The Origin of the Legumes is a Complex Paleopolyploid Phylogenomic Tangle Closely Associated with the Cretaceous–Paleogene (K–Pg) Mass Extinction Event

Abstract

The consequences of the Cretaceous-Paleogene (K-Pg) boundary (KPB) mass extinction for the evolution of plant diversity remain poorly understood, even though evolutionary turnover of plant lineages at the KPB is central to understanding assembly of the Cenozoic biota. The apparent concentration of whole genome duplication (WGD) events around the KPB may have played a role in survival and subsequent diversification of plant lineages. To gain new insights into the origins of Cenozoic biodiversity, we examine the origin and early evolution of the globally diverse legume family (Leguminosae or Fabaceae). Legumes are ecologically (co-)dominant across many vegetation types, and the fossil record suggests that they rose to such prominence after the KPB in parallel with several well-studied animal clades including Placentalia and Neoaves. Furthermore, multiple WGD events are hypothesized to have occurred early in legume evolution. Using a recently inferred phylogenomic framework, we investigate the placement of WGDs during early legume evolution using gene tree reconciliation methods, gene count data and phylogenetic supernetwork reconstruction. Using 20 fossil calibrations we estimate a revised timeline of legume evolution based on 36 nuclear genes selected as informative and evolving in an approximately clock-like fashion. To establish the timing of WGDs we also date duplication nodes in gene trees. Results suggest either a pan-legume WGD event on the stem lineage of the family, or an allopolyploid event involving (some of) the earliest lineages within the crown group, with additional nested WGDs subtending subfamilies Papilionoideae and Detarioideae. Gene tree reconciliation methods that do not account for allopolyploidy may be misleading in inferring an earlier WGD event at the time of divergence of the two parental lineages of the polyploid, suggesting that the allopolyploid scenario is more likely. We show that the crown age of the legumes dates to the Maastrichtian or early Paleocene and that, apart from the Detarioideae WGD, paleopolyploidy occurred close to the KPB. We conclude that the early evolution of the legumes followed a complex history, in which multiple auto- and/or allopolyploidy events coincided with rapid diversification and in association with the mass extinction event at the KPB, ultimately underpinning the evolutionary success of the Leguminosae in the Cenozoic.

A phylogenomic perspective on gene tree conflict and character evolution in Caprifoliaceae using target enrichment data, with Zabelioideae recognized as a new subfamily

“…6), similar to the results of Beaulieu et al (2013). Our result showed a very short node (Morales-Briones et al 2020a) and legumes (Koenen et al, 2020), and in lichenized fungi such as Lobariaceae (Ascomycota) (Widhelm et al, 2019). It is generally accepted that soon after the K-Pg boundary, due to mass extinctions, new habitats became available and diverse organisms experienced rapid diversifications (Schulte et al, 2010).…”

Tectonics, climate and the diversification of the tropical African terrestrial flora and fauna

“…This is mirrored by few dated molecular phylogenies stretching back to the KPB (e.g. Koenen et al ., 2020). Based on these few data, extinction events are inferred at the KPB across the tropical African flora and fauna (Coetzee, 1993; Morley, 2000; Pan et al ., 2006; Schulte et al ., 2010).…”

“…Rather the KPB initiated an increase in speciation leading to a rapid increase in generic diversity (Cascales‐Miñana & Cleal, 2014). Overall, the KPB also provided more ecological opportunities for increased global diversification of major animal groups such as mammals (Meredith et al ., 2011), frogs (Feng et al ., 2017; Portik et al ., 2019), birds (Feduccia, 2014; Jarvis et al ., 2014) and certain plant groups such as Leguminosae (or Fabaceae), one of the most dominant plant families in African biomes (Koenen et al ., 2020). Thus, the meteorite impact and the Deccan volcanism could have led to short‐lived ecosystem traumas and extinction, with plant and animal clades quickly recovering (Spicer & Collinson, 2014), especially in tropical ecosystems (Johnson & Ellis, 2002).…”

“…Thus, the meteorite impact and the Deccan volcanism could have led to short‐lived ecosystem traumas and extinction, with plant and animal clades quickly recovering (Spicer & Collinson, 2014), especially in tropical ecosystems (Johnson & Ellis, 2002). Overall, the KPB was the start of a second large‐scale flowering plant and animal diversification burst (O'Leary et al ., 2013; Silvestro et al ., 2015; Feng et al ., 2017; Koenen et al ., 2020), which initiated the diversification of tropical African biota (Linder, 2014).…”

Analysis of paralogs in target enrichment data pinpoints multiple ancient polyploidy events inAlchemillas.l. (Rosaceae)

“…While GRAMPA has been shown to be useful to identify multiple polyploidy events in the same tree (e.g., Thomas et al 2017;Koenen et al 2020), this tree-based approach can also be sensitive to gene tree estimation error or ILS (Thomas et al 2017).…”