Abstract
Wolbachia are the most common bacterial endosymbionts of insects. Wolbachia may alter host behaviour and reproduction, and also influence the development of insecticide resistance. Understanding the prevalence and distribution of Wolbachia can therefore be important when developing pest management strategies. We screened Wolbachia in Tribolium castaneum Herbst (Tenebrionidae; Coleoptera), Rhyzopertha dominica Fab. (Bostrichidae; Coleoptera), and Sitophilus oryzae L. (Curculionidae; Coleoptera) across India. The abundance of Wolbachia infection varied across these species, despite them sharing the same resources. Wolbachia infected S. oryzae individuals were detected at all sites, though the proportion of infected individuals at each site ranged from 20–100%. Wolbachia infection was less common in T. castaneum, with infected individuals detected at only 19% of all sites. Wolbachia infection was not detected in R. dominica. Wolbachia was most prevalent in the southern India, though there was no significant association between temperature and Wolbachia prevalence. Our results illustrate how the prevalence of Wolbachia can differ across species sharing an identical resource, and emphasise that broad geographic screening is required to accurately quantify the distribution and abundance of endosymbionts.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Agarwal R, Singh K, Srivastava P, Varma B (1979) Assessment of storage losses in wheat and different refractions in periodic arrivals in mandis of Haryana. Bull Grain Tech 17:202–204
Ahmed MZ, Arauho-Jnr EV, Welch JJ, Kawahara AY (2015a) Wolbachia in butterflies and moths: geographic structure in infection frequency. Front Zool 12:16. https://doi.org/10.1186/s12983-015-0107-z
Ahmed MZ, Li SJ, Xue X, Yin XJ, Ren SX, Jiggins FM, Greef JM, Qiu BL (2015b) The intracellular bacterium Wolbachia uses parasitoid wasps as phoretic vectors for efficient horizontal transmission. PLoS Pathog 11:e1004672. https://doi.org/10.1371/journal.ppat.1004672
Ali H, Muhammad A, Bala NS, Wang G, Chen Z, Peng Z, Hou Y (2018) Genomic evaluations of Wolbachia and mtDNA in the population of coconut hispine beetle, Brontispa longissima (Coleoptera: Chrysomelidae). Mol Phylogenet Evol 127:1000–1009. https://doi.org/10.1016/j.ympev.2018.07.003
Asgharian H, Chang PL, Mazzoglio PJ, Negri L (2014) Wolbachia is not all about sex: male-feminizing Wolbachia alters the leafhopper Zyginidia pullula transcriptome in a mainly sex-dependent manner. Front Microbiol 5:430. https://doi.org/10.3389/fmicb.2014.00430
Baldo L, Dunning Hotopp JC, Jolley KA, Bordenstein SR, Biber SA, Ray Choudhury R, 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
Baldo L, Werren JH (2007) Revisiting Wolbachia super group typing based on wsp: spurious lineages and discordance with MLST. Curr Microbiol 55:81–87. https://doi.org/10.1007/s00284-007-0055-8
Bell CH (2000) Fumigation in the 21st century. Crop Prot 19:563–569
Berticat C, Rousset F, Raymond M, Berthomieu A, Weill M (2002) High Wolbachia density in insecticide resistant mosquitoes. Proc R Soc B 269:1413–1416. https://doi.org/10.1098/rspb.2002.2022
Bing XL, Ruan YM, Rao Q, Wang XW, Liu SS (2012) Diversity of secondary endosymbionts among different putative species of the whitefly Bemisiatabaci. Insect Sci 20:194–206. https://doi.org/10.1111/j.1744-7917.2012.01522.x
Bleidorn C, Gerth M (2018) A critical re-evaluation of multilocus sequence typing (MLST) efforts in Wolbachia FEMS Microbiol Ecol 94. https://doi.org/10.1093/femsec/fix163
