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Contribution to understanding the evolution of holometaboly: transformation of internal head structures during the metamorphosis in the green lacewingChrysopa pallens(Neuroptera: Chrysopidae)

文献类型: 外文期刊

作者: Zhao, Chenjing 1 ; Ang, Yuchen 3 ; Wang, Mengqing 4 ; Gao, Caixia 5 ; Zhang, Kuiyan 5 ; Tang, Chufei 6 ; Liu, Xingyue; 1 ;

作者机构: 1.Taiyuan Normal Univ, Dept Biol, Jinzhong 030619, Peoples R China

2.China Agr Univ, Dept Entomol, Beijing, Peoples R China

3.Natl Univ Singapore, Dept Biol Sci, Singapore 117543, Singapore

4.Chinese Acad Agr Sci, Inst Plant Protect, Beijing, Peoples R China

5.Chinese Acad Sci, Inst Zool, Beijing 100080, Peoples R China

6.Jiangsu Acad Agr Sci, Inst Leisure Agr, Nanjing 210014, Peoples R China

关键词: Chrysopidae; Neuroptera; 3D reconstruction; Transformation

期刊名称:BMC EVOLUTIONARY BIOLOGY ( 影响因子:3.26; 五年影响因子:3.732 )

ISSN: 1471-2148

年卷期: 2020 年 20 卷 1 期

页码:

收录情况: SCI

摘要: Background Metamorphosis remains one of the most complicated and poorly understood processes in insects. This is particularly so for the very dynamic transformations that take place within the pupal sheath of holometabolous insects. Only few studies address these transformations especially with regard to cranial structures of those holometabolous species where the larval and adult forms have a similar diet. It thus remains unclear to what extent the internal structures undergo histolysis and rebuilding. Here, the development of the brain and skeleto-muscular system of the head ofChrysopa pallens(Rambur, 1838) is studied. This species is a predator of aphids in the larval and adult stage. Results We used micro-computed-tomography (mu-CT) to study the transformations of the larval, prepupal and pupal head within the cocoon. We first assessed the morphological differences and similarities between the stages. We then determined the point in time when the compound eyes appear and describe the re-orientation of the head capsule which transforms the prognathous larva into a hypognathous adult. The internal head muscles are distinctly more slender in larvae than adults. In addition, the adults have a significantly larger brain which is likely needed for the processing of the signals obtained by the adults vastly expanded sensory organs that are presumably needed for dispersal and mating. Our study shows that the histolysis and modification of the inner muscles and skeletal elements take place within the prepupa. The central nervous system persists throughout metamorphosis but its morphology changes significantly. Conclusion Our study reveals that not only the inner structures, but also the outer morphology continues to change after the final larval moult. The adult cuticle and internal structures form gradually within the cocoon. The histolysis and rebuilding begin with the skeletal elements and is followed by changes in the central nervous system before it concludes with modifications of the musculature. This order of events is likely ancestral for Holometabola because it is also known from Hymenoptera, Diptera, Mecoptera, and Coleoptera.

