Multispecies coalescent delimits structure, not species

Abstract

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. multispecies coalescent | species delimitation | coalescent theory M ajor advances in understanding the patterns of biodiversity and the processes that generate those patterns are being made with increasing rapidity, scope, and scale, as we study species across the tree of life (e.g., refs. 1-3). These advances take the boundaries of the species that constitute their fundamental units as known. Identification of these boundaries-that is, species delimitation-currently is making increasing use of genomic data under statistical model-based approaches, typically using the multispecies coalescent model (4), as opposed to traditional taxonomic work based on phenotypic data. Coupled with technological advances for collecting genomic datasets across many individuals per putative species, inference under the multispecies coalescent model provides us with considerable power in identifying recently diverged taxon boundaries. For example, simulations show that we can delimit lineages with extremely short divergence times, as with the popular program BPP (Bayesian Phylogenetics and Phylogeography) (5). However, these remarkable gains have also paradoxically given rise to a new challenge-determining whether what we delimited genetically represents lineages isolated due to speciation or simply within...

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