Data_Sheet_6_On the Causes of Rapid Diversification in the Páramos: Isolation by Ecology and Genomic Divergence in Espeletia.PDF

How diversity arises and what is the relative role of allopatric and ecological divergence are among the most persistent questions in evolution and ecology. Here, we assessed whether ecological divergence has enhanced the diversification of the Neotropical alpine plant complex Espeletia, also known as frailejones. This genus has one of the highest diversification rates ever reported and is distributed in the world’s fastest evolving biodiversity hotspot, the Páramo (Neotropical alpine grasslands at elevations of c. 2800–4700 m). Our goal was to determine whether ecology plays a role in divergence within the Espeletia complex by quantifying genome-wide patterns of ecological divergence. We characterized 162 samples of the three most common and contrasting ecotypes (distinct morphotypes occupying particular habitats) co-occurring in six localities in the northern Andes using Genotyping by Sequencing. Contrasting ecotypes were caulescent cloud forest populations, caulescent populations from wind-sheltered and well-irrigated depressions and acaulescent populations from wind-exposed drier slopes. We found high polymorphism with a total of 1,273 single nucleotide polymorphisms (SNPs) that defined the relationships among nine genetic clusters. We quantified allelic associations of these markers with localities and habitats using 18 different general and mixed-effects statistical models that accounted for phylogenetic distance. Despite that these models always yielded more SNPs associated with the localities, markers associated with the habitat types were recovered too. We found strong evidence for isolation-by-distance (IBD) across populations despite rampant gene flow, as expected for plant groups with limited seed dispersal. Contrasts between populations of different habitat types showed that an isolation-by-environment (IBE) trend emerged and masked the IBD signal. Maximum likelihood estimation of the number of migrants per generation (Nem) among ecotypes confirmed the IBE pattern. This result illustrates the importance of mountains’ environmental variation at a local scale in generating rapid morphological radiations and maintaining multiple adaptations in a fast-evolving ecosystem like the Páramo.

生物多样性如何起源，以及异域分化（allopatric divergence）与生态分化（ecological divergence）的相对作用为何，始终是进化生物学与生态学领域最经久不衰的核心议题之一。本研究旨在探究生态分化是否推动了新热带高山植物复合群——香蓟属（Espeletia），俗称弗拉耶霍内斯（frailejones）的物种多样化进程。该属是目前已知物种多样化速率最高的类群之一，分布于全球演化最快的生物多样性热点区域——帕拉莫（Páramo，即海拔约2800-4700米的新热带高山草原）。本研究的目标是通过量化生态分化的全基因组模式，明确生态过程是否在香蓟属复合群的物种分化中发挥作用。我们采用测序分型（Genotyping by Sequencing）技术，对安第斯山脉北部6个采样点中共存的3种最常见且差异显著的生态型（ecotype，即占据特定生境的独特形态型）的162份样本进行了遗传特征分析，这3种生态型分别为：云雾林生境的具茎种群、避风且灌溉充足洼地的具茎种群，以及暴露于强风的干燥坡地的无茎种群。本研究检测到较高水平的多态性，共计获得1273个单核苷酸多态性位点（single nucleotide polymorphisms, 简称SNPs），这些位点可解析9个遗传聚类群之间的亲缘关系。我们采用18种不同的广义线性模型与混合效应统计模型（均纳入系统发育距离作为协变量），量化了这些分子标记的等位基因与采样点及生境类型的关联程度。尽管上述模型检测到的与采样点相关联的SNPs数量始终更多，但同样成功识别出了与生境类型相关联的分子标记。尽管种群间存在广泛的基因流，但我们仍检测到显著的距离隔离（isolation-by-distance, 简称IBD）信号，这与种子扩散能力有限的植物类群的预期结果一致。不同生境类型种群间的对比分析显示，存在显著的环境隔离（isolation-by-environment, 简称IBE）趋势，该趋势掩盖了距离隔离信号。通过最大似然法估算不同生态型间的每代迁移者数量（Nem），进一步验证了环境隔离模式的存在。本研究结果表明，在帕拉莫（Páramo）这类快速演化的生态系统中，山地局域尺度的环境异质性对于驱动快速形态辐射演化以及维持多重适应性特征具有重要意义。