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Evolution of genes and genomes on the Drosophila phylogeny

Authors
Andrew Clark,Michael Eisen
Casey Bergman,Therese Markow,Thomas Kaufman,M. Kellis,William Gelbart,Venky Iyer,Daniel Pollard,Timothy Sackton,Nadia Singh,José Abad,Boris Adryan,Hiroshi Akashi,Wyatt Anderson,Charles Aquadro,David Ardell,J. Arguello,Daniel Barbash,Daniel Barker,Paolo Barsanti,Serafim Batzoglou,Dave Begun,Arjun Bhutkar,Enrique Blanco,Robert Bradley,Michael Brent,Angela Brooks,Randall Brown,Roger Butlin,Brian Calvi,Anat Caspi,Sergio Castrezana,S Celniker,Jean Chang,Charles Chapple,Sourav Chatterji,Asif Chinwalla,Sandra Clifton,Josep Comeron,James Costello,Robert David,Arthur Delcher,Kim Delehaunty,Michele Hu,Heather Ebling,Kevin Edwards,Jay Evans,Sven Findeiß,Lucinda Fulton,Robert Fulton,Ana Garcia,Anastasia Gardiner,David Garfield,Barry Garvin,Greg Gibson,Don Gilbert,Sante Gnerre,Jennifer Godfrey,Robert Good,Valer Gotea,Anthony Greenberg,Samuel Gross,Ramin Shiekhattar,Erik Gustafson,Wilfried Haerty,Daniel Halligan,Gillian Halter,Mira Han,Andreas Heger,Angie Hinrichs,Ian Holmes,Melissa Hubisz,Dan Hultmark,David Jaffe,Santosh Jagadeeshan,Justin Johnson,Corbin Jones,William Jordan,Gary Karpen,Eiko Kataoka,Peter Keightley,Pouya Kheradpour,Ewen Kirkness,Leonardo Koerich,Karsten Kristiansen,Rob Kulathinal,Sudhir Kumar,Eric Lander,Charles Langley,Richard Lapoint,Brian Lazzaro,So Lee,Lisa Levesque,Ruiqiang Li,Chiao‐Feng Lin,Kerstin Lindblad-Toh,Ana Llopart,Manyuan Long,Wai Low,Elena Lozovsky,Jian ,Meizhong Luo,Carlos Machado,Wojciech Makałowski,Mar Marzo,Luciano Matzkin,Bryant McAllister,Carolyn McBride,Brendan McKernan,Kevin McKernan,Patrick Minx,Martin Mollenhauer,Kristi Montooth,Stephen Mount,Eugene Myers,Stuart Newfeld,Stuar Newfeld,Rasmus Nielsen,Mohamed Noor,Lior Pachter,Mariana Parisi,Michael Parisi,Leopold Parts,Jakob Pedersen,Graziano Pesole,Adam Phillippy,Chris Ponting,Mihai Pop,Jeffrey Powell,Sonja Prohaska,Kim Pruitt,Marta Puig,Hadi Quesneville,K. Ram,Matthew Rasmussen,Laura Reed,Robert Reenan,Amy Reily,Karin Remington,Tania Rieger,Michael Ritchie,Charles Robin,Cláudia Rohde,Pascale Roux,Alfredo Ruíz,Susan Russo,Steven Salzberg,Alejandro Sánchez‐Gracia,Hajime Sato,Stephen Schaeffer,Michael Schatz,Todd Schlenke,Russell Schwartz,Carmen Segarra,Laura Sirot,Marina Sirota,Chris Smith,Temple Smith,John Strouboulis,Alexandre Souvorov,Alexander Stark,Robert Strausberg,Sebastian Strempel,David Sturgill,Granger Sutton,Tao Wei,Sarah Teichmann,Yoshihiko Tomimura,Jason Tsolas,Vera Valente,J. Venter,Saverio Vicario,Filipe Vieira,Alfredo Villasanté,Brian Walenz,Jun Wang,Thomas Watts,Derek Wilson,Richard Wilson,Rod Wing,Alex Wong,Gane Wong,WU Garidi,Daisuke Yamamoto,Shiaw-Pyng Yang,James Yorke,Kiyohito Yoshida,Evgeny Zdobnov,Yu Zhang,Aleksey Zimin,Jennifer Baldwin,Amr Abdouelleil,Jamal Abdulkadir,Adal Abebe,Brikti Abera,Justin Abreu,St Acer,Lynne Aftuck,Allen Alexander,Peter An,Erica Anderson,Scott Anderson,Harindra Arachi,Marc Azer,Samy Azer,Andrew Barry,Aaron Berlin,Daniel Bessette,Toby Bloom,Jason Blye,Leonid Boguslavskiy,Boris Boukhgalter,Imane Bourzgui,Adam Brown,Patrick Cahill,Sheridon Channer,Yama Cheshatsang,Lisa Chuda,Mieke Citroen,Alville Collymore,Patrick Cooke,Maura Costello,Katie D'Aco,Riza Daza,Gerald Haan,Christina Demaso,Norbu Dhargay,Kimberly Dooley,Erin Dooley,Missole Doricent,Passang Dorje,Kunsang Dorjee,Richard Elong,Jill Falk,Diallo Ferguson,Sheila Fisher,Chelsea Foley,A Franke,Dennis Friedrich,Loryn Gadbois,Gary Gearin,Christina Gearin,Georgia Giannoukos,T. Goode,Joseph Graham,Edward Grandbois,Shiv Grewal,Kunsang Gyaltsen,Nabil Hafez,Birhane Hagos,Jennifer Hall,Charlotte Henson,Andrew Hollinger,Tracey Honan,Monika Huard,Leanne Hughes,Brian Hurhula,Magne Husby,Asha Kamat,Ben Kanga,Seva Kashin,Dmitry Khazanovich,Peter Kisner,Krista Lance,Marcia Lara,William Lee,Niall Lennon,F Letendre,R Levine,Alex Lipovsky,Xiaohong Liu,Jinlei Liu,Shangtao Liu,Tashi Lokyitsang,Yeshi Lokyitsang,Rakela Lubonja,Annie Lui,Paul Macdonald,Vasilia Magnisalis,Kebede Maru,Charles Matthews,William McCusker,Susan McDonough,Teena Mehta,James Meldrim,Louis Meneus,Oana Mihai,Atanas Mihalev,Tanya Mihova,Valentine Mlenga,Anna Montmayeur,Adam Navidi,Jerome Naylor,Tamrat Negash,Thu Dang,Nga Nguyen,Robert Nicol,Nyima Norbu,Nathaniel Novod,Barry O'Neill,Sahal Osman,Ewa Markiewicz,Otero Oyono,Christopher Patti,Pema Phunkhang,P Fritz,Margaret Priest,Sujaa Raghuraman,Rebecca Reyes,Cecil Rise,Peter Rogov,Kenneth Ross,Elizabeth Ryan,Sampath Settipalli,Terry Shea,Ngawang Sherpa,Lu Shi,Diana Shih,Todd Sparrow,John Spaulding,John Stalker,Nicole Stange-Thomann,Sharon Stavropoulos,Catherine Stone,C. Strader,Senait Tesfaye,Talene Thomson,Yama Thoulutsang,Dawa Thoulutsang,Kerri Topham,Tsamla Tsamla,Helen Vassiliev,Andy Vo,Tsering Wangchuk,Tsering Wangdi,Michael Weiand,Jane Wilkinson,Adam Wilson,Shailendra Yadav,Geneva Young,Qing Yu,Lisa Zembek,Danni Zhong,Andrew Zimmer,Zac Zwirko,Pablo Álvarez,Will Brockman,CheeWhye Chin,Manfred Grabherr,Michael Kleber,Iain MacCallum,Antonio Carvalho,Michèle Hu,Sam Griffiths‐Jones
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,Aaron Halpern
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Published
Nov 1, 2007
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Abstract

