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Evolutionary transition in symbiotic syndromes enabled diversification of phytophagous insects on an imbalanced diet

The ISME Journal volume 9, pages 25872604 (2015) | Download Citation

Abstract

Evolutionary adaptations for the exploitation of nutritionally challenging or toxic host plants represent a major force driving the diversification of phytophagous insects. Although symbiotic bacteria are known to have essential nutritional roles for insects, examples of radiations into novel ecological niches following the acquisition of specific symbionts remain scarce. Here we characterized the microbiota across bugs of the family Pyrrhocoridae and investigated whether the acquisition of vitamin-supplementing symbionts enabled the hosts to diversify into the nutritionally imbalanced and chemically well-defended seeds of Malvales plants as a food source. Our results indicate that vitamin-provisioning Actinobacteria (Coriobacterium and Gordonibacter), as well as Firmicutes (Clostridium) and Proteobacteria (Klebsiella) are widespread across Pyrrhocoridae, but absent from the sister family Largidae and other outgroup taxa. Despite the consistent association with a specific microbiota, the Pyrrhocoridae phylogeny is neither congruent with a dendrogram based on the hosts’ microbial community profiles nor phylogenies of individual symbiont strains, indicating frequent horizontal exchange of symbiotic partners. Phylogenetic dating analyses based on the fossil record reveal an origin of the Pyrrhocoridae core microbiota in the late Cretaceous (81.2–86.5 million years ago), following the transition from crypt-associated beta-proteobacterial symbionts to an anaerobic community localized in the M3 region of the midgut. The change in symbiotic syndromes (that is, symbiont identity and localization) and the acquisition of the pyrrhocorid core microbiota followed the evolution of their preferred host plants (Malvales), suggesting that the symbionts facilitated their hosts’ adaptation to this imbalanced nutritional resource and enabled the subsequent diversification in a competition-poor ecological niche.

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Acknowledgements

We thank Benjamin Weiss for assistance in rearing bugs, Annett Endler and Thomas Henry for providing Pyrrhocoridae specimens, and two anonymous referees for insightful comments on the manuscript. We thank Dr Jürgen Deckert from the Natural History Museum in Berlin for his help in taxonomical identification of the specimens and for providing samples, and Domenica Schnabelrauch and the Department of Entomology (Max Planck Institute for Chemical Ecology) for capillary sequencing. We gratefully acknowledge funding from the Max Planck Society (to SS, FR, CK and MK) and the Volkswagen Foundation (to CK).

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    • Martin Kaltenpoth

    Current address: Department for Evolutionary Ecology, Institute for Zoology, Johannes Gutenberg University Mainz, Mainz, Germany.

Affiliations

  1. Insect Symbiosis Research Group, Max Planck Institute for Chemical Ecology, Jena, Germany

    • Sailendharan Sudakaran
    • , Franziska Retz
    •  & Martin Kaltenpoth
  2. Bioproduction Research Institute, National Institute of Advanced Industrial Science and Technology (AIST) Hokkaido, Sapporo, Japan

    • Yoshitomo Kikuchi
  3. Experimental Ecology and Evolution Research Group, Max Planck Institute for Chemical Ecology, Jena, Germany

    • Christian Kost
  4. Institute of Microbiology, Friedrich Schiller University, Jena, Germany

    • Christian Kost

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