A Good Compromise: Rapid and Robust Species Proxies for Inventorying Biodiversity Hotspots Using the Terebridae (Gastropoda: Conoidea)

Devising a reproducible approach for species delimitation of hyperdiverse groups is an ongoing challenge in evolutionary biology. Speciation processes combine modes of passive and adaptive trait divergence requiring an integrative taxonomy approach to accurately generate robust species hypotheses. However, in light of the rapid decline of diversity on Earth, complete integrative approaches may not be practical in certain species-rich environments. As an alternative, we applied a two-step strategy combining ABGD (Automated Barcode Gap Discovery) and Klee diagrams, to balance speed and accuracy in producing primary species hypotheses (PSHs). Specifically, an ABGD/Klee approach was used for species delimitation in the Terebridae, a neurotoxin-producing marine snail family included in the Conoidea. Delimitation of species boundaries is problematic in the Conoidea, as traditional taxonomic approaches are hampered by the high levels of variation, convergence and morphological plasticity of shell characters. We used ABGD to analyze gaps in the distribution of pairwise distances of 454 COI sequences attributed to 87 morphospecies and obtained 98 to 125 Primary Species Hypotheses (PSHs). The PSH partitions were subsequently visualized as a Klee diagram color map, allowing easy detection of the incongruences that were further evaluated individually with two other species delimitation models, General Mixed Yule Coalescent (GMYC) and Poisson Tree Processes (PTP). GMYC and PTP results confirmed the presence of 17 putative cryptic terebrid species in our dataset. The consensus of GMYC, PTP, and ABGD/Klee findings suggest the combination of ABGD and Klee diagrams is an effective approach for rapidly proposing primary species proxies in hyperdiverse groups and a reliable first step for macroscopic biodiversity assessment.针对高度多样化类群的物种界定方法开发，始终是进化生物学领域的一项长期挑战。物种形成过程兼具被动与适应性性状分化两种模式，因此需要采用整合分类学（integrative taxonomy）方法，才能准确构建稳健可靠的物种类群假说。然而，鉴于全球生物多样性正快速丧失，在某些物种高度富集的生境中，完整的整合分类学方法往往难以实际应用。为此我们采用了结合自动条形码间隙发现法（Automated Barcode Gap Discovery，ABGD）与克利图（Klee diagrams）的两步分析策略，可在生成初始物种类群假说（primary species hypotheses，PSHs）的过程中兼顾速度与精度。具体而言，我们将ABGD/克利图分析方法应用于芋螺总科（Conoidea）下的笋螺科（Terebridae）物种界定工作，该科为产神经毒素的海洋螺类类群。芋螺总科的物种边界界定始终存在难题，这是因为传统分类方法受限于其壳体性状存在高度变异、趋同演化以及形态可塑性强等问题。我们通过ABGD分析了隶属于87个形态种（morphospecies）的454条细胞色素c氧化酶亚基I序列（COI sequences）的两两遗传距离分布间隙，最终得到98至125个初始物种类群假说。随后我们将初始物种类群假说的划分结果以克利图色彩图谱的形式可视化，可直观识别出其中的不一致之处，并另外采用两种物种界定模型——广义混合尤尔趋合模型（General Mixed Yule Coalescent，GMYC）与泊松树过程模型（Poisson Tree Processes，PTP）——对这些不一致之处逐一开展验证。GMYC与PTP的分析结果证实，本数据集中共存在17个推定的隐存笋螺类群。综合GMYC、PTP以及ABGD/克利图的分析结果可知，ABGD与克利图的组合方法可高效用于高度多样化类群的初始物种类群推定，同时也是开展宏观生物多样性评估的可靠前置步骤。