Phylogenomic Species Delimitation Dramatically Reduces Species Diversity in an Antarctic Adaptive Radiation

Application of genetic data to species delimitation often builds confidence in delimitations previously hypothesized using morphological, ecological, and geographic data and frequently yields recognition of previously undescribed cryptic diversity. However, a recent critique of genomic data-based species delimitation approaches is that they have the potential to conflate population structure with species diversity, resulting in taxonomic oversplitting. The need for an integrative approach to species delimitation, in which molecular, morphological, ecological, and geographic lines of evidence are evaluated together, is becoming increasingly apparent. Here, we integrate phylogenetic, population genetic, and coalescent analyses of genome-wide sequence data with investigation of variation in multiple morphological traits to delimit species within the Antarctic barbeled plunderfishes (Artedidraconidae: Pogonophryne). Pogonophryne currently comprises 29 valid species, most of which are distinguished solely by variation in the ornamentation of the mental barbel that projects from the lower jaw, a structure previously shown to vary widely within a single species. However, our genomic and phenotypic analyses result in a dramatic reduction in the number of distinct species recognized within the clade, providing evidence to support the recognition of no more than six species. We propose to synonymize 24 of the currently recognized species with five species of Pogonophryne. We find genomic and phenotypic evidence for a new species of Pogonophryne from specimens collected in the Ross Sea. Our findings represent a rare example in which the application of molecular data provides evidence of taxonomic oversplitting on the basis of morphology, clearly demonstrating the utility of an integrative species delimitation framework.

Automated summary

The application of genetic data to species delimitation can enhance confidence in previously hypothesized delimitations and uncover previously undescribed diversity. However, there is a concern that genetic data-based approaches may result in taxonomic oversplitting by confounding population structure with species diversity. An integrative approach, which evaluates molecular, morphological, ecological, and geographic evidence together, is increasingly recognized as necessary. In this study, the authors used phylogenetic, population genetic, and coalescent analyses of genome-wide sequence data, along with investigation of morphological traits, to delimit species within the Antarctic barbeled plunderfishes. Their findings support the recognition of fewer species than currently recognized and propose the synonymization of multiple species. The study highlights the utility of an integrative species delimitation framework and provides evidence of taxonomic oversplitting based on morphology.