Evolutionary History, Genomic Adaptation to Toxic Diet, and Extinction of the Carolina Parakeet

As the only endemic neotropical parrot to have recently lived in the northern hemisphere, the Carolina parakeet (Conuropsis carolinensis) was an iconic North American bird. The last surviving specimen died in the Cincinnati Zoo in 1918 [1]. The cause of its extinction remains contentious: besides excessive mortality associated to habitat destruction and active hunting, their survival could have been negatively affected by its range having become increasingly patchy [2] or by the exposure to poultry pathogens [3, 4]. In addition, the Carolina parakeet showed a predilection for cockleburs, an herbaceous plant that contains a powerful toxin, carboxyatractyloside, or CAT [5], which did not seem to affect them but made the birds notoriously toxic to most predators [3]. To explore the demographic history of this bird, we generated the complete genomic sequence of a preserved specimen held in a private collection in Espinelves (Girona, Spain), as well as of a close extant relative, Aratinga solstitialis. We identified two non-synonymous genetic changes in two highly conserved proteins known to interact with CAT that could underlie a specific dietary adaptation to this toxin. Our genomic analyses did not reveal evidence of a dramatic past demographic decline in the Carolina parakeet; also, its genome did not exhibit the long runs of homozygosity that are signals of recent inbreeding and are typically found in endangered species. As such, our results suggest its extinction was an abrupt process and thus likely solely attributable to human causes. Gelabert et al. report the whole genome of the extinct Carolina parakeet and provide evidence of its phylogeny, adaptation to a toxic cocklebur diet, and demographic history. The lack of signs of recent inbreeding typically found in endangered species suggests its abrupt extinction was human mediated.

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Main Authors: Gelabert, Pere, Sandoval-Velasco, Marcela, Serres-Armero, Aitor, Manuel, Marc de, Renom, P., Margaryan, Ashot, Stiller, Josefin, De-Dios, Toni, Fang, Qi, Feng, Shaohong, Mañosa, Santi, Pacheco, George, Ferrando-Bernal, Manuel, Shi, Goulin, Hao, Fei, Chen, Xianqing, Petersen, Bent, Olsen, Remi‐André, Navarro, Arcadi, Deng, Yuan, Dalén, Love, Marqués-Bonet, Tomàs, Zhang, Guojie, Antunes, Agostinho, Gilbert, M. Thomas P., Lalueza-Fox, Carles
Other Authors: European Research Council
Format: artículo biblioteca
Published: Cell Press 2020-01-06
Online Access:http://hdl.handle.net/10261/236302
http://dx.doi.org/10.13039/501100011033
http://dx.doi.org/10.13039/501100000780
http://dx.doi.org/10.13039/501100000781
http://dx.doi.org/10.13039/501100001871
http://dx.doi.org/10.13039/501100002809
http://dx.doi.org/10.13039/100000011
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description As the only endemic neotropical parrot to have recently lived in the northern hemisphere, the Carolina parakeet (Conuropsis carolinensis) was an iconic North American bird. The last surviving specimen died in the Cincinnati Zoo in 1918 [1]. The cause of its extinction remains contentious: besides excessive mortality associated to habitat destruction and active hunting, their survival could have been negatively affected by its range having become increasingly patchy [2] or by the exposure to poultry pathogens [3, 4]. In addition, the Carolina parakeet showed a predilection for cockleburs, an herbaceous plant that contains a powerful toxin, carboxyatractyloside, or CAT [5], which did not seem to affect them but made the birds notoriously toxic to most predators [3]. To explore the demographic history of this bird, we generated the complete genomic sequence of a preserved specimen held in a private collection in Espinelves (Girona, Spain), as well as of a close extant relative, Aratinga solstitialis. We identified two non-synonymous genetic changes in two highly conserved proteins known to interact with CAT that could underlie a specific dietary adaptation to this toxin. Our genomic analyses did not reveal evidence of a dramatic past demographic decline in the Carolina parakeet; also, its genome did not exhibit the long runs of homozygosity that are signals of recent inbreeding and are typically found in endangered species. As such, our results suggest its extinction was an abrupt process and thus likely solely attributable to human causes. Gelabert et al. report the whole genome of the extinct Carolina parakeet and provide evidence of its phylogeny, adaptation to a toxic cocklebur diet, and demographic history. The lack of signs of recent inbreeding typically found in endangered species suggests its abrupt extinction was human mediated.
author2 European Research Council
author_facet European Research Council
Gelabert, Pere
Sandoval-Velasco, Marcela
Serres-Armero, Aitor
Manuel, Marc de
Renom, P.
