Phylogenomic Insights into the Independent Origins of Sterile Marginal Flowers inViburnum

Abstract

Premise of research. Many angiosperms produce floral displays with morphologically distinct flower types that together operate in pollinator attraction. In Viburnum, nine species in four widely separated subclades encircle their inflorescences with enlarged sterile marginal flowers (SMFs). Previous phylogenetic analyses of Viburnum were unable to resolve relationships within clades that contain species with SMFs, making it difficult to enumerate the origins/losses of SMFs and to identify possible environmental and organismal commonalities across these origins. Methodology. We analyzed RAD-seq data to estimate phylogenetic relationships within each SMF subclade. We inferred demographic dynamics and historical gene flow to identify sources of phylogenetic discordance. Finally, we specifically tested hypotheses on how climate and plant architecture may have promoted the evolution of SMFs by inferring phylogenetic shifts and correlations across the origins of SMFs. Pivotal results. Our analyses strongly support four origins of SMFs. In the cold-adapted Opulus and Pseudotinus lineages, rapid divergence and population size fluctuations coincided with the origins of SMFs. In the less cold-adapted Euviburnum clade, a rapid radiation in central China yielded one SMF-producing species. In the more subtropical Lutescentia lineage, the origin of SMFs appears to have coincided with a shift into cooler climates, and we found evidence of gene flow between partially sympatric species. SMFs never evolved in tropical or subtropical habitats, and shifts into colder climates may have promoted their origin. Three of the four origins of SMFs are associated with the evolution of distinctive plant growth patterns that amplify the floral display. Conclusions. It appears that the evolution of SMFs was favored by a combination of shifts into colder climates and the evolution of branching patterns that increase the overall apparency of the floral display. However, our findings caution against the common assumption that the same causal factors underlie every instance of parallel evolution within a clade.