Evolutionary Biology

Lacking conservation genomics in the giant Galápagos tortoise

10.24072/pcjournal.24 - Peer Community Journal, Volume 1 (2021), article no. e18.

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Conservation policy in the giant Galpagos tortoise, an iconic endangered animal, has been assisted by genetic markers for 15 years: a dozen loci have been used to delineate thirteen (sub)species, between which hybridization is prevented. Here, comparative reanalysis of a previously published NGS data set reveals a conflict with traditional markers. Genetic diversity and population substructure in the giant Galpagos tortoise are found to be particularly low, questioning the genetic relevance of current conservation practices. Further examination of giant Galapagos tortoise population genomics is critically needed.

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DOI: https://doi.org/10.24072/pcjournal.24
@article{10_24072_pcjournal_24,
     author = {Loire, Etienne and Galtier, Nicolas},
     title = {Lacking conservation genomics in the giant {Gal\'apagos} tortoise},
     journal = {Peer Community Journal},
     eid = {e18},
     publisher = {Peer Community In},
     volume = {1},
     year = {2021},
     doi = {10.24072/pcjournal.24},
     url = {https://peercommunityjournal.org/articles/10.24072/pcjournal.24/}
}
Loire, Etienne; Galtier, Nicolas. Lacking conservation genomics in the giant Galápagos tortoise. Peer Community Journal, Volume 1 (2021), article  no. e18. doi : 10.24072/pcjournal.24. https://peercommunityjournal.org/articles/10.24072/pcjournal.24/

Peer reviewed and recommended by PCI : 10.24072/pci.evolbiol.100031

[1] Abascal, Federico; Corvelo, André; Cruz, Fernando; Villanueva-Cañas, José L.; Vlasova, Anna; Marcet-Houben, Marina; Martínez-Cruz, Begoña; Cheng, Jade Yu; Prieto, Pablo; Quesada, Víctor; Quilez, Javier; Li, Gang; García, Francisca; Rubio-Camarillo, Miriam; Frias, Leonor; Ribeca, Paolo; Capella-Gutiérrez, Salvador; Rodríguez, José M.; Câmara, Francisco; Lowy, Ernesto; Cozzuto, Luca; Erb, Ionas; Tress, Michael L.; Rodriguez-Ales, Jose L.; Ruiz-Orera, Jorge; Reverter, Ferran; Casas-Marce, Mireia; Soriano, Laura; Arango, Javier R.; Derdak, Sophia; Galán, Beatriz; Blanc, Julie; Gut, Marta; Lorente-Galdos, Belen; Andrés-Nieto, Marta; López-Otín, Carlos; Valencia, Alfonso; Gut, Ivo; García, José L.; Guigó, Roderic; Murphy, William J.; Ruiz-Herrera, Aurora; Marques-Bonet, Tomas; Roma, Guglielmo; Notredame, Cedric; Mailund, Thomas; Albà, M. Mar; Gabaldón, Toni; Alioto, Tyler; Godoy, José A. Extreme genomic erosion after recurrent demographic bottlenecks in the highly endangered Iberian lynx, Genome Biology, Volume 17 (2016) no. 1 | Article

[2] Aguilera, Washington Tapia; Málaga, Jeffreys; Gibbs, James P. Giant tortoises hatch on Galapagos island, Nature, Volume 517 (2015) no. 7534, p. 271-271 | Article

[3] Allendorf, Fred W.; Hohenlohe, Paul A.; Luikart, Gordon Genomics and the future of conservation genetics, Nature Reviews Genetics, Volume 11 (2010) no. 10, pp. 697-709 | Article

[4] Ballenghien, Marion; Faivre, Nicolas; Galtier, Nicolas Patterns of cross-contamination in a multispecies population genomic project: detection, quantification, impact, and solutions, BMC Biology, Volume 15 (2017) no. 1 | Article

[5] Bazin, Eric; Glémin, Sylvain; Galtier, Nicolas Population Size Does Not Influence Mitochondrial Genetic Diversity in Animals, Science, Volume 312 (2006) no. 5773, pp. 570-572 | Article

[6] Caccone, Adalgisa; Gentile, Gabriele; Gibbs, James P.; Fritts, Thomas H.; Snell, Howard L.; Betts, Jessica; Powell, Jeffrey R. PHYLOGEOGRAPHY AND HISTORY OF GIANT GALÁPAGOS TORTOISES, Evolution, Volume 56 (2004) no. 10 | Article

