Phylogeography and population genetics reveal ring species patterns in a highly polymorphic California lily

Aim Natural selection typically results in the homogenization of reproductive traits, reducing natural variation within populations; thus, highly polymorphic species present unresolved questions regarding the mechanisms that shape and maintain gene flow given a diversity of phenotypes. We used an integrative framework to characterize phenotypic diversity and assess how evolutionary history and population genetics affect the highly polymorphic nature of a California endemic lily. Location California, United States. Taxon Butterfly mariposa lily, Calochortus venustus (Liliaceae). Methods We summarized phenotypic diversity at both metapopulation and subpopulation scales to explore spatial phenotypic distributions. We sampled 174 individuals across the species range representing multiple samples for each population and each phenotype. We used restriction-site-associated DNA sequencing (RAD-Seq) to detect population clusters, gene flow between phenotypes and between populations, infer haplotype networks, and reconstruct ancestral range evolution to infer historical migration and range expansion. Results Polymorphic floral traits within the species such as petal pigmentation and distal spots are geographically structured, and inferred evolutionary history is consistent with a ring species pattern involving a complex of populations having experienced sequential change in genetic and phenotypic variation from the founding population. Populations remain interconnected yet have differentiated from each other along a bifurcating south-to-north range expansion, consequently indicating parallel evolution towards the white morphotype in the northern range. Thus, our phylogeographical analyses reveal morphological convergence with population genetic cohesion irrespective of phenotypic diversity. Main conclusions Phenotypic variation in the highly polymorphic Calochortus venustus is not due to genetic differentiation between phenotypes; rather there is genetic cohesion within six geographically defined populations, some of which maintain a high level of within-population phenotypic diversity. Our results demonstrate that analyses of polymorphic taxa greatly benefit from disentangling phenotype from genotype at various spatial scales. We discuss results in light of ring species concepts and the need to determine the adaptive significance of the patterns we report.