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
Champ BR, Dyte CE (1976) Report of the FAO Global Survey of Pesticide Susceptibility of Stored Grain Pests. FAO, Rome
Charlesworth J, Weinert LA, Araujo EV, Welch JJ (2019) Wolbachia, Cardinium and climate: an analysis of global data. Biol Lett 15:20190273. https://doi.org/10.1098/rsbl.2019.0273
Correa CC, Ballard JWO (2016) Wolbachia associations with insects: Winning or losing against a master manipulator. Front Ecol Evol 3:153. https://doi.org/10.3389/fevo.2015.00153
Crombie AC (1941) On oviposition, olfactory conditioning and host selection in Rhyzopertha dominica Fab. (Insecta, Coleoptera). J Exp Biol 18:62–79. https://doi.org/10.1242/jeb.18.1.62
Doyle JJ, Doyle DJ (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15
Duron O, Bouchon D, Boutin S, Bellamy L, Zhou L, Engelsadter J, Hurst GD (2008) The diversity of reproductive parasites among arthropods: Wolbachia do not walk alone. BMC Biol 6:27. https://doi.org/10.1186/1741-7007-6-27
Edgar RC (2004) Muscle: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797. https://doi.org/10.1093/nar/gkh340
Eleftherianos L, Atri J, Accetta J, Castillo JC (2013) Endosymbiotic bacteria in insects: guardians of the immune system? Front Physiol 4:1–10. https://doi.org/10.3389/fphys.2013.00046
Engel P, Moran NA (2013) The gut microbiota of insects – diversity in structure and function. FEMS Microbiol Rev 37:699–735. https://doi.org/10.1111/1574-6976.12025
Ferrari J, Vavre F (2011) Bacterial symbionts in insects or the story of communities affecting communities. Philos Trans R Soc Lond B 366:1389–1400. https://doi.org/10.1098/rstb.2010.0226
Fialho RF, Stevens L (2000) Male-killing Wolbachia in a flour beetle. Proc R Soc B 267:1469–1473. https://doi.org/10.1098/rspb.2000.1166
Flinn PW, Hagstrum DW (2001) Augmentative releases of parasitoid wasps in stored wheat reduce insect fragments in flour. J Stored Prod Res 37:179–186. https://doi.org/10.1016/s0022-474x(00)00018-7
Flinn PW, Kramer KJ, Throne JE, Morgan TD (2006) Protection of stored maize from insect pests using a two component biological control method consisting of a hymenopteran parasitoid, Theocolax elegans, and transgenic avid in maize powder. J Stored Prod Res 42:218–225. https://doi.org/10.1016/j.jspr.2005.02.002
Ghanim M, Kontsedalov S (2009) Susceptibility to insecticides in the Q biotype of Bemisia tabaci is correlated with bacterial symbiont densities. Pest Manag Sci 65:939–942. https://doi.org/10.1002/ps.1795
Goodacre SL, Fricke C, Martin OY (2015) A screen for bacterial endosymbionts in the model organisms Tribolium castaneum, T. confusum, Callosobruchus maculatus and related species. Insect Sci 22:165–177. https://doi.org/10.1111/1744-7917.12096
Gowda RH, Abdel-Razek MPB, Shankaranarayana SK, Hoolageri HC, Puttegowda PH (2018) Molecular phylogenetic affiliation of Wolbachia and phage WO in storage pests from India. Indian J Biotechnol 17:514–519
Halstead DGH (1963) External sex differences in stored product Coleoptera. Bull Entomol Res 54:119–134. https://doi.org/10.1017/S0007485300048665
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
Hedges LM, Brownlie JC, O’Neill SL, Johnson KN (2008) Wolbachia and virus protection in insects. Science 322:702. https://doi.org/10.1126/science.1162418
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
