Evidence for Common Horizontal Transmission of Wolbachia among Ants and Ant Crickets: Kleptoparasitism Added to the List
by
, , ,
Shu-Ping Tseng
1
,
Po-Wei Hsu
1,2,
Chih-Chi Lee
1,2,
James K. Wetterer
3,
Sylvain Hugel
4,
Li-Hsin Wu
5,
Chow-Yang Lee
6
,
Tsuyoshi Yoshimura
1 and
Chin-Cheng Scotty Yang
1,7,8,* 1
Research Institute for Sustainable Humanosphere, Kyoto University, Kyoto 611-0011, Japan
2
Laboratory of Insect Ecology, Graduate School of Agriculture, Kyoto University, Kyoto 606-8502, Japan
3
Wilkes Honors College, Florida Atlantic University, 5353 Parkside Drive, Jupiter, FL 33458, USA
4
Institut des Neurosciences Cellulaires et Intégratives, UPR 3212 CNRS-Université de Strasbourg, 67000 Strasbourg, France
5
Department of Plant Medicine, National Pintung University of Science and Technology, Pintung 91201, Taiwan
6
Department of Entomology, University of California, 900 University Avenue, Riverside, CA 92521, USA
7
Department of Entomology, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061, USA
8
Department of Entomology, National Chung Hsing University, Taichung 402204, Taiwan
*
Author to whom correspondence should be addressed.
Microorganisms 2020, 8(6), 805; https://doi.org/10.3390/microorganisms8060805
Submission received: 9 April 2020
/
Revised: 14 May 2020
/
Accepted: 24 May 2020
/
Published: 27 May 2020
(This article belongs to the Special Issue Wolbachia and Other Selfish Symbionts of Arthropods)
Abstract
:While Wolbachia, an intracellular bacterial symbiont, is primarily transmitted maternally in arthropods, horizontal transmission between species has been commonly documented. We examined kleptoparasitism as a potential mechanism for Wolbachia horizontal transmission, using ant crickets and their host ants as the model system. We compared prevalence and diversity of Wolbachia across multiple ant cricket species with different degrees of host specificity/integration level. Our analyses revealed at least three cases of inter-ordinal Wolbachia transfer among ant and ant crickets, and also showed that ant cricket species with high host-integration and host-specificity tend to harbor a higher Wolbachia prevalence and diversity than other types of ant crickets. This study provides empirical evidence that distribution of Wolbachia across ant crickets is largely attributable to horizontal transmission, but also elucidates the role of intimate ecological association in successful Wolbachia horizontal transmission.
1. Introduction
Wolbachia are widespread, maternally-transmitted, intracellular bacteria, present in approximately half of all arthropod species [1,2]. Discordant phylogenies between Wolbachia and their hosts suggest that transmission of Wolbachia also includes horizontal transmission between species [3,4,5,6], which can be analogous to an epidemiological process mediated by the ability of a pathogen to invade and maintain in novel host populations [7]. Wolbachia must pass three main filters before successfully colonizing a new host species [8]. First, Wolbachia must come into physical contact with the potential host (encounter filter), then evade the host’s immune system and replicate in the new host (compatibility filter). Whether Wolbachia can reach a certain infection threshold to ensure its persistence in the population represents the third filter (invasion filter). The community composition may affect filter stringency and thus shapes the epidemiological patterns of Wolbachia in a community. Communities composed of generalist or specialist species will affect both encounter and compatibility filters [9,10]. For example, the intimate interspecific interactions by specialists are predicted to favor Wolbachia transmission. However, these interactions may also restrict the transmission sources to a few species [9].
