Sawfly Genomes Reveal Evolutionary Acquisitions That Fostered the Mega-Radiation of Parasitoid and Eusocial Hymenoptera
Abstract The tremendous diversity of Hymenoptera is commonly attributed to the evolution of parasitoidism in the last common ancestor of parasitoid sawflies (Orussidae) and wasp-waisted Hymenoptera (Apocrita). However, Apocrita and Orussidae differ dramatically in their species richness, indicating...
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| Veröffentlicht in: | Genome biology and evolution 2020-07, Vol.12 (7), p.1099-1188 |
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| creator | Oeyen, Jan Philip Baa-Puyoulet, Patrice Benoit, Joshua B Beukeboom, Leo W Bornberg-Bauer, Erich Buttstedt, Anja Calevro, Federica Cash, Elizabeth I Chao, Hsu Charles, Hubert Chen, Mei-Ju May Childers, Christopher Cridge, Andrew G Dearden, Peter Dinh, Huyen Doddapaneni, Harsha Vardhan Dolan, Amanda Donath, Alexander Dowling, Daniel Dugan, Shannon Duncan, Elizabeth Elpidina, Elena N Friedrich, Markus Geuverink, Elzemiek Gibson, Joshua D Grath, Sonja Grimmelikhuijzen, Cornelis J P Große-Wilde, Ewald Gudobba, Cameron Han, Yi Hansson, Bill S Hauser, Frank Hughes, Daniel S T Ioannidis, Panagiotis Jacquin-Joly, Emmanuelle Jennings, Emily C Jones, Jeffery W Klasberg, Steffen Lee, Sandra L Lesný, Peter Lovegrove, Mackenzie Martin, Sebastian Martynov, Alexander G Mayer, Christoph Montagné, Nicolas Moris, Victoria C Munoz-Torres, Monica Murali, Shwetha Canchi Muzny, Donna M Oppert, Brenda Parisot, Nicolas Pauli, Thomas Peters, Ralph S Petersen, Malte Pick, Christian Persyn, Emma Podsiadlowski, Lars Poelchau, Monica F Provataris, Panagiotis Qu, Jiaxin Reijnders, Maarten J M F von Reumont, Björn Marcus Rosendale, Andrew J Simao, Felipe A Skelly, John Sotiropoulos, Alexandros G Stahl, Aaron L Sumitani, Megumi Szuter, Elise M Tidswell, Olivia Tsitlakidis, Evangelos Vedder, Lucia Waterhouse, Robert M Werren, John H Wilbrandt, Jeanne Worley, Kim C Yamamoto, Daisuke S van de Zande, Louis Zdobnov, Evgeny M Ziesmann, Tanja Gibbs, Richard A Richards, Stephen Hatakeyama, Masatsugu Misof, Bernhard Niehuis, Oliver |
| description | Abstract
The tremendous diversity of Hymenoptera is commonly attributed to the evolution of parasitoidism in the last common ancestor of parasitoid sawflies (Orussidae) and wasp-waisted Hymenoptera (Apocrita). However, Apocrita and Orussidae differ dramatically in their species richness, indicating that the diversification of Apocrita was promoted by additional traits. These traits have remained elusive due to a paucity of sawfly genome sequences, in particular those of parasitoid sawflies. Here, we present comparative analyses of draft genomes of the primarily phytophagous sawfly Athalia rosae and the parasitoid sawfly Orussus abietinus. Our analyses revealed that the ancestral hymenopteran genome exhibited traits that were previously considered unique to eusocial Apocrita (e.g., low transposable element content and activity) and a wider gene repertoire than previously thought (e.g., genes for CO2 detection). Moreover, we discovered that Apocrita evolved a significantly larger array of odorant receptors than sawflies, which could be relevant to the remarkable diversification of Apocrita by enabling efficient detection and reliable identification of hosts. |