Hurst GDD, Jiggins FM (2005) Problems with mitochondrial DNA as marker in population, phylogeographic and phylogenetic studies: the effect of inherited symbionts. Proc R Soc B 272:1525–1534. https://doi.org/10.1098/rspb.2005.3056
Ipekdal K, Kaya T (2020) Screening stored wheat beetles for reproductive parasitic endosymbionts in central Turkey. J Stored Prod Res 89:101732. https://doi.org/10.1016/j.jspr.2020.101732
Johnson KN (2015) The impact of Wolbachia on virus infection in mosquitoes. Viruses 7:5705–5717. https://doi.org/10.3390/v7112903
Kageyama D, Narita S, Imamura T, Miyanoshita A (2010) Detection and identification of Wolbachia endosymbionts from laboratory stocks of stored product insect pests and their parasitoids. J Stored Prod Res 46:13–19. https://doi.org/10.1016/j.jspr.2009.07.003
Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Mentjies P, Drummond A (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649. https://doi.org/10.1093/bioinformatics/bts199
Koehler PG (1994) Rice weevil, Sitophilus oryzae (L.) (Coleoptera; Curculionidae) ENY - 261. Institute of Food and Agricultural Sciences. University of Florida, Florida Cooperative Extension Service, 4p
Li SJ, Ahmed MZ, Lv N, Shi PQ, Wang XM, Huang JL, Qiu BL (2017) Plant mediated horizontal transmission of Wolbachia between whiteflies. ISME J 11:1019–1028. https://doi.org/10.1038/ismej.2016.164
Li Y, Liu X, Guo H (2018) Variations in endosymbiont infection between buprofezin resistant and susceptible strains of Laodelphax striatellus (Fallen). Curr Microbiol 75:709–715. https://doi.org/10.1007/s00284-018-1436-x
Li Y, Liu X, Wang N, Zhang Y, Hoffmann AA, Guo H (2020) Background dependent Wolbachia mediated insecticide resistance in Laodelphax striatellus. Environ Microbiol 22:2653–2663.https://doi.org/10.1111/1462-2920.14974.
Li YY, Fields PG, Pang BP, Coglin PC, Floate KD (2015) Prevalence and diversity of Wolbachia bacteria infecting insect pests of stored products. J Stored Prod Res 62: 93–100.https://doi.org/10.1016/j.jspr.2015.04.009.
Liu X-D, Guo H-F (2019) Importance of endosymbionts Wolbachia and Rickettsia in insect resistance development. Curr Opin Insect Sci 33:84–90. https://doi.org/10.1016/j.cois.2019.05.003
Lu Y, Miao S, Wang Z, Wang S (2019) Prevalence of Wolbachia in 10 Tenebrionidae stored product insects and spatiotemporal infection dynamics in Tribolium confusum (Jaquelin Du Val) (Coleoptera; Tenebrionidae). Grain Oil Sci Technol 2: 85–90. https://doi.org/10.1016/j.gaost.2019.11.002
McCulloch GA, Gurdasani K, Kocak E, Daglish GJ, Walter GH (2020) Significant population genetic structuring in Rhyzopertha dominica across Turkey: Biogeographic and practical implications. J Stored Prod Res 85:101536. https://doi.org/10.1016/j.jspr.2019.101536
McCulloch GA, Mohankumar S, Subramanian S, SonaiRajan T, Rahul C, Surendran R, Gaurav S, Chandrasekaran S, Daglish GJ, Walter GH (2019) Contrasting patterns of phylogeographic structuring in two key beetle pests of stored grain in India and Australia. J Pest Sci 92:1249–1259. https://doi.org/10.1007/s10340-019-01121-9
Ming QL, Shen JF, Cheng C, Liu CM, Feng ZJ (2015) Wolbachia infection dynamics in Tribolium confusum (Coleoptera: Tenebrionidae) and their effects on host mating behavior and reproduction. J Econ Entomol 108:1408–1415. https://doi.org/10.1093/jee/tov053
Morrow JL, Frommer M, Royer JE, Shearman DCA, Riegler M (2015) Wolbachia pseudogenes and low prevalence infections in topical but not temperate Australian tephritid fruit flies: manifestations of lateral gene transfer and endosymbiont spill over? BMC Evol Biol 15:202. https://doi.org/10.1186/s12862-015-0474-2
