Rampant transitions between dispersal syndromes during angiosperm evolution

bioRxiv (Cold Spring Harbor Laboratory)

Abstract

Summary Angiosperms have evolved a diverse range of seed dispersal syndromes that have undoubtedly played a key role in their evolutionary history and rise to dominance. However, it remains largely unknown how ancestral angiosperm seeds were dispersed, when and how frequent dispersal-related characters and syndromes evolved, and whether these syndromes facilitated biome and pollination mode transitions. We integrated a large phylogeny and several dispersal-related characters for >1200 species representing all extant angiosperm families. We used phylogenetic comparative methods to infer ancestral states of major angiosperm clades, trends in the evolution of dispersal syndromes, and evolutionary correlations between dispersal syndromes, biomes and pollination modes. We show that angiosperms were ancestrally most likely animal-dispersed (zoochory) and had fleshy, indehiscent fruits. Over macroevolutionary time, frequent transitions between dispersal syndromes occurred, often with non-specialised (autonomous) dispersal as an intermediate state. Finally, we found that dispersal syndrome evolution affected transition rates among biomes and among pollination modes. The number of dispersal syndrome transitions exceeded pollination mode transitions by a factor of five, emphasizing lability in dispersal syndrome evolution. The progressive evolution of diaspore complexity led to frequent and repeated evolution of dispersal syndromes, critical for the colonization of angiosperms across modern biomes.

Authors 5

1. Dieder de Frens Aachen Naturalis Biodiversity Center

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

   Affiliation as printed

   Biosystematics Group, Wageningen University, Droevendaalsesteeg 1, 6708 PB Wageningen, the Netherlands

   Institute for Systematic and Evolutionary Botany, University of Zurich, Zollikerstr. 107, 8003 Zurich, Switzerland

   Naturalis Biodiversity Center, Darwinweg 2, 2333CR Leiden, The Netherlands

2. Freek T. Bakker

   Wageningen University & Research

   Affiliation as printed

   Biosystematics Group, Wageningen University, Droevendaalsesteeg 1, 6708 PB Wageningen, the Netherlands

3. Hervé Sauquet

   UNSW Sydney

   Affiliation as printed

   Evolution and Ecology Research Centre, School of Biological, Earth and Environmental Sciences, University of New South Wales, Sydney, NSW, 2052 Australia

   National Herbarium of NSW, Botanic Gardens of Sydney, Mount Annan, NSW, Australia

   Evolution and Ecology Research Centre, School of Biological, Earth and Environmental Sciences, University of New South Wales, Sydney, NSW, 202 Australia

4. Ruby E. Stephens

   UNSW Sydney

   Affiliation as printed

   Evolution and Ecology Research Centre, School of Biological, Earth and Environmental Sciences, University of New South Wales, Sydney, NSW, 2052 Australia

   Evolution and Ecology Research Centre, School of Biological, Earth and Environmental Sciences, University of New South Wales, Sydney, NSW, 202 Australia

5. Renske E. Onstein corresponding Aachen Naturalis Biodiversity Center

   Naturalis Biodiversity Center

   Affiliation as printed

   Naturalis Biodiversity Center, Darwinweg 2, 2333CR Leiden, The Netherlands