Abstract
Adalia bipunctata (Coleoptera: Coccinellidae) is the host of three different symbiotic bacteria: Spiroplasma, Rickettsia, and Wolbachia. This paper presents an overview of data on the distribution of these bacteria in populations of the two-spot ladybird from different parts of the area: Sweden (Stockholm), Russia – from Karelia to Transbaikalia, and Kyrgyzstan. It is noted that in Moscow and St. Petersburg, the symbiosis of bacteria with A. bipunctata has been observed for almost 30 years, that is, it persists steadily. Since both symbiotic bacteria and mitochondrial DNA are inherited cytoplasmatically, the long-term existence of symbionts in the population can lead to a change in the frequency ratio of haplotypes. Spiroplasma, Rickettsia, and Wolbachia usually affect the reproduction of A. bipunctata, causing the male killing, however, sometimes there are strains of Wolbachia that do not cause the male killing. Adalia bipunctata has a parasitoid Aprostocetus sp. (Hymenoptera: Eulophidae), which also has a Wolbachia symbiont. However, the Wolbachia strains from the parasitoid are not related to the bacterial strains from A. bipunctata, which indicates the absence of horizontal transfer between the host beetle and the larvae of the parasitoid. The carriers of the symbionts may be Coccipolipus hippodamiae (Acarina: Podapolipidae) mites that parasitize ladybirds.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data Availability
All data generated or analysed during this study are included in this published article.
Code Availability
Not applicable.
References
Ahmed MZ, Ren SX, Mandour NS, Greef JM, Qiu BL (2010) Prevalence of Wolbachia supergroups a and B in Bemisia tabaci (Hemiptera: Aleyrodidae) and some of its natural enemies. J Econ Entomol 103(5):1848–1859. https://doi.org/10.1603/ec10033
Awad M, Piálková R, Haelewaters D, Nedvěd O (2023) Infection patterns of Harmonia axyridis (Coleoptera: Coccinellidae) by ectoparasitic microfungi and endosymbiotic bacteria. J Invertebr Pathol. https://doi.org/10.1016/j.jip.2023.107887
Baldo L, Ayoub NA, Hayashi CY, Russell JA, Stahlhut JK, Werren JH (2008) Insight into the routes of Wolbachia invasion: high levels of horizontal transfer in the spider genus Agelenopsis revealed by Wolbachia strain and mitochondrial DNA diversity. Mol Ecol 17(2):557–569. https://doi.org/10.1111/j.1365-294X.2007.03608.x
Boakes EH, Wang J, Amos W (2007) An investigation of inbreeding depression and purging in captive pedigreed populations. Heredity 98(3):172–182. https://doi.org/10.1038/sj.hdy.6800923
Burland TG (2000) DNASTAR’s lasergene sequence analysis software. Methods Mol Biol 132:71–91. https://doi.org/10.1385/1-59259-192-2:71
Ceryngier P, Roy HE, Poland RL (2012) Natural enemies of ladybird beetles. In: Hodek I, van Emden HF, Honek A (eds) Ecology and behaviour of the ladybird beetles (Coccinellidae). Wiley-Blackwell, Chichester, pp 375–443. https://doi.org/10.1002/9781118223208.ch8
Clewley JP (1995) Macintosh sequence analysis software. DNASTAR’s Lasergene. Mol Biotechnol 3:221–224. https://doi.org/10.1007/BF02789332
Cockburn SN, Haselkorn TS, Hamilton PT, Landzberg E, Jaenike J, Perlman SJ (2013) Dynamics of the continent-wide spread of a Drosophila defensive symbiont. Ecol Lett 16:609–616. https://doi.org/10.1111/ele.12087
Duron O, Bouchon D, Boutin S, Bellamy L, Zhou L, Engelstädter J, Hurst GDD (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
Elnagdy S, Messing S, Majerus MEN (2013) Two strains of male-killing Wolbachia in a ladybird, Coccinella undecimpunctata from a hot climate. PLoS ONE 8(1):e54218. https://doi.org/10.1371/journal.pone.0054218
