in

Transitions in symbiosis: evidence for environmental acquisition and social transmission within a clade of heritable symbionts

  • 1.

    Ewald PW. Transmission modes and evolution of the parasitism-mutualism continuum. Ann NY Acad Sci. 1987;503:295–306.

    CAS 
    PubMed 

    Google Scholar 

  • 2.

    Moran NA, McCutcheon JP, Nakabachi A. Genomics and evolution of heritable bacterial symbionts. Annu Rev Genet. 2008;42:165–90.

    CAS 

    Google Scholar 

  • 3.

    Bright M, Bulgheresi S. A complex journey: transmission of microbial symbionts. Nat Rev Microbiol. 2010;51:505–10.

    Google Scholar 

  • 4.

    Salem H, Florez L, Gerardo N, Kaltenpoth M. An out-of-body experience: the extracellular dimension for the transmission of mutualistic bacteria in insects. Proc R Soc B. 2015;282:1804.

    Google Scholar 

  • 5.

    Ebert D. The epidemiology and evolution of symbionts with mixed-mode transmission. Annu Rev Ecol Evol Syst. 2013;44:623–43.

    Google Scholar 

  • 6.

    Webster JP, Borlase A, Rudge JW. Who acquires infection from whom and how? Disentangling multi-host and multimode transmission dynamics in the ‘elimination’ era. Philos Trans R Soc B Biol Sci. 2017;372:20160091.

  • 7.

    Bennett GM, Moran NA. Heritable symbiosis: the advantages and perils of an evolutionary rabbit hole. Proc Natl Acad Sci USA. 2015;112:10169–76.

    CAS 
    PubMed 

    Google Scholar 

  • 8.

    Law R, Dieckmann U. Symbiosis through exploitation and the merger of lineages in evolution. Proc R Soc B. 1998;265:1245–53.

    Google Scholar 

  • 9.

    Cordaux R, Michel-Salzat A, Bouchon D. Wolbachia infection in crustaceans: novel hosts and potential routes for horizontal transmission. J Evol Biol. 2001;14:237–43.

    CAS 

    Google Scholar 

  • 10.

    Russell JA, Latorre A, Sabater-Muñoz B, Moya A, Moran NA. Side-stepping secondary symbionts: widespread horizontal transfer across and beyond the Aphidoidea. Mol Ecol. 2003;12:1061–75.

    CAS 
    PubMed 

    Google Scholar 

  • 11.

    Zug R, Koehncke A, Hammerstein P. Epidemiology in evolutionary time: the case of Wolbachia horizontal transmission between arthropod host species. J Evol Biol. 2012;25:2149–60.

    PubMed 

    Google Scholar 

  • 12.

    Werren JH, O’Neill SL. The evolution of heritable symbionts. In: O’Neill SL, Hoffmann AA, Werren JH (eds). Influential Passengers: Inherited Microorganisms and Arthropod Reproduction. 1997. Oxford University Press, Oxford, pp 1–41.

  • 13.

    Parratt SR, Frost CL, Schenkel MA, Rice A, Hurst GDD, King KC. Superparasitism drives heritable symbiont epidemiology and host sex ratio in a wasp. PLoS Pathog. 2016;12:1–22.

    Google Scholar 

  • 14.

    Gordon ERL, McFrederick QS, Weirauch C. Comparative phylogenetic analysis of bacterial associates in Pyrrhocoroidea and evidence for ancient and persistent environmental symbiont reacquisition in Largidae (Hemiptera: Heteroptera). Appl Environ Microbiol. 2016;82:064022.

    Google Scholar 

  • 15.

    Kikuchi Y, Hosokawa T, Fukatsu T. Insect-microbe mutualism without vertical transmission: a stinkbug acquires a beneficial gut symbiont from the environment every generation. Appl Environ Microbiol. 2007;73:4308 LP–4316.

    Google Scholar 

  • 16.

    Buchner P. Endosymbiosis of animals with plant microorganisms. Z Für Allg Mikrobiol. 1967;7:168.

    Google Scholar 

  • 17.

    Anderson RM, May RM. Coevolution of hosts and parasites. Parasitology. 1982;85:211–426.

    Google Scholar 

  • 18.

