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 from museum samples of extinct species

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 Galapagos tortoises in the most populated island of the archipelago. 

    National Geographic  

    New Scientist   

    New York Times

    Nature       

    The Guardian

 

    The Conversation

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 developing genomic markers such as Single copy Nucleotide Polymorphisms (SNPs) and others to harness the power of thousand of genetic mark

ers to  increase our ability to address both basic and applied types of questions.

Lab members involved in the project as of December 2015 are Joshua Miller, Kirstin Dion, and Yale undergraduate Andres Valdivieso. Past members include a large number of Yale undergraduate and graduate students. 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. They include: Danielle Edwards, Ryan Garrick, Edgar BenavidesLuciano 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, National Geographic Society, Turtle Conservation, The Paul and Bay Foundation, and the Eppley Foundation.

Publications 1999-2015:

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 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, A. Caccone. Reconstruction of the 3D carapace shape for morphometric analyses of turtles. 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. 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) 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.

25) 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, 6: 377-383.

26) 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.

27) 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.

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

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

30) 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. 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.