Evolutionary genetics and conservation of Galapagos Tortoises

For the past 20 years we have been involved in a long-term project focusing on giant Galapagos tortoises, an iconic complex of 15 species endemic from the Galapagos Islands.  These tortoises, which inspired Charles Darwins theory of evolution by natural selection, include a complex of morphologically and genetically distinct species. They once thrived on the islands, but now are either greatly reduced in number and distribution or extinct. Their demise is due to historical and contemporary factors due to human related activities, such as their massive use as a source of fresh food by whalers and pirates in the late 1800’s and the subsequent impact of invasive species, such as goat, feral cats, donkeys and others that predate on their nests or compete for their food. 

Our work proceeds on two fronts. On one hand we are interested in understanding and reconstructing their evolutionary history, which includes reconstructing their patterns of intra and interisland colonization, and understanding how morphological differentiation relates to environmental differences within and between islands. On the other hand, we are using the information we gather from the evolutionary genetic approaches to help the in situ and ex situ programs managed by the Galapagos National Park (GNP).  Restoring giant tortoises to their natural numbers and distribution is one of the most important GNP priorities, not only for the iconic role of these species but also because of their fundamental role as “ecological engineers” in maintaining the fragile ecosystems of the island they inhabit.

Our work concentrates on genetic and genomic analyses and the integration of genetic, morphological and environmental data. We can do this thanks to our very large sample database which includes more than 6,000 blood samples from all populations of extant species and DNA extracted from bones of museum samples of the extinct species.

Recent highlights from this work include:

1) The discovery of living individuals with genetic material from two extinct species of tortoise, from the island of Floreana and Pinta raising the possibility of rescuing these lineages from extinction through selective breeding program. In December 2015 we completed an expedition that gathered lots of media attention, where we found some of these animals and brought them to the GNP breeding center to start the next phase phase of the project, pending genomic analyses that will provide guidance for breeding strategies.

      New York Times Article

      Flickr photos from recent expedition

2) The discovery of a new species of giant Galapagos tortoises in the most populated island of the archipelago, Santa Cruz island. the species, Chelonoidis donfaustoi, was named after a famous ranger from the Galapagos National Park that has dedicated all his life to breed and manage tortoises in captivity, Mr. Fausto Llerena.

     National Geographic  

     New Scientist   

     New York Times


     The Guardian

     The Conversation

3) The genomic legacy of Lonesome George. We sequenced the complete genome of Lonesome George, the last male of the species Chelonoidis abingdoni, endemic of the island of Pinta in the Galapagos archipelago. Lonesome George was the most famous resident of the Galapagos islands until he died in 2012. We compared the genomic variants in his genome to the ones found in other Giant Galapagos tortoise species from different islands and the other giant tortoise, the Aldabra Giant tortoise, Aldabrachelys gigantea, from the Aldabra atoll in the Indian Ocean. Variants in regions associated with longevity, cancer resistance, immunity in other mammal including humans were identified, providing future research directions in this human health related topics. The data gathered from the analyses of its genome will also contribute to foster the ongoing work on conservation of the extant species and in helping elucidated the patterns and tempo of colonization of the islands.

     New York Times


     PLOS Blogs


     The London Economic

     La Prensa Grafica

Most of our past work used genetic markers such as mitochondrial DNA microsatellite loci to analyze patterns of genetic polymorphism. Although we continue to use them, as for some questions they can still provide powerful answers in a time and cost effective way, we are also using genomic markers such as Single copy Nucleotide Polymorphisms (SNPs) and whole genome analyses to harness the power of thousands of genetic mark for evolutionary and conservation analyses.

A large number of Yale undergraduate, graduate students, and postdocs have contributed to the research. Seminal to our progress has been the inclusion in our team of several very talented and committed postdocs that are now faculty members in Universities across the globe, but still very much involved in several of the ongoing projects. Past and present postdoc and graduate students include: Maud Quinzin, Stephen Gaughram, Josh Miller, Danielle Edwards, Ryan Garrick, Edgar Benavides, Luciano Beheregaray, Claudio Ciofi, Ylenia Chiari, Scott Glaberman, Valerio Ketmeier, Gabriele Gentile, Michel Milinkovitch, Nikos Poulakakis, Michael Russello, and James Gibbs. This work is conducted in full collaboration with the Galapagos National Park and is part of the Giant Galapagos Tortoise Initiative led by the Galapagos Conservancy. Sources of funding include multiple foundations, such as the Galapagos Conservancy, the Swiis Friends of Galapagos, the Oakley foundation, National Geographic Society, Turtle Conservation, The Paul and Bay Foundation, and the Eppley Foundation.