[7] Caccone, Adalgisa; Gentile, Gabriele; Burns, Catherine E.; Sezzi, Erminia; Bergman, Windsong; Ruelle, Morgan; Saltonstall, Kristin; Powell, Jeffrey R. Extreme difference in rate of mitochondrial and nuclear DNA evolution in a large ectotherm, Galápagos tortoises, Molecular Phylogenetics and Evolution, Volume 31 no. 2, pp. 794-798 | Article

[8] Cayot, L. J. The restoration of giant tortoises and land iguana populations in Galápagos, Galápagos Research, Volume 65 (2008)

[9] Chiari, Ylenia; Hyseni, Chaz; Fritts, Tom H.; Glaberman, Scott; Marquez, Cruz; Gibbs, James P.; Claude, Julien; Caccone, Adalgisa Morphometrics Parallel Genetics in a Newly Discovered and Endangered Taxon of Galápagos Tortoise, PLoS ONE, Volume 4 (2009) no. 7 | Article

[10] Ciofi, Claudio; Milinkovitch, Michel C.; Gibbs, James P.; Caccone, Adalgisa; Powell, Jeffrey R. Microsatellite analysis of genetic divergence among populations of giant Galápagos tortoises, Molecular Ecology, Volume 11 (2002) no. 11, pp. 2265-2283 | Article

[11] Der Sarkissian, Clio; Ermini, Luca; Schubert, Mikkel; Yang, Melinda A.; Librado, Pablo; Fumagalli, Matteo; Jónsson, Hákon; Bar-Gal, Gila Kahila; Albrechtsen, Anders; Vieira, Filipe G.; Petersen, Bent; Ginolhac, Aurélien; Seguin-Orlando, Andaine; Magnussen, Kim; Fages, Antoine; Gamba, Cristina; Lorente-Galdos, Belen; Polani, Sagi; Steiner, Cynthia; Neuditschko, Markus; Jagannathan, Vidhya; Feh, Claudia; Greenblatt, Charles L.; Ludwig, Arne; Abramson, Natalia I.; Zimmermann, Waltraut; Schafberg, Renate; Tikhonov, Alexei; Sicheritz-Ponten, Thomas; Willerslev, Eske; Marques-Bonet, Tomas; Ryder, Oliver A.; McCue, Molly; Rieder, Stefan; Leeb, Tosso; Slatkin, Montgomery; Orlando, Ludovic Evolutionary Genomics and Conservation of the Endangered Przewalski’s Horse, Current Biology, Volume 25 (2015) no. 19, pp. 2577-2583 | Article

[12] Dobrynin, Pavel; Liu, Shiping; Tamazian, Gaik; Xiong, Zijun; Yurchenko, Andrey A.; Krasheninnikova, Ksenia; Kliver, Sergey; Schmidt-Küntzel, Anne; Koepfli, Klaus-Peter; Johnson, Warren; Kuderna, Lukas F.K.; García-Pérez, Raquel; Manuel, Marc de; Godinez, Ricardo; Komissarov, Aleksey; Makunin, Alexey; Brukhin, Vladimir; Qiu, Weilin; Zhou, Long; Li, Fang; Yi, Jian; Driscoll, Carlos; Antunes, Agostinho; Oleksyk, Taras K.; Eizirik, Eduardo; Perelman, Polina; Roelke, Melody; Wildt, David; Diekhans, Mark; Marques-Bonet, Tomas; Marker, Laurie; Bhak, Jong; Wang, Jun; Zhang, Guojie; O’Brien, Stephen J. Genomic legacy of the African cheetah, Acinonyx jubatus, Genome Biology, Volume 16 (2015) no. 1 | Article

[13] EDMANDS, SUZANNE Between a rock and a hard place: evaluating the relative risks of inbreeding and outbreeding for conservation and management, Molecular Ecology, Volume 16 (2007) no. 3, pp. 463-475 | Article

[14] Edwards, Danielle L.; Benavides, Edgar; Garrick, Ryan C.; Gibbs, James P.; Russello, Michael A.; Dion, Kirstin B.; Hyseni, Chaz; Flanagan, Joseph P.; Tapia, Washington; Caccone, Adalgisa The genetic legacy of Lonesome George survives: Giant tortoises with Pinta Island ancestry identified in Galápagos, Biological Conservation, Volume 157 (2013), pp. 225-228 | Article

