Data from: Host-specialist lineages dominate the adaptive radiation of reef coral endosymbionts

Bursts in species diversification are well documented among animals and plants, yet few studies have assessed recent adaptive radiations of eukaryotic microbes. Consequently, we examined the radiation of the most ecologically dominant group of endosymbiotic dinoflagellates found in reef-building corals, Symbiodinium Clade C, using nuclear ribosomal (ITS2), chloroplast (psbAncr), and multilocus microsatellite genotyping. Through a hierarchical analysis of high-resolution genetic data, we assessed whether ecologically distinct Symbiodinium, differentiated by seemingly equivocal rDNA sequence differences, are independent species lineages. We also considered the role of host specificity in Symbiodinium speciation and the correspondence between endosymbiont diversification and Caribbean paleo-history. According to phylogenetic, biological, and ecological species concepts, Symbiodinium Clade C comprises many distinct species. Although regional factors contributed to population-genetic structuring of these lineages, Symbiodinium diversification was mainly driven by host specialization. By combining patterns of the endosymbiont's host specificity, water depth distribution, and phylogeography with paleo-historical signals of climate change, we inferred that present-day species diversity on Atlantic coral reefs stemmed mostly from a post-Miocene adaptive radiation. Host-generalist progenitors spread, specialized, and diversified during the ensuing epochs of prolonged global cooling and change in reef-faunal assemblages. Our evolutionary reconstruction thus suggests that Symbiodinium undergoes “boom and bust” phases in diversification and extinction during major climate shifts.

物种多样化的爆发现象在动植物类群中已有大量文献记载，但针对真核微生物（eukaryotic microbes）近期适应性辐射（adaptive radiation）的研究却寥寥无几。有鉴于此，我们针对造礁珊瑚（reef-building corals）中生态占比最高的内共生甲藻（endosymbiotic dinoflagellates）类群——虫黄藻属C分支（Symbiodinium Clade C）的辐射演化展开研究，采用细胞核核糖体（ITS2）、叶绿体（psbAncr）及多位点微卫星基因分型（multilocus microsatellite genotyping）技术进行分析。通过对高分辨率遗传数据进行层级化分析，我们探究了那些仅凭核糖体DNA（rDNA）序列差异难以区分、但生态位显著不同的虫黄藻是否属于独立的物种谱系。此外，我们还探讨了宿主特异性（host specificity）在虫黄藻物种形成（speciation）过程中的作用，以及内共生体多样化与加勒比古地质历史之间的对应关系。基于系统发育（phylogenetic）、生物学及生态学物种概念，虫黄藻属C分支包含多个独立的物种。尽管区域因素对这些谱系的群体遗传结构（population-genetic structuring）形成存在影响，但虫黄藻的多样化主要由宿主特化（host specialization）所驱动。我们结合该内共生体的宿主特异性、水深分布格局及系统地理学（phylogeography）特征，与古气候变迁的地质历史信号进行整合分析，推断大西洋珊瑚礁现今的物种多样性主要源自中新世（Miocene）之后的适应性辐射事件。在随后的长期全球变冷及珊瑚礁动物群（reef-faunal）组成发生改变的地质时期，具有广谱宿主适应性的祖先类群不断扩散、发生特化并实现多样化。因此，我们的演化重建（evolutionary reconstruction）结果表明，虫黄藻在重大气候变迁过程中，会经历多样化与灭绝交替的"boom and bust"（兴衰循环）阶段。