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Heritable bacterial endosymbionts in native and invasive populations of Harmonia axyridis

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Abstract

Harmonia axyridis Pallas (1773) (Coleoptera: Coccinellidae) is the well-studied system of invasive insect species. Native and invasive parts of the area of H. axyridis are isolated geographically. We studied the species composition and the distribution of bacterial symbionts Spiroplasma and Rickettsia in seven localities of the native area and six localities of the invasive area of H. axyridis. Rickettsia was detected in H. axyridis populations for the first time. We found that the proportion of beetles infected with Rickettsia in native and invasive populations of H. axyridis is about 0.03. Spiroplasma was found only in native populations of H. axyridis. The proportion of infected individuals with Spiroplasma in native populations of H. axyridis is about 0.08. All studied native populations of H. axyridis are infected with Spiroplasma, while all invasive populations are not. We discuss the possible influence of Spiroplasma and Rickettsia in the formation of invasive populations of H. axyridis.

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References

  • Ahmed MZ, Ren S-X, Mandour NS, Greeff JM, Qiu B-L (2010) Prevalence of Wolbachia supergroups A and B in Bemisia tabaci (Hemiptera: Aleyrodidae) and some of its natural enemies. J Econ Entomol. doi:10.1603/ec10033

    PubMed  Google Scholar 

  • Blekhman AV, Goryacheva II, Zakharov IA (2010) Differentiation of Harmonia axyridis Pall. according to polymorphic morphological traits and variability of the mitochondrial COI gene. Moscow Univ Biol Sci Bull 65:174–176. doi:10.3103/S0096392510040140

    Article  Google Scholar 

  • Bouzat JL (2010) Conservation genetics of population bottlenecks: the role of chance, selection, and history. Conserv Genet 11:463–478. doi:10.1007/s10592-010-0049-0

    Article  Google Scholar 

  • Brown PJ, Thomas C, Lombaert E, Jeffries D, Estoup A, Lawson Handley LJ (2011) The global spread of Harmonia axyridis (Coleoptera: Coccinellidae): distribution, dispersal and routes of invasion. Biocontrol 56:623–641. doi:10.1007/s10526-011-9379-1

    Article  Google Scholar 

  • Dedeine F, Vavre F, Fleury F, Loppin B, Hochberg ME, Bouletreau M (2001) Removing symbiotic Wolbachia bacteria specifically inhibits oogenesis in a parasitic wasp. Proc Natl Acad Sci USA 98:6247–6252

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dedeine F, Vavre F, Shoemaker DD, Bouletreau M (2004) Intra-individual coexistence of a Wolbachia strain required for host oogenesis with two strains inducing cytoplasmic incompatibility in the wasp Asobara tabida. Evolution 58:2167–2174

    Article  PubMed  Google Scholar 

  • Duron O, Bouchon D, Boutin S, Bellamy L, Zhou L, Engelstadter J, Hurst GD (2008) The diversity of reproductive parasites among arthropods: Wolbachia do not walk alone. BMC Biol 6:27

    Article  PubMed  PubMed Central  Google Scholar 

  • Dyson EA, Hurst GDD (2004) Persistence of an extreme sex-ratio bias in a natural population. Proc Natl Acad Sci USA 101:6520–6523

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Elnagdy S, Majerus MEN, Handley LJL (2011) The value of an egg: resource reallocation in ladybirds (Coleoptera: Coccinellidae) infected with male-killing bacteria. J Evol Biol 24:2164–2172

    Article  CAS  PubMed  Google Scholar 

  • Elnagdy S, Majerus MEN, Gardener M, Lawson Handley LJ (2013) The direct effects of male killer infection on fitness of ladybird hosts (Coleoptera: Coccinellidae). J Evol Biol 26:1816–1825

    Article  CAS  PubMed  Google Scholar 

  • Engelstadter J, Hurst GDD (2007) The impact of male-killing bacteria on host evolutionary processes. Genetics 175:245–254

