Recurrent horizontal transfer identifies mitochondrial positive selection in a transmissible cancer

Andrea Strakova, Thomas J. Nicholls, Adrian Baez-Ortega, Máire Ní Leathlobhair, Alexander T. Sampson, Katherine Hughes, Isobelle A. G. Bolton, Kevin Gori, Jinhong Wang, Ilona Airikkala-Otter, Janice L. Allen, Karen M. Allum, Clara L. Arnold, Leontine Bansse-Issa, Thinlay N. Bhutia, Jocelyn L. Bisson, Kelli Blank, Cristóbal Briceño, Artemio Castillo Domracheva, Anne M. Corrigan, Hugh R. Cran, Jane T. Crawford, Stephen M. Cutter, Eric Davis, Karina F. de Castro, Andrigo B. De Nardi, Anna P. de Vos, Laura Delgadillo Keenan, Edward M. Donelan, Adela R. Espinoza Huerta, Ibikunle A. Faramade, Mohammed Fazil, Eleni Fotopoulou, Skye N. Fruean, Fanny Gallardo-Arrieta, Olga Glebova, Pagona G. Gouletsou, Rodrigo F. Häfelin Manrique, Joaquim J. G. P. Henriques, Rodrigo S. Horta, Natalia Ignatenko, Yaghouba Kane, Cathy King, Debbie Koenig, Ada Krupa, Steven J. Kruzeniski, Marta Lanza-Perea, Mihran Lazyan, Adriana M. Lopez Quintana, Thibault Losfelt, Gabriele Marino, Simón Martínez Castañeda, Mayra F. Martínez-López, Bedan M. Masuruli, Michael Meyer, Edward J. Migneco, Berna Nakanwagi, Karter B. Neal, Winifred Neunzig, Sally J. Nixon, Antonio Ortega-Pacheco, Francisco Pedraza-Ordoñez, Maria C. Peleteiro, Katherine Polak, Ruth J. Pye, Juan C. Ramirez-Ante, John F. Reece, Jose Rojas Gutierrez, Haleema Sadia, Sheila K. Schmeling, Olga Shamanova, Alan G. Sherlock, Audrey E. Steenland-Smit, Alla Svitich, Lester J. Tapia Martínez, Ismail Thoya Ngoka, Cristian G. Torres, Elizabeth M. Tudor, Mirjam G. van der Wel, Bogdan A. Vițălaru, Sevil A. Vural, Oliver Walkinton, Alvaro S. Wehrle-Martinez, Sophie A. E. Widdowson, Irina Zvarich, Patrick F. Chinnery, Maria Falkenberg, Claes M. Gustafsson and Elizabeth P. Murchison ()
Additional contact information
Andrea Strakova: University of Cambridge
Thomas J. Nicholls: University of Gothenburg
Adrian Baez-Ortega: University of Cambridge
Máire Ní Leathlobhair: University of Cambridge
Alexander T. Sampson: University of Cambridge
Katherine Hughes: University of Cambridge
Isobelle A. G. Bolton: University of Cambridge
Kevin Gori: University of Cambridge
Jinhong Wang: University of Cambridge
Ilona Airikkala-Otter: Worldwide Veterinary Service, International Training Center
Janice L. Allen: Animal Management in Rural and Remote Indigenous Communities (AMRRIC)
Karen M. Allum: World Vets
Clara L. Arnold: Hopkins Belize Humane Society
Leontine Bansse-Issa: Animal Shelter, Stichting Dierenbescherming Suriname
Thinlay N. Bhutia: Sikkim Anti-Rabies and Animal Health Programme, Department of Animal Husbandry, Livestock, Fisheries and Veterinary Services, Government of Sikkim
Jocelyn L. Bisson: University of Cambridge
Kelli Blank: Hopkins Belize Humane Society
Cristóbal Briceño: University of Chile
Artemio Castillo Domracheva: University of Panamá
Anne M. Corrigan: St. George’s University
Hugh R. Cran: The Nakuru District Veterinary Scheme Ltd
Jane T. Crawford: Animal Medical Centre
Stephen M. Cutter: Animal Management in Rural and Remote Indigenous Communities (AMRRIC)
Eric Davis: UC Davis School of Veterinary Medicine
Karina F. de Castro: Centro Universitário de Rio Preto (UNIRP), São José do Rio Preto
Andrigo B. De Nardi: São Paulo State University (UNESP)
Anna P. de Vos: Ladybrand Animal Clinic
Laura Delgadillo Keenan: Veterinary Clinic Sr. Dog’s
Edward M. Donelan: Animal Management in Rural and Remote Indigenous Communities (AMRRIC)
Adela R. Espinoza Huerta: World Vets Latin America Veterinary Training Center
Ibikunle A. Faramade: National Veterinary Research Institute
Mohammed Fazil: Animal Clinic
Eleni Fotopoulou: Intermunicipal Stray Animals Care Centre (DIKEPAZ)
Skye N. Fruean: Animal Protection Society of Samoa
Fanny Gallardo-Arrieta: University of Zulia
Olga Glebova: Veterinary Clinic BIOCONTROL
