Skip to main content

Advertisement

Log in

Secondary bacterial symbiont community in aphids responds to plant diversity

Oecologia Aims and scope Submit manuscript

Abstract

Biodiversity is important for ecosystem functioning and biotic interactions. In experimental grasslands, increasing plant species richness is known to increase the diversity of associated herbivores and their predators. If these interactions can also involve endosymbionts that reside within a plant or animal host is currently unknown. In plant-feeding aphids, secondary bacterial symbionts can have strong fitness effects on the host, e.g. resistance to natural enemies or fungal pathogens. We examined the secondary symbiont community in three species of aphid, each feeding on a unique host plant across experimental plots that varied in plant species richness. Aphids were collected in May and June, and the symbiont community identified using species-specific PCR assays. Aphis fabae aphids were found to host six different symbiont species with individual aphids co-hosting up to four symbionts. Uroleucon jaceae and Macrosiphum rosae hosted two and three symbiont species, respectively. We found that, at the aphid population level, increasing plant species richness increased the diversity of the aphid symbiont community, whereas at the individual aphid level, the opposite was found. These effects are potentially driven by varying selective pressures across different plant communities of varying diversities, mediated by defensive protection responses and a changing cost-benefit trade-off to the aphid for hosting multiple secondary symbionts. Our work extends documented effects of plant diversity beyond visible biotic interactions to changes in endosymbiont communities, with potentially far-reaching consequences to related ecosystem processes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Abbas M et al (2014) Plant diversity effects on pollinating and herbivorous insects can be linked to plant stoichiometry. Basic Appl Ecol 15:169–178

    Article  Google Scholar 

  • Ahmed MZ, De Barro PJ, Ren S-X, Greeff JM, Qiu B-L (2013) Evidence for horizontal transmission of secondary endosymbionts in the Bemisia tabaci cryptic species complex. PLoS ONE 8:e53084

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Allan E et al (2013) A comparison of the strength of biodiversity effects across multiple functions. Oecologia 173:223–237. doi:10.1007/s00442-012-2589-0

    Article  PubMed  Google Scholar 

  • Bates D, Maechler M, Bolker B, Walker S (2014) lme4: Linear mixed-effects models using Eigen and S4. R package version 1.1-7. http://CRAN.R-project.org/package=lme4

  • Bensadia F, Boudreault S, Guay JF, Michaud D, Cloutier C (2006) Aphid clonal resistance to a parasitoid fails under heat stress. J Insect Physiol 52:146–157

    Article  CAS  PubMed  Google Scholar 

  • Borer ET, Seabloom EW, Tilman D (2012) Plant diversity controls arthropod biomass and temporal stability. Ecol Lett 15:1457–1464. doi:10.1111/ele.12006

    Article  PubMed  Google Scholar 

  • Brady CM, White JA (2013) Cowpea aphid (Aphis craccivora) associated with different host plants has different facultative endosymbionts. Ecol Entomol 38:433–437. doi:10.1111/een.12020

    Article  Google Scholar 

  • Bukovinszky T, van Veen F, Jongema Y, Dicke M (2008) Direct and indirect effects of resource quality on food web structure. Science 319:804

    Article  CAS  PubMed  Google Scholar 

  • Caspi-Fluger A et al (2012) Horizontal transmission of the insect symbiont Rickettsia is plant-mediated. Proc R Soc Lond B 279:1791–1796

    Article  CAS  Google Scholar 

  • Chen DQ, Purcell AH (1997) Occurrence and transmission of facultative endosymbionts in aphids. Curr Microbiol 34:220–225

    Article  CAS  PubMed  Google Scholar 

  • Chen DQ, Montllor CB, Purcell AH (2000) Fitness effects of two facultative endosymbiotic bacteria on the pea aphid, Acyrthosiphon pisum, and the blue alfalfa aphid A. kondoi. Entomol Exper Appl 95:315–323. doi:10.1046/j.1570-7458.2000.00670.x

