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Fossil amber reveals springtails' longstanding dispersal by social insects
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...
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Published in: | BMC ecology and evolution 2019-11, Vol.19 (1), p.213-213, Article 213 |
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description | 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.
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.
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. |
doi_str_mv | 10.1186/s12862-019-1529-6 |
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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.
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.</description><identifier>ISSN: 1471-2148</identifier><identifier>EISSN: 1471-2148</identifier><identifier>EISSN: 2730-7182</identifier><identifier>DOI: 10.1186/s12862-019-1529-6</identifier><identifier>PMID: 31752661</identifier><language>eng</language><publisher>England: BioMed Central Ltd</publisher><subject>Amber ; Animals ; Antennae ; Ants ; Aquatic insects ; Arthropoda ; Arthropods ; Arthropods - anatomy & histology ; Arthropods - classification ; Arthropods - physiology ; Biodiversity and Ecology ; Biological Evolution ; Castes ; Cenozoic ; Collembola ; Courtship ; Cretaceous ; Devonian ; Dispersal ; Dispersion ; Dominican amber ; Ecosystem ; Entrapment ; Environmental Sciences ; Eusociality ; Fossils ; Greek civilization ; Habitats ; Insects ; Invertebrates ; Isoptera ; Male ; Miocene ; Oceans ; Phoresy ; Social insects ; Soil ; Springtails ; Symphypleona ; Termites ; Terrestrial environments</subject><ispartof>BMC ecology and evolution, 2019-11, Vol.19 (1), p.213-213, Article 213</ispartof><rights>COPYRIGHT 2019 BioMed Central Ltd.</rights><rights>2019. This work is licensed under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2019. This work is licensed under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. 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.</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><rights>The Author(s). 2019</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c722t-89a9c7097eb6a83b4ea110a4783df6d26fcf42117b6046b6b0d8382f819d2ab53</citedby><cites>FETCH-LOGICAL-c722t-89a9c7097eb6a83b4ea110a4783df6d26fcf42117b6046b6b0d8382f819d2ab53</cites><orcidid>0000-0002-1756-3171 ; 0000-0001-6065-0927</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.proquest.com/docview/2546687875/fulltextPDF?pq-origsite=primo$$EPDF$$P50$$Gproquest$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.proquest.com/docview/2328235024?pq-origsite=primo$$EHTML$$P50$$Gproquest$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,25753,27924,27925,37012,37013,44590,53791,53793,75126</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31752661$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-02378619$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Robin, Ninon</creatorcontrib><creatorcontrib>D'Haese, Cyrille</creatorcontrib><creatorcontrib>Barden, Phillip</creatorcontrib><title>Fossil amber reveals springtails' longstanding dispersal by social insects</title><title>BMC ecology and evolution</title><addtitle>BMC Evol Biol</addtitle><description>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.
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.
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.</description><subject>Amber</subject><subject>Animals</subject><subject>Antennae</subject><subject>Ants</subject><subject>Aquatic insects</subject><subject>Arthropoda</subject><subject>Arthropods</subject><subject>Arthropods - anatomy & histology</subject><subject>Arthropods - classification</subject><subject>Arthropods - physiology</subject><subject>Biodiversity and Ecology</subject><subject>Biological Evolution</subject><subject>Castes</subject><subject>Cenozoic</subject><subject>Collembola</subject><subject>Courtship</subject><subject>Cretaceous</subject><subject>Devonian</subject><subject>Dispersal</subject><subject>Dispersion</subject><subject>Dominican amber</subject><subject>Ecosystem</subject><subject>Entrapment</subject><subject>Environmental Sciences</subject><subject>Eusociality</subject><subject>Fossils</subject><subject>Greek civilization</subject><subject>Habitats</subject><subject>Insects</subject><subject>Invertebrates</subject><subject>Isoptera</subject><subject>Male</subject><subject>Miocene</subject><subject>Oceans</subject><subject>Phoresy</subject><subject>Social insects</subject><subject>Soil</subject><subject>Springtails</subject><subject>Symphypleona</subject><subject>Termites</subject><subject>Terrestrial environments</subject><issn>1471-2148</issn><issn>1471-2148</issn><issn>2730-7182</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>PIMPY</sourceid><sourceid>DOA</sourceid><recordid>eNp9kktv1DAUhSMEoqXwA9igSCxoFym-TuLHBmlUtXTQSEg81ta146QeZeLBzozov8dhSmkqhLKwdfOd4-vrk2WvgZwDCPY-AhWMFgRkATWVBXuSHUPFoaBQiacP9kfZixjXhAAXFJ5nRyXwmjIGx9mnKx-j63PcaBvyYPcW-5jHbXBDN6Lr47u890MXRxyaVMobF7c2ROxzfZtHb1zauSFaM8aX2bM2ie2ru_Uk-351-e3iulh9_ri8WKwKwykdCyFRGk4kt5qhKHVlEYBgxUXZtKyhrDVtRQG4ZqRimmnSiFLQVoBsKOq6PMmWB9_G41qlTjcYbpVHp34XfOgUhtGZ3iqwFW0bojGtlRUoJdaoSUutlEYbnrw-HLy2O72xjbHDGLCfmc7_DO5GdX6vmGCSkqmZs4PBzSPZ9WKlphqhJRcM5B4Se3p3WPA_djaOauOisX2Pg_W7qOj0LJIDm_p6-whd-10Y0lgVrSvGBBe8_i9VUkHLmtDqL9VhGokbWp9uYqaj1YIRXnIGQiTq_B9U-hq7ccYPtnWpPhOczQSJGe3PscNdjGr59cuchQNrQopbsO39qICoKcrqEGWVoqymKCuWNG8ePs294k92y1-bretb</recordid><startdate>20191121</startdate><enddate>20191121</enddate><creator>Robin, Ninon</creator><creator>D'Haese, Cyrille</creator><creator>Barden, Phillip</creator><general>BioMed Central Ltd</general><general>BioMed Central</general><general>BMC</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>ISR</scope><scope>3V.