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Prevalence of maternally-inherited bacteria in native and invasive populations of the harlequin ladybird beetle Harmonia axyridis

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Abstract

Harmonia axyridis Pallas (Coleoptera: Coccinellidae) has attracted a growing body of research trying to understand its invasion success in North America and Europe after being introduced from its original range central and east Asia. Its endosymbiotic microorganisms along with the introduction are often assumed to play a potential role in the invasion. We examined the prevalence of three common bacterial groups Rickettsia, Wolbachia and Spiroplasma in H. axyridis populations from 30 geographical locations across mainland China and nine across the Americas. Rickettsia was not detected in both native and non-native H. axyridis populations. Wolbachia infected only one native population at 9.5% but three non-native populations at rates from 3.6 to 25%. All Wolbalchia sequences were aligned to four haplotypes in two groups in the phylogenetic reconstruction. Spiroplasma was not found infecting non-native populations while it infected 15 native ones at rates from 1.6 to 20%. All Spiroplasma sequences were aligned to six haplotypes, among which five were new to H. axyridis populations from China and one was identical to that from Japan. All Spiroplasma lineages in native H. axyridis populations were representative of S. ixodetis. This geographic infection pattern across native and non-native H. axyridis populations suggests that these three groups of maternally-inherited bacteria may not be influential at the initial stages of invasion of H. axyridis in North America.

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References

  • Aebi A, Zindel R (2010) What can endosymbionts tell about the Harmonia axyridis invasion? IOBC/WPRS Bull 58:5–6

    Google Scholar 

  • Ahmed MZ, Li S-J, Xue X et al (2015) The intracellular bacterium Wolbachia uses parasitoid wasps as phoretic vectors for efficient horizontal transmission. PLoS Pathog 11:e1004672

    Article  CAS  PubMed Central  Google Scholar 

  • Brown PJ, Thomas C, Lombaert E et al (2011) The global spread of Harmonia axyridis (Coleoptera: Coccinellidae): distribution, dispersal and routes of invasion. Biocontrol 56:623–641

    Article  Google Scholar 

  • Brown PMJ, Adriaens T, Bathon H et al (2008) Harmonia axyridis in Europe: spread and distribution of a non-native coccinellid. Biocontrol 53:5–21

    Article  Google Scholar 

  • Cheng CH, Wickham JD, Chen L et al (2018) Bacterial microbiota protect an invasive bark beetle from a pine defensive compound. Microbiome 6:132

    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  Google Scholar 

  • Eleftherianos I, Atri J, Accetta J et al (2013) Endosymbiotic bacteria in insects: guardians of the immune system? Front Physiol 4:46

    Article  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 et al (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 

  • Feldhaar H (2011) Bacterial symbionts as mediators of ecologically important traits of insect hosts. Ecol Entomol 36:533–543

    Article  Google Scholar 

  • Frago E, Dicke M, Godfray HCJ (2012) Insect symbionts as hidden players in insect–plant interactions. Trends Ecol Evol 27:705–711

    Article  PubMed  Google Scholar 

  • Goryacheva I, Blekhman A, Andrianov B et al (2017) Heritable bacterial endosymbionts in native and invasive populations of Harmonia axyridis. Biol Invasions 19:493–502

    Article  Google Scholar 

  • Goryacheva I, Blekhman A, Andrianov B et al (2018) Spiroplasma infection in Harmonia axyridis - Diversity and multiple infection. PLoS ONE 13:e0198190

    Article  PubMed  PubMed Central  Google Scholar 

  • Goryacheva I, Blekhmanb AV, Andrianova BV et al (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 

  • Haelewaters D, Zhao SY, Clusella-Trullas S et al (2017) Parasites of Harmonia axyridis: current research and perspectives. Biocontrol 62:355–371

    Article  Google Scholar 

  • Heddi A, Grenier AM, Khatchadourian C, Charles H, Nardon P (1999) Four intracellular genomes direct weevil biology: nuclear, mitochondrial, principal endosymbiont, and Wolbachia. Proc Natl Acad Sci USA 96:6814–6819

    Article  CAS  PubMed  Google Scholar 

  • Hilgenboecker K, Hammerstein P, Schlattmann P et al (2008) How many species are infected with Wolbachia? a statistical analysis of current data. FEMS Microbiol Lett 281:215–220

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Himler AG, Adachi-Hagimori T, Bergen JE et al (2011) Rapid spread of a bacterial symbiont in an invasive whitefly is driven by fitness benefits and female bias. Science 332:254–265

    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 

  • Jiggins FM, Hurst GDD, Jiggins CD et al (2000) The butterfly Danaus chrysippus is infected by a male-killing Spiroplasma bacterium. Parasit 120:439–446

    Article  Google Scholar 

  • Kajtoch L, Kotásková N (2018) Current state of knowledge on Wolbachia infection among Coleoptera: a systematic review. Peer J 6:e4471

    Article  PubMed  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 3:1–16

    Article  Google Scholar 

  • Lombaert E, Guillemaud T, Cornuet JM et al (2010) Bridgehead effect in the worldwide invasion of the biocontrol harlequin ladybird. PLoS ONE 5:e9743

    Article  PubMed  PubMed Central  Google Scholar 

  • Lu M, Wingfield MJ, Gillette NE (2010) Complex interactions among host pines and fungi vectored by an invasive bark beetle. New Phytol 187:859–866

    Article  Google Scholar 

  • Lu M, Hulcr J, Sun JH (2016) The role of symbiotic microbes in insect invasions. Annu Rev Ecol Evol Syst 47:487–505

