Multispecies Coalescent Species Delimitation: Conflating Populations with Species in the Grey Zone

The multispecies coalescent model underlies many approaches used for species delimitation. In previous work assessing the performance of species delimitation under this model, speciation was treated as an instantaneous event rather than as an extended process involving distinct phases of speciation initiation (structuring) and completion. Here, we use data under simulations that explicitly model speciation as an extended process rather than an instantaneous event and carry out species delimitation inference on these data under the multispecies coalescent. We show that the multispecies coalescent diagnoses genetic structure, not species, and that it does not statistically distinguish structure associated with population isolation vs. species boundaries. Because of the misidentification of population structure as putative species, our work raises questions about the practice of genome-based species discovery, with cascading consequences in other fields. Specifically, all fields that rely on species as units of analysis, from conservation biology to studies of macroevolutionary dynamics, will be impacted by inflated estimates of the number of species, especially as genomic resources provide unprecedented power for detecting increasingly finer-scaled genetic structure under the multispecies coalescent. As such, our work also represents a general call for systematic study to reconsider a reliance on genomic data alone. Until new methods are developed that can discriminate between structure due to population-level processes and that due to species boundaries, genomic-based results should only be considered a hypothesis that requires validation of delimited species with multiple data types, such as phenotypic and ecological information.