Beyond the sandy bottom: evolutionary and taxonomic insights into lizardfishes (Teleostei: Aulopiformes)

Lizardfishes (family Synodontidae) are benthic, carnivorous fishes that primarily inhabit tropical and subtropical sandy seabeds and play an important role in benthic ecosystem functioning. They are characterized by cylindrical bodies and large mouths and currently comprise 84 recognized species across four genera: Synodus, Harpadon, Saurida, and Trachinocephalus. However, the systematics of the Synodontidae-from higher-level classification to species-level taxonomy-has remained contentious since the family was established by Gill in 1861, highlighting the need for a robust phylogenetic framework for further revision. This study aimed to (1) reconstruct the phylogeny of the Synodontidae and related Aulopiformes, (2) test the monophyly of the family and its genera, and (3) assess species diversity and validity using an integrated approach.

We analyzed a multi-nuclear gene dataset (RH, RAG1, ZIC1, and ENC1) and complete mitochondrial genomes to investigate higher-level phylogenetic relationships, evolutionary origins, and divergence times within the Aulopiformes. Intra-familial relationships were examined using combined mitochondrial 12S and COI gene datasets, and species-level taxonomy was assessed using 1,688 COI sequences from public and newly generated data.

Higher-level phylogenetic analyses revealed that the Synodontidae is not monophyletic, however, its two subfamilies, Synodontinae and Harpadontinae, formed well-supported, distinct monophyletic groups, justifying their recognition at the family level. Among the four genera, only Harpadon and Trachinocephalus were monophyletic. Divergence time estimates suggest that the last common ancestor of the Synodontinae (=Synodontidae stat. nov.) originated in the Late Cretaceous, while the Harpadontinae (=Harpadontidae stat. nov.) emerged in the Eocene. Species delimitation based on compiled COI sequences, using Assemble Species by Automatic Partitioning (ASAP) and Bayesian Poisson Tree Processes (bPTP) methods and supported by additional evidence, identified 108 putative species among approximately 60 morphospecies, revealing substantial cryptic diversity.

This study clarifies the evolutionary history and taxonomy of the Synodontidae, supporting the reclassification of its subfamilies as distinct families and revealing extensive hidden species diversity. These findings provide a robust framework for future research on the systematics of lizardfishes and other aulopiform fishes.