Nayak MK, Daglish GJ, Phillips TW, Ebert PR (2020) Resistance to the fumigant phosphine and its management in insect pests of store products: A global perspective. Annu Rev Entomol 65:333–350. https://doi.org/10.1146/annurev-ento-011019-025047
Newman LJ (1927) Grain weevils. J Dept Agric, W Australia 45:538–545
Nguyen DT, Spooner-Hart RN, Riegler M (2016) Loss of Wolbachia but not Cardinium in the invasive range of the Australian thrips species Pezothrips kellyanus. Biol Invasions 18:197–214. https://doi.org/10.1007/s10530-015-1002-4
Nguyen TT, Collins PJ, Ebert PR (2015) Inheritance and characterization of strong resistance to phosphine in Sitophilus oryzae (L.). PLoS One 10: e0124335. https://doi.org/10.1371/journal.pone.0124335
Nikolouli K, Colinet H, Renault D, Enriquez T, Moutun L, Gibert P, Sassu F, Caceres C, Stauffer Pereira R, Bourtzis K (2017) Sterile insect technique and Wolbachia symbiosis as potential tools for the control of invasive species Drosophila suzukii. J Pest Sci 91:489–503. https://doi.org/10.1007/s10340-017-0944-y
Potter C (1935) The biology and distribution of Rhyzoperthadominica (Fab.). Trans R Ent Soc London 83:449–482
Rajendran S (1998) Phosphine resistance in stored insect pests in India. In: Jin ZLQ, Liang Y, Tan X, Guan L (Eds.) Proceedings of the 7th International Working Conference on Stored Product Protection, October 14 – 19, 1998, Beijing, China, Sichuan Publishing House of Science and Technology, Chengdu, China, 635 - 641
Rambaut A, Drummond AJ, Xie D, Baele G, Suchard MA (2018) Posterior summarisation in Bayesian phylogenetics using Tracer 1.7. SystBiol67:901–904. https://doi.org/10.1093/sysbio/syy032
Rey O, Estoup A, Facon B, Loiseau A, Aebi A, Duron O, Vavre F, Foucaud J (2013) Distribution of endosymbiotic reproductive manipulators reflects invasion process and not reproductive system polymorphism in the little fire ant Wasmannia auropunctata. PLoS One 8: e58467.https://doi.org/10.1371/journal.pone.0058467
Rodriguero MS, Confalonieri VA, Guedes JVC, Lanteri AA (2010) Wolbachia infection in the tribe Naupactini (Coleoptera; Curculionidae): Association between thelytokous parthenogenesis and infection status. Insect Mol Biol 19:631–640. https://doi.org/10.1111/j.1365-2583.2010.01018.x
Rokas A, Atkinson RJ, Brown GS, West SA, Stone GA (2001) Understanding patterns of genetic diversity in the oak gall wasp Biorhiza pallida: demographic history or a Wolbachia selective sweep? Heredity 87:294–304. https://doi.org/10.1046/j.1365-2540.2001.00872.x
Ronquist F, Huelsenback JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574. https://doi.org/10.1093/bioinformatics/btg180
Sanaei E, Charlat S, Engelstadter J (2021) Wolbachia host shifts: routes, mechanisms, constraints and evolutionary consequences. Biol Rev 96:433–453. https://doi.org/10.1111/brv.12663
Sanaei E, Husemann M, Seiedy M, Rethwisch M, Tuda M, Toshova TB, Kim MJ, Atanasova D, Kim I (2019) Global genetic diversity, lineage distribution, and Wolbachia infection of the alfalfa weevil Hyperapostica (Coleoptera: Curculionidae). Ecol Evol 9:9546–9563. https://doi.org/10.1002/ece3.5474
Sazama EJ, Bosch MJ, Shouldis CS, Ouellette SP, Wesner JS (2017) Incidence of Wolbachia in aquatic insects. Ecol Evol 7:1165–1169. https://doi.org/10.1002/ece3.2742
Sazama EJ, Ouellette SP, Wesner JS (2019) Bacterial endosymbionts are common among, but not necessarily within, insect species. Environ Entomol 48:127–133. https://doi.org/10.1093/ee/nvy188
