Nested whole-genome duplications coincide with diversification and high morphological disparity in Brassicaceae

Nora Walden,Klaus Mummenhoff,Dmitry A German,Christiane Kiefer,Roswitha Schmickl,Barbara Neuffer,Xiao-Chen Huang,Eva M Wolf,Philippe Rigault,Markus Kiefer,Andreas Franzke,Marcus A Koch

doi:10.1038/s41467-020-17605-7

Abstract

Angiosperms have become the dominant terrestrial plant group by diversifying for ~145 million years into a broad range of environments. During the course of evolution, numerous morphological innovations arose, often preceded by whole genome duplications (WGD). The mustard family (Brassicaceae), a successful angiosperm clade with ~4000 species, has been diversifying into many evolutionary lineages for more than 30 million years. Here we develop a species inventory, analyze morphological variation, and present a maternal, plastome-based genus-level phylogeny. We show that increased morphological disparity, despite an apparent absence of clade-specific morphological innovations, is found in tribes with WGDs or diversification rate shifts. Both are important processes in Brassicaceae, resulting in an overall high net diversification rate. Character states show frequent and independent gain and loss, and form varying combinations. Therefore, Brassicaceae pave the way to concepts of phylogenetic genome-wide association studies to analyze the evolution of morphological form and function.

Highlights

Angiosperms have become the dominant terrestrial plant group by diversifying for ~145 million years into a broad range of environments
We analyze if mean morphological disparity has increased after tribal and lineage specific whole genome duplications (WGD), and we study whether early diverging disparity among main evolutionary lineages coincides with shifts of net diversification rates in the early evolutionary history of the family
Our family-wide taxon sampling for the phylogenetic analysis covers all tribes of the Brassicaceae and aims at representing the deepest known phylogenetic split within each tribe

Summary

Introduction

Angiosperms have become the dominant terrestrial plant group by diversifying for ~145 million years into a broad range of environments. WGDs may provide the opportunity to develop new character states, key characters, or even evolutionary innovations, and generally increase the potential to implement increased character and trait variation in a clade and thereby its disparity. Increased morphological disparity may provide the basis to further diversify and eventually even radiate in a changing spatiotemporal context, while only a minority of characters and their states contribute to key traits and innovations and thereby drive clade diversification and radiation. Since polyploidization per se is causing major disadvantages, e.g., during mitosis and meiosis, lineages subjected to WGD usually experience a subsequent phase of diploidization[19] often accompanied by drastic genome reorganization and genome size reduction[20] These processes might be key to subsequent evolutionary success of respective clades evolving new traits and innovations. There are few studies systematically linking morphological diversity and its evolution with WGDs5

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Conclusion