| doi_str_mv | 10.1093/gbe/evaa106 |
| format | Article |
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The tremendous diversity of Hymenoptera is commonly attributed to the evolution of parasitoidism in the last common ancestor of parasitoid sawflies (Orussidae) and wasp-waisted Hymenoptera (Apocrita). However, Apocrita and Orussidae differ dramatically in their species richness, indicating that the diversification of Apocrita was promoted by additional traits. These traits have remained elusive due to a paucity of sawfly genome sequences, in particular those of parasitoid sawflies. Here, we present comparative analyses of draft genomes of the primarily phytophagous sawfly Athalia rosae and the parasitoid sawfly Orussus abietinus. Our analyses revealed that the ancestral hymenopteran genome exhibited traits that were previously considered unique to eusocial Apocrita (e.g., low transposable element content and activity) and a wider gene repertoire than previously thought (e.g., genes for CO2 detection). Moreover, we discovered that Apocrita evolved a significantly larger array of odorant receptors than sawflies, which could be relevant to the remarkable diversification of Apocrita by enabling efficient detection and reliable identification of hosts.</description><identifier>ISSN: 1759-6653</identifier><identifier>EISSN: 1759-6653</identifier><identifier>DOI: 10.1093/gbe/evaa106</identifier><identifier>PMID: 32442304</identifier><language>eng</language><publisher>England: Oxford University Press</publisher><subject>BASIC BIOLOGICAL SCIENCES ; Biodiversity ; Ecology, environment ; hexamerin ; Life Sciences ; major royal jelly protein ; microsynteny ; odorant receptor ; opsin ; phytophagy ; Populations and Evolution ; Symbiosis</subject><ispartof>Genome biology and evolution, 2020-07, Vol.12 (7), p.1099-1188</ispartof><rights>The Author(s) 2020. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. 2020</rights><rights>The Author(s) 2020. 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Stephen</creatorcontrib><creatorcontrib>Hatakeyama, Masatsugu</creatorcontrib><creatorcontrib>Misof, Bernhard</creatorcontrib><creatorcontrib>Niehuis, Oliver</creatorcontrib><creatorcontrib>Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)</creatorcontrib><title>Sawfly Genomes Reveal Evolutionary Acquisitions That Fostered the Mega-Radiation of Parasitoid and Eusocial Hymenoptera</title><title>Genome biology and evolution</title><addtitle>Genome Biol Evol</addtitle><description>Abstract
The tremendous diversity of Hymenoptera is commonly attributed to the evolution of parasitoidism in the last common ancestor of parasitoid sawflies (Orussidae) and wasp-waisted Hymenoptera (Apocrita). However, Apocrita and Orussidae differ dramatically in their species richness, indicating that the diversification of Apocrita was promoted by additional traits. These traits have remained elusive due to a paucity of sawfly genome sequences, in particular those of parasitoid sawflies. Here, we present comparative analyses of draft genomes of the primarily phytophagous sawfly Athalia rosae and the parasitoid sawfly Orussus abietinus. Our analyses revealed that the ancestral hymenopteran genome exhibited traits that were previously considered unique to eusocial Apocrita (e.g., low transposable element content and activity) and a wider gene repertoire than previously thought (e.g., genes for CO2 detection). 