Section: Evolutionary Biology
Topic: Evolution, Genetics/Genomics, Population biology

Lacking conservation genomics in the giant Galápagos tortoise

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

Get full text PDF Peer reviewed and recommended by PCI
article image

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.

Published online:
DOI: 10.24072/pcjournal.24
Type: Research article

Loire, Etienne 1; Galtier, Nicolas 2

1 Centre de Coopération Internationale en Recherche Agronomique pour le Développement (CIRAD), UMR CMAEE and C2B, Montpellier, France
2 ISEM - Univ Montpellier - CNRS - IRD, Montpellier, France
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights
     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 = {}
AU  - Loire, Etienne
AU  - Galtier, Nicolas
TI  - Lacking conservation genomics in the giant Galápagos tortoise
JO  - Peer Community Journal
PY  - 2021
VL  - 1
PB  - Peer Community In
UR  -
DO  - 10.24072/pcjournal.24
ID  - 10_24072_pcjournal_24
ER  - 
%0 Journal Article
%A Loire, Etienne
%A Galtier, Nicolas
%T Lacking conservation genomics in the giant Galápagos tortoise
%J Peer Community Journal
%D 2021
%V 1
%I Peer Community In
%R 10.24072/pcjournal.24
%F 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.

PCI peer reviews and recommendation, and links to data, scripts, code and supplementary information: 10.24072/pci.evolbiol.100031

Conflict of interest of the recommender and peer reviewers:
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.

[1] Abascal, F.; Corvelo, A.; Cruz, F.; Villanueva-Cañas, J. L.; Vlasova, A.; Marcet-Houben, M.; Martínez-Cruz, B.; Cheng, J. Y.; Prieto, P.; Quesada, V.; Quilez, J.; Li, G.; García, F.; Rubio-Camarillo, M.; Frias, L.; Ribeca, P.; Capella-Gutiérrez, S.; Rodríguez, J. M.; Câmara, F.; Lowy, E.; Cozzuto, L.; Erb, I.; Tress, M. L.; Rodriguez-Ales, J. L.; Ruiz-Orera, J.; Reverter, F.; Casas-Marce, M.; Soriano, L.; Arango, J. R.; Derdak, S.; Galán, B.; Blanc, J.; Gut, M.; Lorente-Galdos, B.; Andrés-Nieto, M.; López-Otín, C.; Valencia, A.; Gut, I.; García, J. L.; Guigó, R.; Murphy, W. J.; Ruiz-Herrera, A.; Marques-Bonet, T.; Roma, G.; Notredame, C.; Mailund, T.; Albà, M. M.; Gabaldón, T.; Alioto, T.; Godoy, J. A. Extreme genomic erosion after recurrent demographic bottlenecks in the highly endangered Iberian lynx, Genome Biology, Volume 17 (2016) no. 1 | DOI

[2] Aguilera, W. T.; Málaga, J.; Gibbs, J. P. Giant tortoises hatch on Galapagos island, Nature, Volume 517 (2015) no. 7534, p. 271-271 | DOI

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

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

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

[6] Caccone, A.; Gentile, G.; Gibbs, J. P.; Fritts, T. H.; Snell, H. L.; Betts, J.; Powell, J. R. PHYLOGEOGRAPHY AND HISTORY OF GIANT GALÁPAGOS TORTOISES, Evolution, Volume 56 (2004) no. 10 | DOI

[7] Caccone, A.; Gentile, G.; Burns, C. E.; Sezzi, E.; Bergman, W.; Ruelle, M.; Saltonstall, K.; Powell, J. 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 | DOI

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

[9] Chiari, Y.; Hyseni, C.; Fritts, T. H.; Glaberman, S.; Marquez, C.; Gibbs, J. P.; Claude, J.; Caccone, A. Morphometrics Parallel Genetics in a Newly Discovered and Endangered Taxon of Galápagos Tortoise, PLoS ONE, Volume 4 (2009) no. 7 | DOI

[10] Ciofi, C.; Milinkovitch, M. C.; Gibbs, J. P.; Caccone, A.; Powell, J. R. Microsatellite analysis of genetic divergence among populations of giant Galápagos tortoises, Molecular Ecology, Volume 11 (2002) no. 11, pp. 2265-2283 | DOI

[11] Der Sarkissian, C.; Ermini, L.; Schubert, M.; Yang, M. A.; Librado, P.; Fumagalli, M.; Jónsson, H.; Bar-Gal, G. K.; Albrechtsen, A.; Vieira, F. G.; Petersen, B.; Ginolhac, A.; Seguin-Orlando, A.; Magnussen, K.; Fages, A.; Gamba, C.; Lorente-Galdos, B.; Polani, S.; Steiner, C.; Neuditschko, M.; Jagannathan, V.; Feh, C.; Greenblatt, C. L.; Ludwig, A.; Abramson, N. I.; Zimmermann, W.; Schafberg, R.; Tikhonov, A.; Sicheritz-Ponten, T.; Willerslev, E.; Marques-Bonet, T.; Ryder, O. A.; McCue, M.; Rieder, S.; Leeb, T.; Slatkin, M.; Orlando, L. Evolutionary Genomics and Conservation of the Endangered Przewalski’s Horse, Current Biology, Volume 25 (2015) no. 19, pp. 2577-2583 | DOI