It has been considered that intimate tissue-level interactions between donor and recipient species such as host-parasitoid, host-parasite, or prey-predator interactions are required for interspecific transmission of Wolbachia [11,12,13,14,15]. Nevertheless, some studies have shown that the presence of identical Wolbachia strains among species that do not share parasitoids and/or predators but habitats, suggesting other mechanisms may have been involved in Wolbachia horizontal transmission [10,16,17,18,19]. Previous studies have reported horizontal transfer of Wolbachia between ant hosts and their parasitic ants most likely through intimate contacts [17,18,19], however, whether such a mechanism holds true for distantly related species (e.g., inter-ordinal transfers) remains unknown. Ant nests are often utilized by other myrmecophiles [20], offering an excellent opportunity to test if Wolbachia horizontal transmission remains feasible among distantly related species. Ant crickets (Orthoptera: Myrmecophilidae) are generally considered as kleptoparasites (i.e., parasitism by theft, as a form of resource acquisition where one animal takes resources from another), and represent an intriguing group of myrmecophilous taxa that display differential host specificity and integration levels, rendering them suitable examining for Wolbachia horizontal transmission at the inter-ordinal level. In the present study, we conducted an extensive Wolbachia survey in kleptoparasitic ant crickets and their corresponding ant hosts and asked whether inter-ordinal transfer of Wolbachia occurs frequently through kleptoparasitism. The potential interplays between ant crickets of different host specificity/integration levels and Wolbachia infection patterns are also discussed.
2. Materials and Methods
2.1. Insect Collection, DNA Extraction and PCR Conditions
Ant crickets can be generally classified as three groups according to their host specificity and integration levels: integrated host-specialist, non-integrated host-specialist and host-generalist ant crickets [21,22] (see Tables S1 and S2 for a detailed definition). Integrated host-specialist ant crickets possess low survivorship in the absence of ant hosts, engaging in intimate behavioral interactions with their ant hosts, such as trophallaxis [21]. Despite differences in host specificity, both non-integrated host-specialist and host-generalist ant crickets feed independently, often escape ant attack by swift movements and are capable of surviving without ants [21,22]. Seven ant cricket species and their ant hosts from the same colonies were collected and used in this study, including two integrated host-specialist species Myrmecophilus americanus (n = 40) and M. albicinctus (n = 38), three non-integrated host-specialist species M. dubius (n = 23), M. hebardi (n = 26) and M. antilucanus (n = 26), and two host-generalist species M. quadrispina (n = 31) and Myrmophilellus pilipes (n = 23). Most of the ant cricket species and their ant hosts were collected from Asia (Table S3).
Myrmecophilus albicinctus, M. antilucanus, M. dubius and M. hebardi are host-specialists associated with the yellow crazy ant, A. gracilipes, whereas M. americanus is exclusively associated with the longhorn crazy ant, Paratrechina longicornis [23,24]. The two host-generalist species have been reported in nests of more than ten ant species each [21,23,25], and our host-generalist samples were collected from ant colonies of six ant species (Tables S2 and S3).
Genomic DNA was extracted from the legs of ant crickets and their ant hosts using the Gentra Puregene cell and tissue kit (Qiagen, Frederick, MD, USA). To detect Wolbachia infection, polymerase chain reaction (PCR) was employed to amplify the partial Wolbachia surface protein gene (wsp) (primers are listed in Table S4 and PCR conditions follow [26]), with inclusion of proper positive control and blank (ddH2O). When necessary, to distinguish multiple sequences from individuals with multiple Wolbachia infections, the amplified products of the wsp gene were cloned using the TOPO TA cloning kit (Invitrogen, Carlsbad, CA, USA). Twenty colonies were selected from each PCR reaction and sequenced. To further confirm the infection status of individuals with multiple infections, six additional specific primer sets were designed based on the sequencing results of the cloning experiment (Table S4) and each amplicon was also sequenced. Wolbachia strains were characterized using the multi-locus sequence typing (MLST) system [3]. Five MLST loci (hcpA, ftsZ, gatB, coxA and fbpA; 2565 bp in total) were amplified and sequenced following the protocols described on the PubMLST (https://pubmlst.org/Wolbachia/info/protocols.shtml). Each Wolbachia strain was assigned a sequence type (ST; a unique series of alleles) that defines a combination of five alleles (i.e., allelic profile) at MLST loci. Strains with alleles identical at the five MLST loci are assigned the same ST. For individuals with multiple Wolbachia infections, we relied on next-generation sequencing technologies for identification of MLST alleles and assigned MLST alleles to strains using available allelic profile information for reference (see Supplementary Materials Figure S1 for more details). Obtained Wolbachia sequences were deposited in GenBank and the Wolbachia MLST database (see Table 1 for GenBank accession numbers and MLST ids).