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Genomes Reveal Evolutionary Acquisitions That Fostered the Mega-Radiation of Parasitoid and Eusocial Hymenoptera</title><author>Oeyen, Jan Philip ; Baa-Puyoulet, Patrice ; Benoit, Joshua B ; Beukeboom, Leo W ; Bornberg-Bauer, Erich ; Buttstedt, Anja ; Calevro, Federica ; Cash, Elizabeth I ; Chao, Hsu ; Charles, Hubert ; Chen, Mei-Ju May ; Childers, Christopher ; Cridge, Andrew G ; Dearden, Peter ; Dinh, Huyen ; Doddapaneni, Harsha Vardhan ; Dolan, Amanda ; Donath, Alexander ; Dowling, Daniel ; Dugan, Shannon ; Duncan, Elizabeth ; Elpidina, Elena N ; Friedrich, Markus ; Geuverink, Elzemiek ; Gibson, Joshua D ; Grath, Sonja ; Grimmelikhuijzen, Cornelis J P ; Große-Wilde, Ewald ; Gudobba, Cameron ; Han, Yi ; Hansson, Bill S ; Hauser, Frank ; Hughes, Daniel S T ; Ioannidis, Panagiotis ; Jacquin-Joly, Emmanuelle ; Jennings, Emily C ; Jones, Jeffery W ; Klasberg, Steffen ; Lee, Sandra L ; Lesný, Peter ; Lovegrove, Mackenzie ; Martin, Sebastian ; Martynov, Alexander G ; Mayer, Christoph ; Montagné, Nicolas ; Moris, Victoria C ; Munoz-Torres, Monica ; Murali, Shwetha Canchi ; Muzny, Donna M ; Oppert, Brenda ; Parisot, Nicolas ; Pauli, Thomas ; Peters, Ralph S ; Petersen, Malte ; Pick, Christian ; Persyn, Emma ; Podsiadlowski, Lars ; Poelchau, Monica F ; Provataris, Panagiotis ; Qu, Jiaxin ; Reijnders, Maarten J M F ; von Reumont, Björn Marcus ; Rosendale, Andrew J ; Simao, Felipe A ; Skelly, John ; Sotiropoulos, Alexandros G ; Stahl, Aaron L ; Sumitani, Megumi ; Szuter, Elise M ; Tidswell, Olivia ; Tsitlakidis, Evangelos ; Vedder, Lucia ; Waterhouse, Robert M ; Werren, John H ; Wilbrandt, Jeanne ; Worley, Kim C ; Yamamoto, Daisuke S ; van de Zande, Louis ; Zdobnov, Evgeny M ; Ziesmann, Tanja ; Gibbs, Richard A ; Richards, Stephen ; Hatakeyama, Masatsugu ; Misof, Bernhard ; Niehuis, Oliver</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c515t-df64f0e38cfee9129a5c6165fc75d0ca7fc51b73825acac6ae3837415ce15f9a3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>BASIC BIOLOGICAL SCIENCES</topic><topic>Biodiversity</topic><topic>Ecology, environment</topic><topic>hexamerin</topic><topic>Life Sciences</topic><topic>major royal jelly protein</topic><topic>microsynteny</topic><topic>odorant receptor</topic><topic>opsin</topic><topic>phytophagy</topic><topic>Populations and Evolution</topic><topic>Symbiosis</topic><toplevel>online_resources</toplevel><creatorcontrib>Oeyen, Jan Philip</creatorcontrib><creatorcontrib>Baa-Puyoulet, Patrice</creatorcontrib><creatorcontrib>Benoit, Joshua B</creatorcontrib><creatorcontrib>Beukeboom, Leo W</creatorcontrib><creatorcontrib>Bornberg-Bauer, Erich</creatorcontrib><creatorcontrib>Buttstedt, Anja</creatorcontrib><creatorcontrib>Calevro, Federica</creatorcontrib><creatorcontrib>Cash, Elizabeth I</creatorcontrib><creatorcontrib>Chao, Hsu</creatorcontrib><creatorcontrib>Charles, Hubert</creatorcontrib><creatorcontrib>Chen, Mei-Ju May</creatorcontrib><creatorcontrib>Childers, Christopher</creatorcontrib><creatorcontrib>Cridge, Andrew