Comparative analysis of multiple genomes in a phylogenetic framework dramatically improves the precision and sensitivity of evolutionary inference, producing more robust results than single-genome analyses can provide. The genomes of 12 Drosophila species, ten of which are presented here for the first time (sechellia, simulans, yakuba, erecta, ananassae, persimilis, willistoni, mojavensis, virilis and grimshawi), illustrate how rates and patterns of sequence divergence across taxa can illuminate evolutionary processes on a genomic scale. These genome sequences augment the formidable genetic tools that have made Drosophila melanogaster a pre-eminent model for animal genetics, and will further catalyse fundamental research on mechanisms of development, cell biology, genetics, disease, neurobiology, behaviour, physiology and evolution. Despite remarkable similarities among these Drosophila species, we identified many putatively non-neutral changes in protein-coding genes, non-coding RNA genes, and cis-regulatory regions. These may prove to underlie differences in the ecology and behaviour of these diverse species. This issue includes a landmark collection of papers on the stalwart of the genetics lab, the Drosophila fruit fly. The centrepiece is the publication by the Drosophila 12 Genomes Consortium of the genomic sequence for ten Drosophila species. The paper compares the newly sequenced genomes (sechellia, simulans, yakuba, erecta, ananassae, persimilis, willistoni, mojavensis, virilis and grimshawi species), with the two previously known sequences for D. melanogaster and D. pseudoobscura. The resulting database of genetic variation will be invaluable for the study of the forces of evolutionary change. A second major collaboration has mined the dozen Drosophila genome sequences for conserved elements, and reports the relationship between conservation and function for many specific sequence motifs. A detailed regulatory network emerges, identifying protein-coding genes and exons, RNA genes, microRNAs and their targets. These papers are discussed in News and Views. Two further research papers use the new genomic data to study gene expression, first for genes with male-biased expression and those unique to each species and second, to track the evolution of gene dosage compensation on Drosophila sex chromosomes. Four new reviews focus on how the latest work on Drosophila is taking this genetically pliant lab model into exciting new fields. Pierre Leopold and Norbert Perrimon review advances in the study of endocrinology and homeostasis that are establishing Drosophila as a model for mammalian physiology. Drosophila has proved a powerful system in which to study the pathways controlling cell shape in growing tissue, as reported by Thomas Lecuit and Loïc Le Goff. Leslie Vosshall reviews the remarkable work linking neural circuits and behaviour and John Lis reviews work on Drosophila that has rewritten the textbook view of gene transcription. The cover shows anaesthetized individuals of all twelve Drosophila species. An international consortium reports the genomic sequence for ten Drosophila species, and compares them to two other previously published Drosophila species. These data are invaluable for drawing evolutionary conclusions across an entire phylogeny of species at once.

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