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

Abstract

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 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 application of molecular data provides evidence of taxonomic oversplitting on the basis of morphology, clearly demonstrating the utility of an integrative species delimitation framework.

Genomics of cold adaptations in the Antarctic notothenioid fish radiation

“…The suborder Notothenioidei is a textbook example of a marine fish adaptive radiation, with notothenioids being the dominant fish group of the Southern Ocean, both in terms of species richness and biomass, comprising between 130-140 species [1][2][3] (Fig. 1A).…”

The mitochondrial genome of the red icefish (Channichthys rugosus) casts doubt on its species status

“…The available molecular data for the genus Channichthys does not allow us to perform a formal genetic species delimitation analysis as was recently done for Pogonophryne (Parker et al, 2022). Nevertheless, a comparison of the divergence between the two Channichthys mitochondrial genomes with the levels of between- and within-species sequence divergence in other notothenioid fishes can inform about the existence of one or several species within the genus.…”

“…Spodareva & Balushkin, 2014). This species richness within Pogonophryne could not be confirmed in a recent genetic analysis, which instead led to the synonymization of 24 out of 29 valid species (Parker, Dornburg, Struthers, Jones, & Near, 2022).…”

Species as a Heuristic: Reconciling Theory and Practice

“…In light of this, the discovery of new specimens, properties, or techniques may lead us to adjust our previous delimitations, but no decision can ever be based on all the potentially relevant or actually available data. The integration of different types of data is therefore key to improving the accuracy of species delimitation, especially in the face of low sampling or high uncertainty ( Pante et al 2015 ; Gratton et al 2016 ; Sukumaran and Knowles 2017 ; Federman et al 2018 ; Hundsdoerfer et al 2019 ; Parker et al 2021 ), consistent with the principles of both the USC and cohesion-based approaches. Decisions about what types of potentially available data or properties should be integrated in these analyses are strategic, in that they will be based on our existing knowledge about the group of organisms in question.…”