Oecologia

, Volume 181, Issue 3, pp 895–903

Larval growth rate is associated with the composition of the gut microbiota in the Glanville fritillary butterfly

Plant-microbe-animal interactions - original research

Abstract

The rapidly increasing body of literature on commensal microbiota has revealed a large phylotypic and functional diversity of microbes associated with vertebrates and invertebrates. In insects, the gut microbiota plays a role in digestion and metabolism of the host as well as protects the host against pathogens. In the study reported here, we sampled gut microbiota of the larvae of the Glanville fritillary butterfly (Melitaea cinxia). The larvae were collected from the field or reared in the laboratory. This butterfly has two host plant species, Plantago lanceolata and Veronica spicata, and the host plant species is known from previous studies to influence larval growth rate. However, our results demonstrate that about 50 % of the variation in larval growth rate can be attributed to the effect of the gut microbial composition plus the joint effect of microbiota and the host plant species, while host plant species alone makes no significant contribution. Our results support previous studies showing that diet influences the gut microbiota but, more unexpectedly, that the composition of the gut microbiota significantly influences larval growth rate. We suggest that host plant effects on larval growth and development observed in many previous studies may be mediated via the gut microbiota. While we measured the growth rate only in laboratory-reared larvae, the similarity of the gut microbial composition between samples from field-collected and laboratory-reared larvae suggests that the results can be generalized to natural conditions.

Keywords

Commensal microbiota Herbivorous insect Host plant Melitaea cinxia Variation partitioning 

Supplementary material

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Supplementary material 1 (PDF 506 kb)
442_2016_3603_MOESM2_ESM.txt (17 kb)
Supplementary material 2 (TXT 16 kb)
442_2016_3603_MOESM3_ESM.txt (884 kb)
Supplementary material 3 (TXT 883 kb)
442_2016_3603_MOESM4_ESM.txt (406 kb)
Supplementary material 4 (TXT 406 kb)

