Convergence between the microcosms of Southeast Asian and North American pitcher plants

  1. Leonora S Bittleston  Is a corresponding author
  2. Charles J Wolock
  3. Bakhtiar E Yahya
  4. Xin Yue Chan
  5. Kok Gan Chan
  6. Naomi E Pierce
  7. Anne Pringle
  1. Harvard University, United States
  2. Universiti Malaysia Sabah, Malaysia
  3. University of Malaya, Malaysia
  4. University of Wisconsin-Madison, United States

Abstract

The 'pitchers' of carnivorous pitcher plants are exquisite examples of convergent evolution. An open question is whether the living communities housed in pitchers also converge in structure or function. Using samples from more than 330 field-collected pitchers of eight species of Southeast Asian Nepenthes and six species of North American Sarracenia, we demonstrate that the pitcher microcosms, or miniature ecosystems with complex communities, are strikingly similar. Compared to communities from surrounding habitats, pitcher communities house fewer species. While communities associated with the two genera contain different microbial organisms and arthropods, the species are predominantly from the same phylogenetic clades. Microbiomes from both genera are enriched in degradation pathways and have high abundances of key degradation enzymes. Moreover, in a manipulative field experiment, Nepenthes pitchers placed in a North American bog assembled Sarracenia-like communities. An understanding of the convergent interactions in pitcher microcosms facilitates identification of selective pressures shaping the communities.

Data availability

Amplicon sequencing data have been deposited as NCBI BioProject PRJNA448553: https://www.ncbi.nlm.nih.gov/bioproject/PRJNA448553. Metagenomic sequencing data have been deposited in MG-RAST: http://www.mg-rast.org/linkin.cgi?project=mgp15454. The source code and data for Figures 1-5 and for Tables S3 and S4 have been deposited in a Harvard Dataverse repository: https://doi.org/10.7910/DVN/QYUBN2.

The following data sets were generated

Article and author information

Author details

  1. Leonora S Bittleston

    Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, United States
    For correspondence
    leobit@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4007-5405
  2. Charles J Wolock

    Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Bakhtiar E Yahya

    Institute for Tropical Biology and Conservation, Universiti Malaysia Sabah, Kota Kinabalu, Malaysia
    Competing interests
    The authors declare that no competing interests exist.
  4. Xin Yue Chan

    Division of Genetics and Molecular Biology, Institute of Biological Sciences, Faculty of Science, University of Malaya, Kuala Lumpur, Malaysia
    Competing interests
    The authors declare that no competing interests exist.
  5. Kok Gan Chan

    Division of Genetics and Molecular Biology, Institute of Biological Sciences, Faculty of Science, University of Malaya, Kuala Lumpur, Malaysia
    Competing interests
    The authors declare that no competing interests exist.
  6. Naomi E Pierce

    Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Anne Pringle

    Department of Botany, University of Wisconsin-Madison, Madison, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1526-6739

Funding

National Science Foundation (NSF Graduate Fellowship and Doctoral Dissertation Improvement Grant DEB-1400982)

  • Leonora S Bittleston

Templeton Foundation (Foundational Questions In Evolutionary Biology)

  • Naomi E Pierce
  • Anne Pringle

Harvard University Museum of Comparative Zoology Putnam Expedition Grant (Putnam Grant)

  • Leonora S Bittleston

National Geographic Society

  • Naomi E Pierce

University of Malaya High Impact Research Grant (UM-MOHE HIR Grant UM.C/625/1/HIR/MOHE/CHAN/14/1)

  • Kok Gan Chan

National Science Foundation (SES-0750480)

  • Naomi E Pierce

University of Malaya High Impact Research Grant (H-50001-A000027)

  • Kok Gan Chan

University of Malaya High Impact Research Grant (A-000001-50001)

  • Kok Gan Chan

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Dianne K Newman, Howard Hughes Medical Institute, California Institute of Technology, United States

Version history

  1. Received: March 16, 2018
  2. Accepted: August 8, 2018
  3. Accepted Manuscript published: August 28, 2018 (version 1)
  4. Version of Record published: September 10, 2018 (version 2)

Copyright

© 2018, Bittleston et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 3,676
    views
  • 406
    downloads
  • 28
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Leonora S Bittleston
  2. Charles J Wolock
  3. Bakhtiar E Yahya
  4. Xin Yue Chan
  5. Kok Gan Chan
  6. Naomi E Pierce
  7. Anne Pringle
(2018)
Convergence between the microcosms of Southeast Asian and North American pitcher plants
eLife 7:e36741.
https://doi.org/10.7554/eLife.36741

Share this article

https://doi.org/10.7554/eLife.36741

Further reading

    1. Ecology
    Anna L Erdei, Aneth B David ... Teun Dekker
    Research Article Updated

    Over two decades ago, an intercropping strategy was developed that received critical acclaim for synergizing food security with ecosystem resilience in smallholder farming. The push–pull strategy reportedly suppresses lepidopteran pests in maize through a combination of a repellent intercrop (push), commonly Desmodium spp., and an attractive, border crop (pull). Key in the system is the intercrop’s constitutive release of volatile terpenoids that repel herbivores. However, the earlier described volatile terpenoids were not detectable in the headspace of Desmodium, and only minimally upon herbivory. This was independent of soil type, microbiome composition, and whether collections were made in the laboratory or in the field. Furthermore, in oviposition choice tests in a wind tunnel, maize with or without an odor background of Desmodium was equally attractive for the invasive pest Spodoptera frugiperda. In search of an alternative mechanism, we found that neonate larvae strongly preferred Desmodium over maize. However, their development stagnated and no larva survived. In addition, older larvae were frequently seen impaled and immobilized by the dense network of silica-fortified, non-glandular trichomes. Thus, our data suggest that Desmodium may act through intercepting and decimating dispersing larval offspring rather than adult deterrence. As a hallmark of sustainable pest control, maize–Desmodium push–pull intercropping has inspired countless efforts to emulate stimulo-deterrent diversion in other cropping systems. However, detailed knowledge of the actual mechanisms is required to rationally improve the strategy, and translate the concept to other cropping systems.

    1. Ecology
    Songdou Zhang, Shiheng An
    Insight

    The bacterium responsible for a disease that infects citrus plants across Asia facilitates its own proliferation by increasing the fecundity of its host insect.