    Article  Google Scholar 

  • Majerus MEN (2003) Sex wars: genes, bacteria, and sex ratios. Princeton University Press, Princeton

    Google Scholar 

  • Majerus TMO, Majerus MEN, Knowles B 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 

  • 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 98:96–99

    Article  Google Scholar 

  • Raak-van den Berg CL, Hemerik L, van der Werf W et al (2017) Life history of the harlequin ladybird, Harmonia axyridis: a global meta-analysis. Biocontrol 62:283–296

    Article  Google Scholar 

  • Richard FJ (2017) Symbiotic bacteria influence the odor and mating preference of their hosts. Front Ecol Evol 5:143

    Article  Google Scholar 

  • Rowe M, Veerus L, Trosvik P et al (2020) The reproductive microbiome: an. Emerging driver of sexual selection, sexual conflict, mating systems, and reproductive isolation. Trends Ecol Evol 35:220–234

    Article  PubMed  Google Scholar 

  • Roy HE, Brown PMJ, Adriaens T et al (2016) The harlequin ladybird, Harmonia axyridis: global perspectives on invasion history and ecology. Biol Invasions 18:997–1044

    Article  Google Scholar 

  • Rozas J, Sanchez-Delbarrio JC, Peypoch XM et al (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497

    Article  CAS  PubMed  Google Scholar 

  • Sazama EJ, Bosch MJ, Shouldis CS et al (2017) Incidence of Wolbachia in aquatic insects. Ecol Evol 7:1165–1169

    Article  PubMed  PubMed Central  Google Scholar 

  • Sazama EJ, Ouellette SP, Wesner JS (2019) Bacterial endosymbionts are common among, but not necessarily within, insect species. Environ Entomol 48:127–133

    Article  PubMed  Google Scholar 

  • Sloggett JJ (2012) Harmonia axyrids invasions: deducing evolutionary causes and consequence. Entomol Sci 15:261–273

    Article  Google Scholar 

  • Tamura K, Stecher G, Peterson D et al (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    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

    Article  CAS  PubMed  Google Scholar 

  • Turgeon J, Tayeh A, Facon B 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 Evolution Biol 24:1044–1052

    Article  CAS  Google Scholar 

  • van Lenteren JC (2012) The state of commercial augmentative biological control: plenty of natural enemies, but a frustrating lack of uptake. Biocontrol 57:1–20

    Article  Google Scholar 

  • Vilcinskas A, Stoecker K, Schmidtberg H et al (2013) Invasive harlequin ladybird carries biological weapons against native competitors. Science 340:862–863

    Article  CAS  PubMed  Google Scholar 

  • Weinert LA, Araujo-Jnr EV, Ahmed MZ et al (2015) The incidence of bacterial endosymbionts in terrestrial arthropods. Proc R Soc B 282:1807

    Article  Google Scholar 

  • Weinert LA, Tinsley MC, Temperley M (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 

  • Werren JH, Baldo L, Clark ME (2008) Wolbachia: master manipulators of invertebrate biology. Nat Rev Microbiol 6:741–751

    Article  CAS  PubMed  Google Scholar 

  • Werren JH, Windsor DM (2000) Wolbachia infection frequencies in insects: evidence of a global. equilibrium? Proc R Soc B 267:1277–1285

    Article  CAS  PubMed  Google Scholar 

  • Zakharov IA, Goryacheva I, Suvorov A (2011) Mitochondrial DNA polymorphism in invasive and native populations of Harmonia axyridis. Russ J Environ Sci 1:15–18

    Google Scholar 

  • Zakharov IA, Zinkevich NS, Shaikevich EV et al (1999) Sex ratio and male killing in Siberian populations of Harmonia axyridis (Pass.). Genetika 35:771–776

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Shaokui Wen, Hehe Cao, Yuyang Sheng, Shulei Tai, Zhentai Ge, Haosen Li, Haitian Song, and Guijian Zhang for their help in the collection of H. axyridis samples in China as well as Edison Ryoti Sujii in Brazil. We also thank Jennifer A. White for the suggestions in writing earlier manuscript draft.

Funding

This research was supported by the National Key R&D Program of China (2017YFD0201000) and the Graduate Program of Research & Innovation of Jiangsu Province (KYCX18_0669).

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Authors and Affiliations

  1. College of Plant Protection, Key Laboratory of Integrated Pest Management in Crops in Eastern China, Ministry of Agriculture, Nanjing Agricultural University, Nanjing, 210095, China

    Hongran Li, Xiaohan Shu, Ling Meng & Baoping Li

  2. Department of Entomology, University of Kentucky, Lexington, 40546, USA

    Xuguo Zhou & John J. Obrycki

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  1. Hongran Li
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  2. Xiaohan Shu
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  3. Ling Meng
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  4. Xuguo Zhou
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  5. John J. Obrycki
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  6. Baoping Li
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Contributions

Baoping Li and John J. Obrycki contributed to experiments design. Hongran Li and Xiaohan Shu carried out the experiments. Hongran Li analyzed data and draft the manuscript. Hongran Li, Ling Meng, Xuguo Zhou and Baoping Li revised the manuscript. All authors read and approved the final manuscript.

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Correspondence to Baoping Li.

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Li, H., Shu, X., Meng, L. et al. Prevalence of maternally-inherited bacteria in native and invasive populations of the harlequin ladybird beetle Harmonia axyridis. Biol Invasions 23, 1461–1471 (2021). https://doi.org/10.1007/s10530-020-02451-x

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