           Publications 1999-2019:

1) Caccone A, J.P. Gibbs, V. Ketmaier, El. Suatoni, J. R. Powell. 1999. Origin and evolutionary relationships of giant Gálapagos tortoises. Proceedings National Academy of Sciences  (PNAS) USA, 96: 13223-13228.

2) Caccone, A., G. Gentile, J. P. Gibbs, T. H. Fritts, H. L. Snell, and J. R. Powell. 2002. Phylogeography and history of Giant Galapagos Tortoises. Evolution 56, 2052-2066.

3) Ciofi, C., Milinkovitch M, Gibbs J.P., Caccone A, Powell J. R. 2002. Nuclear DNA microsatellite analysis of genetic divergence among and within island populations of giant Galápagos tortoises. Molecular Ecology 11:2265-2283.

4) Beherengary, L. B., C. Ciofi, A. Caccone, J. P. Gibbs, and J. R. Powell. 2003. Genetic divergence, phylogeography and conservation units of Giant tortoises from Santa Cruz and Pinzon, Galápagos islands. Conservation Genetics, 4:31-46

5) Beheregaray, LB, Ciofi, C, Geist, D., Gibbs, J, Powell, J.R, and A. Caccone. 2003. Genes record a prehistorical volcano eruption in the Galápagos. Science, 302: 75.

6) Burns. C.T., C. Ciofi C., L.B. Beheregaray, T.H. Fritts, J.P. Gibbs., C. Marquez, M. C.    Milinkovitch, J.R. Powell and A. Caccone. 2003. The origin of captive Galápagos tortoises based on DNA analysis: Implications for the management of natural populations. Animal Conservation, 6(4): 329-37.

7) Beheregaray, LB, JP Gibbs, N Havill, TH Fritts, JR Powell, and A Caccone. 2004. Giant tortoises are not so slow: Rapid diversification by recent volcanism in Galápagos. PNAS 101: 6514-6519.

8) Milinkovitch, M., D. Monteyne, J.P. Gibbs, T.H. Fritts, W. Tapia, H. L. Snell, R. Tiedemann, A. Caccone and J.R. Powell. 2003. Genetic analysis of a successful repatriation program: Giant Galápagos tortoises. Proc. Royal. Soc. London B, 271:341-345)

9) Caccone, A., G. Gentile, C. Burns, E. Sezzi, W. Bergman, and J.R. Powell. 2004. Extreme difference in rate of mitochondrial and nuclear DNA evolution in a large ectotherm, Galápagos tortoises. Molecular Phylogenetics and Evolution 31: 794-798.

10) Russello, M, S, Glaberman, ,  C. Marquez, J.R. Powell, and A. Caccone. 2005. A novel taxon of Giant tortoises in conservation peril. Biology Letters 1(3):287-290.

11) Ciofi, c., K. A. Wilson, L. B. Beheregeray, C. Marquez, J. P. Gibbs, W. Tapia, H. L. Snell, A. Caccone and J. R. Powell.  2005. Phylogeographic history and gene flow among giant Galápagos tortoises on southern Isabela island. Genetics 172: 1727-1744

12) Powell, J.R. and A. Caccone 2006. A quick guide to Galapagos tortoises. Current Biology, 16: R144-145.

13) Milinkovitch, M.C., D. Monteyne, M. Russello, J. P. Gibbs, H. L. Snell, W. Tapia, C. Marquez, A. Caccone and J. R. Powelll. 2007. Giant Galápagos Tortoises: Molecular Genetic Analysis Reveals Contamination in a Repatriation Program of an Endangered Taxon” BMC Ecology 2007, 7:2 (15 February 2007)

14) Russello, M.A., L. B. Beheregaray, J. P. Gibbs, T. Fritts, N. Havill, J. R. Powell, and A. Caccone. 2007.  Lonesome George is not alone among Galápagos Tortoises. Current Biology 17: 317-318.

15) Russello,M.A., C. Hyseni, J. P. Gibbs, S. Cruz, C. Marquez, W. Tapia, P. Velensky, J. R. Powell and A. 2007. Caccone. Lineage identification of Galápagos tortoises in captivity worldwide. Animal Conservation 10: 304-311.

16) Powell J.R. and A. Caccone. 2008. CSI tortoise: unraveling the mystery of mysteries. Galapagos News. 26:8-9.