Margaryan, Ashot
Stiller, Josefin
De-Dios, Toni
Fang, Qi
Feng, Shaohong
Mañosa, Santi
Pacheco, George
Ferrando-Bernal, Manuel
Shi, Goulin
Hao, Fei
Chen, Xianqing
Petersen, Bent
Olsen, Remi‐André
Navarro, Arcadi
Deng, Yuan
Dalén, Love
Marqués-Bonet, Tomàs
Zhang, Guojie
Antunes, Agostinho
Gilbert, M. Thomas P.
Lalueza-Fox, Carles
format artículo
author Gelabert, Pere
Sandoval-Velasco, Marcela
Serres-Armero, Aitor
Manuel, Marc de
Renom, P.
Margaryan, Ashot
Stiller, Josefin
De-Dios, Toni
Fang, Qi
Feng, Shaohong
Mañosa, Santi
Pacheco, George
Ferrando-Bernal, Manuel
Shi, Goulin
Hao, Fei
Chen, Xianqing
Petersen, Bent
Olsen, Remi‐André
Navarro, Arcadi
Deng, Yuan
Dalén, Love
Marqués-Bonet, Tomàs
Zhang, Guojie
Antunes, Agostinho
Gilbert, M. Thomas P.
Lalueza-Fox, Carles
spellingShingle Gelabert, Pere
Sandoval-Velasco, Marcela
Serres-Armero, Aitor
Manuel, Marc de
Renom, P.
Margaryan, Ashot
Stiller, Josefin
De-Dios, Toni
Fang, Qi
Feng, Shaohong
Mañosa, Santi
Pacheco, George
Ferrando-Bernal, Manuel
Shi, Goulin
Hao, Fei
Chen, Xianqing
Petersen, Bent
Olsen, Remi‐André
Navarro, Arcadi
Deng, Yuan
Dalén, Love
Marqués-Bonet, Tomàs
Zhang, Guojie
Antunes, Agostinho
Gilbert, M. Thomas P.
Lalueza-Fox, Carles
Evolutionary History, Genomic Adaptation to Toxic Diet, and Extinction of the Carolina Parakeet
author_sort Gelabert, Pere
title Evolutionary History, Genomic Adaptation to Toxic Diet, and Extinction of the Carolina Parakeet
title_short Evolutionary History, Genomic Adaptation to Toxic Diet, and Extinction of the Carolina Parakeet
title_full Evolutionary History, Genomic Adaptation to Toxic Diet, and Extinction of the Carolina Parakeet
title_fullStr Evolutionary History, Genomic Adaptation to Toxic Diet, and Extinction of the Carolina Parakeet
title_full_unstemmed Evolutionary History, Genomic Adaptation to Toxic Diet, and Extinction of the Carolina Parakeet
title_sort evolutionary history, genomic adaptation to toxic diet, and extinction of the carolina parakeet
publisher Cell Press
publishDate 2020-01-06
url http://hdl.handle.net/10261/236302
http://dx.doi.org/10.13039/501100011033
http://dx.doi.org/10.13039/501100000780
http://dx.doi.org/10.13039/501100000781
http://dx.doi.org/10.13039/501100001871
http://dx.doi.org/10.13039/501100002809
http://dx.doi.org/10.13039/100000011
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spelling dig-ibe-es-10261-2363022021-09-29T08:53:52Z Evolutionary History, Genomic Adaptation to Toxic Diet, and Extinction of the Carolina Parakeet Gelabert, Pere Sandoval-Velasco, Marcela Serres-Armero, Aitor Manuel, Marc de Renom, P. Margaryan, Ashot Stiller, Josefin De-Dios, Toni Fang, Qi Feng, Shaohong Mañosa, Santi Pacheco, George Ferrando-Bernal, Manuel Shi, Goulin Hao, Fei Chen, Xianqing Petersen, Bent Olsen, Remi‐André Navarro, Arcadi Deng, Yuan Dalén, Love Marqués-Bonet, Tomàs Zhang, Guojie Antunes, Agostinho Gilbert, M. Thomas P. Lalueza-Fox, Carles European Research Council European Commission Fundación "la Caixa" Generalitat de Catalunya Ministerio de Ciencia, Innovación y Universidades (España) Agencia Estatal de Investigación (España) Howard Hughes Medical Institute Fundação para a Ciência e a Tecnologia (Portugal) As the only endemic neotropical parrot to have recently lived in the northern hemisphere, the Carolina parakeet (Conuropsis carolinensis) was an iconic North American bird. The last surviving specimen died in the Cincinnati Zoo in 1918 [1]. The cause of its extinction remains contentious: besides excessive mortality associated to habitat destruction and active hunting, their survival could have been negatively affected by its range having become