    Frank SA. Host-symbiont conflict over the mixing of symbiotic lineages. Proc Biol Sci. 1996;263:339–44.

    CAS 
    PubMed 

    Google Scholar 

  • 19.

    Sachs JL, Essenberg CJ, Turcotte MM. New paradigms for the evolution of beneficial infections. Trends Ecol Evol. 2011;26:202–9.

    PubMed 

    Google Scholar 

  • 20.

    Shapiro JW, Turner PE. The impact of transmission mode on the evolution of benefits provided by microbial symbionts. Ecol Evol. 2014;4:3350–61.

    PubMed 
    PubMed Central 

    Google Scholar 

  • 21.

    Clayton AL, Oakeson KF, Gutin M, Pontes A, Dunn DM, Von AC, et al. A novel human-infection-derived bacterium provides insights into the evolutionary origins of mutualistic insect—bacterial symbioses. Plos Genet. 2012;8:11.

    Google Scholar 

  • 22.

    Duron O, Noël V, Mccoy KD, Bonazzi M, Sidi K, Morel O, et al. The recent evolution of a maternally- inherited endosymbiont of ticks led to the emergence of the Q fever pathogen Coxiella burnetii. Plos Pathog. 2015;11:1–23.

    CAS 

    Google Scholar 

  • 23.

    Lo WS, Huang YY, Kuo CH. Winding paths to simplicity: genome evolution in facultative insect symbionts. FEMS Microbiol Rev. 2016;40:855–74.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 24.

    Toft C, Andersson SGE. Evolutionary microbial genomics: insights into bacterial host adaptation. Nat Rev Genet. 2010;11:465–75.

    CAS 
    PubMed 

    Google Scholar 

  • 25.

    Wilkes TE, Duron O, Darby AC, Hypša V, Nováková E, Hurst GDD. The Genus Arsenophonus. In: Bourtzis K, Zchori-Fein E, editors. Manipulative tenants: bacteria associated with arthropods. Boca Raton: CRC Press; 2011. p. 225–44.

  • 26.

    Duron O, Bouchon D, Boutin S, Bellamy L, Zhou L, Engelstädter J, et al. The diversity of reproductive parasites among arthropods: Wolbachia do not walk alone. BMC Biol. 2008;6:1–12.

    Google Scholar 

  • 27.

    Nováková E, Hypša V, Moran NA. Arsenophonus, an emerging clade of intracellular symbionts with a broad host distribution. BMC Microbiol. 2009;9:1–14.

    Google Scholar 

  • 28.

    Gherna RL, Werren JH, Weisburg W, Cote R, Woese CR, Mandelco L, et al. Notes: Arsenophonus nasoniae gen. nov., sp. nov., the causative agent of the son-killer trait in the parasitic wasp Nasonia vitripennis. Int J Syst Bacteriol. 1991;41:563–5.

    Google Scholar 

  • 29.

    Qu LY, Lou YH, Fan HW, Ye YX, Huang HJ, Hu MQ, et al. Two endosymbiotic bacteria, Wolbachia and Arsenophonus, in the brown planthopper Nilaparvata lugens. Symbiosis. 2013;61:47–53.

    Google Scholar 

  • 30.

    Kirkness EF, Haas BJ, Sun W, Braig HR, Perotti MA, Clark JM, et al. Genome sequences of the human body louse and its primary endosymbiont provide insights into the permanent parasitic lifestyle. Proc Natl Acad Sci USA. 2010;107:12168–73.

    CAS 
    PubMed 

    Google Scholar 

  • 31.

    Nováková E, Hypša V, Nguyen P, Husník F, Darby AC. Genome sequence of Candidatus Arsenophonus lipopteni, the exclusive symbiont of a blood sucking fly Lipoptena cervi (Diptera: Hippoboscidae). Stand Genom Sci. 2016;11:72.

    Google Scholar 

  • 32.

    Perotti MA, Allen JM, Reed DL, Braig HR. Host-symbiont interactions of the primary endosymbiont of human head and body lice. FASEB J. 2007;21:1058–66.

    CAS 
    PubMed 

    Google Scholar 

  • 33.

