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The complex interaction between megaherbivores, climate and fire has shaped the evolution and distribution of plant spinescence across biogeographical realms

bioRxiv (Cold Spring Harbor Laboratory)

Abstract

The evolutionary arms race between plants and herbivores has led to numerous plant adaptations, including spinescence. However, whether spinescence evolved primarily in response to herbivory, or whether abiotic conditions also played a role, remains unknown. We integrated phylogenetic, geographic, and trait data for 2,686 species of an ecologically diverse and spiny pantropical lineage, mimosoid legumes, with data for 235 extant and 185 extinct mammalian herbivores >10 kg. Using structural equation models, we assessed how herbivores, climate and fire directly and indirectly affected the proportion of spinescent mimosoids across global and continental assemblages. The proportion of spinescent mimosoids in assemblages increased with extant and extinct herbivore richness, drought and heat, while fire influenced spinescence indirectly, by affecting herbivore richness. Notably, correlations of spinescence differed between Africa and America, with increasing importance of extinct herbivores in Africa, illustrating legacy effects on spinescence. Megaherbivores have shaped spinescence in mimosoids, especially in dry environments, where losing plant tissues is costly. Spinescence originated ~35 Mya, with the transition of mimosoids to seasonally dry environments, pre-dating the Miocene expansion of savannas. Our study suggests that both long-term climatic transitions and the emergence of open, herbivore-rich landscapes played crucial roles in the evolution and distribution of spinescence.

Authors 7

  1. Naturalis Biodiversity Center · German Centre for Integrative Biodiversity Research · Leipzig University

    Affiliation as printed

    German Centre for Integrative Biodiversity Research (iDiv);

    German Center for Integrative Biodiversity Research (iDiv) Halle – Jena – Leipzig, Puschstrasse 4, 0403 Leipzig, Germany

    Leipzig University, Johannisallee 1–3, D-04103 Leipzig, Germany

    Naturalis Biodiversity Center, Darwinweg 2, 2 CR, Leiden, The Netherlands

  2. Naturalis Biodiversity Center · University of Zurich · Wageningen University & Research

    Affiliation as printed

    University of Zurich;

    Biosystematics Group, Wageningen University and Research, Radix Building 107, Droevendaalsesteeg 1, 6708 PB Wageningen, the Netherlands

    Naturalis Biodiversity Center, Darwinweg 2, 2 CR, Leiden, The Netherlands

  3. University of Zurich

    Affiliation as printed

    University of Zurich;

    Department of Systematic and Evolutionary Botany, University of Zurich, Zollikerstrasse 107, CH 8008 Zurich, Switzerland

  4. Tel Aviv University

    Affiliation as printed

    Tel Aviv University;

    School of Zoology, George S. Wise Faculty of Life Sciences, Tel Aviv University, Tel Aviv, Israel

  5. Czech University of Life Sciences Prague

    Affiliation as printed

    Czech University of Life Sciences Prague;

    Faculty of Environmental Sciences, Czech University of Life Sciences Prague, Kamýcká 129 165 00 Prague, Czech Republic

  6. Chinese Academy of Sciences

    Affiliation as printed

    Chinese Academy of Sciences;

    Center of Conservation Biology, Core Botanical Gardens, Chinese Academy of Sciences, Menglun, Yunnan 666303, China

  7. Leiden University · Naturalis Biodiversity Center · German Centre for Integrative Biodiversity Research

    Affiliation as printed

    Naturalis Biodiversity center

    German Center for Integrative Biodiversity Research (iDiv) Halle – Jena – Leipzig, Puschstrasse 4, 0403 Leipzig, Germany

    Leiden University, Institute of Biology Leiden, Sylviusweg 72, 2333 BE Leiden, The Netherlands

    Naturalis Biodiversity Center, Darwinweg 2, 2 CR, Leiden, The Netherlands

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