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Recurrent horizontal transfer identifies mitochondrial positive selection in a transmissible cancer.

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.

SUBMITTER: Strakova A 

PROVIDER: S-EPMC7297733 | biostudies-literature | 2020 Jun

REPOSITORIES: biostudies-literature

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Recurrent horizontal transfer identifies mitochondrial positive selection in a transmissible cancer.

Strakova Andrea A   Nicholls Thomas J TJ   Baez-Ortega Adrian A   Ní Leathlobhair Máire M   Sampson Alexander T AT   Hughes Katherine K   Bolton Isobelle A G IAG   Gori Kevin K   Wang Jinhong J   Airikkala-Otter Ilona I   Allen Janice L JL   Allum Karen M KM   Arnold Clara L CL   Bansse-Issa Leontine L   Bhutia Thinlay N TN   Bisson Jocelyn L JL   Blank Kelli K   Briceño Cristóbal C   Castillo Domracheva Artemio A   Corrigan Anne M AM   Cran Hugh R HR   Crawford Jane T JT   Cutter Stephen M SM   Davis Eric E   de Castro Karina F KF   De Nardi Andrigo B AB   de Vos Anna P AP   Delgadillo Keenan Laura L   Donelan Edward M EM   Espinoza Huerta Adela R AR   Faramade Ibikunle A IA   Fazil Mohammed M   Fotopoulou Eleni E   Fruean Skye N SN   Gallardo-Arrieta Fanny F   Glebova Olga O   Gouletsou Pagona G PG   Häfelin Manrique Rodrigo F RF   Henriques Joaquim J G P JJGP   Horta Rodrigo S RS   Ignatenko Natalia N   Kane Yaghouba Y   King Cathy C   Koenig Debbie D   Krupa Ada A   Kruzeniski Steven J SJ   Lanza-Perea Marta M   Lazyan Mihran M   Lopez Quintana Adriana M AM   Losfelt Thibault T   Marino Gabriele G   Martínez Castañeda Simón S   Martínez-López Mayra F MF   Masuruli Bedan M BM   Meyer Michael M   Migneco Edward J EJ   Nakanwagi Berna B   Neal Karter B KB   Neunzig Winifred W   Nixon Sally J SJ   Ortega-Pacheco Antonio A   Pedraza-Ordoñez Francisco F   Peleteiro Maria C MC   Polak Katherine K   Pye Ruth J RJ   Ramirez-Ante Juan C JC   Reece John F JF   Rojas Gutierrez Jose J   Sadia Haleema H   Schmeling Sheila K SK   Shamanova Olga O   Sherlock Alan G AG   Steenland-Smit Audrey E AE   Svitich Alla A   Tapia Martínez Lester J LJ   Thoya Ngoka Ismail I   Torres Cristian G CG   Tudor Elizabeth M EM   van der Wel Mirjam G MG   Vițălaru Bogdan A BA   Vural Sevil A SA   Walkinton Oliver O   Wehrle-Martinez Alvaro S AS   Widdowson Sophie A E SAE   Zvarich Irina I   Chinnery Patrick F PF   Falkenberg Maria M   Gustafsson Claes M CM   Murchison Elizabeth P EP  

Nature communications 20200616 1

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  ...[more]

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