[12] Dobrynin, P.; Liu, S.; Tamazian, G.; Xiong, Z.; Yurchenko, A. A.; Krasheninnikova, K.; Kliver, S.; Schmidt-Küntzel, A.; Koepfli, K.-P.; Johnson, W.; Kuderna, L. F.; García-Pérez, R.; Manuel, M. d.; Godinez, R.; Komissarov, A.; Makunin, A.; Brukhin, V.; Qiu, W.; Zhou, L.; Li, F.; Yi, J.; Driscoll, C.; Antunes, A.; Oleksyk, T. K.; Eizirik, E.; Perelman, P.; Roelke, M.; Wildt, D.; Diekhans, M.; Marques-Bonet, T.; Marker, L.; Bhak, J.; Wang, J.; Zhang, G.; O’Brien, S. J. Genomic legacy of the African cheetah, Acinonyx jubatus, Genome Biology, Volume 16 (2015) no. 1 | DOI

[13] EDMANDS, S. 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 | DOI

[14] Edwards, D. L.; Benavides, E.; Garrick, R. C.; Gibbs, J. P.; Russello, M. A.; Dion, K. B.; Hyseni, C.; Flanagan, J. P.; Tapia, W.; Caccone, A. The genetic legacy of Lonesome George survives: Giant tortoises with Pinta Island ancestry identified in Galápagos, Biological Conservation, Volume 157 (2013), pp. 225-228 | DOI

[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 | DOI

[16] Frankham, R.; Bradshaw, C. J.; Brook, B. 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 | DOI

[17] Frankham, R. 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 | DOI

[18] Funk, W. C.; McKay, J. K.; Hohenlohe, P. A.; Allendorf, F. W. Harnessing genomics for delineating conservation units, Trends in Ecology & Evolution, Volume 27 (2012) no. 9, pp. 489-496 | DOI

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

[20] Gayral, P.; Melo-Ferreira, J.; Glémin, S.; Bierne, N.; Carneiro, M.; Nabholz, B.; Lourenco, J. M.; Alves, P. C.; Ballenghien, M.; Faivre, N.; Belkhir, K.; Cahais, V.; Loire, E.; Bernard, A.; Galtier, N. Reference-Free Population Genomics from Next-Generation Transcriptome Data and the Vertebrate–Invertebrate Gap, PLoS Genetics, Volume 9 (2013) no. 4 | DOI

[21] Garrick, R. C.; Benavides, E.; Russello, M. A.; Gibbs, J. P.; Poulakakis, N.; Dion, K. B.; Hyseni, C.; Kajdacsi, B.; Márquez, L.; Bahan, S.; Ciofi, C.; Tapia, W.; Caccone, A. Genetic rediscovery of an ‘extinct’ Galápagos giant tortoise species, Current Biology, Volume 22 (2012) no. 1 | DOI

[22] Garrick, R. C.; Benavides, E.; Russello, M. A.; Hyseni, C.; Edwards, D. L.; Gibbs, J. P.; Tapia, W.; Ciofi, C.; Caccone, A. Lineage fusion in Galápagos giant tortoises, Molecular Ecology, Volume 23 (2014) no. 21, pp. 5276-5290 | DOI

[23] Gibbs, J. P.; Hunter, E. A.; Shoemaker, K. T.; Tapia, W. H.; Cayot, L. J. Demographic Outcomes and Ecosystem Implications of Giant Tortoise Reintroduction to Española Island, Galapagos, PLoS ONE, Volume 9 (2014) no. 10 | DOI

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

[25] Lamichhaney, S.; Berglund, J.; Almén, M. S.; Maqbool, K.; Grabherr, M.; Martinez-Barrio, A.; Promerová, M.; Rubin, C.-J.; Wang, C.; Zamani, N.; Grant, B. R.; Grant, P. R.; Webster, M. T.; Andersson, L. Evolution of Darwin’s finches and their beaks revealed by genome sequencing, Nature, Volume 518 (2015) no. 7539, pp. 371-375 | DOI

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

[27] Liu, S.; Lorenzen, E. D.; Fumagalli, M.; Li, B.; Harris, K.; Xiong, Z.; Zhou, L.; Korneliussen, T. S.; Somel, M.; Babbitt, C.; Wray, G.; Li, J.; He, W.; Wang, Z.; Fu, W.; Xiang, X.; Morgan, C. C.; Doherty, A.; O’Connell, M. J.; McInerney, J. O.; Born, E. W.; Dalén, L.; Dietz, R.; Orlando, L.; Sonne, C.; Zhang, G.; Nielsen, R.; Willerslev, E.; Wang, J. Population Genomics Reveal Recent Speciation and Rapid Evolutionary Adaptation in Polar Bears, Cell, Volume 157 (2014) no. 4, pp. 785-794 | DOI