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Wyse;Bouskila, Amos;Shacham, Boaz;Gossa, Tegenu;Ballerio, Alberto;Allievi, Alessandro;de Jager, Gerhard;Petroni, Giulio;Peruzzi, Lorenzo;D'Antraccoli, Marco;Serra, Valentina;Bisi, Alessandro;Chiarucci, Alessandro;Hilpold, Andreas;Rosso, Antonietta;Sciuto, Francesco;Mingozzi, Antonio;Giovanni, Boano;Massa, Bruno;Marrone, Federico;Vecchioni, Luca;Guarino, Riccardo;Giusto, Carlo;Lombardi, Chiara;Nepi, Chiara;Scaccini, Davide;Fontaneto, Diego;Banfi, Enrico;Rigato, Fabrizio;Galasso, Gabriele;Chiozzi, Giorgio;Gallo, Enrico;Bertasi, Fabio;Bartolucci, Fabrizio;Fabbriciani, Fabrizio;Andreone, Franco;Polgar, Gianluca;Filibeck, Goffredo;Tessa, Giulia;Gardini, Giulio;Fenu, Giuseppe;Mazzini, Ilaria;Langeneck, Joachim;Bartolozzi, Luca;Bologna, Marco A.;Abeli, Thomas;Dellacasa, Marco;Uliana, Marco;Novarini, Nicola;Faccoli, Massimo;Majorano, Paolo;Zilioli, Michele;Raia, Pasquale;Cerretti, Pierfilippo;Poggi, Roberto;Bertolino, Sandro;Orsenigo, Simone;Martellos, Stefano;Greuter, Werner;Greuter, Werner;Kouakou, Lombart Maurice;Kato, Daichi;Yadav, Harsh;Chiba, Hideyuki;Chiba, Hideyuki;Yoshitomi, Hiroyuki;Kakui, Keiichi;Kwak, Mackenzie L.;Dick, Matthew H.;Ikuno, Kenji;Genka, Masaaki;Yano, Okihito;Kakizoe, Showtaro;Hellemans, Simon;Jashenko, Roman;Dujsebayeva, Tatjana;Kabak, Ilya;Kabak, Ilya;Katumo, Daniel Mutavi;Baasanmunkh, Shukherdorj;Choi, Hyeok Jae;Shin, Jae-Seo;Eun, Lim Ji;Jung, Eui-Kwon;Kim, Young-Dong;Lazkov, Georgii;Strijk, Joeri Sergej;Shavrin, Alexey;Greke, Kristine;Kalnins, Martins;Petrasiunas, Andrius;Uogintas, Domas;Stonis, Jonas R.;Gudzinskas, Zigmantas;Sokolova, Elena;Kharchenko, Viktoria;Andriambololonera, Sylvie;Kumaran, Jayaraj Vijaya;Appalasamy, Suganthi;Prozorov, Alexey M.;Dembele, Jacques;Hanan Alipi, Ana Maria;Solano Gomez, Aniceto Rodolfo;Maruri-Aguilar, Beatriz;Ramirez Diaz, Claudia Janeth;Carnevali Fernandez-Concha, German;Ramirez-Morillo, Ivon M.;Stefano Duno, Rodrigo;Delgadillo-Moya, Claudio;Prieto Torres, David Alexander;Daniel Tejero-Diez, J.;Meave, Jorge A.;Alvarado Cardenas, Leonardo Osvaldo;Terrazas, Teresa;Barradas, Victor L.;Adilson Pinedo-Escatel, J.;Murugan, Gopal;Ruiz Sanchez, Eduardo;Sanchez Martinez, Emiliano;Hernandez Martinez, Maria Magdalena;Gomez-Noguez, Felipe;Montiel Canales, Gustavo;Socorro Gonzalez-Elizondo, M.;Gonzalez Elizondo, Martha;Rolando Bastida-Zavala, J.;del Socorro Garcia-Madrigal, Maria;Alvarado Rodriguez, Jose Fernando;Lopez Mata, Lauro;Gonzalez Ledesma, Manuel;Ramirez-Marcial, Neptali;Cuevas Guzman, Ramon;Martinez-Camilo, Rub'n;Adilson Pinedo-Escatel, J.;Boldgiv, Bazartseren;Mathieu, Chambouleyron;Lermmel, Claude;Leger, Jean-Francois;Farooq, Harith;Irish, John;Shrestha, Krishna;Dop, A. J.;van der Geer, Alexandra;Jaramillo, Angelica Cibrian;Gielis, Cornelis (Cees);Simons, Erik;Sangster, George;Kronenberg, Gijs