Molecular phylogeny and trait evolution in an ancient terrestrial arthropod lineage: Systematic revision and implications for ecological divergence (Collembola, Tomocerinae)

Phylogenetic assessments of functional traits are important for mechanistically understanding the interactions between organisms and environments, but such practices are strongly limited by the availability of phylogenetic frameworks. The tomocerin springtails are an ancient, widespread and ecologically important group of terrestrial arthropods, whereas their phylogeny and trait evolution remained unaddressed. In the present study, we conducted the first comprehensive phylogenetic reconstruction of Tomocerinae, based on a multi-loci molecular dataset covering all major lineages within the subfamily, using Bayesian inference (BI), maximum-likelihood (ML) and maximum-parsimony (MP) approaches. Divergence time was estimated and ancestral character state reconstruction (ACSR) was performed to trace the evolutionary history of five ecomorphological traits correlated with sensory and locomotory functions. Our results support the monophyly of Tomocerinae, and indicate that current classification of Tomocerinae only partially reflects evolutionary relationships, notably the commonest and speciose genus Tomocerus is polyphyletic. The subfamily probably originated in Early Cretaceous and diversified in two Cretaceous and one Eocene radiation events. As indicated by the evolutionary patterns of functional traits, multiple ecological divergences took place during the diversification of Tomocerinae. The study suggests a potential underestimation of ecological divergence and functional diversity in terrestrial arthropods, calls for an update of present trait databases, and demonstrates the value of macroevolutionary knowledge for improving the trait-based ecology. In addition, Tomocerus, Tomocerina and Tritomurus are redefined, a new genus Yoshiicerus gen. n. and new subgenera Coloratomurus subgen. n., Ciliatomurus subgen. n., Striatomurus subgen. n. and Ocreatomurus subgen. n. are described in the appendix.

Automated summary

Phylogenetic reconstruction of Tomocerinae based on a multi-loci molecular dataset reveals the subfamily originated in the Early Cretaceous and underwent multiple radiation events in the Cretaceous and Eocene. Evolutionary patterns of functional traits suggest multiple ecological divergences during Tomocerinae diversification.