    Article  Google Scholar 

  • Clay K (2014) Defensive symbiosis: a microbial perspective. Funct Ecol 28:293–298. doi:10.1111/1365-2435.12258

    Article  Google Scholar 

  • Darby A, Douglas A (2003) Elucidation of the transmission patterns of an insect-borne bacterium. Appl Environ Microbiol 69:4403–4407

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Duffy JE, Cardinale BJ, France KE, McIntyre PB, Thebault E, Loreau M (2007) The functional role of biodiversity in ecosystems: incorporating trophic complexity. Ecol Lett 10:522–538

    Article  PubMed  Google Scholar 

  • Dykstra HR et al (2014) Factors limiting the spread of the protective symbiont Hamiltonella defensa in Aphis craccivora aphids. Appl Environ Microbiol 80:5818–5827

    Article  PubMed  PubMed Central  Google Scholar 

  • Ebeling A, Klein AM, Schumacher J, Weisser WW, Tscharntke T (2008) How does plant richness affect pollinator richness and temporal stability of flower visits? Oikos 117:1808–1815. doi:10.1111/j.1600-0706.2008.16819.x

    Article  Google Scholar 

  • Ebeling A, Klein AM, Weisser WW, Tscharntke T (2012) Multitrophic effects of experimental changes in plant diversity on cavity-nesting bees, wasps, and their parasitoids. Oecologia 169:453–465. doi:10.1007/s00442-011-2205-8

    Article  PubMed  Google Scholar 

  • Ebeling A et al (2014a) Plant diversity impacts decomposition and herbivory via changes in aboveground arthropods. PLoS ONE 9:e106529. doi:10.1371/journal.pone.0106529

    Article  PubMed  PubMed Central  Google Scholar 

  • Ebeling A et al (2014b) A trait-based experimental approach to understand the mechanisms underlying biodiversity–ecosystem functioning relationships. Basic Appl Ecol 15:229–240

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Ferrari J, Vavre F (2011) Bacterial symbionts in insects or the story of communities affecting communities. Philos Trans R Soc Lond B 366:1389–1400

    Article  Google Scholar 

  • Ferrari J, West JA, Via S, Godfray HCJ (2012) Population genetic structure and secondary symbionts in host-associated populations of the pea aphid complex. Evolution 66:375–390. doi:10.1111/j.1558-5646.2011.01436.x

    Article  PubMed  Google Scholar 

  • Frantz A, Calcagno V, Mieutzet L, Plantgenest M, Simon JC (2009) Complex trait differentiation between host-populations of the pea aphid Acyrthosiphon pisum (Harris): implications for the evolution of ecological specialisation. Biol J Linn Soc 97:718–727

    Article  Google Scholar 

  • Gehrer L, Vorburger C (2012) Parasitoids as vectors of facultative bacterial endosymbionts in aphids. Biol Lett 8:613–615. doi:10.1098/rsbl.2012.0144

    Article  PubMed  PubMed Central  Google Scholar 

  • Hackett SC, Karley AJ, Bennett AE (2013) Unpredicted impacts of insect endosymbionts on interactions between soil organisms, plants and aphids. Proc R Soc Lond B 280:2013. doi:10.1098/rspb.2013.1275

    Article  Google Scholar 

  • Haddad NM, Crutsinger GM, Gross K, Haarstad J, Knops JMH, Tilman D (2009) Plant species loss decreases arthropod diversity and shifts trophic structure. Ecol Lett 12:1029–1039

    Article  PubMed  Google Scholar 

  • Haynes S et al (2003) Diversity of bacteria associated with natural aphid populations. Appl Environ Microbiol 69:7216–7223. doi:10.1128/aem.69.12.7216-7223.2003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hector A, Joshi J, Lawler S, Spehn E, Wilby A (2001) Conservation implications of the link between biodiversity and ecosystem functioning. Oecologia 129:624–628

    Article  CAS  PubMed  Google Scholar 

  • Henry LM et al (2013) Horizontally transmitted symbionts and host colonization of ecological niches. Curr Biol 23:1713–1717

