Viviparity in the dermapteran Arixenia esau: respiration inside mother’s body requires both maternal and larval contribution
Earwigs (Dermaptera) use different strategies to increase their reproductive success. Most species lay eggs; however, viviparity of the matrotrophic type has been reported in two groups: Hemimeridae and Arixeniidae. In Arixeniidae, offspring develop in two separate places: inside an ovary (the intra...
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description | Earwigs (Dermaptera) use different strategies to increase their reproductive success. Most species lay eggs; however, viviparity of the matrotrophic type has been reported in two groups: Hemimeridae and Arixeniidae. In Arixeniidae, offspring develop in two separate places: inside an ovary (the intraovarian phase) and within a uterus (the intrauterine phase). Both morphological and physiological aspects of viviparity in Arixeniidae have begun to be unraveled only recently. Here, we characterize how the first instar larvae of
Arixenia esau
, developing inside the mother’s reproductive system, manage respiration and gas exchange. Using modern light and electron microscopy techniques as well as immunological approach, we provide a detailed account of the maternal and larval tissue interactions during the intrauterine development. We demonstrate that respiration in the
Arixenia
first instar larvae relies on the extensive tracheal system of the mother as well as a respiratory pigment (hemocyanin) present within the body cavity of the larvae. Our results indicate that the larval fat body tissue is the likely place of the hemocyanin synthesis. Our study shows that characteristic cone-shaped lobes of the outgrowths located on the larval abdomen are a part of a placenta-like organ and mediate the gas exchange between the maternal and larval organisms. Based on the obtained results, we propose that
Arixenia esau
evolved a unique biphasic system supporting respiration of the first instar larvae during their development inside the mother’s reproductive tract. |
doi_str_mv | 10.1007/s00709-019-01402-1 |
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Arixenia esau
, developing inside the mother’s reproductive system, manage respiration and gas exchange. Using modern light and electron microscopy techniques as well as immunological approach, we provide a detailed account of the maternal and larval tissue interactions during the intrauterine development. We demonstrate that respiration in the
Arixenia
first instar larvae relies on the extensive tracheal system of the mother as well as a respiratory pigment (hemocyanin) present within the body cavity of the larvae. Our results indicate that the larval fat body tissue is the likely place of the hemocyanin synthesis. Our study shows that characteristic cone-shaped lobes of the outgrowths located on the larval abdomen are a part of a placenta-like organ and mediate the gas exchange between the maternal and larval organisms. Based on the obtained results, we propose that
Arixenia esau
evolved a unique biphasic system supporting respiration of the first instar larvae during their development inside the mother’s reproductive tract.</description><identifier>ISSN: 0033-183X</identifier><identifier>EISSN: 1615-6102</identifier><identifier>DOI: 10.1007/s00709-019-01402-1</identifier><identifier>PMID: 31218520</identifier><language>eng</language><publisher>Vienna: Springer Vienna</publisher><subject>Animal reproduction ; Animals ; Biomedical and Life Sciences ; Breeding success ; Cell Biology ; Eggs ; Electron microscopy ; Fat body ; Gas exchange ; Insecta - physiology ; Larvae ; Life Sciences ; Original ; Original Article ; Placenta ; Plant Sciences ; Reproductive system ; Respiration ; Uterus ; Viviparity ; Viviparity, Nonmammalian ; Zoology</subject><ispartof>Protoplasma, 2019-11, Vol.256 (6), p.1573-1584</ispartof><rights>The Author(s) 2019</rights><rights>Protoplasma is a copyright of Springer, (2019). All Rights Reserved. © 2019. This work is published 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><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c474t-bda85d7773b8a39924817c360f65d0c3cda6d6374ed2010bcc9c323a8fd714d23</citedby><cites>FETCH-LOGICAL-c474t-bda85d7773b8a39924817c360f65d0c3cda6d6374ed2010bcc9c323a8fd714d23</cites><orcidid>0000-0002-1606-8339</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1007/s00709-019-01402-1$$EPDF$$P50$$Gspringer$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1007/s00709-019-01402-1$$EHTML$$P50$$Gspringer$$Hfree_for_read</linktohtml><link.rule.ids>230,314,780,784,885,27924,27925,41488,42557,51319</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31218520$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Jaglarz, Mariusz K.</creatorcontrib><creatorcontrib>Tworzydlo, Waclaw</creatorcontrib><creatorcontrib>Rak, Agnieszka</creatorcontrib><creatorcontrib>Kotula-Balak, Malgorzata</creatorcontrib><creatorcontrib>Sekula, Malgorzata</creatorcontrib><creatorcontrib>Bilinski, Szczepan M.</creatorcontrib><title>Viviparity in the dermapteran Arixenia esau: respiration inside mother’s body requires both maternal and larval contribution</title><title>Protoplasma</title><addtitle>Protoplasma</addtitle><addtitle>Protoplasma</addtitle><description>Earwigs (Dermaptera) use different strategies to increase their reproductive success. Most species lay eggs; however, viviparity of the matrotrophic type has been reported in two groups: Hemimeridae and Arixeniidae. In Arixeniidae, offspring develop in two separate places: inside an ovary (the intraovarian phase) and within a uterus (the intrauterine phase). Both morphological and physiological aspects of viviparity in Arixeniidae have begun to be unraveled only recently. Here, we characterize how the first instar larvae of