Gerth M, Röthe J, Bleidorn C (2013) Tracing horizontal Wolbachia movements among bees (Anthophila): a combined approach using multilocus sequence typing data and host phylogeny. Mol Ecol 22:6149–6162. https://doi.org/10.1111/mec.12549
Glémin S (2003) How are deleterious mutations purged? Drift versus nonrandom mating. Evolution 57(12):2678–2687. https://doi.org/10.1111/j.0014-3820.2003.tb01512.x
Goryacheva I, Blekhman A, Andrianov B, Zakharov I (2017) Heritable bacterial endosymbionts in native and invasive populations of Harmonia axyridis. Biol Invas 19(2):493–502. https://doi.org/10.1007/s10530-016-1298-8
Gotoh T, Niijima K (1986) Characteristics and agents of abnormal sex ratio in two aphidophagous coccinellid species. In: Hodek I (ed) Ecology of the Aphidophaga. Academia, Prague, pp 545–550
Hedges LM, Brownlie JC, O’Neil SL, Johnson KN (2008) Wolbachia and virus protection in insects. Science 322(5902):702. https://doi.org/10.1126/science.1162418
Hodek I, Ceryngier P (2000) Sexual activity in Coccinellidae (Coleoptera): a review. Eur J Entomol 97(4):449–456. https://doi.org/10.14411/eje.2000.069
Hurst GDD, Majerus MEN, Walker LE (1992) Cytoplasmic male killing elements in Adalia bipunctata (Linnaeus) (Coleoptera:Coccinellidae). Heredity 69:84–91. https://doi.org/10.1038/hdy.1992.97
Hurst GDD, Sharpe RG, Broomfield AH, Walker LE, Majerus TMO, Zakharov IA, Majerus MEN (1995) Sexually transmitted disease in a promiscuous insect, Adalia bipunctata. Ecol Entomol 20(3):230–236. https://doi.org/10.1111/j.1365-2311.1995.tb00452.x
Hurst GDD, Schulenburg JHG, Majerus TMO, Bertrand D, Zakharov IA, Baungaard J, Völkl W, Stouthamer R, Majerus MEN (1999a) Invasion of one insect species, Adalia bipunctata, by two different male-killing bacteria. Ins Mol Biol 8:133–139. https://doi.org/10.1046/j.1365-2583.1999.810133.x
Hurst GDD, Jiggins FM, Schulenburg JHG, Bertrand D, West SA, Goriacheva II, Zakharov IA, Werren JH, Stouthamer R, Majerus MEN (1999b) Male-killing Wolbachia in two species of insects. Proc Biol Sci 266(1420):735–740. https://doi.org/10.1098/rspb.1999.0698
Ilinsky Y, Kosterin OE (2017) Molecular diversity of Wolbachia in Lepidoptera: prevalent allelic content and high recombination of MLST genes. Mol Phylogenet Evol 109:164–179. https://doi.org/10.1016/j.ympev.2016.12.034
Jaenike J (2012) Population genetics of beneficial heritable symbionts. Trends Ecol Evol 27(4):226–232. https://doi.org/10.1016/j.tree.2011.10.005
Jaenike J, Unckless R, Cockburn SN, Boelio LM, Perlman SJ (2010) Adaptation via symbiosis: recent spread of a Drosophila defensive symbiont. Science 329:212–215. https://doi.org/10.1126/science.1188235
Johnstone RA, Hurst GDD (1996) Maternally inherited male-killing microorganisms may confound interpretation of mtDNA variation in insects. Biol J Linn Soc 58:453–470. https://doi.org/10.1111/j.1095-8312.1996.tb01446.x
Kajtoch L, Kotásková N (2018) Current state of knowledge on Wolbachia infection among Coleoptera: a systematic review. PeerJ 6:e4471. https://doi.org/10.7717/peerj.4471
Kartavtsev YF (2013) Genetic divergence of species and other taxa. Geographic species-formation and genetic paradigma of neodarwinism at work. Uspekhi Sovrem Biologii 133(5):419–451 (In Russian)
Knell RJ, Webberley KM (2004) Sexually transmitted diseases of insects: distribution, evolution, ecology and host behaviour. Biol Reviews 79(3):557–581. https://doi.org/10.1017/s1464793103006365
Kremer N, Charif D, Henri H, Gavory F, Wincker P, Mavingui P, Vavre F (2012) Influence of Wolbachia on host gene expression in an obligatory symbiosis. BMC Microbiol 1:7. https://doi.org/10.1186/1471-2180-12-S1-S7