[15] Edwards, D. L.; Garrick, R. C.; Tapia, W.; Caccone, A. Cryptic structure and niche divergence within threatened Galápagos giant tortoises from southern Isabela Island, Conservation Genetics, Volume 15 (2014) no. 6, pp. 1357-1369 | Article

[16] Frankham, Richard; Bradshaw, Corey J.A.; Brook, Barry W. Genetics in conservation management: Revised recommendations for the 50/500 rules, Red List criteria and population viability analyses, Biological Conservation, Volume 170 (2014), pp. 56-63 | Article

[17] Frankham, Richard Genetic rescue of small inbred populations: meta-analysis reveals large and consistent benefits of gene flow, Molecular Ecology, Volume 24 (2015) no. 11, pp. 2610-2618 | Article

[18] Funk, W. Chris; McKay, John K.; Hohenlohe, Paul A.; Allendorf, Fred W. Harnessing genomics for delineating conservation units, Trends in Ecology & Evolution, Volume 27 (2012) no. 9, pp. 489-496 | Article

[19] Galtier, Nicolas Adaptive Protein Evolution in Animals and the Effective Population Size Hypothesis, PLOS Genetics, Volume 12 (2016) no. 1 | Article

[20] Gayral, Philippe; Melo-Ferreira, José; Glémin, Sylvain; Bierne, Nicolas; Carneiro, Miguel; Nabholz, Benoit; Lourenco, Joao M.; Alves, Paulo C.; Ballenghien, Marion; Faivre, Nicolas; Belkhir, Khalid; Cahais, Vincent; Loire, Etienne; Bernard, Aurélien; Galtier, Nicolas Reference-Free Population Genomics from Next-Generation Transcriptome Data and the Vertebrate–Invertebrate Gap, PLoS Genetics, Volume 9 (2013) no. 4 | Article

[21] Garrick, Ryan C.; Benavides, Edgar; Russello, Michael A.; Gibbs, James P.; Poulakakis, Nikos; Dion, Kirstin B.; Hyseni, Chaz; Kajdacsi, Brittney; Márquez, Lady; Bahan, Sarah; Ciofi, Claudio; Tapia, Washington; Caccone, Adalgisa Genetic rediscovery of an ‘extinct’ Galápagos giant tortoise species, Current Biology, Volume 22 (2012) no. 1 | Article

[22] Garrick, Ryan C.; Benavides, Edgar; Russello, Michael A.; Hyseni, Chaz; Edwards, Danielle L.; Gibbs, James P.; Tapia, Washington; Ciofi, Claudio; Caccone, Adalgisa Lineage fusion in Galápagos giant tortoises, Molecular Ecology, Volume 23 (2014) no. 21, pp. 5276-5290 | Article

[23] Gibbs, James P.; Hunter, Elizabeth A.; Shoemaker, Kevin T.; Tapia, Washington H.; Cayot, Linda J. Demographic Outcomes and Ecosystem Implications of Giant Tortoise Reintroduction to Española Island, Galapagos, PLoS ONE, Volume 9 (2014) no. 10 | Article

[24] HUNTER, ELIZABETH A.; GIBBS, JAMES P.; CAYOT, LINDA J.; TAPIA, WASHINGTON Equivalency of Galápagos Giant Tortoises Used as Ecological Replacement Species to Restore Ecosystem Functions, Conservation Biology, Volume 27 (2013) no. 4, pp. 701-709 | Article

[25] Lamichhaney, Sangeet; Berglund, Jonas; Almén, Markus Sällman; Maqbool, Khurram; Grabherr, Manfred; Martinez-Barrio, Alvaro; Promerová, Marta; Rubin, Carl-Johan; Wang, Chao; Zamani, Neda; Grant, B. Rosemary; Grant, Peter R.; Webster, Matthew T.; Andersson, Leif Evolution of Darwin’s finches and their beaks revealed by genome sequencing, Nature, Volume 518 (2015) no. 7539, pp. 371-375 | Article

[26] Li, Heng; Durbin, Richard Inference of human population history from individual whole-genome sequences, Nature, Volume 475 (2011) no. 7357, pp. 493-496 | Article

