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

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. [Allopolyploidy; Cretaceous–Paleogene (K–Pg) boundary; Fabaceae, Leguminosae; paleopolyploidy; phylogenomics; whole genome duplication events]

Ultra-Conserved Elements and morphology reciprocally illuminate conflicting phylogenetic hypotheses in Chalcididae (Hymenoptera, Chalcidoidea)

ABSTRACTRecent technical advances combined with novel computational approaches promised the acceleration of our understanding of the tree of life. However, when it comes to hyperdiverse and poorly known groups of invertebrates, studies are still scarce. As published phylogenies will be rarely challenged by future taxonomists, careful attention must be paid to potential analytical bias. We present the first molecular phylogenetic hypothesis for the family Chalcididae, an emblematic group of parasitoid wasps, with a representative sampling (144 ingroups and 7 outgroups) that covers all described subfamilies and tribes and 82% of the known genera. Analyses of 538 Ultra-Conserved Elements (UCEs) with supermatrix (RAxML and IQTREE) and gene-tree reconciliation approaches (ASTRAL, ASTRID) resulted in highly supported topologies in overall agreement with morphology but reveal conflicting topologies for some of the deepest nodes. To resolve these conflicts, we explored the phylogenetic tree space with clustering and gene genealogy interrogation methods, analyzed marker and taxon properties that could bias inferences and performed a thorough morphological analysis (130 characters encoded for 40 taxa representative of the diversity). This joint analysis reveals that UCEs enable attainment of resolution between ancestry and convergent /divergent evolution when morphology is not informative enough, but also shows that a systematic exploration of bias with different analytical methods and a careful analysis of morphological features is required to prevent publication of artefactual results. We highlight a GC-content bias for ML approaches, an artefactual mid-point rooting of the ASTRAL tree and a deleterious effect of high percentage of missing data on gene tree reconciliation methods. Based on the results we propose a new classification of the family into eight subfamilies and 10 tribes that lay the foundation for future studies on the evolutionary history of Chalcididae.

Gene-Tree Reconciliation with MUL-Trees to Resolve Polyploidy Events

Polyploidy can have a huge impact on the evolution of species, and it is a common occurrence, especially in plants. The two types of polyploids—autopolyploids and allopolyploids—differ in the level of divergence between the genes that are brought together in the new polyploid lineage. Because allopolyploids are formed via hybridization, the homoeologous copies of genes within them are at least as divergent as orthologs in the parental species that came together to form them. This means that common methods for estimating the parental lineages of allopolyploidy events are not accurate, and can lead to incorrect inferences about the number of gene duplications and losses. Here, we have adapted an algorithm for topology-based gene-tree reconciliation to work with multi-labeled trees (MUL-trees). By definition, MUL-trees have some tips with identical labels, which makes them a natural representation of the genomes of polyploids. Using this new reconciliation algorithm we can: accurately place allopolyploidy events on a phylogeny, identify the parental lineages that hybridized to form allopolyploids, distinguish between allo-, auto-, and (in most cases) no polyploidy, and correctly count the number of duplications and losses in a set of gene trees. We validate our method using gene trees simulated with and without polyploidy, and revisit the history of polyploidy in data from the clades including both baker’s yeast and bread wheat. Our re-analysis of the yeast data confirms the allopolyploid origin and parental lineages previously identified for this group. The method presented here should find wide use in the growing number of genomes from species with a history of polyploidy. [Polyploidy; reconciliation; whole-genome duplication.]

Gene-tree reconciliation with MUL-trees to resolve polyploidy events

Polyploidy can have a huge impact on the evolution of species, and it is a common occurrence, especially in plants. The two types of polyploids - autopolyploids and allopolyploids - differ in the level of divergence between the genes that are brought together in the new polyploid lineage. Because allopolyploids are formed via hybridization, the homoeologous copies of genes within them are at least as divergent as orthologs in the parental species that came together to form them. This means that common methods for estimating the parental lineages of allopolyploidy events are not accurate, and can lead to incorrect inferences about the number of gene duplications and losses. Here, we have adapted an algorithm for topology-based gene-tree reconciliation to work with multi-labeled trees (MUL-trees). By definition, MUL-trees have some tips with identical labels, which makes them a natural representation of the genomes of polyploids. Using this new reconciliation algorithm we can: accurately place allopolyploidy events on a phylogeny, identify the parental lineages that hybridized to form allopolyploids, distinguish between allo-, auto-, and (in most cases) no polyploidy, and correctly count the number of duplications and losses in a set of gene trees. We validate our method using gene trees simulated with and without polyploidy, and revisit the history of polyploidy in data from the clades including both baker’s yeast and bread wheat. Our re-analysis of the yeast data confirms the allopolyploid origin and parental lineages previously identified for this group. The method presented here should find wide use in the growing number of genomes from species with a history of polyploidy.