Lukasik P, Guo H, van Asch M, Ferrari J, Godfray HCJ (2013) Protection against a fungal pathogen conferred by the aphid facultative endosymbionts Rickettsia and Spiroplasma is expressed in multiple host genotypes and species and is not influenced by coinfection with another symbiont. J Evol Biol 26:2654–2661. https://doi.org/10.1111/jeb.12260
Lus YY (1947) Some rules of reproduction in populations of Adalia bipunctata: non-male strains in populations. Dokl Akad Nauk SSSR 57:951–954 (In Russian)
Majerus MEN (2003) Sex wars: genes, bacteria, and sex ratios. Princeton University Press, Princeton, p 250
Majerus MEN (2006) The impact of male-killing bacteria on the evolution of aphidophagous coccinellids. Eur J Entomol 103(1):1–7. https://doi.org/10.14411/eje.2006.001
Majerus TMO, Majerus MEN (2010) Discovery and identification of a male-killing agent in the japanese ladybird Propylea japonica (Coleoptera: Coccinellidae). BMC Evol Biol 10:37. https://doi.org/10.1186/1471-2148-10-37
Majerus TMO, Majerus MEN, Knowles B, Wheeler J, Bertrand D, Kuznetzov V, Ueno H, Hurst GDD (1998) Extreme variation in the prevalence of inherited male-killing microorganisms between three populations of Harmonia axyridis (Coleoptera: Coccinellidae). Heredity 81:683–691. https://doi.org/10.1046/j.1365-2540.1998.00438.x
Majerus TMO, Schulenburg JHG, Majerus MEN, Hurst GDD (1999) Molecular identification of a male-killing agent in the ladybird Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae). Insect Mol Biol 8(4):551–555. https://doi.org/10.1046/j.1365-2583.1999.00151.x
Majerus MEN, Hinrich J, Schulenburg GVD, Zakharov IA (2000) Multiple causes of male-killing in a single sample of the two-spot ladybird, Adalia bipunctata (Coleoptera: Coccinellidae) from Moscow. Heredity 84:605–609. https://doi.org/10.1046/j.1365-2540.2000.00710.x
Mathé-Hubert H, Kaech H, Ganesanandamoorthy P, Vorburger C (2019) Evolutionary costs and benefits of infection with diverse strains of Spiroplasma in pea aphids. Evolution 73(7):1466–1481. https://doi.org/10.1111/evo.13740
Matsuka M, Hashi H, Okada I (1975) Abnormal sex-ratio found in the lady beetle, Harmonia axyridis Pallas (Coleoptera: Coccinellidae). Appl Entomol Zool 10(2):84–89. https://doi.org/10.1303/aez.10.84
Michaud J (2003) A comparative study of larval cannibalism in three species of ladybird. Ecol Entomol 28:92–101. https://doi.org/10.1046/j.1365-2311.2002.00481.x
Pietri JE, DeBruhl H, Sullivan W (2016) The rich somatic life of Wolbachia. MicrobiologyOpen 5(6):923–936. https://doi.org/10.1002/mbo3.390
Rhule EL, Majerus MEN, Jiggins FM, Ware RL (2010) Potential role of the sexually transmitted mite Coccipolipus hippodamiae in controlling populations of the invasive ladybird Harmonia axyridis. Biol Control 53(2):243–247. https://doi.org/10.1016/j.biocontrol.2009.12.006
Romanov DA, Matveikina EA (2022) Harmonia axyridis (Pallas, 1773) (Coleoptera: Coccinellidae) in the cities of Moscow and Yalta: its competition with native species of coccinellids and the influence of parasitoids on its number. Rus J Biol Invas 13(1):87–104. https://doi.org/10.1134/S207511172201012X
Romanov DA, Zakharov IA, Shaikevich EV (2020) Wolbachia, Spiroplasma, and Rickettsia symbiotic bacteria in aphids (Aphidoidea). Vavilov J Genet Breed 24(6):673–682. https://doi.org/10.18699/VJ20.661
Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, New York, p 1626
Schulenburg JHG, Habig M, Sloggett JJ, Webberley KM, Bertrand D, Hurst GDD, Majerus MEN (2001) Incidence of male-killing Rickettsia spp. (alpha-proteobacteria) in the ten-spot ladybird beetle Adalia decempunctata L. (Coleoptera: Coccinellidae). Appl Environ Microbiol 67(1):270–277. https://doi.org/10.1128/AEM.67.1.270-277.2001
