Abstract
BackgroundDispersal 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 Diplura), are reported since the Lower Devonian and are thought to have originally been subterranean. The order Symphypleona is reported since the early Cretaceous with genera distributed on every continent. This distribution implies an ability to disperse over oceans, however symphypleonan Collembola have never been reported in marine water contrary to other springtail orders. Despite being highly widespread, modern springtails are 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.ResultsHere, we document the case of a ~ 16 Ma old fossil association: a winged termite and ant displaying not some, but 25 springtails attached or in close proximity to the body. The collembola exhibit rare features for fossils, reflecting their courtship and phoretic behaviours. 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 during the Cenozoic (ants/termites comprising more than a third of insects in Miocene amber), we stress that attachment on winged castes 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 behaviour continues today.ConclusionsThe specific case of tree resin entrapment represents the (so far) only condition uncovering the phoretic dispersal mechanism of springtails - one of the oldest terrestrial arthropod lineages living today.
Highlights
Dispersal is essential for terrestrial organisms living in disjunct habitats and constitutes a significant challenge for the evolution of wingless taxa
By revealing hidden evidence of modern springtails associated with other invertebrates such as ants and termites, new cases of fossil inclusions of Symphypleona and termites, and pointing out the drastic increase of eusocial soil insects’ ecological impact over Cenozoic, we infer that association with winged castes of ants and termites may have been a mechanism for the worldwide dispersal of these springtails
Despite tens of thousands of known insect fossil inclusions, our report corresponds to about 6% of all the previous occurrences of individual springtails reported in Dominican amber and consists of two taxa out of twelve described in total [32,33,34]
Summary
Order Symphypleona Börner 1901 [25]. Suborder Sminthuridida Börner 1986 [26]. 1, 2a, d) are laterally orientated onto the sclerotized anterior margin of the left hindwing (close to the wing scale) and right forewing (distally), their right and left antennae respectively overlaying this margin This lateral posture is observed in the attachment of the single specimen found clasping onto the ant, with the left antenna overlaying the first tarsi of the ant hind leg One specimen clearly exhibits the first undisputable clasping organ in the fossil record (Fig. 2f, 3d, SM1– 2), a synapomorphy of Sminthurididae and major innovative feature allowing their specific mating behaviour This organ, specific to males, is involved in a “dancing” courtship behaviour of sminthuridids, the male dragging the female onto the spot of his sperm drop by grasping her antennae [30, 31].
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