2.2. Sequence Alignment and Phylogenetic Analyses
The phylogenetic status of identified Wolbachia strains and co-phylogenetic patterns of Wolbachia and ant crickets were examined based on three datasets: (1) concatenated wsp and MLST sequences (2) MLST sequences and (3) partial mtDNA cytb sequences of the crickets. The nucleotide sequences of wsp, MLST and cytb sequences were aligned separately on the GUIDANCE2 Server [27] based on codons using the MAFFT algorithm [28]. Ambiguous alignments (e.g., those with the confidence score below 0.7) were excluded, resulting in a removal of 12.4% of columns of wsp gene.
We inferred phylogenetic relationships of Wolbachia strains based on concatenated sequences of wsp and MLST using the maximum-likelihood (ML) method with RAxML Blackbox web-servers [29] implementing the optimal substitution model and partitions estimated in PartitionFinder version 2.1.1 [30]. Phylogenies of Wolbachia MLST were inferred using both the maximum likelihood (ML) and the Bayesian method with the RAxML Blackbox and ClonalFrame 1.1 [31]. In addition to Wolbachia sequence types (STs) detected from ant crickets and ant hosts generated in this study, several other STs (the most similar STs found in the MLST database, selected representative STs from each Wolbachia supergroup and Formicidae STs available in the MLST database) were included in the MLST phylogenetic analysis. ML phylogeny was inferred using the RAxML Blackbox implementing the optimal substitution model and partitions estimated in PartitionFinder version 2.1.1 [30]. Bayesian analyses were conducted using ClonalFrame 1.1 [31]. Two independent runs were performed with 1,000,000 generations each, a sampling frequency of 1000 and a burn-in of 50%. A 50% majority rule consensus tree was built from combined data from the two independent runs. We inferred phylogenetic relationships of ant crickets based on the partial mtDNA cytb gene using the ML method. Sequences of partial mtDNA cytb gene for ant crickets were obtained from a previous study [23] (GenBank accession number: MN064914–MN065077), and inference of ML phylogeny followed the first two datasets.
3. Results
We identified ten and six Wolbachia strains from the studied ant crickets and ants, respectively (Table 1). Nine of the ten Wolbachia strains from ant crickets were fully typed by MLST and assigned to a sequence type (ST) (Table 1). wMsp1–wMsp8 and wMame1 are represented by seven unique MLSTs belonging to either Wolbachia supergroup A or F (Table 1). We excluded wMame2 from the MLST analysis because the wsp sequence of wMame2 differed from all known Wolbachia strains in the PubMLST database, and individual crickets bearing the wMame2 strain were always found to be infected with other closely related strains. Wolbachia wLonA, wLonF, wAgra and wCamA1–wCamA3 from ants are represented by five unique STs (Table 1). Note the allelic profile of strains wMame2 and wCamA1–wCamA3 were assigned based on available allelic profile information as reference, assuming no recombination among strains (see supplementary materials for more details).
Wolbachia infection frequency varied across ant cricket species, with the highest frequency (100%) observed in M. americanus and the lowest (0%) observed in M. dubius (Figure 1a). Most ant crickets were infected with supergroup A Wolbachia, and wMsp4 was among the most widespread strains, which was shared among four species (Figure 1b). Supergroup F Wolbachia was found in two phylogenetically distant species, M. americanus and M. quadrispina (Figure 1b). Comparisons of phylogenetic trees of Wolbachia and their cricket hosts indicated no evidence of cricket-Wolbachia co-divergence (Figure 1b). Myrmecophilus americanus harbored the highest Wolbachia frequency and diversity, with most infected individuals harboring more than two Wolbachia strains (triple infection: 43%; quadruple infection: 55%), while single or double infections were common in other species (Table S3).
