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Diversity in symbiont consortia in the pea aphid complex is associated with large phenotypic variation in the insect host

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Abstract

Virtually all eukaryotes host microbial symbionts that influence their phenotype in many ways. In a host population, individuals may differ in their symbiotic complement in terms of symbiont species and strains. Hence, the combined expression of symbiont and host genotypes may generate a range of phenotypic diversity on which selection can operate and influence host population ecology and evolution. Here, we used the pea aphid to examine how the infection with various symbiotic complements contributes to phenotypic diversity of this insect species. The pea aphid hosts an obligate symbiont (Buchnera aphidicola) and several secondary symbionts among which is Hamiltonella defensa. This secondary symbiont confers a protection against parasitoids but can also reduce the host’s longevity and fecundity. These phenotypic effects of H. defensa infection have been described for a small fraction of the pea aphid complex which encompasses multiple plant-specialized biotypes. In this study, we examined phenotypic differences in four pea aphid biotypes where H. defensa occurs at high frequency and sometimes associated with other secondary symbionts. For each biotype, we measured the fecundity, lifespan and level of parasitoid protection in several aphid lineages differing in their symbiotic complement. Our results showed little variation in longevity and fecundity among lineages but strong differences in their protection level. These differences in protective levels largely resulted from the strain type of H. defensa and the symbiotic consortium in the host. This study highlights the important role of symbiotic complement in the emergence of phenotypic divergence among host populations of the same species.

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References

  • Bilodeau E, Simon JC, Guay JF et al (2013) Does variation in host plant association and symbiont infection of pea aphid populations induce genetic and behaviour differentiation of its main parasitoid, Aphidius ervi? Evol Ecol 27:165–184

    Article  Google Scholar 

  • Dawkins R (1982) The extended phenotype: the gene as the unit of selection. Oxford University Press, Oxford

    Google Scholar 

  • Degnan PH, Moran NA (2008) Diverse phage-encoded toxins in a protective insect endosymbiont. Appl Environ Microbiol 74:6782–6791

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Derocles SAP, Plantegenest M, Rasplus JY et al (2016) Are generalist Aphidiinae (Hym. Braconidae) mostly cryptic species complexes? Syst Entomol 41:379–391

    Article  Google Scholar 

  • Dion E, Polin SE, Simon J-C, Outreman Y (2011a) Symbiont infection affects aphid defensive behaviours. Biol Lett 7:743–746

    Article  PubMed  PubMed Central  Google Scholar 

  • Dion E, ZéLé F, Simon J-C, Outreman Y (2011b) Rapid evolution of parasitoids when faced with the symbiont-mediated resistance of their hosts: symbiont effects on host-parasitoid evolution. J Evol Biol 24:741–750

    Article  CAS  PubMed  Google Scholar 

  • Douglas AE (2009) The microbial dimension in insect nutritional ecology. Funct Ecol 23:38–47

    Article  Google Scholar 

  • Engelstädter J, Hurst GDD (2009) The ecology and evolution of microbes that manipulate host reproduction. Annu Rev Ecol Evol Syst 40:127–149

    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, Darby AC, Daniell TJ et al (2004) Linking the bacterial community in pea aphids with host-plant use and natural enemy resistance. Ecol Entomol 29:60–65

    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: population genetics and symbionts in the pea aphid. Evolution 66:375–390

    Article  PubMed  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 

  • Frantz A, Calcagno V, Mieuzet L et al (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 

  • Friesen ML, Porter SS, Stark SC et al (2011) Microbially mediated plant functional traits. Annu Rev Ecol Evol Syst 42:23–46

    Article  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  • Guay J-F, Boudreault S, Michaud D, Cloutier C (2009) Impact of environmental stress on aphid clonal resistance to parasitoids: role of Hamiltonella defensa bacterial symbiosis in association with a new facultative symbiont of the pea aphid. J Insect Physiol 55:919–926

    Article  CAS  PubMed  Google Scholar 

  • Haine ER (2008) Symbiont-mediated protection. Proc R Soc B Biol Sci 275:353–361

    Article  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Henry LM, Maiden MCJ, Ferrari J, Godfray HCJ (2015) Insect life history and the evolution of bacterial mutualism. Ecol Lett 18:516–525

    Article  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: Wolbachia infection rates. FEMS Microbiol Lett 281:215–220

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hufbauer RA, Via S (1999) Evolution of an aphid-parasitoid interaction: variation in resistance to parasitism among aphid populations specialized on different plants. Evolution 53:1435–1445