C.;Henrot, Jacqueline;Arntzen, Jan W.;Monsch, Kenneth A.;Duistermaat, Leni;Schilthuizen, Menno;d'Oliveira, Micha C.;van Eck, Andre P. W.;Egberts, E.;Peeters, Edwin;Sival, Francisca;Kessels, Han;Rutjes, Hendrikus Antonius;van Dam, Herman;Huang, Huasheng;van Eck, Iris;Klinge, Marcel;Graveland, Jaap;van der Vleuten, Jan;van Zuijlen, Jan Willem;Stroom, Jasper;Collombon, Miriam;van Valkenburg, Johan;Melis, John;Bruins, Linda;Knapp, Markus;Soesbergen, Martin;Beuk, Paul L. T.;van Els, Paul;Haveman, Rense;Lansdown, Richard;Suijkerbuijk, Rob;Pot, Roelf;van Manen, Willem;Marshall, Andrew;de Lange, Peter J.;Blanchon, Dan;Early, John W.;Leduc, Daniel;Gordon, Dennis Preston;Kelly, Michelle;Lowe, David J.;Gordon, Dennis;Ford, Kerry;Harper, Margaret;Marinov, Milen;Marinov, Milen;Maes, Jean-Michel;Perez, Rosa Maria Reyes;Valqui, Thomas;Seid, Abel Gizaw;Langangen, Anders;Bjora, Charlotte Sletten;Di Martino, Emanuela;Nakrem, Hans Arne;Lifjeld, Jan T.;Eidesen, Pernille Bronken;Elven, Reidar;Gusarov, Vladimir I.;Tandberg, Anne Helene Solberg;Andersson, Carin;Westergaard, Kristine Bakke;Ekrem, Torbjorn;Malaquias, Manuel Antonio E.;Majid, Abdul;Hanif, Uzma;Aiello, Annette;Carrion, Juan F.;Garcete-Barrett, Bolivar R.;Soria Rey, Nelida;Cano, Asuncion;Rojas-Fox, Jenny;Reynel Rodriguez, Carlos;Heredia Huarino, Din Olger;Fany Palomino, Elva;Gagliardi-Urrutia, Giussepe;Pino, Guillermo;Trevino Zevallos, Italo Francisco;Trevino Zevallos, Italo Francisco;Cabrera Melendez, Jorge Luis;Cabrera Melendez, Jorge Luis;Dupo, Aimee Lynn;Lit, Ireneo L., Jr.;Lucanas, Cristian C.;General, David Emmanuel M.;Tolentino, Haira Jill;Calaramo, Michael Agbayani;Calaramo, Michael Agbayani;Kaczmarek, Adam;Kaim, Andrzej;Hryniewicz, Krzysztof;Taszakowski, Artur;Tokarska-Guzik, Barbara;Wisniowski, Bogdan;Moniuszko, Hanna;Garcia-Cunchillos, Ivan;De Baets, Kenneth;Talanda, Mateusz;Wieclaw, Helena;Koopman, Jacob;Tyszka, Jaroslaw;Lis, Jerzy;Piatek, Marcin;Wanat, Marek;Zakrzewska, Marta;Kuklinski, Piotr;Salamatin, Ruslan;Solarz, Wojciech;Casimiro Justo Carapeto, Andre de Matos;Muriel, Andreu Santin;Sampaio, Iris;Calado, Antonio Jose;Esquete, Patricia;Sa, Artur A.;Serrano, Artur R. M.;Gois-Marques, Carlos A.;Vila-Vicosa, Carlos;Parrinha, Diogo;Grosso-Silva, Jose Manuel;Ceriaco, Luis M. 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Luisa;Sanz Arnal, Maria;Miguez Rios, Monica;Sanchez Villegas, Rogelio;Alvarez, Elena;Fabado Alos, Javier;Baixeras, Joaquin;Gabriel Segarra-Moragues, Jose;Lucas Lledo, Jose Ignacio;Perez Santa-Rita, Jose Vicente;Monros, Juan S.;Monros Gonzalez, Juan S.;Angel Gomez-Serrano, Miguel;Lopez-Lopez, Pascual;Garilleti, Ricardo;Laguna, Emilio;Penalver Molla, Enrique;Jose Carreras, Esther San;Sanchez Frances, Raul;Gomez Valle, Silvia;Javier Jimenez-Lopez, F.;Fernandez-Gonzalez, Federico;Luis Yela, Jose;Torres Gonzalez, Felix;Garcia Martin, Joaquina Maria;Montserrat