Abstract
Bacterial endosymbionts, such as Wolbachia, are widespread in arthropods, with vertical transmission (from mother to offspring) deemed to be the dominant route. Although horizontal transmission of Wolbachia is considered possible as a conveyance route for infections to be introduced to new individuals, evidence for such transmission remains limited. Thus, to elucidate the horizontal transmission of Wolbachia among hosts, we conducted parasitism, predation, cannibalism, and mating experiments in small spider species Hylyphantes graminicola. While no direct evidence was found for horizontal transmission via parasitism or predation, cannibalism and mating behavior were shown to be potential Wolbachia transmission pathways, with copulatory transmission identified from Wolbachia-positive females to Wolbachia-negative males (and vice versa). Based on these findings, our study suggests that horizontal transmission of Wolbachia is more likely to occur within species than between species.
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References
Ahmed MZ, Li SJ, Xue X, Yin XJ, Ren SX, Jiggins FM, Greeff JM, Qiu BL (2015) The intracellular bacterium Wolbachia uses parasitoid wasps as phoretic vectors for efficient horizontal transmission. PLoS Pathog 10:e1004672. https://doi.org/10.1371/journal.ppat.1004672
Baldo L, Dunning Hotopp JC, Jolley KA, Bordenstein SR, Biber SA, Choudhury RR, Hayashi C, Maiden MCJ, Tettelin H, Werren JH (2006) Multilocus sequence typing system for the endosymbiont Wolbachia pipientis. Appl Environ Microbiol 72:7098–7110. https://doi.org/10.1128/AEM.00731-06
Boyle L, O'Neill S, Robertson H, Karr T (1993) Interspecific and intraspecific horizontal transfer of Wolbachia in Drosophila. Science 260:1796–1799. https://doi.org/10.1126/science.8511587
Brown AN, Lloyd VK (2015) Evidence for horizontal transfer of Wolbachia by a Drosophila mite. Exp Appl Acarol 66:301–311. https://doi.org/10.1007/s10493-015-9918-z
Clancy DJ, Hoffmann AA (1997) Behavior of Wolbachia endosymbionts from Drosophila simulans in Drosophila serrata, a novel host. Am Nat 149:975–988. https://doi.org/10.1086/286033
Enigl M, Zchori-Fein E, Schausberger P (2005) Negative evidence of Wolbachia in the predaceous mite Phytoseiulus persimilis. Exp Appl Acarol 36:249–262. https://doi.org/10.1007/s10493-005-6075-9
Faria VG, Paulo TF, Sucena É (2016) Testing cannibalism as a mechanism for horizontal transmission of Wolbachia in Drosophila. Symbiosis 68:79–85. https://doi.org/10.1007/s13199-015-0354-y
Foelix R (2011) Biology of spiders. In: Reproduction, 3rd edn. Oxford Univ. Press, New York, pp 245-249
Goodacre SL, Martin OY, Thomas CFG, Hewitt GM (2006) Wolbachia and other endosymbiont infections in spiders. Mol Ecol 15:517–527. https://doi.org/10.1111/j.1365-294X.2005.02802.x
Heath BD, Butcher RDJ, Whitfield WGF, Hubbard SF (1999) Horizontal transfer of Wolbachia between phylogenetically distant insect species by a naturally occurring mechanism. Curr Biol 9:313–316. https://doi.org/10.1016/S0960-9822(99)80139-0
Herbert RI, McGraw EA (2018) The nature of the immune response in novel Wolbachia-host associations. Symbiosis 74:225–236. https://doi.org/10.1007/s13199-017-0503-6
Hilgenboecker K, Hammerstein P, Schlattmann P, Telschow A, Werren JH (2008) How many species are infected with Wolbachia?--a statistical analysis of current data. FEMS Microbiol Lett 281:215–220. https://doi.org/10.1111/j.1574-6968.2008.01110.x
Houck M, Clark J, Peterson K, Kidwell M (1991) Possible horizontal transfer of Drosophila genes by the mite Proctolaelaps regalis. Science 253:1125–1128. https://doi.org/10.1126/science.1653453
Jaenike J, Polak M, Fiskin A, Helou M, Minhas M (2007) Interspecific transmission of endosymbiotic Spiroplasma by mites. Biol Lett 3:23–25. https://doi.org/10.1098/rsbl.2006.0577
Jeyaprakash A, Hoy MA (2000) Long PCR improves Wolbachia DNA amplification: wsp sequences found in 76% of sixty-three arthropod species. Insect Mol Biol 9:393–405. https://doi.org/10.1046/j.1365-2583.2000.00203.x
Le Clec'h W, Braquart-Varnier C, Raimond M, Ferdy JB, Bouchon D, Sicard M (2012) High virulence of Wolbachia after host switching: when autophagy hurts. PLoS Pathog 8:e1002844. https://doi.org/10.1371/journal.ppat.1002844
