Contrasting evolutionary processes during Quaternary climatic changes and historical orogenies: a case study of the Japanese endemic primroses Primula sect. Reinii.

Abstract

Recent biogeographic studies have illustrated that Quaternary climatic changes and historical orogenies have driven the development of high levels of biodiversity. In this context, phylogenetic niche conservatism may play a role as a major precursor of allopatric speciation. However, the effects of niche evolution on the diversification patterns of plant species under rapid habitat changes are still unknown. Here, Primula section Reinii, one of the few primroses endemic to the Japanese Archipelago, was investigated. This study aimed to clarify the phylogenetic position and relationships of section Reinii, interpret the biogeographic and diversification patterns of this group and gain a better understanding of the role of climatic niche evolution in the Japanese endemic primroses. Dated phylogeny for Primula section Reinii is presented based on the sequences of six chloroplast genes and one nuclear gene. Biogeographic history was reconstructed using statistical dispersal-vicariance analysis. Macro-evolutionary modelling of the climatic niche was combined with biogeographic inferences. Section Reinii was shown to be monophyletic based on chloroplast and nuclear sequences. Fossil-calibrated dating analysis estimated that this section diverged from its sister taxon, sect. Cortusoides, around 1.82 million years ago, and intraspecific diversification occurred within the last million years. This time frame was characterized by Quaternary climatic oscillations and uplift of high mountains in Japan. Biogeographic inference suggested that this section originated at the northern end of the Japanese Archipelago and then dispersed southward to other islands. Models of climatic niche evolution indicated that the closely related species P. reinii and P. tosanensis have contrasting niche optima and rates of niche evolution. Our results highlight that spatiotemporal heterogeneity in the Japanese islands may play a significant role in the biogeographic history of Japanese endemic primroses. Contrasting evolutionary processes found in closely related species illustrate the effects of climatic niche evolution on species' diversification patterns.