increasingly patchy [2] or by the exposure to poultry pathogens [3, 4]. In addition, the Carolina parakeet showed a predilection for cockleburs, an herbaceous plant that contains a powerful toxin, carboxyatractyloside, or CAT [5], which did not seem to affect them but made the birds notoriously toxic to most predators [3]. To explore the demographic history of this bird, we generated the complete genomic sequence of a preserved specimen held in a private collection in Espinelves (Girona, Spain), as well as of a close extant relative, Aratinga solstitialis. We identified two non-synonymous genetic changes in two highly conserved proteins known to interact with CAT that could underlie a specific dietary adaptation to this toxin. Our genomic analyses did not reveal evidence of a dramatic past demographic decline in the Carolina parakeet; also, its genome did not exhibit the long runs of homozygosity that are signals of recent inbreeding and are typically found in endangered species. As such, our results suggest its extinction was an abrupt process and thus likely solely attributable to human causes. Gelabert et al. report the whole genome of the extinct Carolina parakeet and provide evidence of its phylogeny, adaptation to a toxic cocklebur diet, and demographic history. The lack of signs of recent inbreeding typically found in endangered species suggests its abrupt extinction was human mediated. This work was supported by ERC Consolidator Grant 681396 “Extinction Genomics” to M.T.P.G. and M.S.-V., Obra Social ‘‘La Caixa’’ and Secretaria d’Universitats i Recerca ( GRC2017-SGR880 ) to T.M.-B. and C.L.-F., BFU2017-86471-P and PGC2018-101927-B-I00 from MINECO/FEDER, UE to T.M.-B, and PGC2018-095931-B-100 from MINECO/FEDER, UE to C.L.-F. T.M.-B. is also supported by a U01 MH106874 grant and Howard Hughes International Early Career and CERCA Programme (Generalitat de Catalunya). A.A. is partially supported by the Strategic Funding UID/Multi/04423/2019 through national funds provided by the Portuguese Foundation for Science and Technology (FCT) and the European Regional Development Fund —program PT2020 , by the European Structural and Investment Funds —Competitiveness and Internationalization Operational Program-COMPETE 2020, and by National Funds through the FCT under the project PTDC/CTA-AMB/31774/2017(POCI-01-0145-FEDER/031774/2017 ). 2021-03-29T11:30:03Z 2021-03-29T11:30:03Z 2020-01-06 2021-03-29T11:30:03Z artículo http://purl.org/coar/resource_type/c_6501 doi: 10.1016/j.cub.2019.10.066 issn: 0960-9822 e-issn: 1879-0445 Current Biology 30: 108-114.e5 (2020) http://hdl.handle.net/10261/236302 10.1016/j.cub.2019.10.066 http://dx.doi.org/10.13039/501100011033 http://dx.doi.org/10.13039/501100000780 http://dx.doi.org/10.13039/501100000781 http://dx.doi.org/10.13039/501100001871 http://dx.doi.org/10.13039/501100002809 http://dx.doi.org/10.13039/100000011 #PLACEHOLDER_PARENT_METADATA_VALUE# #PLACEHOLDER_PARENT_METADATA_VALUE# #PLACEHOLDER_PARENT_METADATA_VALUE# #PLACEHOLDER_PARENT_METADATA_VALUE# #PLACEHOLDER_PARENT_METADATA_VALUE# #PLACEHOLDER_PARENT_METADATA_VALUE# #PLACEHOLDER_PARENT_METADATA_VALUE# info:eu-repo/grantAgreement/EC/H2020/681396 info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/BFU2017-86471-P info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PGC2018-101927-B-I00 BFU2017-86471-P/AEI/10.13039/501100011033 PGC2018-101927-B-I00/AEI/10.13039/501100011033 info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PGC2018-095931-B-100 PGC2018-095931-B-100/AEI/10.13039/501100011033 Publisher's version http://dx.doi.org/10.1016/j.cub.2019.10.066 Sí open Cell Press