Plastid phylogenomic insights into relationships, divergence, and evolution of Apiales

Main conclusion Members of Apiales are monophyletic and radiated in the Late Cretaceous. Fruit morphologies are critical for Apiales evolution and negative selection and mutation pressure play important roles in environmental adaptation. Apiales include many foods, spices, medicinal, and ornamental plants, but the phylogenetic relationships, origin and divergence, and adaptive evolution remain poorly understood. Here, we reconstructed Apiales phylogeny based on 72 plastid genes from 280 species plastid genomes representing six of seven families of this order. Highly supported phylogenetic relationships were detected, which revealed that each family of Apiales is monophyletic and confirmed that Pennanticeae is a member of Apiales. Genera Centella and Dickinsia are members of Apiaceae, and the genus Hydrocotyle previously classified into Apiaceae is confirmed to belong to Araliaceae. Besides, coalescent phylogenetic analysis and gene trees cluster revealed ten genes that can be used for distinguishing species among families of Apiales. Molecular dating suggested that the Apiales originated during the mid-Cretaceous (109.51 Ma), with the families' radiation occurring in the Late Cretaceous. Apiaceae species exhibit higher differentiation compared to other families. Ancestral trait reconstruction suggested that fruit morphological evolution may be related to shifts in plant types (herbaceous or woody), which in turn is related to the distribution areas and species numbers. Codon bias and positive selection analyses suggest that negative selection and mutation pressure may play important roles in environmental adaptation of Apiales members. Our results improve the phylogenetic framework of Apiales and provide insights into the origin, divergence, and adaptive evolution of this order and its members.

Automated summary

Apiales members are monophyletic and radiated in the Late Cretaceous. Fruit morphologies are critical for Apiales evolution, and negative selection and mutation pressure play important roles in environmental adaptation. However, phylogenetic relationships, origin, divergence, and adaptive evolution of Apiales are still poorly understood. In this study, the phylogeny of Apiales was reconstructed based on plastid genomes, revealing monophyletic families and providing insights into the origin, divergence, and adaptive evolution of this order and its members. Coalescent phylogenetic analysis and gene trees cluster also identified genes that can be used for species distinction among families. Molecular dating indicated the mid-Cretaceous origin of Apiales and radiation in the Late Cretaceous, with higher differentiation observed in the Apiaceae species. Ancestral trait reconstruction suggested a relationship between fruit morphological evolution and plant types and distribution areas. Codon bias and positive selection analyses further highlighted the role of negative selection and mutation pressure in the environmental adaptation of Apiales members.