The Case of the Floreana Galápagos Giant Tortoise Chelonoidis 2 Elephantopus 3 4 Joshua M
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bioRxiv preprint doi: https://doi.org/10.1101/143131; this version posted May 27, 2017. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 Reviving a Lost Species: The Case of the Floreana Galápagos Giant Tortoise Chelonoidis 2 elephantopus 3 4 Joshua M. Miller1†*, Maud C. Quinzin1†, Nikos Poulakakis2,3, James P. Gibbs4, Luciano B. 5 Beheregaray5, Ryan C. Garrick6, Michael A. Russello7, Claudio Ciofi8, Danielle L. Edwards9, 6 Elizabeth A. Hunter10, Washington Tapia11,12, Danny Rueda12, Jorge Carrión12, Andrés A. 7 Valdivieso1, Adalgisa Caccone1* 8 9 1. Department of Ecology and Evolutionary Biology, Yale University, 21 Sachem St. New 10 Haven, Connecticut, 06520, United States of America 11 2. Department of Biology, School of Sciences and Engineering, University of Crete, 12 Vasilika Vouton, Gr-71300, Heraklio, Crete, Greece 13 3. Natural History Museum of Crete, School of Sciences and Engineering, University of 14 Crete, Knossos Av., GR-71409, Heraklio, Crete, Greece 15 4. College of Environmental Science & Forestry, State University of New York, Syracuse, 16 New York, 13210, United States of America 17 5. Molecular Ecology Lab, School of Biological Sciences, Flinders University, GPO 18 Box 2100, Adelaide, SA, 5001, Australia 19 6. Department of Biology, University of Mississippi, Oxford, Mississippi, 38677, United 20 States of America 21 7. Department of Biology, University of British Columbia, Okanagan Campus, Kelowna, 22 BC V1V 1V7, Canada 23 8. Department Biology, University of Florence, 50019 Sesto Fiorentino (FI), Italy 24 9. Life and Environmental Sciences, University of California, Merced, 5200 N Lake Rd, 25 Merced, California, 95343, United States of America 26 10. Department of Natural Resources and Environmental Science, University of Nevada – 27 Reno, Max Fleischmann Agricultural Building, Reno NV 89557 USA 28 11. Galapagos Conservancy, Fairfax, Virginia, 22030, United States of America 29 12. Galápagos National Park Directorate, Puerto Ayora, Galápagos, Ecuador 30 *Corresponding authors: [email protected], [email protected] 31 †These authors contributed equally to this work 1 bioRxiv preprint doi: https://doi.org/10.1101/143131; this version posted May 27, 2017. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 32 Abstract 33 Species are being lost at an unprecedented rate due to human-driven environmental changes. The 34 cases in which species declared extinct can be revived are extremely rare. However, here we 35 report that a remote volcano in the Galápagos Islands hosts many giant tortoises with extremely 36 high ancestry from a species previously declared as extinct: Chelonoidis elephantopus or the 37 Floreana tortoise. Of 150 individuals with distinctive morphology sampled from the volcano, 38 genetic analyses revealed that 65 had C. elephantopus ancestry Thirty-two were translocated 39 from the volcano’s slopes to a captive breeding center. A genetically informed captive breeding 40 program now being initiated will, over the next decades, return C. elephantopus tortoises to 41 Floreana Island to serve as engineers of the island’s ecosystems. Ironically, it was the haphazard 42 translocations by mariners killing tortoises for food centuries ago that created the unique 43 opportunity to revive this “lost” species today. 44 45 Introduction 46 Human activities have generated an extreme and rapid loss of biodiversity1. Many actions 47 have been undertaken to prevent species extinctions, including creating laws to protect 48 endangered species and critical habitats2, translocations of individuals among populations or into 49 new habitats3,4, and ex situ management including captive breeding5. For many species, such 50 actions come too late to facilitate recovery6–8. Although ‘de-extinction’ using laboratory 51 techniques is currently being debated9, such methods are viable only for some taxa and will 52 generate significant anticipated, and unanticipated, risks10,11. Generally, extinction is final and 53 cases where lost species can be revived will be extremely rare. 54 Despite their insularity, even remote oceanic islands are not exempt from rapid 55 anthropogenic changes. For example, the ecosystems of the Galápagos Islands, located ~900 56 kilometers off the Pacific coast of Ecuador, have been degraded by human activities since the 57 archipelago was discovered in 1535. The resulting loss of biodiversity, including many endemic 58 species, has been chiefly due to the introduction of non-native species12,13. In response, concerted 59 efforts have been taken to restore ecosystems on the islands, including removal of introduced 60 pests14,15 and population restoration via captive breeding and repatriation of threatened native 61 species (e.g. 16,17). 