Geometric Morphometric Versus Genomic Patterns in a Large Polyploid Plant Species Complex

SIMPLE SUMMARY: Plant species complexes with hybridization and asexual reproduction often exhibit complex morphological patterns, which is problematic for classifications. Here, we analyze geometric morphometric, genomic, and ecological data with comprehensive statistics to evaluate phenotypic variation in the Eurasian Ranunculus auricomus complex. Genomic clusters correspond largely to morphological groupings, but most described asexual hybrid taxa cannot be discriminated from each other. Phenotypic variation is more influenced by genomic composition than by climatic conditions, and the phenotypic variation of asexual hybrids resembles a mosaic of intermediate and transgressive phenotypes. Our results support a taxonomic revision of the complex. ABSTRACT: Plant species complexes represent a particularly interesting example of taxonomically complex groups (TCGs), linking hybridization, apomixis, and polyploidy with complex morphological patterns. In such TCGs, mosaic-like character combinations and conflicts of morphological data with molecular phylogenies present a major problem for species classification. Here, we used the large polyploid apomictic European Ranunculus auricomus complex to study relationships among five diploid sexual progenitor species and 75 polyploid apomictic derivate taxa, based on geometric morphometrics using 11,690 landmarked objects (basal and stem leaves, receptacles), genomic data (97,312 RAD-Seq loci, 48 phased target enrichment genes, 71 plastid regions) from 220 populations. We showed that (1) observed genomic clusters correspond to morphological groupings based on basal leaves and concatenated traits, and morphological groups were best resolved with RAD-Seq data; (2) described apomictic taxa usually overlap within trait morphospace except for those taxa at the space edges; (3) apomictic phenotypes are highly influenced by parental subgenome composition and to a lesser extent by climatic factors; and (4) allopolyploid apomictic taxa, compared to their sexual progenitor, resemble a mosaic of ecological and morphological intermediate to transgressive biotypes. The joint evaluation of phylogenomic, phenotypic, reproductive, and ecological data supports a revision of purely descriptive, subjective traditional morphological classifications.