</scope><scope>7QP</scope><scope>7QR</scope><scope>7SN</scope><scope>7SS</scope><scope>7TK</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M7P</scope><scope>P64</scope><scope>PATMY</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>1XC</scope><scope>VOOES</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0002-1756-3171</orcidid><orcidid>https://orcid.org/0000-0001-6065-0927</orcidid></search><sort><creationdate>20191121</creationdate><title>Fossil amber reveals springtails' longstanding dispersal by social insects</title><author>Robin, Ninon ; D'Haese, Cyrille ; Barden, Phillip</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c722t-89a9c7097eb6a83b4ea110a4783df6d26fcf42117b6046b6b0d8382f819d2ab53</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Amber</topic><topic>Animals</topic><topic>Antennae</topic><topic>Ants</topic><topic>Aquatic insects</topic><topic>Arthropoda</topic><topic>Arthropods</topic><topic>Arthropods - anatomy & histology</topic><topic>Arthropods - classification</topic><topic>Arthropods - physiology</topic><topic>Biodiversity and Ecology</topic><topic>Biological Evolution</topic><topic>Castes</topic><topic>Cenozoic</topic><topic>Collembola</topic><topic>Courtship</topic><topic>Cretaceous</topic><topic>Devonian</topic><topic>Dispersal</topic><topic>Dispersion</topic><topic>Dominican amber</topic><topic>Ecosystem</topic><topic>Entrapment</topic><topic>Environmental Sciences</topic><topic>Eusociality</topic><topic>Fossils</topic><topic>Greek civilization</topic><topic>Habitats</topic><topic>Insects</topic><topic>Invertebrates</topic><topic>Isoptera</topic><topic>Male</topic><topic>Miocene</topic><topic>Oceans</topic><topic>Phoresy</topic><topic>Social insects</topic><topic>Soil</topic><topic>Springtails</topic><topic>Symphypleona</topic><topic>Termites</topic><topic>Terrestrial environments</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Robin, Ninon</creatorcontrib><creatorcontrib>D'Haese, Cyrille</creatorcontrib><creatorcontrib>Barden, Phillip</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Science (Gale in Context)</collection><collection>ProQuest Central (Corporate)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Neurosciences Abstracts</collection><collection>ProQuest_Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni)</collection><collection>ProQuest Central</collection><collection>Agricultural & Environmental Science Collection</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>ProQuest Natural Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>PML(ProQuest Medical Library)</collection><collection>ProQuest Biological Science Journals</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Environmental Science Database</collection><collection>Publicly Available Content Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>Environmental Science Collection</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>Hyper Article en Ligne (HAL)</collection><collection>Hyper Article en Ligne (HAL) (Open Access)</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>BMC ecology and evolution</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Robin, Ninon</au><au>D'Haese, Cyrille</au><au>Barden, Phillip</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Fossil amber reveals springtails' longstanding dispersal by social insects</atitle><jtitle>BMC ecology and evolution</jtitle><addtitle>BMC Evol Biol</addtitle><date>2019-11-21</date><risdate>2019</risdate><volume>19</volume><issue>1</issue><spage>213</spage><epage>213</epage><pages>213-213</pages><artnum>213</artnum><issn>1471-2148</issn><eissn>1471-2148</eissn><eissn>2730-7182</eissn><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 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.
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.
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.</abstract><cop>England</cop><pub>BioMed Central Ltd</pub><pmid>31752661</pmid><doi>10.1186/s12862-019-1529-6</doi><tpages>1</tpages><orcidid>https://orcid.org/0000-0002-1756-3171</orcidid><orcidid>https://orcid.org/0000-0001-6065-0927</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Amber Animals Antennae Ants Aquatic insects Arthropoda Arthropods Arthropods - anatomy & histology Arthropods - classification Arthropods - physiology Biodiversity and Ecology Biological Evolution Castes Cenozoic Collembola Courtship Cretaceous Devonian Dispersal Dispersion Dominican amber Ecosystem Entrapment Environmental Sciences Eusociality Fossils Greek civilization Habitats Insects Invertebrates Isoptera Male Miocene Oceans Phoresy Social insects Soil Springtails Symphypleona Termites Terrestrial environments |
title | Fossil amber reveals springtails' longstanding dispersal by social insects |
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