in

Genetic identity and genotype × genotype interactions between symbionts outweigh species level effects in an insect microbiome

[adace-ad id="91168"]
  • 1.

    McFall-Ngai M, Hadfield MG, Bosch TCG, Carey HV, Domazet-Lošo T, Douglas AE, et al. Animals in a bacterial world, a new imperative for the life sciences. Proc Natl Acad Sci. 2013;110:3229–36.

    CAS  PubMed  Article  Google Scholar 

  • 2.

    Thompson LR, Sanders JG, McDonald D, Amir A, Ladau J, Locey KJ, et al. A communal catalogue reveals Earth’s multiscale microbial diversity. Nature. 2017;551:457–63.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 3.

    Feldhaar H, Gross R. Insects as hosts for mutualistic bacteria. Int J Med Microbiol. 2009;299:1–8.

    PubMed  Article  Google Scholar 

  • 4.

    Hosokawa T, Ishii Y, Nikoh N, Fujie M, Satoh N, Fukatsu T. Obligate bacterial mutualists evolving from environmental bacteria in natural insect populations. Nat Microbiol. 2016;1:15011.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 5.

    de Bekker C, Merrow M, Hughes DP. From behavior to mechanisms: an integrative approach to the manipulation by a parasitic fungus (Ophiocordyceps unilateralis s.l.) of its host ants (Camponotus spp.). Integr Comp Biol. 2014;54:166–76.

    PubMed  Article  Google Scholar 

  • 6.

    Koskella B, Meaden S, Crowther WJ, Leimu R, Metcalf CJE. A signature of tree health? Shifts in the microbiome and the ecological drivers of horse chestnut bleeding canker disease. N. Phytol. 2017;215:737–46.

    CAS  Article  Google Scholar 

  • 7.

    Smee MR, Baltrus DA, Hendry TA. Entomopathogenicity to two Hemipteran insects is common but variable across epiphytic Pseudomonas syringae strains. Front Plant Sci. 2017;8:2149.

    PubMed  PubMed Central  Article  Google Scholar 

  • 8.

    Oliver KM, Degnan PH, Burke GR, Moran NA. Facultative symbionts in aphids and the horizontal transfer of ecologically important traits. Annu Rev Entomol. 2010;55:247–66.

    CAS  PubMed  Article  Google Scholar 

  • 9.

    McLean AH. Cascading effects of defensive endosymbionts. Curr Opin Insect Sci. 2019;32:42–46.

    PubMed  Article  Google Scholar 

  • 10.

    Adair KL, Douglas AE. Making a microbiome: the many determinants of host-associated microbial community composition. Curr Opin Microbiol. 2017;35:23–29.

    PubMed  Article  Google Scholar 

  • 11.

    Wedin M, Maier S, Fernandez-Brime S, Cronholm B, Westberg M, Grube M. Microbiome change by symbiotic invasion in lichens. Environ Microbiol. 2015;18:1428–39.

    PubMed  Article  CAS  Google Scholar 

  • 12.

    King KC, Brockhurst MA, Vasieva O, Paterson S, Betts A, Ford SA, et al. Rapid evolution of microbe-mediated protection against pathogens in a worm host. ISME J. 2016;10:1915–24.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 13.

    Ford SA, Williams D, Paterson S, King KC. Co-evolutionary dynamics between a defensive microbe and a pathogen driven by fluctuating selection. Mol Ecol. 2017;26:1778–89.

    CAS  PubMed  Article  Google Scholar 

  • 14.

    Weldon SR, Russell JA, Oliver KM. More is not always better: coinfections with defensive symbionts generate highly variable outcomes. Appl Environ Microbiol. 2020;86:e02537-19.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 15.

    Bongrand C, Ruby EG. Achieving a multi-strain symbiosis: strain behavior and infection dynamics. ISME J 2019;13:698-706.

    PubMed  Article  Google Scholar 

  • 16.

    Doremus MR, Oliver KM. Aphid heritable symbiont exploits defensive mutualism. Appl Environ Microbiol. 2017;83:e03276–16.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 17.

    McLean AHC, Parker BJ, Hrček J, Kavanagh JC, Wellham PAD, Godfray HCJ. Consequences of symbiont co-infections for insect host phenotypes. J Anim Ecol 2018;87:478-488.

    PubMed  Article  Google Scholar 

  • 18.

