Data_Sheet_5_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.

物种多样性的起源机制，以及异域分化（allopatric divergence）与生态分化（ecological divergence）的相对贡献，始终是进化生物学与生态学领域最具持续性的核心议题之一。本研究针对新热带高山植物复合体杯菊属（Espeletia，俗称frailejones），探究生态分化是否推动了其物种多样化进程。该属是目前已报道的物种多样化速率最高的类群之一，其分布区位于全球演化最快的生物多样性热点区域——帕拉莫（Páramo，海拔约2800-4700米的新热带高山草原）。本研究的核心目标为：通过量化全基因组范围的生态分化模式，明确生态因子在杯菊属复合体的物种分化过程中是否发挥调控作用。本研究采用测序分型（Genotyping by Sequencing）技术，对安第斯山脉北部6个采样点中共存的3类最具代表性且生态位分化显著的生态型（占据特定生境的独特形态型）的162份样本进行了基因分型分析；这三类生态型分别为：具茎干的云雾林种群、生于防风且灌溉充足洼地的具茎干种群，以及生于多风干旱坡地的无茎干种群。本研究检测到较高的多态性水平，共获得1273个单核苷酸多态性位点（SNPs），这些位点可明确9个遗传簇之间的演化关系。研究采用18种纳入系统发育距离校正的广义线性模型与混合效应统计模型，量化了这些分子标记与采样点及生境类型的等位基因关联模式；尽管上述模型均检测到更多与采样点相关联的SNPs，但同样识别出了与生境类型显著关联的分子标记。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, IBD）信号，这与种子传播能力有限的植物类群的预期演化模式一致。不同生境类型种群间的对比分析显示，存在环境隔离（isolation-by-environment, IBE）趋势，该趋势掩盖了距离隔离信号。对生态型间每代迁移个体数（Nem）的最大似然估计结果，进一步验证了环境隔离模式。本研究结果阐明了山地局域尺度的环境异质性，对于帕拉莫这类快速演化生态系统中快速形态辐射演化与多重适应性维持的重要意义。