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hooper D et al (2005) Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecol Monogr 75:3–35

    Article  Google Scholar 

  • Leonardo TE, Muiru GT (2003) Facultative symbionts are associated with host plant specialization in pea aphid populations. Proc R Soc Lond B 270:S209

    Article  Google Scholar 

  • Loranger H et al (2014) Invertebrate herbivory increases along an experimental gradient in grassland plant diversity. Oecologia 174:183–193

    Article  PubMed  Google Scholar 

  • Lukasik P, Guo H, van Asch M, Ferrari J, Godfray HC (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 co-infection with another symbiont. J Evol Biol 26:2654–2661. doi:10.1111/jeb.12260

    Article  CAS  PubMed  Google Scholar 

  • McLean A, van Asch M, Ferrari J, Godfray H (2011) Effects of bacterial secondary symbionts on host plant use in pea aphids. Proc R Soc Lond B 278:760

    Article  CAS  Google Scholar 

  • Mitchell CE (2003) Trophic control of grassland production and biomass by pathogens. Ecol Lett 6:147–155. doi:10.1046/j.1461-0248.2003.00408.x

    Article  Google Scholar 

  • Montllor CB, Maxmen A, Purcell AH (2002) Facultative bacterial endosymbionts benefit pea aphids Acyrthosiphon pisum under heat stress. Ecol Entomol 27:189–195

    Article  Google Scholar 

  • Moran NA, Dunbar HE (2006) Sexual acquisition of beneficial symbionts in aphids. Proc Natl Acad Sci USA 103:12803–12806

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Müller CB, Williams IS, Hardie J (2001) The role of nutrition, crowding and interspecific interactions in the development of winged aphids. Ecol Entomol 26:330–340

    Article  Google Scholar 

  • Nyabuga FN, Outreman Y, Simon JC, Heckel DG, Weisser WW (2010) Effects of pea aphid secondary endosymbionts on aphid resistance and development of the aphid parasitoid Aphidius ervi: a correlative study. Entomol Exp Appl 136:243–253. doi:10.1111/j.1570-7458.2010.01021.x

    Google Scholar 

  • Oksanen J, Guillaume Blanchet F, Kindt R, Legendre P, Minchin PR, O'Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H (2015). vegan: Community Ecology Package. R package version 2.3-0. http://CRAN.R-project.org/package=vegan

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oliver KM, Moran NA, Hunter MS (2006) Costs and benefits of a superinfection of facultative symbionts in aphids. Proc R Soc Lond B 273:1273–1280

    Article  Google Scholar 

  • Oliver KM, Campos J, Moran NA, Hunter MS (2008) Population dynamics of defensive symbionts in aphids. Proc R Soc Lond B 275:293

    Article  Google Scholar 

  • Oliver KM, Smith AH, Russell JA (2014) Defensive symbiosis in the real world—advancing ecological studies of heritable, protective bacteria in aphids and beyond. Funct Ecol 28:341–355. doi:10.1111/1365-2435.12133

    Article  Google Scholar 

  • Omacini M, Chaneton EJ, Ghersa CM, Müller CB (2001) Symbiotic fungal endophytes control insect host–parasite interaction webs. Nature 409:78–81

    Article  CAS  PubMed  Google Scholar 

  • Pérez-Brocal V et al (2006) A small microbial genome: the end of a long symbiotic relationship? Science 314:312–313

    Article  PubMed  Google Scholar 

  • Petermann JS, Muller CB, Roscher C, Weigelt A, Weisser WW, Schmid B (2010a) Plant species loss affects life-history traits of aphids and their parasitoids. PLoS ONE 5:e12053. doi:10.1371/journal.pone.0012053

    Article  PubMed  PubMed Central  Google Scholar 

  • Petermann JS, Müller CB, Weigelt A, Weisser WW, Schmid B (2010b) Effect of plant species loss on aphid–parasitoid communities. J Anim Ecol 79:709–720. doi:10.1111/j.1365-2656.2010.01674.x