[27] Liu, Shiping; Lorenzen, Eline D.; Fumagalli, Matteo; Li, Bo; Harris, Kelley; Xiong, Zijun; Zhou, Long; Korneliussen, Thorfinn Sand; Somel, Mehmet; Babbitt, Courtney; Wray, Greg; Li, Jianwen; He, Weiming; Wang, Zhuo; Fu, Wenjing; Xiang, Xueyan; Morgan, Claire C.; Doherty, Aoife; O’Connell, Mary J.; McInerney, James O.; Born, Erik W.; Dalén, Love; Dietz, Rune; Orlando, Ludovic; Sonne, Christian; Zhang, Guojie; Nielsen, Rasmus; Willerslev, Eske; Wang, Jun Population Genomics Reveal Recent Speciation and Rapid Evolutionary Adaptation in Polar Bears, Cell, Volume 157 (2014) no. 4, pp. 785-794 | Article

[28] Loire, Etienne; Chiari, Ylenia; Bernard, Aurélien; Cahais, Vincent; Romiguier, Jonathan; Nabholz, Benoît; Lourenço, Joao; Galtier, Nicolas Population genomics of the endangered giant Galápagos tortoise, Genome Biology, Volume 14 (2013) no. 12 | Article

[29] Márquez, Cruz; Gibbs, James P.; Carrión, Victor; Naranjo, Sixto; Llerena, Alizon Population Response of Giant Galápagos Tortoises to Feral Goat Removal, Restoration Ecology, Volume 21 (2013) no. 2, pp. 181-185 | Article

[30] Milinkovitch, Michel C.; Monteyne, Daniel; Gibbs, James P.; Fritts, Thomas H.; Tapia, Washington; Snell, Howard L.; Tiedemann, Ralph; Caccone, Adalgisa; Powell, Jeffrey R. Genetic analysis of a successful repatriation programme: giant Galápagos tortoises, Proceedings of the Royal Society of London. Series B: Biological Sciences, Volume 271 (2004) no. 1537, pp. 341-345 | Article

[31] Milinkovitch, Michel C; Monteyne, Daniel; Russello, Michael; Gibbs, James P; Snell, Howard L; Tapia, Washington; Marquez, Cruz; Caccone, Adalgisa; Powell, Jeffrey R Giant Galápagos tortoises; molecular genetic analyses identify a trans-island hybrid in a repatriation program of an endangered taxon, BMC Ecology, Volume 7 (2007) no. 1 | Article

[32] Moore, Jean-Sébastien; Bourret, Vincent; Dionne, Mélanie; Bradbury, Ian; O'Reilly, Patrick; Kent, Matthew; Chaput, Gérald; Bernatchez, Louis Conservation genomics of anadromous Atlantic salmon across its North American range: outlier loci identify the same patterns of population structure as neutral loci, Molecular Ecology, Volume 23 (2014) no. 23, pp. 5680-5697 | Article

[33] Nicholls, Henry Lonesome George 'look-alike' captured for tortoise-breeding effort, Nature (2015) | Article

[34] Perry, George H.; Melsted, Páll; Marioni, John C.; Wang, Ying; Bainer, Russell; Pickrell, Joseph K.; Michelini, Katelyn; Zehr, Sarah; Yoder, Anne D.; Stephens, Matthew; Pritchard, Jonathan K.; Gilad, Yoav Comparative RNA sequencing reveals substantial genetic variation in endangered primates, Genome Research, Volume 22 (2012) no. 4, pp. 602-610 | Article

[35] Poulakakis, Nikos; Glaberman, Scott; Russello, Michael; Beheregaray, Luciano B.; Ciofi, Claudio; Powell, Jeffrey R.; Caccone, Adalgisa Historical DNA analysis reveals living descendants of an extinct species of Galápagos tortoise, Proceedings of the National Academy of Sciences, Volume 105 (2008) no. 40, pp. 15464-15469 | Article

[36] POULAKAKIS, NIKOS; RUSSELLO, MICHAEL; GEIST, DENNIS; CACCONE, ADALGISA Unravelling the peculiarities of island life: vicariance, dispersal and the diversification of the extinct and extant giant Galápagos tortoises, Molecular Ecology, Volume 21 (2012) no. 1, pp. 160-173 | Article

[37] Poulakakis, Nikos; Edwards, Danielle L.; Chiari, Ylenia; Garrick, Ryan C.; Russello, Michael A.; Benavides, Edgar; Watkins-Colwell, Gregory J.; Glaberman, Scott; Tapia, Washington; Gibbs, James P.; Cayot, Linda J.; Caccone, Adalgisa Description of a New Galapagos Giant Tortoise Species (Chelonoidis; Testudines: Testudinidae) from Cerro Fatal on Santa Cruz Island, PLOS ONE, Volume 10 (2015) no. 10 | Article

[38] Romiguier, J.; Gayral, P.; Ballenghien, M.; Bernard, A.; Cahais, V.; Chenuil, A.; Chiari, Y.; Dernat, R.; Duret, L.; Faivre, N.; Loire, E.; Lourenco, J. M.; Nabholz, B.; Roux, C.; Tsagkogeorga, G.; Weber, A. A.-T.; Weinert, L. A.; Belkhir, K.; Bierne, N.; Glémin, S.; Galtier, N. Comparative population genomics in animals uncovers the determinants of genetic diversity, Nature, Volume 515 (2014) no. 7526, pp. 261-263 | Article

[39] Romiguier, Jonathan; Fournier, Axel; Yek, Sze Huei; Keller, Laurent Convergent evolution of social hybridogenesis in Messor harvester ants, Molecular Ecology, Volume 26 (2017) no. 4, pp. 1108-1117 | Article

[40] Roux, Camille; Fraïsse, Christelle; Romiguier, Jonathan; Anciaux, Yoann; Galtier, Nicolas; Bierne, Nicolas Shedding Light on the Grey Zone of Speciation along a Continuum of Genomic Divergence, PLOS Biology, Volume 14 (2016) no. 12 | Article

[41] Russello, Michael A.; Beheregaray, Luciano B.; Gibbs, James P.; Fritts, Thomas; Havill, Nathan; Powell, Jeffrey R.; Caccone, Adalgisa Lonesome George is not alone among Galápagos tortoises, Current Biology, Volume 17 (2007) no. 9 | Article

[42] Shafer, Aaron B.A.; Wolf, Jochen B.W.; Alves, Paulo C.; Bergström, Linnea; Bruford, Michael W.; Brännström, Ioana; Colling, Guy; Dalén, Love; De Meester, Luc; Ekblom, Robert; Fawcett, Katie D.; Fior, Simone; Hajibabaei, Mehrdad; Hill, Jason A.; Hoezel, A. Rus; Höglund, Jacob; Jensen, Evelyn L.; Krause, Johannes; Kristensen, Torsten N.; Krützen, Michael; McKay, John K.; Norman, Anita J.; Ogden, Rob; Österling, E. Martin; Ouborg, N. Joop; Piccolo, John; Popović, Danijela; Primmer, Craig R.; Reed, Floyd A.; Roumet, Marie; Salmona, Jordi; Schenekar, Tamara; Schwartz, Michael K.; Segelbacher, Gernot; Senn, Helen; Thaulow, Jens; Valtonen, Mia; Veale, Andrew; Vergeer, Philippine; Vijay, Nagarjun; Vilà, Carles; Weissensteiner, Matthias; Wennerström, Lovisa; Wheat, Christopher W.; Zieliński, Piotr Genomics and the challenging translation into conservation practice, Trends in Ecology & Evolution, Volume 30 (2015) no. 2, pp. 78-87 | Article

[43] Taylor, Barbara L.; Perrin, William F.; Reeves, Randall R.; Rosel, Patricia E.; Wang, John Y.; Cipriano, Frank; Scott Baker, C.; Brownell, Robert L. Why we should develop guidelines and quantitative standards for using genetic data to delimit subspecies for data-poor organisms like cetaceans, Marine Mammal Science, Volume 33 (2017) no. S1, pp. 12-26 | Article

[44] Walling, Craig A; Nussey, Daniel H; Morris, Alison; Clutton-Brock, Tim H; Kruuk, Loeske EB; Pemberton, Josephine M Inbreeding depression in red deer calves, BMC Evolutionary Biology, Volume 11 (2011) no. 1 | Article

[45] Weir, B. S.; Cockerham, C. Clark ESTIMATING F -STATISTICS FOR THE ANALYSIS OF POPULATION STRUCTURE, Evolution, Volume 38 (1984) no. 6, pp. 1358-1370 | Article

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