MLST analysis indicated that some Wolbachia strains from ants and ant crickets shared identical or similar allelic profiles at MLST loci (Table 1, Figure 2). The MLST sequence type of wMsp6 (ST19) was identical to two Wolbachia strains (wLonA and wCamA1) detected from two ant host species of ant crickets, P. longicornis and Camponotus sp. (Table 1, Figure 2a,b). ST19 was widespread in ants as it has been found in eight strains from eight ant species (Figure 2b, species information was obtained from the PubMLST database). wMsp4 and wMsp7 (ST528) are virtually identical to two ant-associated STs, ST577 (from Camponotus sp.; wCamA3) and ST57 (from Camponotus leonardi; [32]), differing only by 1 bp across MLST loci (Figure 2a,b). ST471 was shared between host-specialist ant cricket, M. americanus (wMame1) and its ant host P. longicornis (wLonF) (Figure 2a,c).
The relationships among Wolbachia strains inferred by the wsp gene were similar, yet not completely congruent, to those inferred by MLST dataset. In some cases, strains that carry closely related MLST sequences possessed similar wsp sequences: Wolbachia wMsp6, wMsp4 and wMame1 had wsp sequences identical to Wolbachia wLonA/wCamA1, wCamA3 and wLonF, respectively (Table 1, Table 2). On the other hand, some strains with similar wsp sequences could be divergent at MLST loci: wMsp2, wMsp3, wMame1 and one Wolbachia strain, wMul (wsp: MN044106; MLST: ST527), detected from parasitoid mites possessed closely related wsp sequences (percentage identity between all pairs of strain ranges from 99.23% to 100%; Table 2, also see Figure S2b for the wsp gene tree), while all these strains share either none or one identical MLST allele among each other with percentage identity between all pairs of strain ranging from 98.75% to 99.04%.
4. Discussion
One major finding of this study is the extensive sharing of Wolbachia strains among ants and ant crickets, including three cases where ants and ant crickets share identical or nearly identical Wolbachia strains (wMame1, wMsp4 and wMsp6). The wMame1 (ST471) Wolbachia is only known from M. americanus and its exclusive host, P. longicornis. The wMsp6 (ST19) strain was shared between the host-generalist ant cricket Myrmophilellus pilipes and its ant host P. longicornis (and also Camponotus sp.). Surprisingly, we failed to detect wMsp4 (ST528) Wolbachia from the ant-crickets’ hosts (i.e., P. longicornis and A. gracilipes), yet found wMsp4-like Wolbachia in Camponotus sp.
Identical Wolbachia (wMame1) shared between M. americanus and its ant host P. longicornis suggest the occurrence of horizontal transmission. Integrated host-specialists possess high degrees of host dependence, and acquire food exclusively via trophallaxis with ants [21,33,34], readily providing opportunities for interspecific transfer of Wolbachia. This pattern is consistent with the prediction in which social interactions may facilitate Wolbachia horizontal transmission between cohabiting species [17,18,19]. Nevertheless, the absence of shared Wolbachia between host-specialist M. albicinctus and its ant host A. gracilipes suggests cohabitation may not always result into successful Wolbachia horizontal transmission.
wMsp6 (ST19) was shown to have a wide host range infecting hosts from three different insect orders (Hymenoptera, Lepidoptera and Coleoptera), implying inter-ordinal transfers of this Wolbachia may have occurred multiple times [6,32]. Our study not only expands the current knowledge of host range of wMsp6 (e.g., Orthoptera) but also indicates this strain in ant crickets likely results from inter-ordinal transfers from ant hosts, considering that wMsp6 was shared among ant crickets and ant hosts, and detected in only one ant cricket species with relatively low prevalence. Given that predation often serves as a route for Wolbachia horizontal transmission [12,14,15], host-generalist ant crickets may acquire novel Wolbachia strains through utilization of host ants as prey or stealing ant food [21,25,35,36].