    Article  PubMed  PubMed Central  Google Scholar 

  • Facon B, Crespin L, Loiseau A, Lombaert E, Magro A, Estoup A (2011a) Can things get worse when an invasive species hybridizes? The harlequin ladybird Harmonia axyridis in France as a case study. Evol Appl 4:71–88

    Article  PubMed  Google Scholar 

  • Facon B et al (2011b) Inbreeding depression is purged in the invasive insect Harmonia axyridis. Curr Biol 21:424–427

    Article  CAS  PubMed  Google Scholar 

  • Fleury F, Vavre F, Ris N, Fouillet P, Bouletreau M (2000) Physiological cost induced by the maternally-transmitted endosymbiont Wolbachia in the Drosophila parasitoid Leptopilina heterotoma. Parasitology 121(Pt 5):493–500

    Article  PubMed  Google Scholar 

  • Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299

    CAS  PubMed  Google Scholar 

  • Glemin S (2003) How are deleterious mutations purged? Drift versus nonrandom mating. Evolution 57:2678–2687

    Article  PubMed  Google Scholar 

  • Goodnight CJ (1988) Epistasis and the effect of founder events on the additive genetic variance. Evolution 42:441–454. doi:10.2307/2409030

    Article  Google Scholar 

  • Goryacheva II, Blekhman AV, Andrianov BV, Gorelova TV, Zakharov IA (2015) Genotypic diversity of Wolbachia pipientis in native and invasive Harmonia axyridis Pall., 1773 (Coleoptera, Coccinellidae) populations. Russ J Genet 51:731–736

    Article  CAS  Google Scholar 

  • Hedges LM, Brownlie JC, O’Neill SL, Johnson KN (2008) Wolbachia and virus protection in insects. Science 322:702

    Article  CAS  PubMed  Google Scholar 

  • Hendry TA, Hunter MS, Baltrus DA (2014) The facultative symbiont rickettsia protects an invasive whitefly against entomopathogenic Pseudomonas syringae strains. Appl Environ Microbiol 80:7161–7168

    Article  PubMed  PubMed Central  Google Scholar 

  • Himler AG et al (2011) Rapid spread of a bacterial symbiont in an invasive whitefly is driven by fitness benefits and female bias. Science 332:254–256

    Article  CAS  PubMed  Google Scholar 

  • Hurst GD, Jiggins FM (2000) Male-killing bacteria in insects: mechanisms, incidence, and implications. Emerg Infect Dis 6:329–336

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hurst GD, Hammarton TC, Obrycki JJ, Majerus TM, Walker LE, Bertrand D, Majerus ME (1996) Male-killing bacterium in a fifth ladybird beetle, Coleomegilla maculata (Coleoptera: Coccinellidae). Heredity 77(2):177–185

    Article  PubMed  Google Scholar 

  • Hurst GD, Bandi C, Sacchi L, Cochrane AG, Bertrand D, Karaca I, Majerus ME (1999a) Adonia variegata (Coleoptera: Coccinellidae) bears maternally inherited Flavobacteria that kill males only. Parasitology 118(2):125–134

    Article  PubMed  Google Scholar 

  • Hurst GD et al (1999b) Invasion of one insect species, Adalia bipunctata, by two different male-killing bacteria. Insect Mol Biol 8:133–139

    Article  CAS  PubMed  Google Scholar 

  • Hurst GDD et al (1999c) Male-killing Wolbachia in two species of insect. Proc R Soc London B Biol Sci. doi:10.1098/rspb.1999.0698

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Jiggins FM, Hurst GDD, Majerus MEN (1998) Sex ratio distortion in Acraea encedon (Lepidoptera: Nymphalidae) is caused by a male-killing bacterium. Heredity 81:87–91. doi:10.1046/j.1365-2540.1998.00357.x

    Article  Google Scholar 

  • Jiggins FM, Hurst GD, Majerus ME (2000) Sex-ratio-distorting Wolbachia causes sex-role reversal in its butterfly host. Proc Biol Sci 267:69–73

