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

  • Plant-microbe-animal interactions - original research
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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.

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Acknowledgments

We thank Emily Hornett, Guillaume Minard, Marjo Saastamoinen, and anonymous reviewers for comments on the manuscript.

Author contribution statement

IH designed the experiment; IS and MH collected the samples and performed the laboratory experiment; LR analyzed the sequence data and performed statistical analyses; LR and IH wrote the manuscript. All authors have approved the final version of the manuscript.

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Authors and Affiliations

  1. Department of Biosciences, University of Helsinki, Viikinkaari 1, P.O. Box 65, 00014, Helsinki, Finland

    L. Ruokolainen, H. Makkonen & I. Hanski

  2. Lammi Biological Station, University of Helsinki, Lammi, Finland

    S. Ikonen

Authors
  1. L. Ruokolainen
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  2. S. Ikonen
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  3. H. Makkonen
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  4. I. Hanski
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Correspondence to L. Ruokolainen.

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Funding

This research was supported by the Academy of Finland (Grants 255350 and 250444 to IH and 13579 to LR).

Conflict of interest

The authors declare that they have no competing interests.

Statement of human and animal rights

This article does not contain any studies with human participants or animals (except invertebrates, which are except from ethical concerns) performed by any of the authors.

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Communicated by Corné Pieterse.

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Ruokolainen, L., Ikonen, S., Makkonen, H. et al. Larval growth rate is associated with the composition of the gut microbiota in the Glanville fritillary butterfly. Oecologia 181, 895–903 (2016). https://doi.org/10.1007/s00442-016-3603-8

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