17) Parent, C, E. A. Caccone and K. Petren. 2008. Colonization and diversification of Galápagos terrestrial fauna: a phylogenetic and biogeographical synthesis. Philos Trans R Soc Lond B Biol Sci. 2008 Oct 27;363(1508):3347-61.

18) Ciofi, C.  A. Caccone, L.B. Beheregaray, M.C. Milinkovitch, M.A.Russello and J.R. Powell. Genetics and conservation on islands: the Galápagos giant tortoise as a case study. In: A Population Genetics for Animal Conservation, Cambridge University Press, pages: 269-293.

19) Chiari, Y., B. Wang, H. Rushmeier, and A. CACCONE. 2008. Using digital images to reconstruct 3D biological forms: a new tool for morphometric studies. Biol. J. of the Linnean Soc., 95 (2): 425-436.

20) Poulakakis, N., S.Glaberman, M.Russello, L. B. Beheregaray, C. Ciofi, J. R. Powell, and A. Caccone. 2008. Rediscovery of an extinct species of giant Galápagos tortoise. PNAS 2008 105:15464-15469.

21) Chiari, Y., C. Hyseni, T. H. Fritts, S. Glaberman, C. Marquez, J. P. Gibbs, J. Claude, A. Caccone. 2009. Morphometrics parallel genetics in a newly discovered and endangered taxon of Galápagos tortoise. PLoS ONE 4(7): e6272.

22) Russello, M.A., N. Poulakakis, J. P. Gibbs, W. Tapia, J. R. Powell, and A. Caccone. 2010. Ex situ conservation in crisis: an “extinct” species of Galápagos tortoise identified in captivity. PLoS ONE 5(1): e8683.

23) Benavides, E., M. Russello, D. Boyer, B. Wiese, B. Kajdacsi, L. Marquez., R.,Garrick, A. Caccone. 2011. Lineage Identification and Genealogical Relationships Among Captive Galápagos Tortoise. Zoo Biology, 31:107–120.

24) Poulakakis, N., M. A. Russello, D. Geist, and A.CACCONE. Unraveling the Peculiarities of Island Life: Vicariance, Dispersal and the Diversification of the Extinct and Extant Giant Galápagos Tortoises. Molecular Ecology 21, 160–173.

25) Garrick, R.C, E. Benavides, M.A. Russello, J.P. Gibbs, N. Poulakakis, K. Dion, C. Hyseni, B. Kajdacsi, L. Márquez, S. Bahan, C. Ciofi, W. Tapia, A. Caccone. 2012. Genetic rediscovery of an ‘extinct’ Galápagos giant tortoise species. Current Biology 22: R10-R11.

26) Milinkovitch. M.C., R. Kanitz, R. Tiedemann, W. Tapia, F. Llerena, A. Caccone, J. P. Gibbs, and J.R. Powell. 2012. Recovery of a nearly extinct Galápagos tortoise despite minimal genetic variation. Evolutionary Applications, 6: 377-383.

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

28) Edwards, D.L., Ryan C. Garrick, W.H. Tapia, and A. Caccone. 2014. Cryptic structure between ecologically distinct genetic clusters in threatened giant Galápagos tortoises from southern Isabela Island. Conservation Genetics, 15: 1357-1369.

29) Garrick, R.C., E. Benavides, M. A. Russello, C. Hyseni, D. L. Edwards, J. P. Gibbs, W. Tapia, C. Ciofi and A. CACCONE. 2012. Lineage fusion in Galápagos giant tortoises. Molecular Ecology, 23: 5276–5290. PMID: 25223395.

30) Garrick, R.C., B. Kajdacsi, M.l A. Russello, J.P. Gibbs, W. Tapia and A. Caccone. 2015. Naturally rare versus newly rare: demographic inferences on two timescales inform conservation of Galapagos giant tortoises. Evolution and Ecology 5(3): 676–694

31) Jensen, E.L., W. Tapia, A. Caccone, M. Russello. 2015. Genetics of a head-start program to guide conservation of an endangered Galápagos tortoise (Chelonoidis epphipium). Conservation Genetics, 4: 31-46.

32) Poulakakis, N., D.L Edwards, Y.Chiari, R.C Garrick, E. Benavides, M. A. Russello, G. J. Watkins-Colwell, S. Glaberman, W. Tapia, J. P Gibbs, L. J. Cayot, A. Caccone. 2015. Description of a new Galapagos Giant Tortoise Species (Chelonoidis; Testudines: Testudinidae) from Cerro Fatal on Santa Cruz Island. PlosOne. Published: October 21, 2015. DOI: 10.1371/journal.pone.0138779.

