基于群体基因组学解析连香树对环境梯度适应的演化过程和机理

Studying how forest species with a wide geographical distribution range adapt to different ecological environments is very important for the conservation and management of forest ecosystems in the context of global climate change. Cercidiphyllum japonicum is one of the most widely distributed trees in East Asian Tertiary-relic deciduous forests, and grows in different habitats including warm temperate, cold temperate and subalpine zones. C. japonicum provides an ideal system for studying the adaptive evolution of East Asian Tertiary-relic deciduous forests species, because it has a long evolutionary history, obvious ecological niche differentiation, and ancient asymmetric introgression with C. magnificum, as well as displays sympatric and allopatric areas with C. magnificum. In this project, we will employ genome sequencing and population genomic analyses, in combination with the information of paleogeography and paleoenvironment and ecological niche analysis, to clarify the evolutionary history of C. japonicum adapted to different environments. Based on comparative analyses of the genome sequences of sympatric and allopatric populations of C. japonicum and C. magnificum, we will characterize genome-wide patterns of introgression using Patterson’s D statistics and phylogenetic methods. And then, we will use landscape genomics methods to test whether some introgressed genes were involved in the adaptive evolution of C. japonicum. Moreover, we will employ the genome scanning and landscape genomics approaches to detect the candidate loci under nature selection. After annotating adaptive introgressed genes and adaptive genes along environmental gradients, we will analyze the variation and allele frequencies of these adaptive genes across different populations. Based on the above results, we expect to clarify the evolutionary process and mechanisms of ecological adaptation of C. japonicum. This study will be very important for deeply understanding the mechanisms of adaptive evolution of C. japonicum, and also be the solid basis for developing scientific conservation and appropriate management strategies of East Asian Tertiary-relic deciduous forests.

研究森林广布树种如何适应不同的生态环境对于全球气候变化背景下森林生态系统的保护与管理至关重要。连香树是东亚特有第三纪“孑遗落叶林”分布最广的森林树种之一，其进化历史时间长，分布范围广，生态位分化明显（差异适应于暖温带、寒温带以及亚高山生境），在地质历史时期与大叶连香树发生了不对称渐渗杂交现象，且目前种间具有同域和异域分布群体，是研究差异环境适应性进化机理的理想材料。本项目拟利用群体基因组数据与理论模型分析，结合地质、气候资料以及生态位分析，阐明连香树属进化历史以及适应不同环境的演化过程。基于种间基因渐渗分析，检验是否有渐渗基因参与了连香树适应性进化过程，并利用基因组扫描与景观基因组学空间统计方法，揭示广布种连香树环境梯度适应性的遗传基础。最终阐明广布种连香树适应不同环境的演化过程与生态适应机理，为理解生物适应性进化这一基本科学问题提供重要线索，也为该森林的保护与管理提供坚实的理论基础。

项目利用高通量测序技术，对连香树属两个孑遗种进行了全基因组测序、组装及群体水平的重测序分析。比较基因学研究发现，连香树中多个与抗性相关的基因家族如NBS-LRR发生了显著扩张，这些基因家族扩张可能提高了连香树适应不同环境的能力。鉴定了连香树MADS-box基因数量及雄性连锁区域，确定了连香树为雄性异配型性系统。基于群体基因组学数据计算得到连香树属两个种的遗传多样性水平均较低。中新世中期（c. 10 Ma）干冷的环境导致了连香树和大叶连香树的物种分化，分化初期种间存在较低水平的历史基因流，而近代种间基因流几乎可以忽略不计。连香树种内由于中新世末期陆桥隔离和气候变冷变干进一步分化为中国和日本两个谱系。第四纪剧烈的气候变化对连香树属有效种群大小具有显著的影响，尤其是上新世到更新世的交替时期，寒冷的气候使得连香树和大叶连香树都发生了急剧的种群压缩，末次盛冰期使它们再次经历了严重瓶颈效应。通过基因组扫描和选择分析在连香树14号染色体上鉴定到一段长度约为3.5 Mb的选择清除区间。同时，在3号、16号、17号和19号染色体上鉴定到平衡选择信号和明显杂合子优势区间，区间内的基因主要与应激反应、控制开花时间、植物生长发育有关。因此，长期的平衡选择可能是连香树在冰川瓶颈期存活下来并能广泛分布的最重要原因。此外，在连香树全基因组范围内鉴定到5,791个位点（823个基因）与环境因子具有显著相关性，这些基因主要与细胞发育和增殖、新陈代谢、生殖以及压力响应有关，其中102个基因位于高度分化的选择区间内。基因渐渗分析发现，日本连香树和大叶连香树之间存在基因渐渗现象，多个渐渗基因的功能与植物的抗寒或耐寒能力相关，部分渐渗基因还呈现自然选择和局域适应信号，表明了适应性基因渐渗对于日本连香树向北部扩张适应寒冷的环境发挥了重要的作用。总之，与环境异质性相关的选择清除、平衡选择以及适应性基因渐渗共同维持了参与关键生理过程基因的遗传变异，提高了连香树的局域适应性和适应潜力。综上所述，基于高通量测序数据和群体遗传学的理论和方法，本研究全面解析了连香树属植物的物种形成和适应性进化。研究结果对理解东亚暖温带孑遗落叶林关键类群如何响应全球气候变化有重要的启示作用。