    Oliver KM, Moran NA, Hunter MS. Costs and benefits of a superinfection of facultative symbionts in aphids. Proc R Soc B-Biol Sci. 2006;273:1273–80.

    Article  Google Scholar 

  • 19.

    Greenblum S, Carr R, Borenstein E. Extensive strain-level copy-number variation across human gut microbiome species. Cell. 2015;160:583–94.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 20.

    Lloyd-Price J, Mahurkar A, Rahnavard G, Crabtree J, Orvis J, Hall AB, et al. Strains, functions and dynamics in the expanded human microbiome project. Nature. 2017;550:61–66.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 21.

    Des Roches S, Post DM, Turley NE, Bailey JK, Hendry AP, Kinnison MT, et al. The ecological importance of intraspecific variation. Nat Ecol Evol. 2018;2:57–64.

    PubMed  Article  Google Scholar 

  • 22.

    Barbour MA, Fortuna MA, Bascompte J, Nicholson JR, Julkunen-Tiitto R, Jules ES, et al. Genetic specificity of a plant–insect food web: implications for linking genetic variation to network complexity. Proc Natl Acad Sci. 2016;113:2128–33.

    CAS  PubMed  Article  Google Scholar 

  • 23.

    Reznick DN, Losos J, Travis J. From low to high gear: there has been a paradigm shift in our understanding of evolution. Ecol Lett. 2019;22:233–44.

    PubMed  Article  Google Scholar 

  • 24.

    Koskella B, Bergelson J. The study of host–microbiome (co)evolution across levels of selection. Philos Trans R Soc B Biol Sci. 2020;375:20190604.

    Article  Google Scholar 

  • 25.

    Whitham TG, Allan GJ, Cooper HF, Shuster SM. Intraspecific Genetic Variation and Species Interactions Contribute to Community Evolution. Annu Rev Ecol Evol Syst. 2020;51:587–612.

    Article  Google Scholar 

  • 26.

    Ferrari J, West JA, Via S, Godfray HCJ. Population genetic structure and secondary symbionts in host-associated populations of the pea aphid complex. Evolution. 2012;66:375–90.

    PubMed  Article  Google Scholar 

  • 27.

    Henry LM, Peccoud J, Simon J-C, Hadfield JD, Maiden MJC, Ferrari J, et al. Horizontally transmitted symbionts and host colonization of ecological niches. Curr Biol. 2013;23:1713–7.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 28.

    Reuter M, Keller L. High levels of multiple Wolbachia infection and recombination in the ant Formica exsecta. Mol Biol Evol. 2003;20:748–53.

    CAS  PubMed  Article  Google Scholar 

  • 29.

    Gauthier J-P, Outreman Y, Mieuzet L, Simon J-C. Bacterial communities associated with host-adapted populations of pea aphids revealed by deep sequencing of 16S ribosomal DNA. PloS One. 2015;10:e0120664.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 30.

    Douglas AE. Nutritional interactions in insect-microbial symbioses: aphids and their symbiotic bacteria Buchnera. Annu Rev Entomol. 1998;43:17–37.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 31.

    Douglas AE. The nutritional physiology of aphids. Advances in Insect Physiology. Oxford, UK: Academic Press; 2003. pp 73–140.

  • 32.

    Zytynska SE, Weisser WW. The natural occurrence of secondary bacterial symbionts in aphids. Ecol Entomol. 2016;41:13–26.

    Article  Google Scholar 

  • 33.

    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.

    PubMed  Article  Google Scholar 

  • 34.

    Oliver KM, Russell JA, Moran NA, Hunter MS. Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. Proc Natl Acad Sci USA. 2003;100:1803–7.

    CAS  PubMed  Article  Google Scholar 

  • 35.

    Scarborough CL, Ferrari J, Godfray HCJ. Aphid protected from pathogen by endosymbiont. Science. 2005;310:1781–1781.

    CAS  PubMed  Article  Google Scholar 

  • 36.

    Montllor CB, Maxmen A, Purcell AH. Facultative bacterial endosymbionts benefit pea aphids Acyrthosiphon pisum under heat stress. Ecol Entomol. 2002;27:189–95.

    Article  Google Scholar 

  • 37.

    Hrček J, McLean AHC, Godfray HCJ. Symbionts modify interactions between insects and natural enemies in the field. J Anim Ecol. 2016;85:1605–12.

