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

Pere Gelabert; Marcela Sandoval-Velasco; Aitor Serres; Marc de Manuel; Pere Renom; Ashot Margaryan; Josefin Stiller; Toni de-Dios; Qi Fang; Shaohong Feng; Santi Mañosa; George Pacheco; Manuel Ferrando-Bernal; Guolin Shi; Fei Hao; Xianqing Chen; Bent Petersen; Remi-André Olsen; Arcadi Navarro; Yuan Deng; Love Dalén; Tomàs Marquès-Bonet; Guojie Zhang; Agostinho Antunes; M Thomas P Gilbert; Carles Lalueza-Fox

doi:10.1016/j.cub.2019.10.066

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

Pere Gelabert, Marcela Sandoval-Velasco, Aitor Serres, Marc de Manuel, Pere Renom, Ashot Margaryan, Josefin Stiller, Toni de-Dios, Qi Fang, Shaohong Feng, Santi Mañosa, George Pacheco, Manuel Ferrando-Bernal, Guolin Shi, Fei Hao, Xianqing Chen, Bent Petersen, Remi-André Olsen, Arcadi Navarro, Yuan DengLove Dalén, Tomàs Marquès-Bonet, Guojie Zhang, Agostinho Antunes, M Thomas P Gilbert, Carles Lalueza-Fox

Ecology and Evolution

6 Citations (Scopus)

Abstract

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.

Original language	English
Journal	Current biology : CB
Volume	30
ISSN	0960-9822
DOIs	https://doi.org/10.1016/j.cub.2019.10.066
Publication status	Published - 6 Jan 2020

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Gelabert, P., Sandoval-Velasco, M., Serres, A., de Manuel, M., Renom, P., Margaryan, A., Stiller, J., de-Dios, T., Fang, Q., Feng, S., Mañosa, S., Pacheco, G., Ferrando-Bernal, M., Shi, G., Hao, F., Chen, X., Petersen, B., Olsen, R-A., Navarro, A., ... Lalueza-Fox, C. (2020). Evolutionary History, Genomic Adaptation to Toxic Diet, and Extinction of the Carolina Parakeet. Current biology : CB, 30. https://doi.org/10.1016/j.cub.2019.10.066

Gelabert, P, Sandoval-Velasco, M, Serres, A, de Manuel, M, Renom, P, Margaryan, A , Stiller, J, de-Dios, T, Fang, Q, Feng, S, Mañosa, S, Pacheco, G, Ferrando-Bernal, M, Shi, G, Hao, F, Chen, X, Petersen, B, Olsen, R-A, Navarro, A, Deng, Y, Dalén, L, Marquès-Bonet, T, Zhang, G, Antunes, A, Gilbert, MTP & Lalueza-Fox, C 2020, 'Evolutionary History, Genomic Adaptation to Toxic Diet, and Extinction of the Carolina Parakeet', Current biology : CB, vol. 30. https://doi.org/10.1016/j.cub.2019.10.066

@article{3229ab3a32944a4cac952e0e0c830295,

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

abstract = "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.",

author = "Pere Gelabert and Marcela Sandoval-Velasco and Aitor Serres and {de Manuel}, Marc and Pere Renom and Ashot Margaryan and Josefin Stiller and Toni de-Dios and Qi Fang and Shaohong Feng and Santi Ma{\~n}osa and George Pacheco and Manuel Ferrando-Bernal and Guolin Shi and Fei Hao and Xianqing Chen and Bent Petersen and Remi-Andr{\'e} Olsen and Arcadi Navarro and Yuan Deng and Love Dal{\'e}n and Tom{\`a}s Marqu{\`e}s-Bonet and Guojie Zhang and Agostinho Antunes and Gilbert, {M Thomas P} and Carles Lalueza-Fox",

year = "2020",

month = jan,

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doi = "10.1016/j.cub.2019.10.066",

language = "English",

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journal = "Current Biology",

issn = "0960-9822",

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T1 - Evolutionary History, Genomic Adaptation to Toxic Diet, and Extinction of the Carolina Parakeet

AU - Gelabert, Pere

AU - Sandoval-Velasco, Marcela

AU - Serres, Aitor

AU - de Manuel, Marc

AU - Renom, Pere

AU - Margaryan, Ashot

AU - Stiller, Josefin

AU - de-Dios, Toni

AU - Fang, Qi

AU - Feng, Shaohong

AU - Mañosa, Santi

AU - Pacheco, George

AU - Ferrando-Bernal, Manuel

AU - Shi, Guolin

AU - Hao, Fei

AU - Chen, Xianqing

AU - Petersen, Bent

AU - Olsen, Remi-André

AU - Navarro, Arcadi

AU - Deng, Yuan

AU - Dalén, Love

AU - Marquès-Bonet, Tomàs

AU - Zhang, Guojie

AU - Antunes, Agostinho

AU - Gilbert, M Thomas P

AU - Lalueza-Fox, Carles

PY - 2020/1/6

Y1 - 2020/1/6

N2 - 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.

AB - 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.

U2 - 10.1016/j.cub.2019.10.066

DO - 10.1016/j.cub.2019.10.066

M3 - Journal article

C2 - 31839456

SN - 0960-9822

VL - 30

JO - Current Biology

JF - Current Biology

ER -

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

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