Shaikevich EV, Romanov DA (2023) Symbiotic Wolbachia bacteria in coccinellid parasitoids: genetic diversity, horizontal transfer, and recombination. Int Microbiol 26:269–280. https://doi.org/10.1007/s10123-022-00295-0
Shaikevich EV, Ivshina EV, Zakharov IA (2012) Polymorphism of mitochondrial DNA and distribution of cytoplasmic symbionts in the populations of two-spot ladybird beetle Adalia bipunctata. Rus J Genet 48(5):567–571. https://doi.org/10.1134/S1022795412040102
Shaikevich EV, Romanov DA, Zakharov IA (2021) The diversity of Wolbachia and its effects on host reproduction in a single Adalia bipunctata (Coleoptera: Coccinellidae) population. Symbiosis 85(2):249–257. https://doi.org/10.1007/s13199-021-00808-x
Shaikevich EV, Gorbacheva AA, Romanov DA (2023) Ectoparasitic mites: vectors of bacterial symbionts among insects. Biol Bull 50(3):338–347. https://doi.org/10.1134/S1062359023700231
Shull HF (1948) An all-female strain of lady beetles with reversions to normal sex ratio. Am Nat 82:241–251. https://doi.org/10.1086/281581
Tabata J, Hattori Y, Sakamoto H, Yukuhiro F, Fujii T, Kugimiya S, Mochizuki A, Ishikawa Y, Kageyama D (2011) Male killing and incomplete inheritance of a novel Spiroplasma in the moth Ostrinia zaguliaevi. Microb Ecol 61:254–263. https://doi.org/10.1007/s00248-010-9799-y
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) Mol Biol Evol 30(12):2725–2729. https://doi.org/10.1093/molbev/mst197. MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0
Teixeira L, Ferreira A, Ashburner M (2008) The bacterial symbiont Wolbachia induces resistance to RNA virus infections in Drosophila melanogaster. PLoS Biol 6(12):e2. https://doi.org/10.1371/journal.pbio.1000002
Tinsley MC, Majerus MEN (2006) A new male-killing parasitism: Spiroplasma bacteria infect the ladybird beetle Anisosticta novemdecimpunctata (Coleoptera: Coccinellidae). Parasitology 132(6):757–765. https://doi.org/10.1017/S0031182005009789
Vorburger C, Perlman SJ (2018) The role of defensive symbionts in host-parasite coevolution. Biol Rev Camb Philos Soc 93(4):1747–1764. https://doi.org/10.1111/brv.12417
Webberley KM, Hurst GDD (2002) The effect of aggregative overwintering on an insect sexually transmitted parasite system. J Parasitol 88(4):707–712. https://doi.org/10.1645/0022-3395(2002)088[0707:TEOAOO]2.0.CO;2
Webberley KM, Hurst GDD, Husband RW, Schulenburg JHGVD, Sloggett JJ, Isham V, Buszko J, Majerus MEN (2004) Host reproduction and a sexually transmitted disease: causes and consequences of Coccipolipus hippodamiae distribution on coccinellid beetles. J Anim Ecol 73(1):1–10. https://doi.org/10.1111/j.1365-2656.2004.00769.x
Weinert LA, Tinsley MC, Temperley M, Jiggins FM (2007) Are we underestimating the diversity and incidence of insect bacterial symbionts? A case study in ladybird beetles. Biol Lett 3(6):678–681. https://doi.org/10.1098/rsbl.2007.0373
Weinert LA, Araujo-Jnr EV, Ahmed MZ, Welch JJ (2015) The incidence of bacterial endosymbionts in terrestrial arthropods. Proc Biol Sci 282:20150249. https://doi.org/10.1098/rspb.2015.0249
Werren JH, Hurst GDD, Zhang W, Breeuwer JA, Stouthamer R, Majerus MEN (1994) Rickettsial relative associated with male-killing in the ladybird beetle (Adalia bipunctata). J Bacteriol 176(2):388–394. https://doi.org/10.1128/jb.176.2.388-394.1994
Werren JH, Baldo L, Clark ME (2008) Wolbachia: master manipulators of invertebrate biology. Nat Rev Microbiol 6(10):741–751. https://doi.org/10.1038/nrmicro1969
Xie J, Vilchez I, Mateos M (2010) Spiroplasma bacteria enhance survival of Drosophila hydei attacked by the parasitic wasp Leptopilina heterotoma. PLoS ONE 5(8):e12149. https://doi.org/10.1371/journal.pone.0012149