References

  1. Ahola V, Lehtonen R, Somervuo P et al (2014) The Glanville fritillary genome retains an ancient karyotype and reveals selective chromosomal fusions in Lepidoptera. Nat Commun 5:4737 doi: 10.1038/ncomms5737
  2. Anders S, Huber W (2010) Differential expression analysis for sequence count data. Genome Biol 11:R106. doi:10.1186/gb-2010-11-10-r106 CrossRefPubMedPubMedCentralGoogle Scholar
  3. Awmack CS, Leather SR (2002) Host plant quality and fecundity in herbivorous insects. Annu Rev Entomol 47:817–844. doi:10.1146/annurev.ento.47.091201.145300 CrossRefPubMedGoogle Scholar
  4. Bernays EA, Bright KL, Gonzalez N, Angel J (1994) Dietary mixing in a generalist herbivore: tests of two hypotheses. Ecology 75:1997–2006. doi:10.2307/1941604 CrossRefGoogle Scholar
  5. Borcard D, Gillet F, Legendre P (2011) Numerical ecology with R. Springer SBM, BerlinCrossRefGoogle Scholar
  6. Broderick NA, Lemaitre B (2012) Gut-associated microbes of Drosophila melanogaster. Gut Microbes 3:307–321. doi:10.4161/gmic.19896 CrossRefPubMedPubMedCentralGoogle Scholar
  7. Broderick NA, Raffa KF, Goodman RM, Handelsman J (2004) Census of the bacterial community of the gypsy moth larval midgut by using culturing and culture-independent methods. Appl Environ Microbiol 70:293–300CrossRefPubMedPubMedCentralGoogle Scholar
  8. Brune A, Ohkuma M (2011) Role of the termite gut microbiota in symbiotic digestion. In: Bignell DW, Roisin Y, Lo N (eds) Biology of termites: a modern synthesis. Springer SBM, Berlin, pp 439–475Google Scholar
  9. Calderón-Cortés N, Quesada M, Watanabe H et al (2012) Endogenous plant cell wall digestion: a key mechanism in insect evolution. Annu Rev Ecol Evol Syst 43:45–71CrossRefGoogle Scholar
  10. Chandler JA, Lang JM, Bhatnagar S et al (2011) Bacterial communities of diverse Drosophila species: ecological context of a host–microbe model system. PLoS Genet 7:e1002272CrossRefPubMedPubMedCentralGoogle Scholar
  11. Coley PD, Bateman ML, Kursar TA (2006) The effects of plant quality on caterpillar growth and defense against natural enemies. Oikos 115:219–228. doi:10.1111/j.2006.0030-1299.14928.x CrossRefGoogle Scholar
  12. Coon KL, Vogel KJ, Brown MR, Strand MR (2014) Mosquitoes rely on their gut microbiota for development. Mol Ecol 23:2727–2739. doi:10.1111/mec.12771 CrossRefPubMedPubMedCentralGoogle Scholar
  13. Dietrich C, Köhler T, Brune A (2014) The cockroach origin of the termite gut microbiota: patterns in bacterial community structure reflect major evolutionary events. Appl Environ Microbiol 80:2261–2269CrossRefPubMedPubMedCentralGoogle Scholar
  14. Dillon RJ, Dillon VM (2004) The gut bacteria of insects: nonpathogenic interactions. Annu Rev Entomol 49:71–92CrossRefPubMedGoogle Scholar
  15. Douglas AE (2015) Multiorganismal insects: diversity and function of resident microorganisms. Annu Rev Entomol 60:17–34. doi:10.1146/annurev-ento-010814-020822 CrossRefPubMedGoogle Scholar
  16. Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–998CrossRefPubMedGoogle Scholar
  17. Edwards U, Rogall T, Blöcker H et al (1989) Isolation and direct complete nucleotide determination of entire genes. Characterization of a gene coding for 16S ribosomal RNA. Nucleic Acids Res 17:7843–7853CrossRefPubMedPubMedCentralGoogle Scholar
  18. Engel P, Moran NA (2013) The gut microbiota of insects—diversity in structure and function. FEMS Microbiol Rev 37:699–735CrossRefPubMedGoogle Scholar
  19. Haegeman B, Hamelin J, Moriarty J et al (2013) Robust estimation of microbial diversity in theory and in practice. ISME J 7:1092–1101. doi:10.1038/ismej.2013.10 CrossRefPubMedPubMedCentralGoogle Scholar
  20. Hammer TJ, Bowers MD (2015) Gut microbes may facilitate insect herbivory of chemically defended plants. Oecologia 79(1):1–14. doi: 10.1007/s00442-015-3327-1
  21. Hammer TJ, McMillan WO, Fierer N (2014) Metamorphosis of a butterfly-associated bacterial community. PLoS One 9:e86995CrossRefPubMedPubMedCentralGoogle Scholar
  22. Hanski IA (2011) Eco-evolutionary spatial dynamics in the Glanville fritillary butterfly. Proc Natl Acad Sci USA 108:14397–14404CrossRefPubMedPubMedCentralGoogle Scholar
  23. Hanski I, Saastamoinen M, Ovaskainen O (2006) Dispersal-related life-history trade-offs in a butterfly metapopulation. J Anim Ecol 75:91–100CrossRefPubMedGoogle Scholar
  24. Ho C, Pennings SC, Carefoot TH et al (2010) Is diet quality an overlooked mechanism for Bergmann’s rule? Am Nat 175:269–276. doi:10.1086/649583 CrossRefPubMedGoogle Scholar
  25. Jong MA, Wong SC, Lehtonen R, Hanski I (2014) Cytochrome P450 gene CYP337 and heritability of fitness traits in the Glanville fritillary butterfly. Mol Ecol 23:1994–2005CrossRefPubMedGoogle Scholar
  26. Klemme I, Hanski I (2009) Heritability of and strong single gene (Pgi) effects on life-history traits in the Glanville fritillary butterfly. J Evol Biol 22:1944–1953CrossRefPubMedGoogle Scholar
  27. Kohl KD, Dearing MD (2012) Experience matters: prior exposure to plant toxins enhances diversity of gut microbes in herbivores. Ecol Lett 15:1008–1015. doi:10.1111/j.1461-0248.2012.01822.x CrossRefPubMedGoogle Scholar
  28. Koskinen K, Hultman J, Paulin L et al (2011) Spatially differing bacterial communities in water columns of the northern Baltic Sea. FEMS Microbiol Ecol 75:99–110CrossRefPubMedGoogle Scholar
  29. Kuussaari M, van Nouhuys S, Hellman J, Singer MC (2004) Larval biology of checkerspots. In: Ehrlich PR, Hanski I (eds) On the wings of checkerspots: a model system for population biology. Oxford University Press, Oxford, pp 138–160Google Scholar
