Complex Reticulation in Backbone Subfamily Relationships in Leguminosae

Abstract

Contradictory lines of evidence have made it difficult to resolve the phylogenetic history of the legume diversification era; this is true for the backbone topology, and for the number and timing of whole genome duplications (WGDs). By analyzing the transcriptomic data for 473 gene families in 76 species covering all six accepted legume subfamilies, we assessed the phylogenetic relationships of the legume backbone and uncovered evidence of independent whole genome duplications in each of the six legume subfamilies. Three subfamilies -- Cercidoideae, Dialioideae, and Caesalpinioideae -- bear evidence of an allopolyploid duplication pattern suggestive of ancient hybridization. In Cercidoideae and Dialioideae, the hybridization appears to be within-subfamily, with the genera Cercis and Poeppigia apparently unduplicated descendants of one of the parental lineages; in Caesalpinioideae, the hybridization appears to involve a member of the Papilionoideae lineage, and some other lineage, potentially extinct. Three independent lines of evidence, consisting of a concatenated superalignment, concordance factor analysis of the set of gene family alignments and topologies, and direct inference of reticulation events via maximum pseudo-likelihood implemented by PhyloNet, converged on a single backbone hypothesis and the above hypotheses of reticulate evolution. Significance StatementIn a hybridization event, genes that have already been evolving separately for potentially millions of years become sister chromosomes, yet remain related to one another not at the moment of hybridization, but at the speciation node of the hybrids parents. Methodologies based on counts of bursts of duplicated genes, can therefore be fundamentally vulnerable to incorrect and contradictory conclusions about the number and timing of WGD events, unless interpreted carefully and in combination with data from gene trees discordant with the consensus backbone. Our assessment of the legume backbone in that light, resolves previous contradictory findings by concluding that three legume subfamilies are allopolyploid relative to the ur-legume.