    Nováková E, Husník F, Šochová E, Hypša V. Arsenophonus and Sodalis symbionts in louse flies: An analogy to the Wigglesworthia and Sodalis system in tsetse flies. Appl Environ Microbiol. 2015;81:6189–99.

    PubMed 
    PubMed Central 

    Google Scholar 

  • 34.

    Duron O, Wilkes TE, Hurst GDD. Interspecific transmission of a male-killing bacterium on an ecological timescale. Ecol Lett. 2010;13:1139–48.

    PubMed 

    Google Scholar 

  • 35.

    Huger AM, Skinner SW, Werren JH. Bacterial infections associated with the son-killer trait in the parasitoid wasp Nasonia (= Mormoniella) vitripennis (Hymenoptera: Pteromalidae). J Invertebr Pathol. 1985;46:272–80.

    CAS 
    PubMed 

    Google Scholar 

  • 36.

    Bressan A. Emergence and evolution of Arsenophonus bacteria as insect-vectored plant pathogens. Infect Genet Evol. 2014;22:81–90.

    PubMed 

    Google Scholar 

  • 37.

    Bressan A, Terlizzi F, Credi R. Independent origins of vectored plant pathogenic bacteria from arthropod-associated Arsenophonus endosymbionts. Micro Ecol. 2012;63:628–38.

    Google Scholar 

  • 38.

    Bressan A, Sémétey O, Arneodo J, Lherminier J, Boudon-Padieu E. Vector transmission of a plant-pathogenic bacterium in the Arsenophonus clade sharing ecological traits with facultative insect endosymbionts. Phytopathology. 2009;99:1289–96.

    CAS 
    PubMed 

    Google Scholar 

  • 39.

    Aizenberg-Gershtein Y, Izhaki I, Halpern M. Do honeybees shape the bacterial community composition in floral nectar? PLoS ONE. 2013;8:e67556.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 40.

    Babendreier D, Joller D, Romeis J, Bigler F, Widmer F. Bacterial community structures in honeybee intestines and their response to two insecticidal proteins. FEMS Microbiol Ecol. 2007;59:600–10.

    CAS 
    PubMed 

    Google Scholar 

  • 41.

    Corby-Harris V, Maes P, Anderson KE. The bacterial communities associated with honey bee (Apis mellifera) foragers. PLoS ONE. 2014;9:e95056.

    PubMed 
    PubMed Central 

    Google Scholar 

  • 42.

    Donkersley P, Rhodes G, Pickup RW, Jones KC, Wilson K. Bacterial communities associated with honeybee food stores are correlated with land use. Ecol Evol. 2018;8:4743–56.

    PubMed 
    PubMed Central 

    Google Scholar 

  • 43.

    Yañez O, Gauthier L, Chantawannakul P, Neumann P. Endosymbiotic bacteria in honey bees: Arsenophonus spp. are not transmitted transovarially. FEMS Microbiol Lett. 2016;363:1–7.

    Google Scholar 

  • 44.

    Budge GE, Adams I, Thwaites R, Pietravalle S, Drew GC, Hurst GDD, et al. Identifying bacterial predictors of honey bee health. J Invertebr Pathol. 2016;141:41–4.

    PubMed 

    Google Scholar 

  • 45.

    Cornman RS, Tarpy DR, Chen Y, Jeffreys L, Lopez D, Pettis JS, et al. Pathogen webs in collapsing honey bee colonies. PLoS ONE. 2012;7:e43562.

  • 46.

    Hughes DP, Pierce NE, Boomsma JJ. Social insect symbionts: evolution in homeostatic fortresses. Trends Ecol Evol. 2008;23:672–7.

    PubMed 

    Google Scholar 

  • 47.

    Schmid-Hempel P. Parasites and their social hosts. Trends Parasitol. 2017;33:453–62.

    PubMed 

    Google Scholar 

  • 48.

    Wilson EO. The insect societies. Harvard University Press: Cambridge, MA, 1971.

  • 49.

    Onchuru TO, Javier Martinez A, Ingham CS, Kaltenpoth M. Transmission of mutualistic bacteria in social and gregarious insects. Curr Opin Insect Sci. 2018;28:50–58.

    PubMed 

    Google Scholar 

  • 50.