Schulenburg JH, Hurst GD, Huigens TM, van Meer MM, Jiggins FJ, Majerus ME (2000) Molecular evolution and phylogenetic utility of Wolbachia ftsZ and wsp gene sequences with special reference to the origin of male-killing. Mol Biol Evol 17:584–600
Semple RL (1992) Inspection and detection methods for storage insect pests. In: Semple RL, Hicks PA, Lozare JV, Castermans A (Ed.), Towards integrated commodity and pest management in grain storage. Food and Agricultural Organization, Rome, Italy p. 526
Shoemaker DD, Keller G, Ross KG (2003) Effects of Wolbachia on mtDNA variation in two fire ant species. Mol Ecol 12:1757–1771. https://doi.org/10.1046/j.1365-294x.2003.01864.x
Sokoloff A (1977) The biology of Tribolium with special emphasis on genetic aspects, vol 3. Clarendon Press, Oxford
Sonai Rajan T, Mohan Kumar S, Chandrasekaran S (2017) Studies on spatial distribution of phosphine resistance in rice weevil, Sitophilus oryzae (L.) (Curculionidae; Coleoptera) collected from Tamil Nadu. Indian J Entomol 79:307–311. https://doi.org/10.5958/0974-8172-.2017.00061.x
Sumi T, Miura K, Miyatake T (2017) Wolbachia density changes seasonally amongst populations of the pale grass butterfly, Zizeeriamaha (Lepidoptera: Lycaenidae). PLoS ONE 12:e0175373. https://doi.org/10.1371/journal.pone.0175373
Thangaraj SR, McCulloch GA, Sabtharishi S, Chandel RK, Debnath S, Subramaniam C, Walter GH, Subbarayalu M (2019) Genetic diversity and its geographic structure in Sitophilus oryzae (Coleoptera; Curculionidae) across India: implications for managing phosphine resistance. J Stored Prod Res 84:101512. https://doi.org/10.1016/j.jspr.2019.101512
Weinert LA, Araujo-Jnr EV, Ahmed MZ, Welch JJ (2015) The incidence of bacterial endosymbionts in terrestrial arthropods. Proc R Soc London Ser B 282:20150249. https://doi.org/10.1098/rspb.2015.0249
Werren JH, Baldo L, Clark ME (2008) Wolbachia: master manipulators of invertebrate biology. Nat Rev Microbiol 6:741–751. https://doi.org/10.1038/nrmicro1969
Zabalou S, Riegler M, Theodorakopoulou M, Stauffer C, Savakis C, Bourtzis K (2004) Wolbachia induced cytoplasmic incompatibility as a means for insect pest population control. Proc Natl Acad Sci USA 101:15042–15045. https://doi.org/10.1073/pnas.0403853101
Zhou W, Roussel F, O’Neill S (1998) Phylogeny and PCR based classification of Wolbachia strains using wsp gene sequences. Proc R Soc London Ser B 265:509–515. https://doi.org/10.1098/rspb.1998.0324
Zug R, Hammerstein P (2015) Bad guys turned nice? A critical assessment of Wolbachia mutualisms in arthropod hosts. Biol Rev 90:89–111. https://doi.org/10.1111/brv.12098
Acknowledgements
This work was financially supported by the Indo-Australian Biotechnology Fund (IABF) (BT/Indo-Aus/09/04/2015) jointly sponsored by the Department of Biotechnology, Government of India, New Delhi and the Department of Innovation, Industry, Science and Research (DIISR, AISRF -48516), Canberra, Australia. The authors thank the managers and technical staff at the Food Corporation of India, Central Warehousing Corporation, and State Civil Supply Corporation for assisting in sample collection.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Sabtharishi, S., Thangaraj, S.R., McCulloch, G.A. et al. Contrasting prevalence of Wolbachia infection across three key stored product beetles in India. Int J Trop Insect Sci 42, 3175–3183 (2022). https://doi.org/10.1007/s42690-022-00877-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s42690-022-00877-5