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khan IA, Wan F-H (2015) Prey consumption by Harmonia axyridis of un-parasitized and Encarsia formosa parasitized Bemisia tabaci biotype B prey. J Entomol Zool Stud 3:122–127

    Google Scholar 

  • Koch RL (2003) The multicolored Asian lady beetle, Harmonia axyridis: a review of its biology, uses in biological control, and non-target impacts. J Insect Sci 3:32

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lawson ET, Mousseau TA, Klaper R, Hunter MD, Werren JH (2001) Rickettsia associated with male-killing in a buprestid beetle. Heredity 86:497–505

    Article  CAS  PubMed  Google Scholar 

  • Lombaert E, Guillemaud T, Cornuet JM, Malausa T, Facon B, Estoup A (2010) Bridgehead effect in the worldwide invasion of the biocontrol harlequin ladybird. PLoS ONE 5:e9743

    Article  PubMed  PubMed Central  Google Scholar 

  • Lombaert E et al (2014) Complementarity of statistical treatments to reconstruct worldwide routes of invasion: the case of the Asian ladybird Harmonia axyridis. Mol Ecol 23:5979–5997

    Article  PubMed  Google Scholar 

  • Lusis JJ (1947) Some rules of reproduction in populations of Adalia bipunctata: non-male strains in populations. Dokl Akad Nauk SSR 57:951–954

    Google Scholar 

  • Magro A, Lecompte E, Magne F, Hemptinne JL, Crouau-Roy B (2010) Phylogeny of ladybirds (Coleoptera: Coccinellidae): are the subfamilies monophyletic? Mol Phylogenet Evol 54:833–848

    Article  CAS  PubMed  Google Scholar 

  • 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. doi:10.1186/1471-2148-10-37

    Article  PubMed  PubMed Central  Google Scholar 

  • Majerus TMO et al (1998) Extreme variation in the prevalence of inherited male-killing microorganisms between three populations of Harmonia axyridis (Coleoptera: Coccinellidae). Heredity 81:683–691

    Article  Google Scholar 

  • Majerus TM, Graf von der Schulenburg JH, Majerus ME, Hurst GD (1999) Molecular identification of a male-killing agent in the ladybird Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae). Insect Mol Biol 8:551–555

    Article  CAS  PubMed  Google Scholar 

  • Majerus ME, Hinrich J, Schulenburg GV, 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(5):605–609

    Article  PubMed  Google Scholar 

  • Matsuka M, Hashi H, Okada I (1975) Abnormal sex-ratio found in the lady beetle, Harmonia axyridis Pallas (Coleoptera: Coccinellidae). Appl Entomol Zool 10:84–89. doi:10.1303/aez.10.84

    Google Scholar 

  • Min KT, Benzer S (1997) Wolbachia, normally a symbiont of Drosophila, can be virulent, causing degeneration and early death. Proc Natl Acad Sci USA 94:10792–10796

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakamura K, Ueno H, Miura K (2005) Prevalence of inherited male-killing microorganisms in Japanese population of ladybird beetle Harmonia axyridis (Coleoptera: Coccinellidae). Ann Entomol Soc Am. doi:10.1603/0013-8746(2005)098[0096:POIMMI]2.0.CO;2

  • Nikoh N, Hosokawa T, Moriyama M, Oshima K, Hattori M, Fukatsu T (2014) Evolutionary origin of insect—Wolbachia nutritional mutualism. Proc Natl Acad Sci USA 111:10257–10262

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Noda H, Miyoshi T, Zhang Q, Watanabe K, Deng K, Hoshizaki S (2001) Wolbachia infection shared among planthoppers (Homoptera: Delphacidae) and their endoparasite (Strepsiptera: Elenchidae): a probable case of interspecies transmission. Mol Ecol 10:2101–2106