It is noteworthy that the integrated host-specialists (e.g., M. americanus and M. albicinctus) tend to harbor higher Wolbachia prevalence and diversity among three types of ant cricket species. wMsp4 persists with a high frequency only in M. americanus (Figure 1b) but not in other wMsp4-infected ant cricket species, suggesting that M. americanus is particularly prone to Wolbachia infection. While the reasoning behind high diversity and prevalence of Wolbachia in integrated host-specialists remains unclear, one hypothesis is that the degree of host dependence may interact with Wolbachia persistence within host populations due to different selection forces operating on hosts, or factors related to a lifestyle beneficial for the establishment of Wolbachia (e.g., limited dispersal [37]). Support for this observation is available in the system involving fire ants and their social parasites in which an unexpectedly high Wolbachia diversity was found in the social parasites (up to eight strains), while the free-living hosts rarely harbor more than one Wolbachia strain [17,38]. However, one could also argue that these two sister species share common traits/genetic backgrounds encouraging the Wolbachia persistence in the populations.
We note that some Wolbachia strains in this study share similar wsp sequences but exhibit a comparatively low level of similarity at MLST loci (i.e., wMsp2, wMsp3, wMame and wMul, Figure S2, Table 2). This is perfectly in line with earlier studies where incongruence between the wsp gene and MLST is shown to be widespread in insects [3,39]. Furthermore, the finding of a high level of similarity at a fast evolving gene (i.e., wsp) but divergent at housekeeping genes (i.e., MLST) for these Wolbachia strains indicates that horizontal transfer of wsp sequences may have occurred through recombination [3,39]. It is speculated that the wsp participates in facilitating the early settlement and persistence of Wolbachia into a new host, and extensive horizontal gene transfer may have played one of key roles in adaptive evolution of this gene [40]. We argue that Wolbachia in ants and their associated myrmecophiles may represent a good study system to elucidate the role of the wsp during host exploitation.
In conclusion, our data suggest that horizontal transmission is key to explaining the distribution of Wolbachia across ant crickets. The shared Wolbachia among ant crickets and ant hosts indicates that kleptoparasitism represents an additional mechanism of inter-ordinal transfer of Wolbachia. Further Wolbachia surveys on species with similar kleptoparasitic nature may uncover the generality of this phenomenon as well as its underlying mechanisms.
Supplementary Materials
The following are available online at https://www.mdpi.com/2076-2607/8/6/805/s1; Figure S1: Alignment of Illumina paired-end sequence reads to the reference MLST sequences, Figure S2: Genealogical relationships of Wolbachia strains based on the wsp gene, Table S1: Behavioral differences between non-integrated and integrated ant crickets based on Ooi (2019), Table S2: Recorded host ants of the tested ant cricket species, Table S3: Profile information of the ant cricket samples used in this study, Table S4: Primer sequences for the wsp gene and PCR conditions used in this study.
Author Contributions
Conceptualization, S.-P.T., C.-Y.L., T.Y. and C.-C.S.Y.; methodology, S.-P.T.; analysis, S.-P.T. and C.-C.L.; writing—original draft preparation, S.-P.T., P.-W.H. and C.-C.S.Y.; writing—review and editing, S.-P.T., P.-W.H., C.-C.L., J.K.W., S.H., L.-H.W., C.-Y.L., T.Y. and C.-C.S.Y.; supervision, T.Y. and C.-C.S.Y.; funding acquisition, L.-H.W., T.Y. and C.-C.S.Y. All authors have read and agreed to the published version of the manuscript.