    Article  PubMed  Google Scholar 

  • Pettersson J, Tjallingii WF, Hardie J (2007) Host plant selection and feeding. In: VanEmden HF, Harrington R (eds) Aphids as crop pests. CABI, Wallingford, pp 87–113

  • Pinheiro J, Bates D, DebRoy S, Sarkar D, Team RC (2015) nlme: linear and nonlinear mixed effects models. R package version 3:1–120

    Google Scholar 

  • Powell G, Tosh CR, Hardie J (2006) Host plant selection by aphids: behavioral, evolutionary, and applied perspectives. Annu Rev Entomol 51:309–330

    Article  CAS  PubMed  Google Scholar 

  • R Core Development Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Roscher C et al (2004) The role of biodiversity for element cycling and trophic interactions: an experimental approach in a grassland community. Basic Appl Ecol 5:107–121

    Article  Google Scholar 

  • Ruijven J, De Deyn GB, Berendse F (2003) Diversity reduces invasibility in experimental plant communities: the role of plant species. Ecol Lett 6:910–918

    Article  Google Scholar 

  • Russell JA, Moran NA (2006) Costs and benefits of symbiont infection in aphids: variation among symbionts and across temperatures. Proc R Soc Lond B 273:603–610

    Article  Google Scholar 

  • Russell J, Latorre A, Sabater-Muñoz B, Moya A, Moran N (2003) Side-stepping secondary symbionts: widespread horizontal transfer across and beyond the Aphidoidea. Mol Ecol 12:1061–1075

    Article  CAS  PubMed  Google Scholar 

  • Russell JA et al (2013) Uncovering symbiont-driven genetic diversity across North American pea aphids. Mol Ecol 22:2045–2059. doi:10.1111/mec.12211

    Article  PubMed  Google Scholar 

  • Rzanny M, Voigt W (2012) Complexity of multitrophic interactions in a grassland ecosystem depends on plant species diversity. J Anim Ecol 81:614–627. doi:10.1111/j.1365-2656.2012.01951.x

    Article  PubMed  Google Scholar 

  • Rzanny M, Kuu A, Voigt W (2013) Bottom–up and top–down forces structuring consumer communities in an experimental grassland. Oikos 122:967–976. doi:10.1111/j.1600-0706.2012.00114.x

    Article  Google Scholar 

  • Sandström JP, Russell JA, White JP, Moran NA (2001) Independent origins and horizontal transfer of bacterial symbionts of aphids. Mol Ecol 10:217–228

    Article  PubMed  Google Scholar 

  • Scarborough CL, Ferrari J, Godfray H (2005) Aphid protected from pathogen by endosymbiont. Science 310:1781

    Article  CAS  PubMed  Google Scholar 

  • Scherber C et al (2006) Effects of plant diversity on invertebrate herbivory in experimental grassland. Oecologia 147:489–500

    Article  PubMed  Google Scholar 

  • Scherber C et al (2010) Bottom-up effects of plant diversity on multitrophic interactions in a biodiversity experiment. Nature 468:553–556. doi:10.1038/nature09492

    Article  CAS  PubMed  Google Scholar 

  • Smith AH et al (2015) Patterns, causes and consequences of defensive microbiome dynamics across multiple scales. Mol Ecol 24:1135–1149. doi:10.1111/mec.13095

    Article  PubMed  Google Scholar 

  • Su Q, Oliver KM, Xie W, Wu Q, Wang S, Zhang Y (2015) The whitefly-associated facultative symbiont Hamiltonella defensa suppresses induced plant defenses in tomato. Funct Ecol. doi:10.1111/1365-2435.12405

    Google Scholar 

  • Sunnucks P, Hales DF (1996) Numerous transposed sequences of mitochondrial cytochrome oxidase I-II in aphids of the genus Sitobion (Hemiptera: Aphididae). Mol Biol Evol 13:510–524