    Article  CAS  PubMed  Google Scholar 

  • Osawa N (1992) Sibling cannibalism in the ladybird beetleHarmonia axyridis: fitness consequences for mother and offspring. Res Popul Ecol 34:45–55. doi:10.1007/bf02513521

    Article  Google Scholar 

  • Pattabhiramaiah M (2010) Horizontal transmission of Wolbachia in the honeybee subspecies Apis mellifera carnica and its ectoparasite Varroa destructor. Int J Environ Sci 2:514–523. doi:10.6088/ijes.00202020013

    Google Scholar 

  • Ronquist F et al (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542

    Article  PubMed  PubMed Central  Google Scholar 

  • Rousset F, Bouchon D, Pintureau B, Juchault P, Solignac M (1992) Wolbachia endosymbionts responsible for various alterations of sexuality in arthropods. Proc R Soc London B Biol Sci 250:91–98. doi:10.1098/rspb.1992.0135

    Article  CAS  Google Scholar 

  • Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual. vol 1. Cold Spring Harbor Laboratory Press, Cold Spring Harbor

    Google Scholar 

  • Sloggett JJ (2012) Harmonia axyridis invasions: deducing evolutionary causes and consequences. Entomol Sci 15:261–273. doi:10.1111/j.1479-8298.2012.00519.x

    Article  Google Scholar 

  • Stouthamer R, Werren JH (1993) Microbes associated with parthenogenesis in wasps of the genus Trichogramma. J Invertebr Pathol 61:6–9. doi:10.1006/jipa.1993.1002

    Article  Google Scholar 

  • Swindell WR, Bouzat JL (2006) Reduced inbreeding depression due to historical inbreeding in Drosophila melanogaster: evidence for purging. J Evol Biol 19:1257–1264

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739. doi:10.1093/molbev/msr121

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tayeh A et al (2013) Investigating the genetic load of an emblematic invasive species: the case of the invasive harlequin ladybird Harmonia axyridis. Ecol Evol 3:864–871. doi:10.1002/ece3.490

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tayeh A, Hufbauer RA, Estoup A, Ravigne V, Frachon L, Facon B (2015) Biological invasion and biological control select for different life histories. Nat Commun 6:7268

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tinsley MC, Majerus ME (2006) A new male-killing parasitism: Spiroplasma bacteria infect the ladybird beetle Anisosticta novemdecimpunctata (Coleoptera: Coccinellidae). Parasitology 132:757–765. doi:10.1017/S0031182005009789

    Article  CAS  PubMed  Google Scholar 

  • Turelli M, Hoffmann AA (1991) Rapid spread of an inherited incompatibility factor in California Drosophila. Nature 353:440–442

    Article  CAS  PubMed  Google Scholar 

  • Turelli M, Hoffmann AA (1995) Cytoplasmic incompatibility in Drosophila simulans: dynamics and parameter estimates from natural populations. Genetics 140:1319–1338

    CAS  PubMed  PubMed Central  Google Scholar 

  • Turgeon J et al (2011) Experimental evidence for the phenotypic impact of admixture between wild and biocontrol Asian ladybird (Harmonia axyridis) involved in the European invasion. J Evol Biol 24:1044–1052. doi:10.1111/j.1420-9101.2011.02234.x

    Article  CAS  PubMed  Google Scholar 

  • Vavre F, Fleury F, Lepetit D, Fouillet P, Bouletreau M (1999) Phylogenetic evidence for horizontal transmission of Wolbachia in host-parasitoid associations. Mol Biol Evol 16:1711–1723

    Article  CAS  PubMed  Google Scholar 

  • Vilcinskas A, Stoecker K, Schmidtberg H, Rohrich CR, Vogel H (2013) Invasive harlequin ladybird carries biological weapons against native competitors. Science 340:862–863. doi:10.1126/science.1234032