Funding
This research was funded by the Humanosphere Mission Research Project (Kyoto University), Grants-in-Aid for Scientific Research (Japan Society for the Promotion of Science), the Environment Research and Technology Development Fund (Ministry of the Environment, Japan), and the Higher Education Sprout Project (National Pingtung University of Science and Technology). The APC was funded by Kyoto University.
Acknowledgments
We thank Kazuki Tsuji, Hung-Wei Hsu, Li Yan Gan, Mark Ooi, Su-Chart Lee, Yi-Ming Weng and Zhengwei Jong for their assistance in field collection, and two anonymous reviewers for constructive comments on earlier versions of the manuscript.
Conflicts of Interest
The authors declare no conflict of interest. The funders had no role in the design of the study, in the collection, analyses, or interpretation of data, in the writing of the manuscript, or in the decision to publish the results.
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Figure 1.
(a) Wolbachia infection rates of ant crickets; (b) Maximum Likelihood (ML) phylogeny of ant crickets (left) and their corresponding Wolbachia strains (right) based on cytb sequences and concatenated sequences of wsp and MLST, respectively. Numbers at nodes indicate bootstrap support values (100 replicates). Ant cricket-Wolbachia associations are indicated by lines (black: supergroup A; gray: supergroup F), and the number above the line indicates the infection rate of each Wolbachia strain. Wolbachia strain wMame2 was excluded from the phylogenetic analysis due to the lack of reliable MLST data.
Figure 1.
(a) Wolbachia infection rates of ant crickets; (b) Maximum Likelihood (ML) phylogeny of ant crickets (left) and their corresponding Wolbachia strains (right) based on cytb sequences and concatenated sequences of wsp and MLST, respectively. Numbers at nodes indicate bootstrap support values (100 replicates). Ant cricket-Wolbachia associations are indicated by lines (black: supergroup A; gray: supergroup F), and the number above the line indicates the infection rate of each Wolbachia strain. Wolbachia strain wMame2 was excluded from the phylogenetic analysis due to the lack of reliable MLST data.
Figure 2.
(a) Maximum Likelihood (ML) phylogeny of Wolbachia based on MLST data, with ML bootstrap values (left) and Bayesian posterior probability (right) given. Note that both Bayesian inference and ML yielded a highly similar topology. Black circles denote the Wolbachia STs identified in the present study. Wolbachia from ants, ant crickets and Wolbachia shared between ants and ant crickets are colored blue, yellow and green, respectively. Relationships among supergroup A Wolbachia and supergroup F Wolbachia strains based on MLST data are shown in (b,c), respectively. Strains that differ in a single mutation are connected with a solid line. Host information is provided in the white box with the number of host species indicated in parentheses.
Figure 2.
(a) Maximum Likelihood (ML) phylogeny of Wolbachia based on MLST data, with ML bootstrap values (left) and Bayesian posterior probability (right) given. Note that both Bayesian inference and ML yielded a highly similar topology. Black circles denote the Wolbachia STs identified in the present study. Wolbachia from ants, ant crickets and Wolbachia shared between ants and ant crickets are colored blue, yellow and green, respectively. Relationships among supergroup A Wolbachia and supergroup F Wolbachia strains based on MLST data are shown in (b,c), respectively. Strains that differ in a single mutation are connected with a solid line. Host information is provided in the white box with the number of host species indicated in parentheses.
Table 1.
wsp accession number and multi-locus sequence type (MLST) allelic profiles of the Wolbachia strains recovered from the tested ant crickets and ants in this study.