G</creatorcontrib><creatorcontrib>Dearden, Peter</creatorcontrib><creatorcontrib>Dinh, Huyen</creatorcontrib><creatorcontrib>Doddapaneni, Harsha Vardhan</creatorcontrib><creatorcontrib>Dolan, Amanda</creatorcontrib><creatorcontrib>Donath, Alexander</creatorcontrib><creatorcontrib>Dowling, Daniel</creatorcontrib><creatorcontrib>Dugan, Shannon</creatorcontrib><creatorcontrib>Duncan, Elizabeth</creatorcontrib><creatorcontrib>Elpidina, Elena N</creatorcontrib><creatorcontrib>Friedrich, Markus</creatorcontrib><creatorcontrib>Geuverink, Elzemiek</creatorcontrib><creatorcontrib>Gibson, Joshua D</creatorcontrib><creatorcontrib>Grath, Sonja</creatorcontrib><creatorcontrib>Grimmelikhuijzen, Cornelis J P</creatorcontrib><creatorcontrib>Große-Wilde, Ewald</creatorcontrib><creatorcontrib>Gudobba, Cameron</creatorcontrib><creatorcontrib>Han, Yi</creatorcontrib><creatorcontrib>Hansson, Bill S</creatorcontrib><creatorcontrib>Hauser, Frank</creatorcontrib><creatorcontrib>Hughes, Daniel S T</creatorcontrib><creatorcontrib>Ioannidis, Panagiotis</creatorcontrib><creatorcontrib>Jacquin-Joly, Emmanuelle</creatorcontrib><creatorcontrib>Jennings, Emily C</creatorcontrib><creatorcontrib>Jones, Jeffery W</creatorcontrib><creatorcontrib>Klasberg, Steffen</creatorcontrib><creatorcontrib>Lee, Sandra L</creatorcontrib><creatorcontrib>Lesný, Peter</creatorcontrib><creatorcontrib>Lovegrove, Mackenzie</creatorcontrib><creatorcontrib>Martin, Sebastian</creatorcontrib><creatorcontrib>Martynov, Alexander G</creatorcontrib><creatorcontrib>Mayer, Christoph</creatorcontrib><creatorcontrib>Montagné, Nicolas</creatorcontrib><creatorcontrib>Moris, Victoria C</creatorcontrib><creatorcontrib>Munoz-Torres, Monica</creatorcontrib><creatorcontrib>Murali, Shwetha Canchi</creatorcontrib><creatorcontrib>Muzny, Donna M</creatorcontrib><creatorcontrib>Oppert, Brenda</creatorcontrib><creatorcontrib>Parisot, Nicolas</creatorcontrib><creatorcontrib>Pauli, Thomas</creatorcontrib><creatorcontrib>Peters, Ralph S</creatorcontrib><creatorcontrib>Petersen, Malte</creatorcontrib><creatorcontrib>Pick, Christian</creatorcontrib><creatorcontrib>Persyn, Emma</creatorcontrib><creatorcontrib>Podsiadlowski, Lars</creatorcontrib><creatorcontrib>Poelchau, Monica F</creatorcontrib><creatorcontrib>Provataris, Panagiotis</creatorcontrib><creatorcontrib>Qu, Jiaxin</creatorcontrib><creatorcontrib>Reijnders, Maarten J M F</creatorcontrib><creatorcontrib>von Reumont, Björn Marcus</creatorcontrib><creatorcontrib>Rosendale, Andrew J</creatorcontrib><creatorcontrib>Simao, Felipe A</creatorcontrib><creatorcontrib>Skelly, John</creatorcontrib><creatorcontrib>Sotiropoulos, Alexandros G</creatorcontrib><creatorcontrib>Stahl, Aaron L</creatorcontrib><creatorcontrib>Sumitani, Megumi</creatorcontrib><creatorcontrib>Szuter, Elise M</creatorcontrib><creatorcontrib>Tidswell, Olivia</creatorcontrib><creatorcontrib>Tsitlakidis, Evangelos</creatorcontrib><creatorcontrib>Vedder, Lucia</creatorcontrib><creatorcontrib>Waterhouse, Robert M</creatorcontrib><creatorcontrib>Werren, John H</creatorcontrib><creatorcontrib>Wilbrandt, Jeanne</creatorcontrib><creatorcontrib>Worley, Kim C</creatorcontrib><creatorcontrib>Yamamoto, Daisuke S</creatorcontrib><creatorcontrib>van de Zande, Louis</creatorcontrib><creatorcontrib>Zdobnov, Evgeny