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Blocking then stinging as a case of two-step evolution of defensive cage architectures in herbivore-driven ecosystems

Nature Plants volume 10, pages 587–597 (2024)Cite this article

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An Author Correction to this article was published on 20 March 2024

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Abstract

Dense branching and spines are common features of plant species in ecosystems with high mammalian herbivory pressure. While dense branching and spines can inhibit herbivory independently, when combined, they form a powerful defensive cage architecture. However, how cage architecture evolved under mammalian pressure has remained unexplored. Here we show how dense branching and spines emerged during the age of mammalian radiation in the Combretaceae family and diversified in herbivore-driven ecosystems in the tropics. Phylogenetic comparative methods revealed that modern plant architectural strategies defending against large mammals evolved via a stepwise process. First, dense branching emerged under intermediate herbivory pressure, followed by the acquisition of spines that supported higher speciation rates under high herbivory pressure. Our study highlights the adaptive value of dense branching as part of a herbivore defence strategy and identifies large mammal herbivory as a major selective force shaping the whole plant architecture of woody plants.

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Fig. 1: Traits studied and hypotheses tested.
Fig. 2: Global herbivore richness, herbivory regimes and their relationship with biome types.
Fig. 3: Plant defensive architectural traits in association with environmental factors, ancestral state and herbivory regime inferences.
Fig. 4: Speciation rates of species with dense architectures under herbivory regimes according to the best-fitting models in the MuSSE framework.
Fig. 5: Speciation rates of spiny species under herbivory regimes according to the best-fitting models in the MuSSE framework.
Fig. 6: Combretaceae architecture evolution under different herbivory regimes.
Fig. 7: Speciation rates of spiny species with dense architectures according to the best-fitting models in the MuSSE framework.

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Data availability

The descriptions data (cagey index and spines), the herbivory richness data and outputs for all analyses that support the findings of this study have been deposited in figshare (https://doi.org/10.6084/m9.figshare.24454609).

The additional datasets used in this study are GBIF datasets (GBIF.org, 27 October 2022, GBIF Occurrence Download: https://doi.org/10.15468/dl.7p2kpa) and data from the IUCN Red List Database (The IUCN Red List of Threatened Species v.2022-2; https://www.iucnredlist.org).

Code availability

The R code used for all analyses of this study have been deposited in figshare (https://doi.org/10.6084/m9.figshare.24454609).

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Acknowledgements

A.A. was sponsored by the 2018 CAS-TWAS President’s Fellowship for International Doctoral Students (20180479). The work was supported by a Yunnan Province 1000 Talents grant to K.W.T. (E0YN021). Calculations were performed using HPC resources from DNUM CCUB (Centre de Calcul de l’Université de Bourgogne).

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Authors and Affiliations

  1. Center for Integrative Conservation and Yunnan Key Laboratory for Conservation of Tropical Rainforests and Asian Elephants, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Menglun, Mengla, China

    Artémis Anest & Kyle W. Tomlinson

  2. University of Chinese Academy of Sciences, Beijing, China

    Artémis Anest

  3. AMAP, Univ Montpellier, CIRAD, CNRS, INRAE, IRD, Montpellier, France

    Artémis Anest, Tristan Charles-Dominique & Yves Caraglio

  4. Agroécologie, Univ. Bourgogne, Univ. Bourgogne Franche-Comté, INRAE, Institut Agro, Dijon, France

    Yanis Bouchenak-Khelladi

  5. Centre National de la Recherche Scientifique (CNRS), Sorbonne University, Paris, France

    Tristan Charles-Dominique

  6. Royal Botanic Gardens, Kew, Richmond, UK

    Félix Forest & Olivier Maurin

  7. Ecology and Environmental Change, School of Biodiversity, One Health and Veterinary Medicine, University of Glasgow, Glasgow, UK

    Gareth P. Hempson

  8. Center of Conservation Biology, Core Botanical Gardens, Chinese Academy of Sciences, Menglun, Mengla, China

    Kyle W. Tomlinson

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Contributions

A.A., T.C.-D. and K.W.T. designed the project. A.A. conducted data collection and processing. A.A. and Y.B.-K. performed the analyses. A.A., Y.B.-K., T.C.-D., Y.C., F.F., G.P.H., O.M. and K.W.T. wrote the manuscript.

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Correspondence to Artémis Anest or Kyle W. Tomlinson.

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Nature Plants thanks Domingos Cardoso and Guillaume Chomicki for their contribution to the peer review of this work.

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Anest, A., Bouchenak-Khelladi, Y., Charles-Dominique, T. et al. Blocking then stinging as a case of two-step evolution of defensive cage architectures in herbivore-driven ecosystems. Nat. Plants 10, 587–597 (2024). https://doi.org/10.1038/s41477-024-01649-4

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