Zakharov IA, Goryacheva II (1998) Sex ratios in Adalia bipunctata populations and population-genetic significance of male killing. Rus J Genet 34(12):1389–1395
Zakharov IA, Shaikevich EV (2001) The Stockholm populations of Adalia bipunctata (L) (Coleoptera: Coccinellidae) – a case of extreme female-biased population sex ratio. Hereditas 134(3):263–266. https://doi.org/10.1111/J.1601-5223.2001.00263.X
Zakharov IA, Shaikevich EV (2012) An mtDNA polymorphism in the St. Petersburg population of Adalia bipunctata and its correlation with infection by the symbiotic bacterium Spiroplasma. Rus J Genet: Appl Res 2(2):110–113. https://doi.org/10.1134/S207905971202013X
Zakharov IA, Shaikevich EV (2013) Comparative study of mtDNA in species of the genus Adalia (Coleoptera: Coccinellidae) and origin of ancient mitochondrial haplotypes in the gene pool of Adalia bipunctata. Eur J Entomol 110(3):427–433. https://doi.org/10.14411/eje.2013.057
Zakharov IA, Chernysheva NE, Hurst GDD, Majerus MEN (1996) Maternally inherited bacterium causing female bias in the St. Petersburg population of Adalia bipunctata does not belong to the genus Rickettsia. Rus J Genet 32(11):1303–1306
Zakharov IA, Shaikevich EV, Goryacheva II (1998a) Bacteria of the Spiroplasma genus infect two-spot ladybugs (Adalia bipunctata L.) in Russia. Dokl Akad Nauk 362(4):570–573 (In Russian)
Zakharov IA, Goryacheva II, Rydkina EB, Roux V, Raoult D (1998b) Cytoplasmically inherited female-biased sex ratio in Kyrgyz population of Adalia bipunctata turanica caused by bacteria of the genus Rickettsia. Rus J Genet 34(2):171–175
Zakharov IA, Zinkevich NS, Shaikevich EV, Vysotskaya LV, Dorzhu CM, Majerus MEN (1999) Sex ratio and male killing in siberian populations of Harmonia axyridis Pall. Rus J Genet 35(6):653–657
Zakharov IA, Goryacheva II, Shaikevich EV, Schulenburg JH, Majerus MEN (2000a) Wolbachia, a new bacterial agent causing sex-ratio bias in the two-spot ladybird Adalia bipunctata L. Rus J Genet 36(4):385–388
Zakharov IA, Goryacheva II, Shaikevich EV, Dorzhu CM (2000b) Distribution of cytoplasmically inherited bacteria of the genus Spiroplasma causing female bias in eurasian populations of Adalia bipunctata L. Rus J Genet 36(2):135–137
Zélé F, Nicot A, Duron O, Rivero A (2012) Infection with Wolbachia protects mosquitoes against Plasmodium-induced mortality in a natural system. J Evol Biol 25(7):1243–1252. https://doi.org/10.1111/j.1420-9101.2012.02519.x
Funding
The reported study was supported by Russian Science Foundation (Project No. 22-24-00435).
Author information
Authors and Affiliations
Contributions
All authors contributed to the study conception and design. Insect’s collection were performed by Ilya Zakharov (in 1994–2019) and Denis Romanov (in 2020–2022). Molecular-genetic analysis were performed by Denis Romanov. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Declarations
We declare that this paper consists of original, unpublished work, which is not under consideration for publication elsewhere.
Ethics approval
Not applicable.
Consent to participate
Not applicable.
Consent for publication
Not applicable.
Conflicts of interest/Competing interests
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) 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
Romanov, D.A., Zakharov, I.A. Distribution of symbiotic bacteria Spiroplasma, Rickettsia, Wolbachia in populations of Adalia bipunctata (Linnaeus, 1758). Symbiosis 91, 1–13 (2023). https://doi.org/10.1007/s13199-023-00942-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13199-023-00942-8