  30. Kvist J, Wheat CW, Kallioniemi E et al (2013) Temperature treatments during larval development reveal extensive heritable and plastic variation in gene expression and life history traits. Mol Ecol 22:602–619CrossRefPubMedGoogle Scholar
  31. Lane DJ (1991) 16S/23S rRNA sequencing, nucleic acids in bacterial systematics. Wiley, New YorkGoogle Scholar
  32. Lee YK, Mazmanian SK (2010) Has the microbiota played a critical role in the evolution of the adaptive immune system? Science 330:1768–1773CrossRefPubMedPubMedCentralGoogle Scholar
  33. Legendre P, Legendre L (2012) Numerical ecology. Elsevier, AmsterdamGoogle Scholar
  34. Ley RE, Lozupone CA, Hamady M et al (2008) Worlds within worlds: evolution of the vertebrate gut microbiota. Nat Rev Microbiol 6:776–788. doi:10.1038/nrmicro1978 CrossRefPubMedPubMedCentralGoogle Scholar
  35. Lozupone CA, Stombaugh JI, Gordon JI et al (2012) Diversity, stability and resilience of the human gut microbiota. Nature 489:220–230CrossRefPubMedPubMedCentralGoogle Scholar
  36. Mason CJ, Raffa KF (2014) Acquisition and structuring of midgut bacterial communities in gypsy moth (Lepidoptera: Erebidae) larvae. Environ Entomol 43:595–604. doi:10.1603/EN14031 CrossRefPubMedGoogle Scholar
  37. McMurdie PJ, Holmes S (2014) Waste not, want not: why rarefying microbiome data is inadmissible. PLoS Comput Biol 10:e1003531. doi:10.1371/journal.pcbi.1003531 CrossRefPubMedPubMedCentralGoogle Scholar
  38. Oh J, Byrd AL, Deming C et al (2014) Biogeography and individuality shape function in the human skin metagenome. Nature 514:59–64CrossRefPubMedPubMedCentralGoogle Scholar
  39. Oksanen J, Blanchet G, Kindt R et al. (2015) vegan: Community ecology package. R package version 2.3-0. Available at: http://CRAN.R-project.org/package=vegan.
  40. Ottman N, Smidt H, De Vos WM, Belzer C (2012) The function of our microbiota: who is out there and what do they do? Front Cell Infect Microbiol 2:104. doi: 10.3389/fcimb.2012.00104
  41. Pernice M, Simpson SJ, Ponton F (2014) Towards an integrated understanding of gut microbiota using insects as model systems. J Insect Physiol 69:12–18CrossRefPubMedGoogle Scholar
  42. Ridley EV, Wong AC, Westmiller S, Douglas AE (2012) Impact of the resident microbiota on the nutritional phenotype of Drosophila melanogaster. PLoS One 7:e36765–e36765CrossRefPubMedPubMedCentralGoogle Scholar
  43. Robinson CJ, Schloss P, Ramos Y et al (2010a) Robustness of the bacterial community in the cabbage white butterfly larval midgut. Microb Ecol 59:199–211CrossRefPubMedGoogle Scholar
  44. Robinson MD, McCarthy DJ, Smyth GK (2010b) edgeR: a bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26:139–140. doi:10.1093/bioinformatics/btp616 CrossRefPubMedGoogle Scholar
  45. Saastamoinen M (2008) Heritability of dispersal rate and other life history traits in the Glanville fritillary butterfly. Heredity 100:39–46CrossRefPubMedGoogle Scholar
  46. Saastamoinen M, van Nouhuys S, Nieminen M et al (2007) Development and survival of a specialist herbivore, Melitaea cinxia, on host plants producing high and low concentrations of iridoid glycosides. Ann Zool Fenn 44:70–80Google Scholar
  47. Saastamoinen M, Ikonen S, Wong SC et al (2013) Plastic larval development in a butterfly has complex environmental and genetic causes and consequences for population dynamics. J Anim Ecol 82:529–539CrossRefPubMedGoogle Scholar
  48. Santo Domingo JW, Kaufman MG, Klug MJ et al (1998) Influence of diet on the structure and function of the bacterial hindgut community of crickets. Mol Ecol 7:761–767CrossRefGoogle Scholar
  49. Schmidt TS, Matias Rodrigues JF, Mering C (2014) Limits to robustness and reproducibility in the demarcation of operational taxonomic units. Environ Microbiol 17(5):1689–16706. doi: 10.1111/1462-2920.12610
  50. Sharon G, Segal D, Ringo JM et al (2010) Commensal bacteria play a role in mating preference of Drosophila melanogaster. Proc Natl Acad Sci USA 107:20051–20056CrossRefPubMedPubMedCentralGoogle Scholar
  51. Shin SC, Kim S-H, You H et al (2011) Drosophila microbiome modulates host developmental and metabolic homeostasis via insulin signaling. Science 334:670–674CrossRefPubMedGoogle Scholar
  52. Storelli G, Defaye A, Erkosar B et al (2011) Lactobacillus plantarum promotes Drosophila systemic growth by modulating hormonal signals through TOR-dependent nutrient sensing. Cell Metab 14:403–414CrossRefPubMedGoogle Scholar
  53. Stuart J (2015) Insect effectors and gene-for-gene interactions with host plants. Curr Opin Insect Sci 9:56–61. doi:10.1016/j.cois.2015.02.010 CrossRefGoogle Scholar
  54. Sugio A, Dubreuil G, Giron D, Simon J-C (2014) Plant–insect interactions under bacterial influence: ecological implications and underlying mechanisms. J Exp Bot. doi:10.1093/jxb/eru435
  55. Tang X, Freitak D, Vogel H et al (2012) Complexity and variability of gut commensal microbiota in polyphagous lepidopteran larvae. PLoS One 7:e36978CrossRefPubMedPubMedCentralGoogle Scholar
  56. Tuomisto H (2010) A consistent terminology for quantifying species diversity? Yes, it does exist. Oecologia 164:853–860CrossRefPubMedGoogle Scholar
  57. Yun J-H, Roh SW, Whon TW et al (2014) Insect gut bacterial diversity determined by environmental habitat, diet, developmental stage, and phylogeny of host. Appl Environ Microbiol 80:5254–5264CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.Department of BiosciencesUniversity of HelsinkiHelsinkiFinland
  2. 2.Lammi Biological StationUniversity of HelsinkiLammiFinland

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