/L110011030102
LINE/R111010100010
LINE/R221000000001
LTR/Copia31132213111
LTR/ERV100000110011
LTR/ERVK01000010020
LTR/ERVL00000010000
LTR/Gypsy21101122111
LTR/Ngaro20010002200
LTR/Pao10117211032
SINE/ID00000001000
Total (per species)3417242135334839513438
The consensus sequences not clearly annotated as a family (i.e., “unknown” sequences) are excluded (all-inclusive count result data are available in Supplemental Data S2). The nomenclatures of the TE families were defined previously [2]. Family names belonging to class II TEs and class I TEs are represented with red and blue text, respectively. The degree of red shading indicates the number of the consensus sequences found where darker shading indicates higher numbers.
Table
Table 3. Percentages of repetitive elements present in each Apis genome.
Table 3. Percentages of repetitive elements present in each Apis genome.
AccAcjAckAdAfAlAmAmiAmmAmcarAmcau
9.97%7.87%6.83%10.09%8.20%10.26%11.02%8.01%12.09%11.61%11.41%
Table
Table 4. Total copy numbers of class II TE families in the Apis genomes listed Table 1.
Table 4. Total copy numbers of class II TE families in the Apis genomes listed Table 1.
Family NameAccAcjAckAdAfAlAmAmiAmmAmcarAmcau
DNA/CMC-EnSpm13871684179788010606922761538220013051518
DNA/IS3EU000001070016900
DNA/MULE-MuDR0000477000000
DNA/Maverick0001650000590193
DNA/Merlin001070000033500
DNA/PIF-Harbinger0000004065969800
DNA/PiggyBac1380316845474826456318848797678
DNA/TcMar0000000000364
DNA/TcMar-Mariner1254630798631903134318921495264124783475
DNA/TcMar-Tc1618159110031360810101507165614612300
DNA/TcMar-Tigger230000118000000
DNA/hAT00009820100000
DNA/hAT-Ac65751023382167340917024049743511736
DNA/hAT-Charlie0018800642004660447
RC/Heliton003800028520000
Total (per species)42842983358733424116482811,079432110,046639210,711
The total numbers of TE families (detected using RepeatModeler2) were calculated using output files from RepeatMasker. The degree of red shading reflects the copy numbers found, where darker shading indicates higher copy numbers. Family names belonging to class II TEs and class I TEs are represented with red.
Table
Table 5. Total copy numbers of class I TE families in the Apis genomes listed in Table 1.
Table 5. Total copy numbers of class I TE families in the Apis genomes listed in Table 1.
Family NameAccAcjAckAdAfAlAmAmiAmmAmcarAmcau
LINE/Dong-R40000100000000
LINE/I000002400000
LINE/L12600121341065404800261
LINE/R174570810161000750
LINE/R23325100000000249
LTR/Copia82982101749354466257321318109268
LTR/ERV1000002174190035075
LTR/ERVK035600003260013160
LTR/ERVL000000520000
LTR/Gypsy574464401472331000426417203499
LTR/Ngaro15300910004848300
LTR/Pao4402284167302136775703001237
SINE/ID000000024000
Total (per species)20325923731458167213143385876169823532589
The total numbers of TE families (detected using RepeatModeler2) were calculated using output files from RepeatMasker. The degree of red shading indicates the number of the consensus sequences found, where darker shading indicates higher numbers. Family names belonging to class II TEs and class I TEs are represented with blue text.
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Yokoi, K.; Kimura, K.; Bono, H. Revealing Landscapes of Transposable Elements in Apis Species by Meta-Analysis. Insects 2022, 13, 698. https://doi.org/10.3390/insects13080698

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Yokoi K, Kimura K, Bono H. Revealing Landscapes of Transposable Elements in Apis Species by Meta-Analysis. Insects. 2022; 13(8):698. https://doi.org/10.3390/insects13080698

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Yokoi, Kakeru, Kiyoshi Kimura, and Hidemasa Bono. 2022. "Revealing Landscapes of Transposable Elements in Apis Species by Meta-Analysis" Insects 13, no. 8: 698. https://doi.org/10.3390/insects13080698

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