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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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).
Change history
20 March 2024
A Correction to this paper has been published: https://doi.org/10.1038/s41477-024-01675-2
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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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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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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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DOI: https://doi.org/10.1038/s41477-024-01649-4