    Rubin BER, Sanders JG, Turner KM, Pierce NE, Kocher SD. Social behaviour in bees influences the abundance of Sodalis (Enterobacteriaceae) symbionts. R Soc Open Sci. 2018;5:180369.

  • 51.

    Anderson KE, Russell JA, Moreau CS, Kautz S, Sullam KE, Hu Y, et al. Highly similar microbial communities are shared among related and trophically similar ant species. Mol Ecol. 2012;21:2282–96.

    PubMed 

    Google Scholar 

  • 52.

    Frost CL, FernÁndez-MarÍn H, Smith JE, Hughes WOH. Multiple gains and losses of Wolbachia symbionts across a tribe of fungus-growing ants. Mol Ecol. 2010;19:4077–85.

    CAS 
    PubMed 

    Google Scholar 

  • 53.

    Keller L, Liautard C, Reuter MAX, Brown WD, Chapuisat M, Sundstro L. Sex ratio and Wolbachia infection in the ant Formica exsecta. Heredity. 2001;87:227–33.

    CAS 
    PubMed 

    Google Scholar 

  • 54.

    Van Borm S, Wenseleers T, Billen J, Boomsma JJ. Wolbachia in leafcutter ants: a widespread symbiont that may induce male killing or incompatible matings. J Evol Biol. 2001;14:805–14.

    Google Scholar 

  • 55.

    Wenseleers T, Sundström L, Billen J. Deleterious Wolbachia in the ant Formica truncorum. Proc R Soc B Biol Sci. 2002;269:623–9.

    CAS 

    Google Scholar 

  • 56.

    Gauthier L, Cornman S, Hartmann U, Cousserans F, Evans JD, De Miranda JR, et al. The Apis mellifera filamentous virus genome. Viruses. 2015;7:3798–815.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 57.

    Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics. 2014;30:2068–9.

    CAS 
    PubMed 

    Google Scholar 

  • 58.

    Simão FA, Waterhouse RM, Ioannidis P, Kriventseva EV, Zdobnov EM. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics. 2015;31:3210–2.

    PubMed 

    Google Scholar 

  • 59.

    Walsh PS, Metzger DA, Higuchi R. Chelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. BioTechniques. 1991;10:506–13.

    CAS 
    PubMed 

    Google Scholar 

  • 60.

    Lourenço AP, Mackert A, Cristino A, dos S, Simões ZLP. Validation of reference genes for gene expression studies in the honey bee, Apis mellifera, by quantitative real-time RT-PCR. Apidologie. 2008;39:372–85.

    Google Scholar 

  • 61.

    Boncristiani H, Li J, Evans JD, Pettis J, Chen Y. Scientific note on PCR inhibitors in the compound eyes of honey bees, Apis mellifera. Apidologie. 2011;42:457–60.

    Google Scholar 

  • 62.

    Gottlieb Y, Ghanim M, Gueguen G, Kontsedalov S, Vavre F, Fleury F, et al. Inherited intracellular ecosystem: symbiotic bacteria share bacteriocytes in whiteflies. FASEB J. 2008;22:2591–9.

    CAS 
    PubMed 

    Google Scholar 

  • 63.

    Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nat Methods. 2012;9:671–5.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 64.

    R Core Team. A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2013. http://www.R-project.org/.

  • 65.

    Bates D, Mächler M, Bolker B, Walker S. Fitting linear mixed-effects models Using lme4. J Stat Softw. 2015;1:1–48.

  • 66.

    Akaike H. A new look at the statistical model identification. IEEE Trans Autom Control. 1974;19:716–23.

    Google Scholar 

  • 67.

    Burnham KP, Anderson DR. Model selection and multimodel inference: a practical information-theoretic approach. Springer Science & Business Media: New York, NY, 2003.

  • 68.

    Zuur AF, Ieno EN, Elphick CS. A protocol for data exploration to avoid common statistical problems. Methods Ecol Evol. 2009;1:3–14.

    Google Scholar 

  • 69.

    Frost CL, Siozios S, Nadal-Jimenez P, Brockhurst MA, King KC, Darby AC, et al. The hypercomplex genome of an insect reproductive parasite highlights the importance of lateral gene transfer in symbiont biology. mBio. 2020;11:e02590–19.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 70.

