Abstract

The warm‐temperate and subtropical climate zones of East Asia are a hotspot of plant species richness and endemism, including a noticeable number of species‐poor Tertiary relict tree genera. However, little is understood about when East Asian Tertiary relict plants diversified, how they responded demographically to past environmental change, and to what extent their current genomic composition (and adaptive capacity) might mitigate the effects of global warming. Here, we obtained genomic (RAD‐SNP) data for 171 samples from two extant species of Euptelea in China (24 E. pleiosperma populations) and Japan (11 E. polyandra populations) to elucidate their divergence and demographic histories, genome‐wide associations with current environmental variables, and genomic vulnerability to future climate change. Our results indicate that Late Miocene changes in climate and/or sea level promoted species divergence, whereas Late Pliocene uplifting in southwest China likely fostered lineage divergence within E. pleiosperma. Its subsequent range expansion into central/east (CE) China bears genomic signatures of climate‐driven selection, yet extant CE populations are predicted to be most vulnerable to future climate change. For E. polyandra, geography was the only significant predictor of genomic variation. Our findings indicate a profound impact of Late Neogene geological and climate change on the evolutionary history of Euptelea, with much stronger signals of local adaptation left in China than in Japan. This study deepens our understanding of the complex evolutionary forces that influence the distribution of genetic variation of Tertiary relict trees, and provides insights into their susceptibility to global change and potential for adaptive responses. Our results lay the groundwork for future conservation and restoration programs for Euptelea.

Highlights

  • The warm-temperate and subtropical climate zones of cluster model. Within E. pleiosperma (China) and south/central Japan are a hotspot of plant biodiversity in East Asia (Qian & Ricklefs, 2000; Qiu, Fu, & Comes, 2011; Wang, 1992)

  • This study aims to further clarify (a) when and how the two extant species of Euptelea diverged; (b) how they responded demographically to past environmental change; (c) to what extent historical, geographical, and/or climatic factors contribute to their current genomic variation; and (d) which populations of E. pleiosperma might be most vulnerable to future climate change

  • Using approximate Bayesian computation (ABC) simulations, we dated the split between E. pleiosperma (China) and E. polyandra (Japan) at about the Late Miocene, c. 6.39 Ma (Scenario 2; Figure 3a)

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Summary

Introduction

The warm-temperate and subtropical climate zones of China and south/central Japan are a hotspot of plant biodiversity in East Asia (Qian & Ricklefs, 2000; Qiu, Fu, & Comes, 2011; Wang, 1992) In both regions, habitats associated with mountain riparian forests (MRFs) in particular feature high levels of species richness and endemism, including a noticeable number of species-poor Tertiary relict tree genera (e.g., Cercidiphyllum, Euptelea, Eurycorymbus; Tang & Ohsawa, 2002; Wei et al, 2009). Cercidiphyllum japonicum (Qi et al, 2012) has been cited as “more dynamic in history than previously thought” (cf Mao & Liu, 2012), and the same is true for other Tertiary relicts showing a wide geographic distribution (e.g., Euptelea: Cao, Comes, Sakaguchi, Chen, & Qiu, 2016; see below) Given their limited number of variable loci, previous studies using traditional markers might be inadequate for characterizing the current genomic composition of species with complex demographic histories (Bay et al, 2018; Hancock et al, 2011). Further studies are required to disentangle the relative roles of historic-environmental (geographical, climatic) and contemporary factors (e.g., drift, gene flow) in shaping the genomic architecture of East Asia's Tertiary relict tree species

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