Patterns of Adaptive and Neutral Diversity Identify the Xiaoxiangling Mountains as a Refuge for the Giant Panda

Genetic variation plays a significant role in maintaining the evolutionary potential of a species. Comparing the patterns of adaptive and neutral diversity in extant populations is useful for understanding the local adaptations of a species. In this study, we determined the fine-scale genetic structure of 6 extant populations of the giant panda (Ailuropoda melanoleuca) using mtDNA and DNA fingerprints, and then overlaid adaptive variations in 6 functional Aime-MHC class II genes (DRA, DRB3, DQA1, DQA2, DQB1, and DQB2) on this framework. We found that: (1) analysis of the mtDNA and DNA fingerprint-based networks of the 6 populations identified the independent evolutionary histories of the 2 panda subspecies; (2) the basal (ancestral) branches of the fingerprint-based Sichuan-derived network all originated from the smallest Xiaoxiangling (XXL) population, suggesting the status of a glacial refuge in XXL; (3) the MHC variations among the tested populations showed that the XXL population exhibited extraordinary high levels of MHC diversity in allelic richness, which is consistent with the diversity characteristics of a glacial refuge; (4) the phylogenetic tree showed that the basal clades of giant panda DQB sequences were all occupied by XXL-specific sequences, providing evidence for the ancestor-resembling traits of XXL. Finally, we found that the giant panda had many more DQ alleles than DR alleles (33∶13), contrary to other mammals, and that the XXL refuge showed special characteristics in the DQB loci, with 7 DQB members of 9 XXL-unique alleles. Thus, this study identified XXL as a glacial refuge, specifically harboring the most number of primitive DQB alleles.

遗传变异对维持物种的进化潜力至关重要。比较现存种群中适应性多样性与中性多样性的分布模式，有助于解析物种的本地适应性机制。本研究借助线粒体DNA（mtDNA）与DNA指纹（DNA fingerprint）技术，解析了6个现存大熊猫（Ailuropoda melanoleuca）种群的精细遗传结构，并在此基础上叠加了6个功能性Aime-MHC II类基因（DRA、DRB3、DQA1、DQA2、DQB1及DQB2）的适应性变异。本研究获得以下发现：（1）对6个种群的线粒体DNA与DNA指纹网络分析，明确了2个大熊猫亚种各自独立的进化历程；（2）基于DNA指纹的四川起源网络的基干（祖先）分支均源自最小的小相岭（XXL）种群，这表明XXL种群具备冰期避难所的属性；（3）受试种群的MHC变异分析显示，XXL种群在等位基因丰富度维度展现出极高的MHC多样性，这与冰期避难所的多样性特征相符；（4）系统发育树显示，大熊猫DQB序列的基干演化支均由XXL种群特有的序列所占据，为XXL种群具有类祖先性状提供了实证支持。最后，本研究发现大熊猫的DQ等位基因数量远多于DR等位基因（33∶13），这与其他哺乳动物的情况相悖；且XXL避难所在DQB基因座呈现出特殊特征：9个XXL特有等位基因中有7个属于DQB基因类型。综上，本研究证实XXL种群为一处冰期避难所，其种群中携带着数量最多的原始DQB等位基因。