    Article  CAS  PubMed  Google Scholar 

  • Thao ML, Baumann P (2004) Evidence for multiple acquisition of Arsenophonus by whitefly species (Sternorrhyncha: Aleyrodidae). Curr Microbiol 48:140–144

    Article  CAS  PubMed  Google Scholar 

  • Tilman D, Wedin D, Knops J (1996) Productivity and sustainability influenced by biodiversity in grassland ecosystems. Nature 379:718–720

    Article  CAS  Google Scholar 

  • Tsuchida T, Koga R, Shibao H, Matsumoto T, Fukatsu T (2002) Diversity and geographic distribution of secondary endosymbiotic bacteria in natural populations of the pea aphid, Acyrthosiphon pisum. Mol Ecol 11:2123–2135. doi:10.1046/j.1365-294X.2002.01606.x

    Article  CAS  PubMed  Google Scholar 

  • Tsuchida T, Koga R, Fukatsu T (2004) Host plant specialization governed by facultative symbiont. Science 303:1989

    Article  CAS  PubMed  Google Scholar 

  • Tsuchida T et al (2010) Symbiotic bacterium modifies aphid body color. Science 330:1102–1104

    Article  CAS  PubMed  Google Scholar 

  • Vorburger C, Gouskov A (2011) Only helpful when required: a longevity cost of harbouring defensive symbionts. J Evol Biol 24:1611–1617. doi:10.1111/j.1420-9101.2011.02292.x

    Article  CAS  PubMed  Google Scholar 

  • Vorburger C, Ganesanandamoorthy P, Kwiatkowski M (2013) Comparing constitutive and induced costs of symbiont-conferred resistance to parasitoids in aphids. Ecol Evol 3:706–713. doi:10.1002/ece3.491

    Article  PubMed  PubMed Central  Google Scholar 

  • Wagner SM et al (2015) Facultative endosymbionts mediate dietary breadth in a polyphagous herbivore. Funct Ecol. doi:10.1111/1365-2435.12459

    Google Scholar 

  • Wulff JA, White JA (2015) The endosymbiont Arsenophonus provides a general benefit to soybean aphid (Hemiptera: Aphididae) regardless of host plant resistance (Rag). Environ Entomol 44:574–581

    Article  PubMed  Google Scholar 

  • Wulff JA, Buckman KA, Wu K, Heimpel GE, White JA (2013) The endosymbiont Arsenophonus is widespread in soybean aphid, Aphis glycines, but does not provide protection from parasitoids or a fungal pathogen. PLoS ONE 8:e62145. doi:10.1371/journal.pone.0062145

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zytynska SE, Preziosi RF (2011) Genetic interactions influence host preference and performance in a plant-insect system. Evol Ecol 25:1321–1333

    Article  Google Scholar 

  • Zytynska SE, Weisser W (2015) The natural occurrence of secondary bacterial symbionts in aphids. Ecol Entomol (in press)

  • Zytynska SE, Franz L, Hurst B, Johnson A, Preziosi RF, Rowntree J (2014) Host plant genotypic diversity and community genetic interactions mediate aphid spatial distribution. Ecol Evol 4:121–131

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

This work was funded by the DFG through the Jena Experiment (FOR 1451, WE 3081). We thank Anne Ebeling and the Jena Experiment gardeners for managing and maintaining the experimental plots.

Author contribution statement

SEZ, WWW and STM designed the experiment, SEZ, MM and WU conducted fieldwork, SS performed the molecular work, WU performed the chemical analyses. SEZ analysed the data and wrote the first draft, with STM and WWW contributing substantially to revisions.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Sharon E. Zytynska.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by Merijn Kant.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 341 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zytynska, S.E., Meyer, S.T., Sturm, S. et al. Secondary bacterial symbiont community in aphids responds to plant diversity. Oecologia 180, 735–747 (2016). https://doi.org/10.1007/s00442-015-3488-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-015-3488-y

Keywords

Navigation