Le Clec'h W, Chevalier FD, Genty L, Bertaux J, Bouchon D, Sicard M (2013) Cannibalism and predation as paths for horizontal passage of Wolbachia between terrestrial isopods. PLoS One 8:e60232. https://doi.org/10.1371/journal.pone.0060232
Li SJ, Ahmed MZ, Lv N, Shi PQ, Wang XM, Huang JL, Qiu BL (2017) Plantmediated horizontal transmission of Wolbachia between whiteflies. ISME J 11:1019–1028. https://doi.org/10.1038/ismej.2016.164
Mitsuhashi W, Saiki T, Wei W, Kawakita H, Sato M (2002) Two novel strains of Wolbachia coexisting in both species of mulberry leafhoppers. Insect Mol Biol 11:577–584. https://doi.org/10.1046/j.1365-2583.2002.00368.x
Moran NA, Dunbar HE (2006) Sexual acquisition of beneficial symbionts in aphids. Proc Natl Acad Sci U S A 103:12803–12806. https://doi.org/10.1073/pnas.0605772103
Riechert SE, Lockley T (1984) Spiders as biological control agents. Annu Rev Entomol 29:299–320. https://doi.org/10.1146/annurev.en.29.010184.001503
Riegler M, Charlat S, Stauffer C, Mercot H (2004) Wolbachia transfer from Rhagoletis cerasi to Drosophila simulans: investigating the outcomes of host-symbiont coevolution. Appl Environ Microbiol 70:273–279. https://doi.org/10.1128/aem.70.1.273-279.2004
Ruang-Areerate T, Kittayapong P (2006) Wolbachia transinfection in Aedes aegypti: a potential gene driver of dengue vectors. Proc Natl Acad Sci U S A 103:12534–12539. https://doi.org/10.1073/pnas.0508879103
Schuler H, Bertheau C, Egan SP, Feder JL, Riegler M, Schlick-Steiner BC, Steiner FM, Johannesen J, Kern P, Tuba K, Lakatos F, Köppler K, Arthofer W, Stauffer C (2013) Evidence for a recent horizontal transmission and spatial spread of Wolbachia from endemic Rhagoletis cerasi (Diptera: Tephritidae) to invasive Rhagoletis cingulata in Europe. Mol Ecol 22:4101–4111. https://doi.org/10.1111/mec.12362
Sintupachee S, Milne JR, Poonchaisri S, Baimai V, Kittayapong P (2006) Closely related Wolbachia strains within the pumpkin arthropod community and the potential for horizontal transmission via the plant. Microb Ecol 51:294–301. https://doi.org/10.1007/s00248-006-9036-x
Vavre F, Fleury F, Lepetit D, Fouillet P, Boulétreau M (1999) Phylogenetic evidence for horizontal transmission of Wolbachia in host-parasitoid associations. Mol Biol Evol 16:1711–1723. https://doi.org/10.1093/oxfordjournals.molbev.a026084
Wang Z, Deng C, Yun Y, Jian C, Peng Y (2010) Molecular detection and the phylogenetics of Wolbachia in Chinese spiders (Araneae). J Arachnol 38:237–241. https://doi.org/10.1636/JOA_B09-69.1
Werren JH (1997) Biology of Wolbachia. Annu Rev Entomol 42:587–609. https://doi.org/10.1146/annurev.ento.42.1.587
Yun Y, Peng Y, Liu FX, Lei C (2011) Wolbachia screening in spiders and assessment of horizontal transmission between predator and prey. Neotrop Entomol 40:164–169. https://doi.org/10.1590/S1519-566X2011000200002
Zhang Z (1999) Biology and ecology of trombidiid mites (Acari: Trombidioidea). In: Bruin J, van der Geest LPS, Sabelis MW (eds) Ecology and evolution of the Acari: Proceedings of the 3rd Symposium of the European Association of Acarologists 1–5 July 1996, Amsterdam, The Netherlands. Springer Netherlands, Dordrecht, pp 277–289. https://doi.org/10.1007/978-94-017-1343-6_19
Zhou W, Rousset F, O'Neill S (1998) Phylogeny and PCR–based classification of Wolbachia strains using wsp gene sequences. Proc R Soc Lond B Biol Sci 265:509–515. https://doi.org/10.1098/rspb.1998.0324
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This work was supported by the National Natural Science Fund of China (31401982, 31672317). We thank Dr. Christine Watts for manuscript suggestions and Zhi-Qiang Zhang for mite identification.
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Supplementary Figure S1
Agarose gel electrophoresis of PCR-amplified standard product of wsp at various dilutions. 1–9: successive DNA concentrations 1.66 × 109, 1.66 × 108, 1.66 × 107, 1.66 × 106, 1.66 × 105, 1.66 × 104, 1.66 × 103, 1.66 × 102, 1.66 × 10 copies; 10: Blank control; M: marker. (JPG 29 kb)
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Su, Q., Hu, G., Yun, Y. et al. Horizontal transmission of Wolbachia in Hylyphantes graminicola is more likely via intraspecies than interspecies transfer. Symbiosis 79, 123–128 (2019). https://doi.org/10.1007/s13199-019-00623-5
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DOI: https://doi.org/10.1007/s13199-019-00623-5