Table 1.
wsp accession number and multi-locus sequence type (MLST) allelic profiles of the Wolbachia strains recovered from the tested ant crickets and ants in this study.
| Strain | Host Type | Host Species | wsp Accession No. | MLST id | ST a | Supergroup | gatB | coxA | hcpA | ftsZ | fbpA |
|---|---|---|---|---|---|---|---|---|---|---|---|
| wMsp1 | Ant cricket | M. albicinctus | MK995471 | 1926 | 525 | A | 294 | 291 | 331 | 251 | 459 |
| wMsp2 | Ant cricket | M. quadrispina | MK995472 | 1927 | 526 | F | 170 | 147 | 178 | 252 | 125 |
| wMsp3 | Ant cricket | M. quadrispina | MK995473 | 1928 | 526 | F | 170 | 147 | 178 | 252 | 125 |
| wMsp4 | Ant cricket | M. americanus, M. albicinctus, M. hebardi, M. antilucanus | MK995474 | 1929 | 528 | A | 49 | 44 | 297 | 42 | 49 |
| wMsp5 | Ant cricket | M. americanus, M. quadrispina | MK995475 | 1930 | 529 | F | 295 | 94 | 332 | 85 | 460 |
| wMsp6 | Ant cricket | Myrmophilellus pilipes | MK995476 | 1931 | 19 | A | 7 | 6 | 7 | 3 | 8 |
| wMsp7 | Ant cricket | M. hebardi | MK995477 | 1932 | 528 | A | 49 | 44 | 297 | 42 | 49 |
| wMsp8 | Ant cricket | M. albicinctus | MK995478 | 1933 | 531 | A | 49 | 44 | 333 | 253 | 49 |
| wMame1 | Ant cricket | M. americanus | MK995479 | 2024 | 471 a | F | 168 | 147 | 262 | 132 | 226 |
| wMame2 | Ant cricket | M. americanus | MK995480 | NA | NA | NA | NA | NA | NA | NA | NA |
| wLonA | Ant | Paratrechina longicornis | MN927214 | 1827 | 19 | A | 7 | 6 | 7 | 3 | 8 |
| wLonF | Ant | Paratrechina longicornis | MN927215 | 1828 | 471 | F | 168 | 147 | 262 | 132 | 226 |
| wAgra | Ant | Anoplolepis gracilipes | MN927216 | 2017 | 52 | A | 22 | 2 | 51 | 32 | 36 |
| wCamA1 | Ant | Camponotus sp. | MN927217 | 2021 | 19 b | A | 7 | 6 | 7 | 3 | 8 |
| wCamA2 | Ant | Camponotus sp. | MN927218 | 2022 | 576 b | A | 323 | 2 | 47 | 45 | 481 |
| wCamA3 | Ant | Camponotus sp. | MN967009 | 2023 | 577 b | A | 49 | 44 | 297 | 42 | 482 |
a ST: sequence type; b An inferred ST based on next-generation sequencing data and available allelic profile in the MLST database; NA: not applicable
Table 2.
Comparisons of wsp sequences of Wolbachia from tested ant crickets and those in the GenBank and PubMLST databases.
Table 2.
Comparisons of wsp sequences of Wolbachia from tested ant crickets and those in the GenBank and PubMLST databases.
| Strain | GenBank Accession no./ PubMLST id | Percent Identity | Host (Strain) | Common Name |
|---|---|---|---|---|
| wMame1 | MN927215/ id: #1828 | 100% | Paratrechina longicornis (wLonF) | longhorn crazy ant |
| wMame2 | KC161941 | 97.22% | Tachinid sp. | tachinid fly |
| KC161936 | 97.22% | Pyralidid sp. | pyralid moth | |
| wMsp1 | MG797608 | 99.63% | Loxoblemmus equestris | hard-headed cricket |
| wMsp2 | MN044106 | 100% | Macrodinychus multispinosus | parasitoid mite |
| MN927215/ id: #1828 | 99.62% | Paratrechina longicornis (wLonF) | longhorn crazy ant | |
| wMsp3 | MN044106 | 99.62% | Macrodinychus multispinosus | parasitoid mite |
| MN927215/ id: #1828 | 99.23% | Paratrechina longicornis (wLonF) | longhorn crazy ant | |
