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Fossil amber reveals springtails’ longstanding dispersal by social insects

BACKGROUND: 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 Diplura), are reported since the Lower Devonian and are thought to have...

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Autores principales: Robin, Ninon, D’Haese, Cyrille, Barden, Phillip
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6869205/
https://www.ncbi.nlm.nih.gov/pubmed/31752661
http://dx.doi.org/10.1186/s12862-019-1529-6
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author Robin, Ninon
D’Haese, Cyrille
Barden, Phillip
author_facet Robin, Ninon
D’Haese, Cyrille
Barden, Phillip
author_sort Robin, Ninon
collection PubMed
description BACKGROUND: 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 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. RESULTS: 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 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. CONCLUSIONS: The 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.
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spelling pubmed-68692052019-12-12 Fossil amber reveals springtails’ longstanding dispersal by social insects Robin, Ninon D’Haese, Cyrille Barden, Phillip BMC Evol Biol Research Article BACKGROUND: 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 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. RESULTS: 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 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. CONCLUSIONS: The 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. BioMed Central 2019-11-21 /pmc/articles/PMC6869205/ /pubmed/31752661 http://dx.doi.org/10.1186/s12862-019-1529-6 Text en © The Author(s). 2019 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Robin, Ninon
D’Haese, Cyrille
Barden, Phillip
Fossil amber reveals springtails’ longstanding dispersal by social insects
title Fossil amber reveals springtails’ longstanding dispersal by social insects
title_full Fossil amber reveals springtails’ longstanding dispersal by social insects
title_fullStr Fossil amber reveals springtails’ longstanding dispersal by social insects
title_full_unstemmed Fossil amber reveals springtails’ longstanding dispersal by social insects
title_short Fossil amber reveals springtails’ longstanding dispersal by social insects
title_sort fossil amber reveals springtails’ longstanding dispersal by social insects
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6869205/
https://www.ncbi.nlm.nih.gov/pubmed/31752661
http://dx.doi.org/10.1186/s12862-019-1529-6
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