Arixenia esau
, developing inside the mother’s reproductive system, manage respiration and gas exchange. Using modern light and electron microscopy techniques as well as immunological approach, we provide a detailed account of the maternal and larval tissue interactions during the intrauterine development. We demonstrate that respiration in the
Arixenia
first instar larvae relies on the extensive tracheal system of the mother as well as a respiratory pigment (hemocyanin) present within the body cavity of the larvae. Our results indicate that the larval fat body tissue is the likely place of the hemocyanin synthesis. Our study shows that characteristic cone-shaped lobes of the outgrowths located on the larval abdomen are a part of a placenta-like organ and mediate the gas exchange between the maternal and larval organisms. Based on the obtained results, we propose that
Arixenia esau
evolved a unique biphasic system supporting respiration of the first instar larvae during their development inside the mother’s reproductive tract.</description><subject>Animal reproduction</subject><subject>Animals</subject><subject>Biomedical and Life Sciences</subject><subject>Breeding success</subject><subject>Cell Biology</subject><subject>Eggs</subject><subject>Electron microscopy</subject><subject>Fat body</subject><subject>Gas exchange</subject><subject>Insecta - physiology</subject><subject>Larvae</subject><subject>Life Sciences</subject><subject>Original</subject><subject>Original Article</subject><subject>Placenta</subject><subject>Plant Sciences</subject><subject>Reproductive system</subject><subject>Respiration</subject><subject>Uterus</subject><subject>Viviparity</subject><subject>Viviparity, Nonmammalian</subject><subject>Zoology</subject><issn>0033-183X</issn><issn>1615-6102</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>C6C</sourceid><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><recordid>eNp9kcFu1DAQhi1ERZfCC3CoLHEOjO0k9nKoVFWlIFXi0lbcrInt7bra2KmdrLoXxGvwen0SvGxp6YWD7bHmm3_G_gl5x-ADA5Afc9lgXgHbrhp4xV6QGWtZU7UM-EsyAxCiYkp83yevc74BgIZD84rsC8aZKvGM_Ljyaz9g8uOG-kDHpaPWpR6H0SUM9Dj5Oxc8Updx-kSTy4NPOPoYCp29dbSPpSbd__yVaRftpiC3ky9cuY1L2mPRCbiiGCxdYVqX0MQwJt9NW5U3ZG-Bq-zePpwH5PLz6cXJl-r829nXk-PzytSyHqvOomqslFJ0CsV8zmvFpBEtLNrGghHGYmtbIWtnOTDojJkbwQWqhZWstlwckKOd7jB1vbPGlRFwpYfke0wbHdHr55ngl_o6rnWryo8pWQTePwikeDu5POqbOG1fljXntWCyFQoKxXeUSTHn5BaPHRjorWd655kunuk_nmlWig7_ne2x5K9JBRA7IJdUuHbpqfd_ZH8DXk-mtw</recordid><startdate>20191101</startdate><enddate>20191101</enddate><creator>Jaglarz, Mariusz K.</creator><creator>Tworzydlo, Waclaw</creator><creator>Rak, Agnieszka</creator><creator>Kotula-Balak, Malgorzata</creator><creator>Sekula, Malgorzata</creator><creator>Bilinski, Szczepan M.</creator><general>Springer Vienna</general><general>Springer Nature B.V</general><scope>C6C</scope><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>3V.</scope><scope>7RV</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>88G</scope><scope>8AO</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB0</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M2M</scope><scope>M7P</scope><scope>NAPCQ</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PSYQQ</scope><scope>Q9U</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-1606-8339</orcidid></search><sort><creationdate>20191101</creationdate><title>Viviparity in the dermapteran Arixenia esau: respiration inside mother’s body requires both maternal and larval contribution</title><author>Jaglarz, Mariusz K. ; 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Most species lay eggs; however, viviparity of the matrotrophic type has been reported in two groups: Hemimeridae and Arixeniidae. In Arixeniidae, offspring develop in two separate places: inside an ovary (the intraovarian phase) and within a uterus (the intrauterine phase). Both morphological and physiological aspects of viviparity in Arixeniidae have begun to be unraveled only recently. Here, we characterize how the first instar larvae of
Arixenia esau
, developing inside the mother’s reproductive system, manage respiration and gas exchange. Using modern light and electron microscopy techniques as well as immunological approach, we provide a detailed account of the maternal and larval tissue interactions during the intrauterine development. We demonstrate that respiration in the
Arixenia
first instar larvae relies on the extensive tracheal system of the mother as well as a respiratory pigment (hemocyanin) present within the body cavity of the larvae. Our results indicate that the larval fat body tissue is the likely place of the hemocyanin synthesis. Our study shows that characteristic cone-shaped lobes of the outgrowths located on the larval abdomen are a part of a placenta-like organ and mediate the gas exchange between the maternal and larval organisms. Based on the obtained results, we propose that
Arixenia esau
evolved a unique biphasic system supporting respiration of the first instar larvae during their development inside the mother’s reproductive tract.</abstract><cop>Vienna</cop><pub>Springer Vienna</pub><pmid>31218520</pmid><doi>10.1007/s00709-019-01402-1</doi><tpages>12</tpages><orcidid>https://orcid.org/0000-0002-1606-8339</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Animal reproduction Animals Biomedical and Life Sciences Breeding success Cell Biology Eggs Electron microscopy Fat body Gas exchange Insecta - physiology Larvae Life Sciences Original Original Article Placenta Plant Sciences Reproductive system Respiration Uterus Viviparity Viviparity, Nonmammalian Zoology |
title | Viviparity in the dermapteran Arixenia esau: respiration inside mother’s body requires both maternal and larval contribution |
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