    Article  Google Scholar 

  • Jukes TH, Cantor CR (1969) Evolution of protein molecules. Mamm Protein Metab 3:132

    Google Scholar 

  • Kearse M, Moir R, Wilson A et al (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649

    Article  PubMed  PubMed Central  Google Scholar 

  • Kwiatkowski M, Vorburger C (2012) Modeling the ecology of symbiont-mediated protection against parasites. Am Nat 179:595–605

    Article  PubMed  Google Scholar 

  • Lamelas A, Gosalbes MJ, Manzano-Marín A et al (2011) Serratia symbiotica from the aphid Cinara cedri: a missing link from facultative to obligate insect endosymbiont. PLoS Genet 7(e1002357):7

    Google Scholar 

  • Leclair M, Polin S, Jousseaume T et al (2016) Consequences of co-infection with protective symbionts on the host phenotype and symbiont titres in the pea aphid system. Insect Sci. doi:10.1111/1744-7917.12380

    PubMed  Google Scholar 

  • Legendre P, Legendre LF (2012) Numerical ecology. Elsevier, Amsterdam

    Google Scholar 

  • Martinez AJ, Ritter SG, Doremus MR et al (2014) Aphid-encoded variability in susceptibility to a parasitoid. BMC Evol Biol 14:1

    Article  Google Scholar 

  • McBrien H, Mackauer M (1990) Heterospecific larval competition and host discrimination in two species of aphid parasitoids: Aphidius ervi and Aphidius smithi. Entomol Exp Appl 56:145–153

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Moran NA, Degnan PH, Santos SR et al (2005) The players in a mutualistic symbiosis: insects, bacteria, viruses, and virulence genes. Proc Natl Acad Sci USA 102:16919–16926

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moran NA, McCutcheon JP, Nakabachi A (2008) Genomics and evolution of heritable bacterial symbionts. Annu Rev Genet 42:165–190

    Article  CAS  PubMed  Google Scholar 

  • Mouton L, Dedeine F, Henri H et al (2004) Virulence, multiple infections and regulation of symbiotic population in the Wolbachia-Asobara tabida symbiosis. Genetics 168:181–189

    Article  PubMed  PubMed Central  Google Scholar 

  • Oliver KM, Martinez AJ (2014) How resident microbes modulate ecologically-important traits of insects. Curr Opin Insect Sci 4:1–7

    Article  Google Scholar 

  • Oliver KM, Russell JA, Moran NA, Hunter MS (2003) Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. Proc Natl Acad Sci 100:1803–1807

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    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 B Biol Sci 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 B Biol Sci 275:293–299

    Article  Google Scholar 

  • Oliver KM, Degnan PH, Hunter MS, Moran NA (2009) Bacteriophages encode factors required for protection in a symbiotic mutualism. Science 325:992–994

    Article  CAS  PubMed  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

    Article  Google Scholar 

  • Peccoud J, Figueroa CC, Silva AX et al (2008) Host range expansion of an introduced insect pest through multiple colonizations of specialized clones. Mol Ecol 17:4608–4618

    Article  CAS  PubMed  Google Scholar 

  • Peccoud J, Ollivier A, Plantegenest M, Simon J-C (2009) A continuum of genetic divergence from sympatric host races to species in the pea aphid complex. Proc Natl Acad Sci 106:7495–7500

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peccoud J, Bonhomme J, Mahéo F et al (2014) Inheritance patterns of secondary symbionts during sexual reproduction of pea aphid biotypes: sex and inheritance of aphid symbionts. Insect Sci 21:291–300

    Article  CAS  PubMed  Google Scholar 

  • Peccoud J, Mahéo F, de la Huerta M et al (2015) Genetic characterisation of new host-specialised biotypes and novel associations with bacterial symbionts in the pea aphid complex. Insect Conserv Divers 8:484–492

    Article  Google Scholar 

  • Polin S, Simon J-C, Outreman Y (2014) An ecological cost associated with protective symbionts of aphids. Ecol Evol 4:836–840

    Article  Google Scholar 

  • Polin S, Le Gallic J-F, Simon J-C et al (2015) Conditional reduction of predation risk associated with a facultative symbiont in an insect. PLoS ONE 10:e0143728

    Article  PubMed  PubMed Central  Google Scholar 

  • Rao Q, Rollat-Farnier P-A, Zhu D-T et al (2015) Genome reduction and potential metabolic complementation of the dual endosymbionts in the whitefly Bemisia tabaci. BMC Genomics 16:226

