The oldest continuous association between astigmatid mites and termites preserved in Cretaceous amber reveals the evolutionary significance of phoresy.

BACKGROUND: Among minute-sized and wingless arthropods, astigmatid mites stand out for their diverse range of symbiotic associations (parasitic, neutral and mutualistic), with both invertebrate and vertebrate hosts. When inhabiting discontinuous and ephemeral environments, astigmatid mites adapt their life cycle to produce a phoretic heteromorphic nymph. When feeding resources are depleted, phoretic nymphs disperse to new habitats through phoresy, attaching to a larger animal which transports them to new locations. This dispersal strategy is crucial for accessing patchy resources, otherwise beyond the reach of these minute arthropods. In Astigmata, the phoretic nymph is highly specialized for dispersal, equipped with an attachment organ and lacking a mouth and pharynx. Despite the common occurrence of phoretic associations in modern mites, their evolutionary origins remain poorly understood. Among Astigmata, the family Schizoglyphidae represents an early derivative lineage with phoretic tritonymphs; however, our knowledge of this family is limited to a single observation. RESULTS: Here, we report the oldest biotic association of arthropods fossilised in amber (~ 130 Ma, Lebanon): an alate termite with 16 phoretic tritonymphs of Schizoglyphidae (Plesioglyphus lebanotermi gen. et sp. n.). The mites are primarily attached to the membranes of the host's hindwings, using their attachment organs, pretarsal claws and tarsal setae. Additionally, we report new modern phoretic tritonymphs of this same family, on one of the earliest lineages of termites. These data collectively indicate that schizoglyphid-termite associations represent the oldest continuous mite-host associations. Notably, phoretic schizoglyphids retain a distinct mouth and pharynx, whereas these structures are absent in the modern phoretic stages of non-schizoglyphid Astigmata. CONCLUSION: The discovery of Schizoglyphidae mites in Lebanese amber represents the oldest known continuous association between acariform mites and their hosts. This finding demonstrates the long-term evolutionary significance of phoresy in Astigmata, evidencing a relationship sustained for over 130 Ma. It indicates that these early mites lived inside termite nests as inquilines and used alate termites for dispersal. This ancient association offers key insights into the coevolution of both mites and termites, highlighting a potential for the future discoveries of similar mites. This fossil -a stem-group Astigmata- is important for the accurate calibration of acariform mite phylogenies, advancing our understanding of these mites evolutionary history.