Pliocene intraspecific divergence and Plio-Pleistocene range expansions within Picea likiangensis (Lijiang spruce), a dominant forest tree of the Qinghai-Tibet Plateau

A knowledge of intraspecific divergence and range dynamics of dominant forest trees in response to past geological and climate change is of major importance to an understanding of their recent evolution and demography. Such knowledge is informative of how forests were affected by environmental factors in the past and may provide pointers to their response to future environmental change. However, genetic signatures of such historical events are often weak at individual loci due to large effective population sizes and long generation times of forest trees. This problem can be overcome by analysing genetic variation across multiple loci. We used this approach to examine intraspecific divergence and past range dynamics in the conifer Picea likiangensis, a dominant tree of forests occurring in eastern and southern areas of the Qinghai-Tibet Plateau (QTP). We sequenced 13 nuclear loci, two mitochondrial DNA regions and three plastid (chloroplast) DNA regions in 177 individuals sampled from 22 natural populations of this species, and tested the hypothesis that its evolutionary history was markedly affected by Pliocene QTP uplifts and Quaternary climatic oscillations. Consistent with the taxonomic delimitation of the three morphologically divergent varieties examined, all individuals clustered into three genetic groups with inter-variety admixture detected in regions of geographical overlap. Divergence between varieties was estimated to have occurred within the Pliocene and ecological niche modeling based on 20 ecological variables suggested that niche differentiation was high. Furthermore, modeling of population genetic data indicated that two of the varieties (var. rubescens and var. linzhiensis) expanded their population sizes after the largest Quaternary glaciation in the QTP, while expansion of the third variety (var. likiangensis) began prior to this, probably following the Pliocene QTP uplift. These findings point to the importance of geological and climatic changes during the Pliocene and Pleistocene as causes of intraspecific diversification and range shifts of dominant tree species in the QTP biodiversity hotspot region.

掌握优势林木响应古地质与气候变化的种内分化及分布区动态规律，对解析其近期演化历程与种群统计学特征具有核心意义。此类认知不仅能够揭示过往环境因子对森林生态系统的影响机制，还可为预测林木对未来环境变化的响应提供参考依据。然而，由于林木拥有较大的有效种群大小（effective population size）与较长的世代周期，单基因座上记录的历史事件遗传信号往往较为微弱。通过分析多基因座的遗传变异，即可克服这一难题。我们采用该方法，对青藏高原（Qinghai-Tibet Plateau, QTP）东南区域的优势针叶林树种丽江云杉（*Picea likiangensis*）的种内分化与历史分布区动态展开研究。我们从该物种的22个天然种群中采集了177个个体，对13个核基因座、2个线粒体DNA（mitochondrial DNA）区域以及3个质体（叶绿体）DNA（plastid (chloroplast) DNA）区域进行测序，并验证了如下假说：其演化历史显著受上新世（Pliocene）青藏高原隆升与更新世（Quaternary）气候波动的影响。研究结果与所检视的3个形态分化显著的变种的分类界定相符：所有个体均可划分为3个遗传类群，且在地理重叠区域检测到变种间的遗传渐渗现象。变种间的分化时间估算为上新世时期；基于20个生态变量构建的生态位模型（ecological niche modeling）显示，其生态位分化程度较高。此外，种群遗传数据的建模分析表明，其中两个变种（红皮变种var. rubescens与林芝变种var. linzhiensis）在青藏高原第四纪最大冰期后出现种群扩张，而第三个变种（丽江原变种var. likiangensis）的种群扩张则早于该冰期，大概率伴随上新世青藏高原隆升事件发生。本研究结果表明，上新世至更新世期间的地质与气候变化，是驱动青藏高原生物多样性热点区域内优势林木种内分化与分布区迁移的核心因素。