M</creatorcontrib><creatorcontrib>Ziesmann, Tanja</creatorcontrib><creatorcontrib>Gibbs, Richard A</creatorcontrib><creatorcontrib>Richards, Stephen</creatorcontrib><creatorcontrib>Hatakeyama, Masatsugu</creatorcontrib><creatorcontrib>Misof, Bernhard</creatorcontrib><creatorcontrib>Niehuis, Oliver</creatorcontrib><creatorcontrib>Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)</creatorcontrib><collection>Oxford Journals Open Access Collection</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Hyper Article en Ligne (HAL)</collection><collection>Hyper Article en Ligne (HAL) (Open Access)</collection><collection>OSTI.GOV - Hybrid</collection><collection>OSTI.GOV</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Genome biology and evolution</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Oeyen, Jan Philip</au><au>Baa-Puyoulet, Patrice</au><au>Benoit, Joshua B</au><au>Beukeboom, Leo W</au><au>Bornberg-Bauer, Erich</au><au>Buttstedt, Anja</au><au>Calevro, Federica</au><au>Cash, Elizabeth I</au><au>Chao, Hsu</au><au>Charles, Hubert</au><au>Chen, Mei-Ju May</au><au>Childers, Christopher</au><au>Cridge, Andrew G</au><au>Dearden, Peter</au><au>Dinh, Huyen</au><au>Doddapaneni, Harsha Vardhan</au><au>Dolan, Amanda</au><au>Donath, Alexander</au><au>Dowling, Daniel</au><au>Dugan, Shannon</au><au>Duncan, Elizabeth</au><au>Elpidina, Elena N</au><au>Friedrich, Markus</au><au>Geuverink, Elzemiek</au><au>Gibson, Joshua D</au><au>Grath, Sonja</au><au>Grimmelikhuijzen, Cornelis J P</au><au>Große-Wilde, Ewald</au><au>Gudobba, Cameron</au><au>Han, Yi</au><au>Hansson, Bill S</au><au>Hauser, Frank</au><au>Hughes, Daniel S T</au><au>Ioannidis, Panagiotis</au><au>Jacquin-Joly, Emmanuelle</au><au>Jennings, Emily C</au><au>Jones, Jeffery W</au><au>Klasberg, Steffen</au><au>Lee, Sandra L</au><au>Lesný, Peter</au><au>Lovegrove, Mackenzie</au><au>Martin, Sebastian</au><au>Martynov, Alexander G</au><au>Mayer, Christoph</au><au>Montagné, Nicolas</au><au>Moris, Victoria C</au><au>Munoz-Torres, Monica</au><au>Murali, Shwetha Canchi</au><au>Muzny, Donna M</au><au>Oppert, Brenda</au><au>Parisot, Nicolas</au><au>Pauli, Thomas</au><au>Peters, Ralph S</au><au>Petersen, Malte</au><au>Pick, Christian</au><au>Persyn, Emma</au><au>Podsiadlowski, Lars</au><au>Poelchau, Monica F</au><au>Provataris, Panagiotis</au><au>Qu, Jiaxin</au><au>Reijnders, Maarten J M F</au><au>von Reumont, Björn Marcus</au><au>Rosendale, Andrew J</au><au>Simao, Felipe A</au><au>Skelly, John</au><au>Sotiropoulos, Alexandros G</au><au>Stahl, Aaron L</au><au>Sumitani, Megumi</au><au>Szuter, Elise M</au><au>Tidswell, Olivia</au><au>Tsitlakidis, Evangelos</au><au>Vedder, Lucia</au><au>Waterhouse, Robert M</au><au>Werren, John H</au><au>Wilbrandt, Jeanne</au><au>Worley, Kim C</au><au>Yamamoto, Daisuke S</au><au>van de Zande, Louis</au><au>Zdobnov, Evgeny M</au><au>Ziesmann, Tanja</au><au>Gibbs, Richard A</au><au>Richards, Stephen</au><au>Hatakeyama, Masatsugu</au><au>Misof, Bernhard</au><au>Niehuis, Oliver</au><aucorp>Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)</aucorp><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Sawfly Genomes Reveal Evolutionary Acquisitions That Fostered the Mega-Radiation of Parasitoid and Eusocial Hymenoptera</atitle><jtitle>Genome biology and evolution</jtitle><addtitle>Genome Biol Evol</addtitle><date>2020-07-01</date><risdate>2020</risdate><volume>12</volume><issue>7</issue><spage>1099</spage><epage>1188</epage><pages>1099-1188</pages><issn>1759-6653</issn><eissn>1759-6653</eissn><abstract>Abstract
The tremendous diversity of Hymenoptera is commonly attributed to the evolution of parasitoidism in the last common ancestor of parasitoid sawflies (Orussidae) and wasp-waisted Hymenoptera (Apocrita). However, Apocrita and Orussidae differ dramatically in their species richness, indicating that the diversification of Apocrita was promoted by additional traits. These traits have remained elusive due to a paucity of sawfly genome sequences, in particular those of parasitoid sawflies. Here, we present comparative analyses of draft genomes of the primarily phytophagous sawfly Athalia rosae and the parasitoid sawfly Orussus abietinus. Our analyses revealed that the ancestral hymenopteran genome exhibited traits that were previously considered unique to eusocial Apocrita (e.g., low transposable element content and activity) and a wider gene repertoire than previously thought (e.g., genes for CO2 detection). Moreover, we discovered that Apocrita evolved a significantly larger array of odorant receptors than sawflies, which could be relevant to the remarkable diversification of Apocrita by enabling efficient detection and reliable identification of hosts.</abstract><cop>England</cop><pub>Oxford University Press</pub><pmid>32442304</pmid><doi>10.1093/gbe/evaa106</doi><tpages>90</tpages><orcidid>https://orcid.org/0000-0002-0116-2234</orcidid><orcidid>https://orcid.org/0000-0002-6220-5613</orcidid><orcidid>https://orcid.org/0000-0002-0363-3837</orcidid><orcidid>https://orcid.org/0000-0001-5618-0547</orcidid><orcidid>https://orcid.org/0000-0003-4199-9052</orcidid><orcidid>https://orcid.org/0000-0002-7033-7245</orcidid><orcidid>https://orcid.org/0000-0002-0809-4705</orcidid><orcidid>https://orcid.org/0000-0001-5217-8415</orcidid><orcidid>https://orcid.org/0000-0001-9330-2689</orcidid><orcidid>https://orcid.org/0000-0001-7856-9617</orcidid><orcidid>https://orcid.org/0000-0001-7601-9873</orcidid><orcidid>https://orcid.org/0000-0002-6904-2036</orcidid><orcidid>https://orcid.org/0000000262205613</orcidid><orcidid>https://orcid.org/0000000201162234</orcidid><orcidid>https://orcid.org/0000000203633837</orcidid><orcidid>https://orcid.org/0000000341999052</orcidid><orcidid>https://orcid.org/0000000156180547</orcidid><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1759-6653 |
| ispartof | Genome biology and evolution, 2020-07, Vol.12 (7), p.1099-1188 |
| issn | 1759-6653 1759-6653 |
| language | eng |
| recordid | cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_7455281 |
| source | Oxford Journals Open Access Collection; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central |
| subjects | BASIC BIOLOGICAL SCIENCES Biodiversity Ecology, environment hexamerin Life Sciences major royal jelly protein microsynteny odorant receptor opsin phytophagy Populations and Evolution Symbiosis |
| title | Sawfly Genomes Reveal Evolutionary Acquisitions That Fostered the Mega-Radiation of Parasitoid and Eusocial Hymenoptera |
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