Genome-wide species delimitation analyses of a silverside fish species complex in central Mexico indicate taxonomic over-splitting

Abstract

Background Delimiting species across a speciation continuum is a complex task, as the process of species origin is not generally instantaneous. The use of genome-wide data provides unprecedented resolution to address convoluted species delimitation cases, often unraveling cryptic diversity. However, because genome-wide approaches based on the multispecies coalescent model are known to confound population structure with species boundaries, often resulting in taxonomic over-splitting, it has become increasingly evident that species delimitation research must consider multiple lines of evidence. In this study, we used phylogenomic, population genomic, and coalescent-based species delimitation approaches, and examined those in light of morphological and ecological information, to investigate species numbers and boundaries comprising the Chirostoma “humboltianum group” (family Atherinidae). The humboltianum group is a taxonomically controversial species complex where previous morphological and mitochondrial studies produced conflicting species delimitation outcomes. We generated ddRADseq data for 77 individuals representing the nine nominal species in the group, spanning their distribution range in the central Mexican plateau. Results Our results conflict with the morphospecies and ecological delimitation hypotheses, identifying four independently evolving lineages organized in three geographically cohesive clades: (i) chapalae and sphyraena groups in Lake Chapala, (ii) estor group in Lakes Pátzcuaro and Zirahuén, and (iii) humboltianum sensu stricto group in Lake Zacapu and Lerma river system. Conclusions Overall, our study provides an atypical example where genome-wide analyses delineate fewer species than previously recognized on the basis of morphology. It also highlights the influence of the geological history of the Chapala-Lerma hydrological system in driving allopatric speciation in the humboltianum group.

Acknowledging more biodiversity without more species

“…In parallel, widely used species delimitation algorithms (such as the multispecies coalescent) might statistically define every population as a distinct “species” provided sufficient genetic resolution, even those that clearly lack reproductive isolation ( 41 – 43 ). Furthermore, morphological or ecological differences may reflect processes other than evolutionary divergence and speciation, as they are greatly influenced by phenotypic plasticity and local adaptation ( 44 , 45 ). The reported differences may not even be meaningful.…”

Unsupervised Machine Learning for Species Delimitation, Integrative Taxonomy, and Biodiversity Conservation

“…The first is the concept of taxonomic inflation, particularly when relying on limited molecular datasets and phylogenetic delimitation (Zachos et al, 2013). Yet, numerous recent studies demonstrate the potential for taxonomic reduction from integrated datasets (Freitas et al, 2020;Hundsdoerfer et al, 2019;Parker et al, 2022;Piñeros et al, 2022;Pyron et al, 2016). Second is the concern that common evolutionary models will over-split species based on population-level divergence (Sukumaran and Knowles, 2017).…”

“…I term this the "taxonomic convergence hypothesis" and suggest that UML methods such as SuperSOMs can facilitate this systematic unification of species delimitation and integrative taxonomy. This can overcome the potential issue of over-splitting (Parker et al, 2022;Piñeros et al, 2022), and should robust and stable estimates of species boundaries in all but the most difficult cases (O'Connell et al, 2022;Eric Pante et al, 2015).…”

Mitogenomic Architecture and Phylogenetic Relationship of European Barracuda, Sphyraena sphyraena (Teleostei: Sphyraenidae) from the Atlantic Ocean

“…Nevertheless, data on the nuclear and mitochondrial genetics of Sphyraenidae species has been generated sporadically [28][29][30][31][32][33][34][35][36]. More recently, comprehensive genome-wide analyses of Sphyraenidae species have been initiated to uncover cryptic diversity, employing phylogenomic, population genomic, and coalescent-based species delimitation approaches while considering morphological and ecological data [37]. However, our understanding of barracudas based on mitochondrial genomes is still fragmentary.…”