    Smith AH, Łukasik P, O’Connor MP, Lee A, Mayo G, Drott MT, et al. Patterns, causes and consequences of defensive microbiome dynamics across multiple scales. Mol Ecol. 2015;24:1135–49.

    Google Scholar 

  • 71.

    Nadal-Jimenez P, Griffin JS, Davies L, Frost CL, Marcello M, Hurst GDD. Genetic manipulation allows in vivo tracking of the life cycle of the son-killer symbiont, Arsenophonus nasoniae, and reveals patterns of host invasion, tropism and pathology. Environ Microbiol. 2019;21:3172–82.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 72.

    Perlman SJ, Hunter MS, Zchori-Fein E. The emerging diversity of Rickettsia. Proc Biol Sci. 2006;273:2097–106.

    PubMed 
    PubMed Central 

    Google Scholar 

  • 73.

    Sachs JL, Skophammer RG, Regus JU. Evolutionary transitions in bacterial symbiosis. Proc Natl Acad Sci USA. 2011;108:10800–7.

    CAS 
    PubMed 

    Google Scholar 

  • 74.

    Walterson AM, Stavrinides J. Pantoea: insights into a highly versatile and diverse genus within the Enterobacteriaceae. FEMS Microbiol Rev. 2015;39:968–84.

    CAS 
    PubMed 

    Google Scholar 

  • 75.

    Chrudimský T, Husník F, Nováková E, Hypša V. Candidatus Sodalis melophagi sp. nov.: phylogenetically independent comparative model to the tsetse fly symbiont Sodalis glossinidius. PLoS ONE. 2012;7:e40354.

    PubMed 
    PubMed Central 

    Google Scholar 

  • 76.

    Dale C, Maudlin I. Sodalis gen. nov. and Sodalis glossinidius sp. nov., a microaerophilic secondary endosymbiont of the tsetse fly Glossina morsitans morsitans. Int J Syst Bacteriol. 1999;1:267–75.

    Google Scholar 

  • 77.

    Kenyon LJ, Meulia T, Sabree ZL. Habitat visualization and genomic analysis of ‘Candidatus Pantoea carbekii,’ the primary symbiont of the brown marmorated stink bug. Genome Biol Evol. 2015;7:620–35.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 78.

    Fischer-Le Saux M, Viallard V, Brunel B, Normand P, Boemare NE. Polyphasic classification of the genus Photorhabdus and proposal of new taxa: P. luminescens subsp. luminescens subsp. nov., P. luminescens subsp. akhurstii subsp. nov., P. luminescens subsp. laumondii subsp. nov., P. temperata sp. nov., P. temperata subsp. temperata subsp. nov. and P. asymbiotica sp. nov. Int J Syst Evol Microbiol. 1999;49:1645–56.

    Google Scholar 

  • 79.

    Forst S, Dowds B, Boemare N, Stackebrandt E. Xenorhabdus and Photorhabdus spp.: bugs that kill bugs. Annu Rev Microbiol. 1997;51:47–72.

    CAS 
    PubMed 

    Google Scholar 

  • 80.

    Costa SCP, Girard PA, Brehélin M, Zumbihl R. The emerging human pathogen Photorhabdus asymbiotica is a facultative intracellular bacterium and induces apoptosis of macrophage-like cells. Infect Immun. 2009;77:1022–30.

    CAS 
    PubMed 

    Google Scholar 

  • 81.

    Gerrard J, Waterfield N, Vohra R, ffrench-Constant R. Human infection with Photorhabdus asymbiotica: an emerging bacterial pathogen. Microbes Infect. 2004;6:229–37.

    CAS 
    PubMed 

    Google Scholar 

  • 82.

    Schmid-Hempel P. Parasites in social insects. Princeton University Press: Princeton, NJ, 1998.

  • 83.

    Frost CL, Pollock SW, Smith JE, Hughes WOH. Wolbachia in the flesh: symbiont intensities in germ-line and somatic tissues challenge the conventional view of Wolbachia transmission routes. PLoS ONE. 2014;9:e95122.

  • 84.

    Graystock P, Goulson D, Hughes WOH. Parasites in bloom: Flowers aid dispersal and transmission of pollinator parasites within and between bee species. Proc R Soc B Biol Sci. 2015;282:1471–2954.