    Article  CAS  PubMed  Google Scholar 

  • Vilcinskas A, Schmidtberg H, Estoup A, Tayeh A, Facon B, Vogel H (2015) Evolutionary ecology of microsporidia associated with the invasive ladybird Harmonia axyridis. Insect Sci 22:313–324. doi:10.1111/1744-7917.12159

    Article  PubMed  Google Scholar 

  • von der Schulenburg JH, Habig M, Sloggett JJ, Webberley KM, Bertrand D, Hurst GD, Majerus ME (2001) Incidence of male-killing Rickettsia spp. (alpha-proteobacteria) in the Ten-Spot Ladybird BeetleAdalia decempunctata L. (Coleoptera: Coccinellidae). Appl Environ Microbiol 67:270–277

    Article  PubMed  PubMed Central  Google Scholar 

  • Weeks AR, Turelli M, Harcombe WR, Reynolds KT, Hoffmann AA (2007) From parasite to mutualist: rapid evolution of Wolbachia in natural populations of Drosophila. PLoS Biol 5:e114

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 3:678–681

    Article  PubMed  PubMed Central  Google Scholar 

  • Weinert LA, Werren JH, Aebi A, Stone GN, Jiggins FM (2009) Evolution and diversity of Rickettsia bacteria. BMC Biol 7:6

    Article  PubMed  PubMed Central  Google Scholar 

  • Werren JH, Hurst GD, Zhang W, Breeuwer JA, Stouthamer R, Majerus ME (1994) Rickettsial relative associated with male killing in the ladybird beetle (Adalia bipunctata). J Bacteriol 176:388–394

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Werren JH, Windsor D, Guo L (1995) Distribution of Wolbachia among neotropical arthropods. Proc R Soc London B Biol Sci 262:197–204. doi:10.1098/rspb.1995.0196

    Article  Google Scholar 

  • Yen JH, Barr AR (1971) New hypothesis of the cause of cytoplasmic incompatibility in Culex pipiens L. Nature 232:657–658

    Article  CAS  PubMed  Google Scholar 

  • Zakharov IA, Blekhman A (2013) Comparative analysis of invasive and native populations of Harmonia axyridis by a complex of morphological traits. IOBC/WPRS Bull 94:131–139

    Google Scholar 

  • Zakharov IA, Goryacheva II, Rydkina EB, Roux V, Raoult D (1998) Cytoplasmically inherited female-biased sex ratio in Kyrgyz population of Adalia bipunctata turanica caused by bacteria of the genus Rickettsia. Russ J Genet 34:235–239

    Google Scholar 

  • Zakharov IA, Zinkevich NS, Shaikevich EV, Vysotskaia LV, Dorzhu CM, Majerus ME (1999) Sex ratio and male killing in Siberian populations of Harmonia axyridis (Pass.). Genetika 35:771–776

    CAS  PubMed  Google Scholar 

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Acknowledgments

Funding for this work was provided by the Russian Foundation for Basic Research (Project No. 15-04-07466_A) and by the Russian Science Foundation (Project No. 16-16-00079). The authors are grateful to M. Ya. Orlova-Ben’kovskaya, L. V. Frisman, V. P. Korablev, and A. V. Zimenko for providing them with the H. axyridis collections.

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Authors and Affiliations

  1. Vavilov Institute of General Genetics, Russian Academy of Sciences, Gubkina str. 3, Moscow, Russia, 119991

    Irina Goryacheva, Boris Andrianov & Ilia Zakharov

  2. Koltsov Institute of Developmental Biology, Russian Academy of Sciences, Vavilova str. 26, Moscow, Russia, 119334

    Alla Blekhman

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  1. Irina Goryacheva
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  2. Alla Blekhman
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  3. Boris Andrianov
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  4. Ilia Zakharov
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Correspondence to Boris Andrianov.

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Goryacheva, I., Blekhman, A., Andrianov, B. et al. Heritable bacterial endosymbionts in native and invasive populations of Harmonia axyridis . Biol Invasions 19, 493–502 (2017). https://doi.org/10.1007/s10530-016-1298-8

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