The Origin and Early Evolution of the Legumes are a Complex Paleopolyploid Phylogenomic Tangle closely associated with the Cretaceous-Paleogene (K-Pg) Boundary

Abstract

The consequences of the Cretaceous-Paleogene (K-Pg) boundary (KPB) mass extinction for the evolution of plant diversity are poorly understood, even although evolutionary turnover of plant lineages at the KPB is central to understanding the assembly of the Cenozoic biota. One aspect that has received considerable attention is the apparent concentration of whole genome duplication (WGD) events around the KPB, which may have played a role in survival and subsequent diversification of plant lineages. In order to gain new insights into the origins of Cenozoic biodiversity, we examine the origin and early evolution of the legume family, one of the most important angiosperm clades that rose to prominence after the KPB and for which multiple WGD events are found to have occurred early in its evolution. The legume family (Leguminosae or Fabaceae), with c. 20.000 species, is the third largest family of Angiospermae, and is globally widespread and second only to the grasses (Poaceae) in economic importance. Accordingly, it has been intensively studied in botanical, systematic and agronomic research, but a robust phylogenetic framework and timescale for legume evolution based on large-scale genomic sequence data is lacking, and key questions about the origin and early evolution of the family remain unresolved. We extend previous phylogenetic knowledge to gain insights into the early evolution of the family, analysing an alignment of 72 protein-coding chloroplast genes and a large set of nuclear genomic sequence data, sampling thousands of genes. We use a concatenation approach with heterogeneous models of sequence evolution to minimize inference artefacts, and evaluate support and conflict among individual nuclear gene trees with internode certainty calculations, a multi-species coalescent method, and phylogenetic supernetwork reconstruction. Using a set of 20 fossil calibrations we estimate a revised timeline of legume evolution based on a selection of genes that are both informative and evolving in an approximately clock-like fashion. We find that the root of the family is particularly difficult to resolve, with strong conflict among gene trees suggesting incomplete lineage sorting and/or reticulation. Mapping of duplications in gene family trees suggest that a WGD event occurred along the stem of the family and is shared by all legumes, with additional nested WGDs subtending subfamilies Papilionoideae and Detarioideae. We propose that the difficulty of resolving the root of the family is caused by a combination of ancient polyploidy and an alternation of long and very short internodes, shaped respectively by extinction and rapid divergence. Our results show that the crown age of the legumes dates back to the Maastrichtian or Paleocene and suggests that it is most likely close to the KPB. We conclude that the origin and early evolution of the legumes followed a complex history, in which multiple nested polyploidy events coupled with rapid diversification are associated with the mass extinction event at the KPB, ultimately underpinning the evolutionary success of the Leguminosae in the Cenozoic.