    Google Scholar 

  • 85.

    Graystock P, Goulson D, Hughes WOH. The relationship between managed bees and the prevalence of parasites in bumblebees. PeerJ. 2014;2:e522.

    PubMed 
    PubMed Central 

    Google Scholar 

  • 86.

    Koch H, Abrol DP, Li J, Schmid-Hempel P. Diversity and evolutionary patterns of bacterial gut associates of corbiculate bees. Mol Ecol. 2013;22:2028–44.

    CAS 
    PubMed 

    Google Scholar 

  • 87.

    McFrederick QS, Thomas JM, Neff JL, Vuong HQ, Russell KA, Hale AR, et al. Flowers and wild megachilid bees share microbes. Micro Ecol. 2017;73:188–200.

    Google Scholar 

  • 88.

    Satterfield DA, Altizer S, Williams MK, Hall RJ. Environmental persistence influences infection dynamics for a butterfly pathogen. PLoS ONE. 2017;12:1–16.

    Google Scholar 

  • 89.

    Darby AC, Choi JH, Wilkes T, Hughes MA, Werren JH, Hurst GDD, et al. Characteristics of the genome of Arsenophonus nasoniae, son-killer bacterium of the wasp Nasonia. Insect Mol Biol. 2010;19:75–89.

    CAS 
    PubMed 

    Google Scholar 

  • 90.

    Dale C, Beeton M, Harbison C, Jones T, Pontes M. Isolation, pure culture, and characterization of ‘Candidatus Arsenophonus arthropodicus,’ an intracellular secondary endosymbiont from the hippoboscid louse fly Pseudolynchia canariensis. Appl Environ Microbiol. 2006;72:2997–3004.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 91.

    Clark T. Honeybee spiroplasmosis, a new problem for beekeepers. Am Bee J. 1978;118:18–19.

    Google Scholar 

  • 92.

    Schwarz RS, Teixeira ÉW, Tauber JP, Birke JM, Martins MF, Fonseca I, et al. Honey bee colonies act as reservoirs for two Spiroplasma facultative symbionts and incur complex, multiyear infection dynamics. MicrobiologyOpen. 2014;3:341–55.

    PubMed 
    PubMed Central 

    Google Scholar 

  • 93.

    Levin MD. Interactions among foraging honey bees from different apiaries in the same field. Insectes Sociaux. 1961;8:195–201.

    Google Scholar 

  • 94.

    Parmentier A, Billiet A, Smagghe G, Vandamme P, Deforce D, Van Nieuwerburgh F, et al. A prokaryotic–eukaryotic relation in the fat body of Bombus terrestris. Environ Microbiol Rep. 2018;10:644–50.

    CAS 
    PubMed 

    Google Scholar 

  • 95.

    Nussbaumer AD, Fisher CR, Bright M. Horizontal endosymbiont transmission in hydrothermal vent tubeworms. Nature. 2006;441:345–8.

    CAS 
    PubMed 

    Google Scholar 

  • 96.

    Werren JH, Skinner SW, Huger AM. Male-killing bacteria in a parasitic wasp. Science. 1986;231:990–2.

    CAS 
    PubMed 

    Google Scholar 

  • 97.

    Gerth M, Saeed A, White JA, Bleidorn C. Extensive screen for bacterial endosymbionts reveals taxon-specific distribution patterns among bees (Hymenoptera, Anthophila). FEMS Microbiol Ecol. 2015;91:1–12.

    Google Scholar 

  • 98.

    McFrederick QS, Mueller UG, James RR. Interactions between fungi and bacteria influence microbial community structure in the Megachile rotundata larval gut. Proc R Soc B Biol Sci. 2014;281:1471–2954.

    Google Scholar 

  • 99.

    Saeed A, White JA. Surveys for maternally-inherited endosymbionts reveal novel and variable infections within solitary bee species. J Invertebr Pathol. 2015;132:111–4.

    PubMed 

    Google Scholar 


  • Source: Ecology - nature.com

    Robotic solution for disinfecting food production plants wins agribusiness prize

    Undergraduates explore practical applications of artificial intelligence