Phylogenomics of Elongate-Bodied Springtails Reveals Independent Transitions from Aboveground to Belowground Habitats in Deep Time

Abstract

Abstract Soil has become a major hotspot of biodiversity studies, yet the pattern and timing of the evolution of soil organisms are poorly known because of the scarcity of paleontological data. To overcome this limitation, we conducted a genome-based macroevolutionary study of an ancient, diversified, and widespread lineage of soil fauna, the elongate-bodied springtails (class Collembola, order Entomobryomorpha). To build the first robust backbone phylogeny of this previously refractory group, we sampled representatives of major higher taxa (6 out of 8 families, 11 out of 16 subfamilies) of the order with an emphasis on the most problematic superfamily Tomoceroidea, applied whole-genome sequencing methods, and compared the performance of different combinations of data sets (universal single-copy orthologs [USCO] vs. ultraconserved elements]) and modeling schemes. The fossil-calibrated timetree was used to reconstruct the evolution of body size, sensory organs, and pigmentation to establish a time frame of the ecomorphological divergences. The resultant trees based on different analyses were congruent in most nodes. Several discordant nodes were carefully evaluated by considering method fitness, morphological information, and topology test. The evaluation favored the well-resolved topology from analyses using USCO amino acid matrices and complex site-heterogeneous models (CAT$+$GTR and LG$+$PMSF (C60)). The preferred topology supports the monophyletic superfamily Tomoceroidea as an early-diverging lineage and a sister relationship between Entomobryoidea and Isotomoidea. The family Tomoceridae was recovered as monophyletic, whereas Oncopoduridae was recovered as paraphyletic, with Harlomillsia as a sister to Tomoceridae and hence deserving a separate family status as Harlomillsiidae Yu and Zhang fam. n. Ancestral Entomobryomorpha were reconstructed as surface-living, supporting independent origins of soil-living groups across the Paleozoic–Mesozoic, and highlighting the ancient evolutionary interaction between aboveground and belowground fauna. [Collembola; phylogenomics; soil-living adaptation; whole-genome sequencing.]