Pagona G. Gouletsou: University of Thessaly
Rodrigo F. Häfelin Manrique: University of Chile
Joaquim J. G. P. Henriques: OnevetGroup, Hospital Veterinário Berna
Rodrigo S. Horta: Universidade Vila Velha
Natalia Ignatenko: Veterinary Clinic Zoovetservis
Yaghouba Kane: École Inter-états des Sciences et Médecine Vétérinaires de Dakar
Cathy King: World Vets
Debbie Koenig: World Vets
Ada Krupa: Utrecht University
Steven J. Kruzeniski: World Vets Latin America Veterinary Training Center
Marta Lanza-Perea: St. George’s University
Mihran Lazyan: Vetexpert Veterinary Group
Adriana M. Lopez Quintana: Lopez Quintana Veterinary Clinic
Thibault Losfelt: Clinique Veterinaire de Grand Fond, Saint Gilles les Bains
Gabriele Marino: University of Messina
Simón Martínez Castañeda: Universidad Autónoma del Estado de México
Mayra F. Martínez-López: Universidad de las Américas
Bedan M. Masuruli: Veterinary Council of Tanzania
Michael Meyer: Touray & Meyer Vet Clinic
Edward J. Migneco: Hillside Animal Hospital
Berna Nakanwagi: The Kampala Veterinary Surgery
Karter B. Neal: Asavet Veterinary Charities
Winifred Neunzig: World Vets
Sally J. Nixon: Vets Beyond Borders
Antonio Ortega-Pacheco: Autonomous University of Yucatan
Francisco Pedraza-Ordoñez: Universidad de Caldas
Maria C. Peleteiro: University of Lisbon
Katherine Polak: Four Paws International
Ruth J. Pye: Vets Beyond Borders
Juan C. Ramirez-Ante: Universidad de Caldas
John F. Reece: Help in Suffering
Jose Rojas Gutierrez: Veterinary Clinic Dr José Rojas
Haleema Sadia: Balochistan University of Information Technology, Engineering and Management Sciences
Sheila K. Schmeling: Corozal Veterinary Clinic
Olga Shamanova: Veterinary Clinic Vetmaster
Alan G. Sherlock: Vets Beyond Borders
Audrey E. Steenland-Smit: Animal Shelter, Stichting Dierenbescherming Suriname
Alla Svitich: State Hospital of Veterinary Medicine
Lester J. Tapia Martínez: World Vets Latin America Veterinary Training Center
Ismail Thoya Ngoka: Jomo Kenyatta University of Agriculture and Technology
Cristian G. Torres: University of Chile
Elizabeth M. Tudor: University of Melbourne
Mirjam G. van der Wel: Animal Anti Cruelty League
Bogdan A. Vițălaru: Clinical Sciences Department, Faculty of Veterinary Medicine Bucharest
Sevil A. Vural: Ankara University
Oliver Walkinton: Vets Beyond Borders
Alvaro S. Wehrle-Martinez: National University of Asuncion
Sophie A. E. Widdowson: Lilongwe Society for Protection and Care of Animals (LSPCA)
Irina Zvarich: Veterinary clinic Canine Heart
Patrick F. Chinnery: University of Cambridge
Maria Falkenberg: University of Gothenburg
Claes M. Gustafsson: University of Gothenburg
Elizabeth P. Murchison: University of Cambridge

Nature Communications, 2020, vol. 11, issue 1, 1-11

Abstract: Abstract Autonomous replication and segregation of mitochondrial DNA (mtDNA) creates the potential for evolutionary conflict driven by emergence of haplotypes under positive selection for ‘selfish’ traits, such as replicative advantage. However, few cases of this phenomenon arising within natural populations have been described. Here, we survey the frequency of mtDNA horizontal transfer within the canine transmissible venereal tumour (CTVT), a contagious cancer clone that occasionally acquires mtDNA from its hosts. Remarkably, one canine mtDNA haplotype, A1d1a, has repeatedly and recently colonised CTVT cells, recurrently replacing incumbent CTVT haplotypes. An A1d1a control region polymorphism predicted to influence transcription is fixed in the products of an A1d1a recombination event and occurs somatically on other CTVT mtDNA backgrounds. We present a model whereby ‘selfish’ positive selection acting on a regulatory variant drives repeated fixation of A1d1a within CTVT cells.

Date: 2020
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DOI: 10.1038/s41467-020-16765-w

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