Neogene and Quaternary climate changes shaped the lineage differentiation and demographic history of Fokienia hodginsii (Cupressaceae s.l.), a Tertiary relict in East Asia

Historical climate oscillations and tectonic events have influenced the speciation and evolutionary history of many organisms. In this study, we chose Fokienia hodginsii (Dunn) A. Henry & H. H. Thomas (Cupressaceae s.l.), a Tertiary relict conifer, for the inference of the demographic history since the Neogene. Five chloroplast regions and two single-copy nuclear genes were amplified and sequenced in 497 individuals from 28 populations. The chloroplast data showed that F. hodginsii presented a high level of genetic diversity (H-T = 0.860 +/- 0.0279) and significant phylogeographic structure (N-ST > G(ST), P < 0.05). According to beast analysis, the divergence time of the two major lineages indicated by the phylogenetic construction produced from chloroplast and nuclear data could be dated to the early Miocene (ca. 19.34-19.95 Ma), which coincided with the onset and intensification of the Asian monsoon. During this time, environmental adaption under the different climatic conditions on either side of the Tanaka Line could have played important roles in maintaining and/or reinforcing the divergence of the two major lineages. The ecological niche modeling results showed that F. hodginsii experienced habitat fragmentation and strengthening of genetic barriers during the Last Glacial Maximum, followed by local expansion during postglacial periods. Our findings show that paleoclimate changes since the Neogene might have triggered the extinction of all but one Fokienia species and its intraspecific lineage differentiation. This study also suggests that Tertiary relicts in subtropical and tropical areas might have had a complex evolutionary history and their intraspecific differentiation time might have been earlier than expected.