Fossil amber reveals springtails’ longstanding dispersal by social insects

Abstract

Dispersal is essential for terrestrial organisms living in disjunct habitats and constitutes a significant challenge for the evolution of wingless taxa. Springtails (Collembola), the sister-group of all insects (with dipluran), are reported since the Lower Devonian and thought to have originally been subterranean. The order Symphypleona is reported since the early Cretaceous with genera distributed on every continent, implying an ability to disperse over oceans although never reported in marine water contrary to other springtail orders. Despite being highly widespread, modern springtails are generally rarely reported in any kind of biotic association. Interestingly, the fossil record has provided occasional occurrences of Symphypleona attached by the antennae onto the bodies of larger arthropods. Here, we document the case of a ~16 Ma old fossil association: a winged termite and ant displaying not some, but 25 springtails attached or closely connected to the body. The collembola exhibit rare features for fossils, reflecting their courtship and phoretic behaviors. By observing the modes of attachment of springtails on different arthropods, the sex representation and ratios in springtail antennal anatomies in new and previously reported cases, we infer a likely mechanism for dispersal in Symphypleona. By revealing hidden evidence of modern springtail associations with other invertebrates such as ants and termites, new compelling assemblages of fossil springtails and the drastic increase of eusocial insects’ abundance over Cenozoic (ants/termites comprising more than the third of insects in Miocene amber), we stress that attachment with winged casts of ants and termites may have been a mechanism for the worldwide dispersal of this significant springtail lineage. Moreover, by comparing the general constraints applying to the other wingless soil-dwelling arthropods known to disperse through phoresy, we suggest biases in the collection and observation of phoretic Symphypleona related to their reflexive detachment and infer that this behavior continues today. The specific case of tree resin entrapment represents the (so far) only condition uncovering the actual dispersal mechanism of springtails - one of the oldest terrestrial arthropod lineages living today. Associations with soil-dwelling social insects over time would have been at the origin of this behavioural specialization.