33) Jensen E.L., A.Ø. Mooers, A. Caccone, and M.A. Russello MA. 2016. I-HEDGE: determining the optimum complementary sets of taxa for conservation using evolutionary isolation. PeerJ 4:e2350 https://doi.org/10.7717/peerj.2350.

34)  Miller, J.M,  M.C. Quinzin, N. Poulakakis, L. B. Beheregaray, J.P. Gibbs, C. Garrick, M. A. Russello, C. Ciofi, D. L. Edwards, E. A. Hunter, W. Tapia, D. Rueda, J. Carrión, A.A. Valdivieso, A. Caccone. 2017.  Identification of genetically important individuals of the rediscovered Floreana Galapagos Giant tortoises (Chelonoidis elephantopus) provides forunders for species restoration program.  Scientific Reports 7, Article number: 11471 (2017).

35) Gaughran, S.J., M.C. Quinzin, J.M. Miller, R.C. Garrick, D.L. Edwards, M.A. Russello, N. Poulakakis, C. Ciofi7, L.B. Beheregaray, A. Caccone. 2017. Theory, practice, and conservation in the age of genomics: the Galápagos giant tortoise as a case study. Evolutionary Application 2017. 1-10. DOI: 10.1111/eva.12551.

36) Chiari, Y, A. van der Meijden, A. Caccone, J. Claude, B. Gilles. 2017.  Self-righting potential and the evolution of shell shape in Galápagos tortoises. Scientific reports Scientific Reports 2017: 7, 15828.

37) Jensen, E.L, D.L. Edwards, R.C. Garrick, J. M. Miller, J. P. Gibbs, L.J. Cayot, W. Tapi, A. Caccone and M.A. Russello. 2018. Temporal mitogenomics of the Galapagos giant tortoise from Pinzón reveals potential biases in population genetic inference. Journal of Heredity, esy016, https://doi.org/10.1093/jhered/esy016.

38) Miller, J.M., M. C. Quinzin, E. Scheibe, C. Ciofi, F. G. Villalva Sanchez, W. Tapia, A. Caccone. 2018. Genetic pedigree analysis of pilot breeding program for the rediscovered giant Galapagos giant tortoise from Floreana island. J. of Heredity, 2018, 1–11.

39) Miller, J. M., Quinzin, M. C., Edwards, D. L., Eaton, D. A., Jensen, E. L., Russello, M. A., … & Caccone, A. (2018). Genome-wide assessment of diversity and divergence among extant galapagos giant tortoise species. Journal of Heredity, 109(6), 611-619.

40) Jensen, E. L., Edwards, D. L., Garrick, R. C., Miller, J. M., Gibbs, J. P., Cayot, L. J., Tapia, W., Caccone, A. & Russello, M. A. (2018). Population genomics through time provides insights into the consequences of decline and rapid demographic recovery through head‐starting in a Galapagos giant tortoise. Evolutionary Applications, 11(10), 1811-1821.

41) Quesada, V., S. Freitas-Rodríguez, . Miller, J. G. Pérez-Silva, W. Tapia, O. Santiago-Fernández, D. Campos-Iglesias, L. F.K. Kuderna, M. Quinzin, M. G. Alvarez, D. Carrero, Z. Jiang, L. Beheregaray, J. P. Gibbs, Y. Chiari, S. Glaberman, C. Ciofi, M. Araujo, P. Mayoral, J. R. Arango, I. Tamargo, D. Roiz-Valle, B. R. Evans, D. L. Edwards, R. C. Garrick, M A. Russello, N. Poulakakis, Da. O. Rueda, G. Bretones, T. Marqués-Bonet, K. P. White, A. CACCONE^, C. López-Otín^. (2019). Giant tortoise genomes provide insights into longevity and age-related disease. Nature ecology & evolution, 3(1), 87.

In review:

Hunter, E.A., J. P. Gibbs, L. J. Cayot, W. Tapia, M. C. Quinzin, J. M. Miller, A. CACCONE, K. T. Shoemaker. Seeking compromise across competing goals in conservation translocations: The case of the “extinct” Floreana Island Galapagos giant tortoise. J. of Applied Ecology (in review).

Quinzin, M.C, J. Sandoval-Castillo, J. M. Miller, L. B. Beheregaray, M.A. Russello, E. A. Hunter, J. P. Gibbs, W. Tapia, F. Villalva, A. Caccone. Genetically informed captive breeding of hybrids with an extinct species of Galapagos giant tortoise. Conservation Biology (submitted)