    PubMed  PubMed Central  Article  Google Scholar 

  • 38.

    Rock DI, Smith AH, Joffe J, Albertus A, Wong N, O’Connor M, et al. Context-dependent vertical transmission shapes strong endosymbiont community structure in the pea aphid, Acyrthosiphon pisum. Mol Ecol. 2018;27:2039–56.

    PubMed  Article  PubMed Central  Google Scholar 

  • 39.

    Moran NA, Russell JA, Koga R, Fukatsu T. Evolutionary relationships of three new species of Enterobacteriaceae living as symbionts of aphids and other insects. Appl Environ Microbiol. 2005;71:3302–10.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 40.

    Manzano-Marín A, Szabó G, Simon J-C, Horn M, Latorre A. Happens in the best of subfamilies: establishment and repeated replacements of co-obligate secondary endosymbionts within Lachninae aphids. Environ Microbiol. 2017;19:393–408.

    PubMed  Article  CAS  Google Scholar 

  • 41.

    Henry LM, Maiden MCJ, Ferrari J, Godfray HCJ. Insect life history and the evolution of bacterial mutualism. Ecol Lett. 2015;18:516–25.

    PubMed  Article  Google Scholar 

  • 42.

    Oliver KM, Moran NA, Hunter MS. Variation in resistance to parasitism in aphids is due to symbionts not host genotype. Proc Natl Acad Sci USA. 2005;102:12795–12800.

    CAS  PubMed  Article  Google Scholar 

  • 43.

    Oliver KM, Degnan PH, Hunter MS, Moran NA. Bacteriophages encode factors required for protection in a symbiotic mutualism. Science. 2009;325:992–4.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 44.

    Degnan PH, Moran NA. Evolutionary genetics of a defensive facultative symbiont of insects: exchange of toxin-encoding bacteriophage. Mol Ecol. 2008;17:916–29.

    CAS  PubMed  Article  Google Scholar 

  • 45.

    Chevignon G, Boyd BM, Brandt JW, Oliver KM, Strand MR. Culture-facilitated comparative genomics of the facultative symbiont Hamiltonella defensa. Genome Biol Evol. 2018;10:786–802.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 46.

    Heyworth ER, Ferrari J. A facultative endosymbiont in aphids can provide diverse ecological benefits. J Evol Biol. 2015;28:1753–60.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 47.

    Moran NA, Degnan PH, Santos SR, Dunbar HE, Ochman H. The players in a mutualistic symbiosis: Insects, bacteria, viruses, and virulence genes. Proc Natl Acad Sci USA. 2005;102:16919–26.

    CAS  PubMed  Article  Google Scholar 

  • 48.

    Oliver KM, Higashi CH. Variations on a protective theme: Hamiltonella defensa infections in aphids variably impact parasitoid success. Curr Opin Insect Sci. 2019;32:1–7.

    PubMed  Article  Google Scholar 

  • 49.

    Martinez AJ, Doremus MR, Kraft LJ, Kim KL, Oliver KM. Multi-modal defences in aphids offer redundant protection and increased costs likely impeding a protective mutualism. J Anim Ecol. 2018;87:464–77.

    PubMed  Article  Google Scholar 

  • 50.

    Łukasik P, van Asch M, Guo H, Ferrari J, Charles J, Godfray H. Unrelated facultative endosymbionts protect aphids against a fungal pathogen. Ecol Lett. 2013;16:214–8.

    PubMed  Article  Google Scholar 

  • 51.

    Parker BJ, Hrček J, McLean AHC, Godfray HCJ. Genotype specificity among hosts, pathogens, and beneficial microbes influences the strength of symbiont-mediated protection. Evolution. 2017;71:1222–31.

    PubMed  PubMed Central  Article  Google Scholar 

  • 52.

    Vorburger C. The evolutionary ecology of symbiont-conferred resistance to parasitoids in aphids. Insect Sci. 2014;21:251–64.

    PubMed  Google Scholar 

  • 53.

    Ferrari J, Via S, Godfray HCJ. Population differentiation and genetic variation in performance on eight hosts in the pea aphid complex. Evolution. 2008;62:2508–24.

    PubMed  Article  Google Scholar 

  • 54.

    McLean AHC, van Asch M, Ferrari J, Godfray HCJ. Effects of bacterial secondary symbionts on host plant use in pea aphids. Proc R Soc B-Biol Sci. 2011;278:760–6.

