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A remarkable legion of guests: Diversity and host specificity of army ant symbionts

von Beeren, Christoph and Blüthgen, Nico and Hoenle, Philipp O. and Pohl, Sebastian and Brückner, Adrian and Tishechkin, Alexey K. and Maruyama, Munetoshi and Brown, Brian V. and Hash, John M. and Hall, W. E. and Kronauer, Daniel J. C. (2021) A remarkable legion of guests: Diversity and host specificity of army ant symbionts. Molecular Ecology, 30 (20). pp. 5229-5246. ISSN 0962-1083. doi:10.1111/mec.16101. https://resolver.caltech.edu/CaltechAUTHORS:20210921-152951282

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Abstract

Tropical rainforests are among the most diverse biomes on Earth. While species inventories are far from complete for any tropical rainforest, even less is known about the intricate species interactions that form the basis of these ecological communities. One fascinating but poorly studied example are the symbiotic associations between army ants and their rich assemblages of parasitic arthropod guests. Hundreds of these guests, or myrmecophiles, have been taxonomically described. However, because previous work has mainly been based on haphazard collections from disjunct populations, it remains challenging to define species boundaries. We therefore know little about the species richness, abundance and host specificity of most guests in any given population, which is crucial to understand co-evolutionary and ecological dynamics. Here, we report a quantitative community survey of myrmecophiles parasitizing the six sympatric Eciton army ant species in a Costa Rican rainforest. Combining DNA barcoding with morphological identification of over 2,000 specimens, we discovered 62 species, including 49 beetles, 11 flies, one millipede and one silverfish. At least 14 of these species were new to science. Ecological network analysis revealed a clear signal of host partitioning, and each Eciton species was host to both specialists and generalists. These varying degrees in host specificities translated into a moderate level of network specificity, highlighting the system's level of biotic pluralism in terms of biodiversity and interaction diversity. By providing vouchered DNA barcodes for army ant guest species, this study provides a baseline for future work on co-evolutionary and ecological dynamics in these species-rich host–symbiont networks across the Neotropical realm.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1111/mec.16101DOIArticle
ORCID:
AuthorORCID
von Beeren, Christoph0000-0002-0072-5795
Blüthgen, Nico0000-0001-6349-4528
Hoenle, Philipp O.0000-0001-8160-8859
Pohl, Sebastian0000-0003-3122-339X
Brückner, Adrian0000-0002-9184-8562
Tishechkin, Alexey K.0000-0003-0848-7450
Maruyama, Munetoshi0000-0003-4531-1008
Kronauer, Daniel J. C.0000-0002-4103-7729
Additional Information:© 2021 The Authors. Molecular Ecology published by John Wiley & Sons Ltd. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. Issue Online: 11 October 2021; Version of Record online: 18 August 2021; Manuscript accepted: 27 July 2021; Manuscript revised: 15 July 2021; Manuscript received: 04 February 2021. This study was inspired by the pioneering work on army ant associates of Carl and Marian Rettenmeyer and their coworkers. We thank Luis Mendes, Mikael Sörensson, Taro Eldredge, Emmanuel Arriaga Varela, Martin Fikáček, Mariana Chani-Posse, Henry Disney and Thomas Wegener for help with species identifications, and Cristina Marin Montaner and Stefan Kleinfelder for help with stacking images. We also thank Bryan Ospina Jara for help during fieldwork, as well as Jana Wieschollek and Ana Ailín Paul for help with DNA barcoding. We thank Thomas Parmentier and two anonymous reviewers for helpful comments that improved this work. Last but not least, we thank Adrián Pinto Tomás, Carlos de la Rosa, Bernal Matarrita Carranza and Danilo Brenes Madrigal, as well as the entire staff of La Selva Biological Station, for their generous support throughout the project. Open Access funding enabled and organized by Projekt DEAL. C.v.B. was supported by grants from the German Science Foundation (DFG; BE5177/1-1, BE5177/4-1, and BE5177/4-2), the National Geographic Society's Committee for Research and Exploration, and a Bristol-Myers Squibb Postdoctoral Fellowship from The Rockefeller University. D.J.C.K. was supported by a Carl & Marian Rettenmeyer Ant-Guest Endowment Award. P.O.H. and A.B. were supported by the German Academic Scholarship Foundation. Author Contributions: C.v.B. and D.J.C.K. designed and supervised the study. C.v.B., P.O.H., S.P., A.B. and D.J.C.K. performed field work. C.v.B. processed the collection. C.v.B., A.K.T., M.M., B.V.B., J.M.H. and W.E.H. identified species. C.v.B. acquired and analysed molecular data. C.v.B., N.B., A.B., and D.J.C.K. performed statistics. C.v.B. and D.J.C.K. wrote the manuscript, with feedback from all co-authors. All authors gave final approval for publication. The authors have no competing interests. Data Availability Statement: Sequences are deposited in GenBank and the Barcode of Life Data systems (for accession numbers see Table S1). Voucher specimens are deposited at 15 registered museum collections and the insect collection of the TU Darmstadt currently curated by C.v.B. (Table S1). Specimen images are deposited at BOLD systems (see Table S1).
Funders:
Funding AgencyGrant Number
Deutsche Forschungsgemeinschaft (DFG)BE5177/1‐1
Deutsche Forschungsgemeinschaft (DFG)BE5177/4-1
Deutsche Forschungsgemeinschaft (DFG)BE5177/4-2
National Geographic SocietyUNSPECIFIED
Bristol-Myers SquibbUNSPECIFIED
Carl & Marian Rettenmeyer Ant-Guest EndowmentUNSPECIFIED
Studienstiftung des deutschen VolkesUNSPECIFIED
Projekt DEALUNSPECIFIED
Subject Keywords:biodiversity; community structure; cryptic species; ecological networks; host–symbiont networks; myrmecophiles
Issue or Number:20
DOI:10.1111/mec.16101
Record Number:CaltechAUTHORS:20210921-152951282
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20210921-152951282
Official Citation:von Beeren, C., Blüthgen, N., Hoenle, P. O., Pohl, S., Brückner, A., Tishechkin, A. K., Maruyama, M., Brown, B. V., Hash, J. M., Hall, W. E., & Kronauer, D. J. C. (2021). A remarkable legion of guests: Diversity and host specificity of army ant symbionts. Molecular Ecology, 30, 5229–5246. https://doi.org/10.1111/mec.16101
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:110974
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:21 Sep 2021 15:46
Last Modified:12 Oct 2021 20:40

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