Martinez-Ortega, M.;Andres Sanchez, Santiago;Ojeda, Fernando;Blanco Pastor, Jose Luis;Rodriguez-Iglesias, Manuel A.;Ochoa-Hueso, Raol;Cabezas, Francisco J.;Galan-Diaz, Javier;Munoz-Rodriguez, Pablo;Canto, Paloma;Medina, Rafael;Gavilan, Rosario G.;Magana Ugarte, Rosina;Romero, Sara;Rico, Victor J.;Vazquez, Francisco M.;Mercadal i Corominas, Gabriel;Martinez-Sagarra, Gloria;Antonio Devesa, Juan;de la Estrella, Manuel;Romera, Graciela Gil;Ibarra, Pablo Tejero;Gonzalez-Samperiz, Pen'lope;Lazagabaster, Ignacio A.;Salcedo, Isabel;Etayo, Javier;Denzer, Wolfgang;Lopez-Pujol, Jordi;Garnatje, Teresa;Carlos Miranda, Jose;Rubiales, Juan M.;Martinez Labarga, Juan M.;Capo, Miquel;Andres Ros, Jose Vicente;Carretero Diaz, Jose-Miguel;Padulles Cubino, Josep;Borras, Joshua;Carlos Gutierrez-Marco, Juan;Mota, Juan F.;Pino Perez, Juan Jose;Saez, Llorenc;Serra Laliga, Lluis;Serra Laliga, Lluis;Lopez Merino, Lourdes;Buide del Real, M. Luisa;Vicens Fornes, Magdalena;Sanchez-Angulo, Manuel;Escudero, Marcial;Alcolea, Marta;Sanchez Gomez, Pedro;Fraga i Arguimbau, Pere;Orihuela-Rivero, Raol;Granjel, Rodrigo R.;Molino, Sonia;Garcia Mendizabal, Yoana;Carlsson, Bengt;Svensson, Brita;Bosagna, Carlos Guerrero;Arnqvist, Goran;Cardenas, Paco;Ahlberg, Per;Alstrom, Per;Liu, Zongzhuang;Alonso, German Hernandez;Wahlsteen, Eric;Bisang, Irene;Jonsson, Knud Andreas;Hedenas, Lars;Wedin, Mats;Noren, Michael;Stohr, Sabine;Kiel, Steffen;Rota, Jadranka;Wahlberg, Niklas;Tyler, Torbjorn;Arup, Ulf;Strid, Arne;Liljeblad, Johan;Lundin, Kennet;Nielsen, Peter;Strid, Arne;Alonso, German Hernandez;Chautems, Alain;Charpin, Andre;Mombrial, Florian;Zamora, Juan Carlos;Fumeaux, Nicolas;Clerc, Philippe;Garcia-Martin, Ana B.;Mueller, Andreas;Freitag, Anne;Landry, Bernard;Cuccodoro, Giulio;Sabatinelli, Guido;Lobl, Ivan;Valtotton, Laurent;Ruedi, Manuel;Schuchert, Peter;Praz, Christophe;Thivaiou, Danae;Klopfstein, Seraina;Cherix, Daniel;Mitchell, Edward;Mariaux, Jean;Haenni, Jean-Paul;Theurillat, Jean-Paul;Theurillat, Jean-Paul;Bernasconi, Marvco V.;Hawlitschek, Oliver;Samathi, Adun;Hyde, Kevin;Radji, Raoufou;Morales, J. Francisco;Charfi, Faouzia;El Mokni, Ridha;Gunay, Filiz;Agayeva, Saida;Giusti, Alessandro;Schuiteman, Andr';Goyder, David;Noltie, Henry J.;Larridon, Isabel;Bateman, Richard M.;Whittington, Andrew E.;Stewart, Nick;Leftwich, Ashley;Williams, Christopher David;Little, Crispin;Sherwood, Danniella;Lees, David C.;John, David Michael;Noltie, Henry J.;McLean, Ian F. G.;Badmin, John;Todd, Jonathan A.;Barclay, Maxwell V. L.;Geiser, Michael F.;Chen, Zhe-Yu;Telnov, Dmitry;Dickinson, Edward;Beccaloni, George W.;Badmin, John;McArthur, John M.;Davranoglou, Leonidas Romanos;Taberer, Tabitha R.;Shaw, Mark R.;Blagoderov, Vladimir;Young, Mark T.;Ebejer, Martin;Kelly, Martyn;Kelly, Martyn;Langton, Peter;Marchant, Rob;Schneider, Simon;Horton, Tammy;Wuster, Wolfgang;Telnov, Dmitry;Novikov, Andriy;Dubyna, Dmytro;Olshanskyi, Ihor;Fedoronchuk, Mykola;Shiyan, Natalia