| wMsp4 | MN967009 | 100% | Camponotus sp. (wCamA3) | carpenter ant |
| KU527484 | 100% | Tetramorium lanuginosum | wooly ant | |
| KC137165 | 100% | Odontomachus sp. | trap jaw ant | |
| GU236978 | 100% | Aulacophora nigripennis | leaf beetle | |
| MG551859 | 100% | Octodonta nipae | nipa palm hispid beetle | |
| id: #120 | 100% | Camponotus leonardi | carpenter ant | |
| wMsp5 | KM078883 | 94.64% | Chorthippus parallelus | meadow grasshopper |
| JN701984 | 94.41% | Chorthippus parallelus | meadow grasshopper | |
| wMsp6 | MN927214/ id: #1827 | 100% | Paratrechina longicornis (wLonA) | longhorn crazy ant |
| MN927217 | 100% | Camponotus sp. (wCamA1) | carpenter ant | |
| KU527480 | 100% | Tapinoma sessile | odorous house ant | |
| KU527478 | 100% | Tapinoma melanocephalum | ghost ant | |
| HQ602874 | 100% | Ceutorhynchus neglectus | weevil | |
| AB024571 | 100% | Ephestia cautella | almond moth | |
| id: #111 | 100% | Technomyrmex albipes | white-footed ant | |
| id: #115 | 100% | Leptomyrmex sp. | spider ant | |
| id: #141 | 100% | Pheidole sp. | big-headed ant | |
| id: #146 | 100% | Leptogenys sp. | razorjaw ant | |
| id: #116 | 100% | Myrmecorhynchus sp. | ant | |
| id: #124 | 100% | Pheidole plagiara | big-headed ant | |
| id: #125 | 100% | Pheidole sauberi | big-headed ant | |
| id: #135 | 100% | Ochetellus glaber | black household ant | |
| id: #13 | 100% | Ephestia kuehniella | mediterranean flour moth | |
| id: #123 | 100% | Ornipholidotos peucetia | glasswings | |
| id: #451 | 100% | Aricia artaxerxes | northern brown argus | |
| wMsp7 | MN967009 | 99.81% | Camponotus sp. (wCamA3) | carpenter ant |
| KU527484 | 99.81% | Tetramorium lanuginosum | wooly ant | |
| KC137165 | 99.81% | Odontomachus sp. | trap jaw ant | |
| GU236978 | 99.81% | Aulacophora nigripennis | leaf beetles | |
| MG551859 | 99.81% | Octodonta nipae | nipa palm hispid beetle | |
| id: #120 | 99.81% | Camponotus leonardi | carpenter ants | |
| wMsp8 | EF219194 | 95.47% | Ixodes ricinus | castor bean tick |
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Tseng, S.-P.; Hsu, P.-W.; Lee, C.-C.; Wetterer, J.K.; Hugel, S.; Wu, L.-H.; Lee, C.-Y.; Yoshimura, T.; Yang, C.-C.S. Evidence for Common Horizontal Transmission of Wolbachia among Ants and Ant Crickets: Kleptoparasitism Added to the List. Microorganisms 2020, 8, 805. https://doi.org/10.3390/microorganisms8060805
AMA Style
Tseng S-P, Hsu P-W, Lee C-C, Wetterer JK, Hugel S, Wu L-H, Lee C-Y, Yoshimura T, Yang C-CS. Evidence for Common Horizontal Transmission of Wolbachia among Ants and Ant Crickets: Kleptoparasitism Added to the List. Microorganisms. 2020; 8(6):805. https://doi.org/10.3390/microorganisms8060805
Chicago/Turabian StyleTseng, Shu-Ping, Po-Wei Hsu, Chih-Chi Lee, James K. Wetterer, Sylvain Hugel, Li-Hsin Wu, Chow-Yang Lee, Tsuyoshi Yoshimura, and Chin-Cheng Scotty Yang. 2020. "Evidence for Common Horizontal Transmission of Wolbachia among Ants and Ant Crickets: Kleptoparasitism Added to the List" Microorganisms 8, no. 6: 805. https://doi.org/10.3390/microorganisms8060805
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