Phylogenomic and ecological analyses reveal the spatiotemporal evolution of global pines

How coniferous forests evolved in the Northern Hemisphere remains largely
unknown. Unlike most groups of organisms that generally follow a
latitudinal diversity gradient, most conifer species in the Northern
Hemisphere are distributed in mountainous areas at middle latitudes. It is
of great interest to know whether the mid-latitude region has been an
evolutionary cradle or museum for conifers and how evolutionary and
ecological factors have driven their spatiotemporal evolution. Here, we
investigated the macroevolution of Pinus, the largest conifer genus and
characteristic of northern temperate coniferous forests, based on nearly
complete species sampling. Using 1,662 genes from transcriptome sequences,
we reconstructed the first robust species phylogeny and re-estimated
divergence times of global pines. We found that approximately 90% of
extant pine species originated in the Miocene in sharp contrast to the
ancient origin of Pinus, indicating a Neogene re-diversification.
Surprisingly, species at middle latitudes are much older than those at
other latitudes. This finding, coupled with net diversification rate
analysis, indicates that the mid-latitude region has provided an
evolutionary museum for global pines. Analyses of 31 environmental
variables, together with a comparison of evolutionary rates of niche and
phenotypic traits with net diversification rate, found that topographical
heterogeneity played a primary role in pine diversification, and the
aridity index was decisive for the niche rate shift. Moreover, fire has
forced diversification and adaptive evolution of Pinus. Our study
highlights the importance of integrating phylogenomic and ecological
approaches to address evolution of biological groups at the global scale.

北半球针叶林的演化路径至今仍未被完全明晰。与多数遵循纬度多样性梯度（latitudinal diversity gradient）分布的生物类群不同，北半球的多数针叶树物种集中分布于中纬度山地。厘清中纬度区域是否为针叶树的进化摇篮或进化博物馆，以及演化与生态因子如何驱动其时空演化，是学界高度关注的科学问题。本研究以几乎覆盖所有物种的采样策略，对北半球温带针叶林的代表性类群、最大的松属（Pinus）植物的宏观演化展开探究。本研究利用转录组序列得到的1662个基因，构建了首个稳健的松属物种系统发育树，并重新估算了全球松树的分化时间。研究发现，尽管松属的起源极为古老，但约90%的现存松属物种均形成于中新世，这表明松属在新近纪发生了一次快速的辐射分化。令人意外的是，中纬度分布的松属物种的分化时间远早于其他纬度的物种。结合净分化速率（net diversification rate）分析的结果，这一发现表明中纬度区域是全球松树的进化博物馆。通过对31个环境变量的分析，并将生态位与表型性状的演化速率与净分化速率进行对比，本研究发现地形异质性对松树的分化起到了主导作用，而干旱指数则是驱动生态位速率转变的关键因子。此外，火胁迫驱动了松属的物种分化与适应性演化。本研究强调，整合系统基因组学与生态学研究方法，对于解析全球尺度下生物类群的演化规律具有重要意义。