Plastid genomes reveal evolutionary shifts in elevational range and flowering time of Osmanthus (Oleaceae)

Abstract

Species of Osmanthus are economically important ornamental trees, yet information regarding their plastid genomes (plastomes) have rarely been reported, thus hindering taxonomic and evolutionary studies of this small but enigmatic genus. Here, we performed comparative genomics and evolutionary analyses on plastomes of 16 of the 28 currently accepted species, with 11 plastomes newly sequenced. Phylogenetic studies identified four main lineages within the genus that are here designated the: “Caucasian Osmanthus” (corresponding to O. decorus), “ Siphosmanthus” (corresponding to O. sect. Siphosmanthus), “ O. serrulatus +  O. yunnanensis,” and “Core Osmanthus: (corresponding to O. sect. Osmanthus +  O. sect. Linocieroides). Molecular clock analysis suggested that Osmanthus split from its sister clade c. 15.83 Ma. The estimated crown ages of the lineages were the following: genus Osmanthus at 12.66 Ma; “ Siphosmanthus” clade at 5.85 Ma; “ O. serrulatus +  O. yunnanensis” at 4.89 Ma; and “Core Osmanthus: clade at 6.2 Ma. Ancestral state reconstructions and trait mapping showed that ancestors of Osmanthus were spring flowering and originated at lower elevations. Phylogenetic principal component analysis clearly distinguished spring‐flowering species from autumn‐flowering species, suggesting that flowering time differentiation is related to the difference in ecological niches. Nucleotide substitution rates of 80 common genes showed slow evolutionary pace and low nucleotide variations, all genes being subjected to purifying selection.

Abstract

This is the first well‐sampled report on the plastomes of Osmanthus. Phylogenetic results showed that Osmanthus species were clustered into four lineages, which had a good correspondence with morphological and biogeographic evidence. Molecular dating results suggested that Osmanthus is a tertiary relict genus. The origin and diversification of Osmanthus species are speculated to be closely related to the climatic changes and the orogenesis of the Qinghai–Tibet Plateau during the Miocene. The diversity of flowering time of Osmanthus is related to niche differences. The plastid genes are likely to not be significantly involved in adaptation to altitude or precipitation.