[28] Loire, E.; Chiari, Y.; Bernard, A.; Cahais, V.; Romiguier, J.; Nabholz, B.; Lourenço, J.; Galtier, N. Population genomics of the endangered giant Galápagos tortoise, Genome Biology, Volume 14 (2013) no. 12 | DOI

[29] Márquez, C.; Gibbs, J. P.; Carrión, V.; Naranjo, S.; Llerena, A. Population Response of Giant Galápagos Tortoises to Feral Goat Removal, Restoration Ecology, Volume 21 (2013) no. 2, pp. 181-185 | DOI

[30] Milinkovitch, M. C.; Monteyne, D.; Gibbs, J. P.; Fritts, T. H.; Tapia, W.; Snell, H. L.; Tiedemann, R.; Caccone, A.; Powell, J. 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 | DOI

[31] Milinkovitch, M. C.; Monteyne, D.; Russello, M.; Gibbs, J. P.; Snell, H. L.; Tapia, W.; Marquez, C.; Caccone, A.; Powell, J. 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 | DOI

[32] Moore, J.-S.; Bourret, V.; Dionne, M.; Bradbury, I.; O'Reilly, P.; Kent, M.; Chaput, G.; Bernatchez, L. 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 | DOI

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

[34] Perry, G. H.; Melsted, P.; Marioni, J. C.; Wang, Y.; Bainer, R.; Pickrell, J. K.; Michelini, K.; Zehr, S.; Yoder, A. D.; Stephens, M.; Pritchard, J. K.; Gilad, Y. Comparative RNA sequencing reveals substantial genetic variation in endangered primates, Genome Research, Volume 22 (2012) no. 4, pp. 602-610 | DOI

[35] Poulakakis, N.; Glaberman, S.; Russello, M.; Beheregaray, L. B.; Ciofi, C.; Powell, J. R.; Caccone, A. 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 | DOI

[36] POULAKAKIS, N.; RUSSELLO, M.; GEIST, D.; CACCONE, A. 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 | DOI

[37] Poulakakis, N.; Edwards, D. L.; Chiari, Y.; Garrick, R. C.; Russello, M. A.; Benavides, E.; Watkins-Colwell, G. J.; Glaberman, S.; Tapia, W.; Gibbs, J. P.; Cayot, L. J.; Caccone, A. 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 | DOI

[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 | DOI

[39] Romiguier, J.; Fournier, A.; Yek, S. H.; Keller, L. Convergent evolution of social hybridogenesis in Messor harvester ants, Molecular Ecology, Volume 26 (2017) no. 4, pp. 1108-1117 | DOI

[40] Roux, C.; Fraïsse, C.; Romiguier, J.; Anciaux, Y.; Galtier, N.; Bierne, N. Shedding Light on the Grey Zone of Speciation along a Continuum of Genomic Divergence, PLOS Biology, Volume 14 (2016) no. 12 | DOI

[41] Russello, M. A.; Beheregaray, L. B.; Gibbs, J. P.; Fritts, T.; Havill, N.; Powell, J. R.; Caccone, A. Lonesome George is not alone among Galápagos tortoises, Current Biology, Volume 17 (2007) no. 9 | DOI

[42] Shafer, A. B.; Wolf, J. B.; Alves, P. C.; Bergström, L.; Bruford, M. W.; Brännström, I.; Colling, G.; Dalén, L.; De Meester, L.; Ekblom, R.; Fawcett, K. D.; Fior, S.; Hajibabaei, M.; Hill, J. A.; Hoezel, A. R.; Höglund, J.; Jensen, E. L.; Krause, J.; Kristensen, T. N.; Krützen, M.; McKay, J. K.; Norman, A. J.; Ogden, R.; Österling, E. M.; Ouborg, N. J.; Piccolo, J.; Popović, D.; Primmer, C. R.; Reed, F. A.; Roumet, M.; Salmona, J.; Schenekar, T.; Schwartz, M. K.; Segelbacher, G.; Senn, H.; Thaulow, J.; Valtonen, M.; Veale, A.; Vergeer, P.; Vijay, N.; Vilà, C.; Weissensteiner, M.; Wennerström, L.; Wheat, C. W.; Zieliński, P. Genomics and the challenging translation into conservation practice, Trends in Ecology & Evolution, Volume 30 (2015) no. 2, pp. 78-87 | DOI

[43] Taylor, B. L.; Perrin, W. F.; Reeves, R. R.; Rosel, P. E.; Wang, J. Y.; Cipriano, F.; Scott Baker, C.; Brownell, R. 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 | DOI

[44] Walling, C. A.; Nussey, D. H.; Morris, A.; Clutton-Brock, T. H.; Kruuk, L. E.; Pemberton, J. M. Inbreeding depression in red deer calves, BMC Evolutionary Biology, Volume 11 (2011) no. 1 | DOI

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

Cited by Sources: