Abstract
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.
Highlights
The practice of identifying biological diversity at the species level, referred to as species delimitation, usually consists of first proposing a primary partition of species hypotheses, and testing these hypotheses
The C oxidase subunit mitochondrial region (COI) alignment was analyzed with ABGD to propose partitions with variable numbers of Primary Species Hypotheses (PSHs), depending on the prior threshold and initial or recursive analyses
Based on the COI gene only, General Mixed Yule Coalescent (GMYC) and Poisson Tree Processes (PTP) analyses contained a variable number of clusters, mostly overlapping with ABGD: 110 in the GMYC single threshold, 130 in the GMYC multiple threshold and 112 in the PTP (Fig. S1–S3)
Summary
The practice of identifying biological diversity at the species level, referred to as species delimitation, usually consists of first proposing a primary partition of species hypotheses, and testing these hypotheses. When novel taxa are almost completely unknown, such as in hotspot habitats of high diversity as found in recent explorations of the deep-sea [1,2] or forest canopy [3], a hypothesis-driven approach is not possible as primary species hypotheses (PSHs) are not available for such groups. The analysis required to obtain robust species delimitations using a fully integrative taxonomy approach can be at times unattainable for a number of reasons such as: (1) technical, e.g. in hyperdiverse groups, characterized by an exceedingly high species number, relatively few available variable genes and inapplicable morphological characters; (2) economical, e.g. lack of funds to obtain and analyze sufficient specimens and characters; or (3) strategic, the need to rapidly assess the diversity of a group or an environment that is potentially threatened. Carstens and colleagues recently reviewed several species delimitation methods and suggest species delimitations are robust when several delimitation analyses are applied and are congruent [21]
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