    CAS  Article  Google Scholar 

  • 55.

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

  • 56.

    Bates D, Maechler M, Bolker B, Walker S. Fitting linear mixed-effects models using lme4. J Stat Softw. 2015;67:1–48.

    Article  Google Scholar 

  • 57.

    Russell JA, Weldon S, Smith AH, Kim KL, Hu Y, Łukasik P, et al. Uncovering symbiont-driven genetic diversity across North American pea aphids. Mol Ecol. 2013;22:2045–59.

    PubMed  Article  Google Scholar 

  • 58.

    Jayakar SD. A mathematical model for interaction of gene frequencies in a parasite and its host. Theor Popul Biol. 1970;1:140–64.

    CAS  PubMed  Article  Google Scholar 

  • 59.

    Tellier A, Brown JKM. Stability of genetic polymorphism in host–parasite interactions. Proc R Soc B Biol Sci. 2007;274:809–17.

    Article  Google Scholar 

  • 60.

    Eren AM, Sogin ML, Morrison HG, Vineis JH, Fisher JC, Newton RJ, et al. A single genus in the gut microbiome reflects host preference and specificity. ISME J. 2015;9:90–100.

    CAS  PubMed  Article  Google Scholar 

  • 61.

    Yin Y, Wang Y, Zhu L, Liu W, Liao N, Jiang M, et al. Comparative analysis of the distribution of segmented filamentous bacteria in humans, mice and chickens. ISME J. 2013;7:615–21.

    CAS  PubMed  Article  Google Scholar 

  • 62.

    Parker BJ, McLean AHC, Hrček J, Gerardo NM, Godfray HCJ. Establishment and maintenance of aphid endosymbionts after horizontal transfer is dependent on host genotype. Biol Lett. 2017;13:20170016.

    PubMed  PubMed Central  Article  Google Scholar 

  • 63.

    Nyabuga FN, Outreman Y, Simon J-C, Heckel DG, Weisser WW. Effects of pea aphid secondary endosymbionts on aphid resistance and development of the aphid parasitoid Aphidius ervi: a correlative study. Entomol Exp Appl. 2010;136:243–53.

    Google Scholar 

  • 64.

    Leclair M, Polin S, Jousseaume T, Simon J-C, Sugio A, Morlière S, et al. Consequences of coinfection with protective symbionts on the host phenotype and symbiont titres in the pea aphid system. Insect Sci. 2016;24:798–808.

    PubMed  Article  Google Scholar 

  • 65.

    Zhao D, Hoffmann AA, Zhang Z, Niu H, Guo H. Interactions between facultative symbionts Hamiltonella and Cardinium in Bemisia tabaci (Hemiptera: Aleyrodoidea): cooperation or conflict? J Econ Entomol. 2018;111:2660-2666.

    PubMed  Article  CAS  Google Scholar 

  • 66.

    Vorburger C, Gehrer L, Rodriguez P. A strain of the bacterial symbiont Regiella insecticola protects aphids against parasitoids. Biol Lett. 2010;6:109–11.

    PubMed  Article  Google Scholar 

  • 67.

    McLean AHC, Godfray HCJ. Evidence for specificity in symbiont-conferred protection against parasitoids. Proc R Soc B. 2015;282:20150977.

    Article  Google Scholar 

  • 68.

    Patel V, Chevignon G, Manzano-Marín A, Brandt JW, Strand MR, Russell JA, et al. Cultivation-assisted genome of Candidatus Fukatsuia symbiotica; the enigmatic ‘X-type’ symbiont of aphids. Genome Biol Evol. 2019;11:3510-3522.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 69.

    Rouchet R, Vorburger C. Strong specificity in the interaction between parasitoids and symbiont-protected hosts. J Evol Biol. 2012;25:2369–75.

    PubMed  Article  Google Scholar 

  • 70.

    Sanders D, Kehoe R, Veen FF, van, McLean A, Godfray HCJ, Dicke M, et al. Defensive insect symbiont leads to cascading extinctions and community collapse. Ecol Lett. 2016;19:789–99.

    PubMed  PubMed Central  Article  Google Scholar 


  • Source: Ecology - nature.com

    Visualizing a climate-resilient MIT

    Ants modulate stridulatory signals depending on the behavioural context