Convergence between the microcosms of Southeast Asian and North American pitcher plants
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.
-
Amplicon sequencing dataNCBI BioProject PRJNA448553.
Article and author information
Author details
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
- Dianne K Newman, Howard Hughes Medical Institute, California Institute of Technology, United States
Version history
- Received: March 16, 2018
- Accepted: August 8, 2018
- Accepted Manuscript published: August 28, 2018 (version 1)
- 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
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)
Further reading
-
- Ecology
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.
-
- Ecology
The bacterium responsible for a disease that infects citrus plants across Asia facilitates its own proliferation by increasing the fecundity of its host insect.