M.;Vinogradova, Oxana;Mikhailyuk, Tatiana;Hayova, Vera;Balashov, Igor;Kharchenko, Vitaliy A.;Khodosovtsev, Oleksandr;Kovalchuk, Oleksandr;Dyadichko, Vasily;Nachychko, Viktor O.;Kolomiichuk, Vitalii;Perkovsky, Evgeny E.;Perkovsky, Evgeny E.;Mailhos, Ary;Marchesi, Eduardo;Mauricio Bonifacino, Jose;Valtierra Sierra, Maria Victoria;Bauer, Aaron M.;Adeyemi, Adeyinka;Arnold, Keith;Franck, Alan;Burkett-Cadena, Nathan;Smith-Vaniz, William F.;Pandolfi, Alessandra;Dal Pos, Davide;Norrbom, Allen L.;Moncrieff, Andre E.;Remsen, J. V., Jr.;Esselstyn, Jacob;Eberhard, Jessica;Harms, Kyle E.;Johnson, Andrew;Capparella, Angelo;Rossi, Anthony;Casamatta, Dale;Namayandeh, Armin;Borkent, Art;Smith, Brian Tilston;Engel, Michael S.;Hellenthal, Barbara;Ratcliffe, Brett C.;O'Shea, Brian J.;Schmitt, C. Jonathan;Boufford, David;Morris, Paul J.;Shakya, Subir;Swift, Camm C.;McLeod, Samuel A.;Cohen, Chris M.;Borkent, Christopher J.;Borkent, Christopher J.;Rogers, D. Christopher;Gonzalez, Victor H.;Koenemann, Daniel;Campbell, David;Krause, David W.;Cushing, Paula;Sikes, Derek;Les, Don;DeKeyser, Edward S.;Cruz-Rivera, Edwin;Carter, Emily;Seeholzer, Glenn Fairbanks;Pratt, H. Douglas;Gerwin, John A.;Kaiser, Hinrich;Machio, Irene Villa;Harber, Julian;Zander, Richard H.;Gereau, Roy E.;Applequist, Wendy;Egger, J. Mark;Sagebiel, James Christopher;Lopez-Ribot, Jose L.;Atkinson, Thomas H.;Liebherr, James;Dombroskie, Jason J.;Hoghe, James N.;Wolfe, Jared;McGuire, Jimmy A.;Will, Kipling;Zuparko, Robert L.;Hansen, Robert W.;Brett, Roberta;Leal, Jose H.;Winston, Judith E.;Wen, Jun;Pinheiro, Paulo Duraes Pereira;Lee, Justin L.;Rabeler, Richard;Pargeter, Justin;Gregg, Katharine;Carpenter, Kenneth;McCracken, Kevin;Williams, Kevin;Korneyev, Severyn;Winker, Kevin;Austin, Kyhl A.;Watling, Les;Watson, Linda;Marin, Manuel;Epstein, Marc Edward;Key, Marcus M., Jr.;Marques, Mariana P.;Pyron, Mark;Dovciak, Martin;Hauser, Martin;Sage, Obediah;Garrison, Rosser W.;Winterton, Shaun L.;Gaimari, Stephen D.;West-Eberhard, Mary Jane;Diazgranados, Mauricio;Warren, Mel;Oliver, Michael K.;Ferro, Michael L.;Williams, Kevin;Evenhuis, Neal L.;Snow, Neil;Mizumoto, Nobuaki;Rakes, Patrick;Rohner, Patrick;Rozo-Lopez, Paula;Kerr, Peter H.;Stevens, Peter;Uetz, Peter;Wheeler, Quentin;DeWalt, R. Edward;McClelland, R. Kevan Schoonover;Hellenthal, Ronald;Meier, Rose;Heads, Sam W.;James, Samuel Wooster;Hilty, Steve;Adams, Susan B.;Letcher, Susan G.;Wood, Timothy S.;Walsh, S. J.;Murphy, William L.;Thomas, William Wayt;Khalimov, F. Z.;Rakhimov, Mukhammadtuychi;Abdullajonovich, Shodmonov Feruz;Tashpulatov, Yigitali;Rojas-Runjaic, Fernando J. M.;Cerda Perez, Hugo Gullermo;Torrecilla, Pedro;Zapata, Thirza Ruiz;Hoa, Hoang Quynh;Nguyen, Ngoc;Sharp, Cathy;Fitzpatrick, Moira

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