    Article  PubMed  PubMed Central  Google Scholar 

  • Rouchet R, Vorburger C (2014) Experimental evolution of parasitoid infectivity on symbiont-protected hosts leads to the emergence of genotype specificity: experimental evolution of parasitoid infectivity. Evolution 68:1607–1616

    Article  PubMed  Google Scholar 

  • Sachs JL, Skophammer RG, Regus JU (2011) Evolutionary transitions in bacterial symbiosis. Proc Natl Acad Sci 108:10800–10807

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Simon J-C, Carre S, Boutin M et al (2003) Host-based divergence in populations of the pea aphid: insights from nuclear markers and the prevalence of facultative symbionts. Proc R Soc Lond B Biol Sci 270:1703–1712

    Article  Google Scholar 

  • Simon J-C, Boutin S, Tsuchida T et al (2011) Facultative symbiont infections affect aphid reproduction. PLoS ONE 6:e21831

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smith AH, Łukasik P, O’Connor MP et al (2015) Patterns, causes and consequences of defensive microbiome dynamics across multiple scales. Mol Ecol 24:1135–1149

    Article  PubMed  Google Scholar 

  • Su Q, Oliver KM, Pan H et al (2013) Facultative symbiont Hamiltonella confers benefits to Bemisia tabaci (Hemiptera: Aleyrodidae), an invasive agricultural pest worldwide. Environ Entomol 42:1265–1271

    Article  PubMed  Google Scholar 

  • Su Q, Oliver KM, Xie W et al (2015) The whitefly-associated facultative symbiont Hamiltonella defensa suppresses induced plant defences in tomato. Funct Ecol 29:1007–1018

    Article  Google Scholar 

  • Team RC (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. ISBN 3-900051-07-0

    Google Scholar 

  • Vorburger C, Gouskov A (2011) Only helpful when required: a longevity cost of harbouring defensive symbionts: defensive symbionts reduce host longevity. J Evol Biol 24:1611–1617

    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

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Werren JH, Zhang W, Guo LR (1995) Evolution and phylogeny of Wolbachia: reproductive parasites of arthropods. Proc R Soc Lond B Biol Sci 261:55–63

    Article  CAS  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 

  • Zepeda-Paulo F, Lavandero B, Mahéo F, Dion E, Outreman Y, Simon JC, Figueroa CC (2016) Signatures of genetic bottleneck and differentiation after the introduction of an exotic parasitoid for classical biological control. Biol Inv 18:565–581

    Article  Google Scholar 

  • Zug R, Hammerstein P (2015) Bad guys turned nice? A critical assessment of Wolbachia mutualisms in arthropod hosts: Wolbachia mutualisms in arthropods. Biol Rev 90:89–111

    Article  PubMed  Google Scholar 

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Acknowledgments

We are very grateful to Jean Peccoud for his description of Genista biotypes and stimulating discussions on the pea aphid system, to all people who helped in sampling aphid lineages in natural populations, to Gaëtan Denis for help with aphid cultures, to Jean-François Le Gallic and Grégory Toussain for helping in fitness measurements, to Jean-Pierre Gauthier for phylogenetic analyses and to Bernard Chaubet for the aphid pictures. Two anonymous referees are also acknowledged for their constructive comments on an earlier draft. This work was supported by French ‘Ministère de l’Enseignement Supérieur et de la Recherche’ and by a grant from INRA Santé des Plantes et Environnement department.

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    Authors and Affiliations

    1. UMR 1349 IGEPP, INRA, Agrocampus Ouest, 65, rue de Saint-Brieuc CS 84215, 35042, Rennes Cedex, France

      Mélanie Leclair, Inès Pons & Yannick Outreman

    2. UMR 1349 IGEPP, INRA, Le Rheu, France

      Mélanie Leclair, Inès Pons, Frédérique Mahéo, Stéphanie Morlière & Jean-Christophe Simon

    3. Université Bretagne Loire, Rennes, France

      Mélanie Leclair & Yannick Outreman

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    1. Mélanie Leclair
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    2. Inès Pons
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    3. Frédérique Mahéo
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    5. Jean-Christophe Simon
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    Correspondence to Yannick Outreman.

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    Mélanie Leclair and Inès Pons have contributed equally to this work.

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    Leclair, M., Pons, I., Mahéo, F. et al. Diversity in symbiont consortia in the pea aphid complex is associated with large phenotypic variation in the insect host. Evol Ecol 30, 925–941 (2016). https://doi.org/10.1007/s10682-016-9856-1

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