Becoming mega-diverse: integrative phylogenomics reveals heterogeneous diversification at high rate in Astragalus (Fabaceae)

Abstract

Background Understanding why species diversity is so unevenly distributed across the Tree of Life remains a central question in evolutionary biology. With more than 3,100 species, Astragalus (Fabaceae) is the largest genus of flowering plants and provides an exceptional system for investigating the factors of angiosperm megadiversity. However, despite recent phylogenomic advances, uncertainties in phylogenetic relationships and limited integration of available genomic resources have hindered comprehensive evolutionary analyses. Methods Here, we reconstruct the most comprehensive phylogenomic framework for Astragalus to date by integrating newly generated target enrichment data for 127 samples, representing 123 Astragalus taxa, with previously published target-capture, transcriptomic, and genome-skimming datasets. The resulting phylogeny includes 407 accessions representing 379 Astragalus species and provides a robust backbone for investigating diversification and genome evolution across the genus. Using a representative reduced dataset, we estimated divergence times, quantified diversification-rate heterogeneity, examined phylogenomic conflict, and evaluated evidence for whole-genome duplication (WGD). Key Results Our analyses recover a largely stable backbone for the deeper Astragalus lineages while revealing extensive gene-tree discordance concentrated in younger radiations, consistent with incomplete lineage sorting and reticulate evolution during rapid Miocene diversification. Diversification analyses indicate sustained lineage accumulation over approximately 18 million years, with pronounced rate shifts in several clades, particularly within the species-rich Neo-Astragalus lineage. Comparisons of alternative WGD scenarios across the phylogeny provided strongest support for a WGD at the crown node of Neo-Astragalus, with alternative placements receiving weaker support. This result provides a testable hypothesis for a WGD near the origin of the most rapidly diversifying lineage in the genus, although chromosome-scale genomic data will be required to confirm its occurrence and timing. Conclusions Together, our results indicate that the extraordinary diversity of Astragalus did not arise from a single evolutionary innovation or explosive radiation. Instead, megadiversity arose through the long-term interplay of sustained diversification, reticulate evolution, genome restructuring, and likely environmental change coupled with ecological adaptation. Beyond providing the most comprehensive phylogenomic hypothesis for the genus, this study establishes a robust framework for future investigations of biogeography, trait evolution, genome evolution, and the processes underlying exceptional species richness in flowering plants.