2 bioRxiv preprint doi: https://doi.org/10.1101/143131; this version posted May 27, 2017. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 62 Galápagos giant tortoises (Chelonoidis spp.) are flagship species for ongoing restoration 63 efforts18 in this archipelago and play an important functional role as mega-herbivores in the 64 islands’ ecosystems19. Galápagos giant tortoises can be classified into 15 species based on 65 genetic data20. Generally, there is a single species per island with two exceptions: Isabela Island 66 that has a different endemic species associated with each of its five volcanoes, and Santa Cruz 67 Island that contains two species, one recently described20 (Figure 1a). The 15 species exhibit two 68 general carapace shapes: "domed," a rounded cupola-like form (Figure 1c), and a "saddle- 69 backed" form, with a high anterior opening creating the shape of a saddle (Figure 1d). Five of the 70 15 species have the saddle-backed morphology: C. elephantopus (Floreana), C. hoodensis 71 (Española), C. abingdoni (Pinta), C. ephippium (Pinzón), and C. chathamensis (San Cristóbal; 72 Figure 1a). 73 Over the past three centuries, all giant tortoise populations experienced a ~90% decline21, 74 having been killed mostly for food and oil by whalers, sealers, buccaneers, and early 75 colonists22,23. Four species have been declared Extinct24, including two of the five saddle-backed 76 species: C. elephantopus from Floreana Island and, most recently, C. abingdoni, from Pinta 77 Island. The latter species was represented by a single individual, Lonesome George, until his 78 death in 2012. 79 Surprisingly, recent research found living, wild tortoises with genetic ancestry from two 80 of the extinct saddle-backed species, C. elephantopus and C. abingdoni (hereafter referred to as 81 the Floreana and Pinta tortoises, respectively) outside their native range25–28. These individuals, 82 likely the descendants of tortoises translocated among islands by mariners22,23,29, were discovered 83 on the remote Volcano Wolf on Isabela Island (Figure 1a,b). Among >1600 tortoises sampled 84 from Volcano Wolf in 2008 during an exploratory expedition, 105 individuals were admixed 85 between the locally endemic species, C. becki, and the Floreana (n = 86)5 or Pinta (n = 17)4 86 species. The majority of these genetically admixed individuals were found on the Volcano 87 Wolf’s western slopes, facing Banks Bay (also known as Puerto Bravo, PBR: Figure 1b), with a 88 smaller number located on the volcano’s northwestern slopes near Piedras Blancas (PBL)25,26. 89 No purebred individuals of either of the two non-native species were found in 2008, but genetic 90 simulations and the young age of some mixed ancestry individuals indicated that purebred 91 Floreana and Pinta tortoises might still be present on Volcano Wolf25,26. 3 bioRxiv preprint doi: https://doi.org/10.1101/143131; this version posted May 27, 2017. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 92 Here we build on this previous work. In November 2015 we mounted a 10-day-long 93 search involving ~70 field personnel combined with helicopter- and ship-support. Focusing our 94 search, we explored zones of Volcano Wolf most likely to contain individuals with ancestry from 95 these two “lost” species (Figure 1b) and restricted genetic sampling to those individuals with 96 saddle-backed morphology among the thousands of locally endemic domed C. becki. We then 97 assigned ancestry to these tortoises using reference databases containing both extant and extinct 98 species that have previously been used to assign ancestry to tortoises in the wild and captivity25– 99 31. Based on these assignments, we determined suitability of the tortoises for a genetically 100 informed captive breeding program aimed at reintroducing these key ecosystem engineers to 101 their native islands. 102 103 Results & Discussion 104 In total, we encountered 144 individuals with saddle-backed morphology. Of those, 112 105 were released after taking blood samples, and 32 with pronounced saddle-backed morphology 106 were transported to the Galápagos National Park Service’s captive tortoise breeding facility on 107 Santa Cruz Island32–34. We assigned ancestry to all 144 of these individuals along with six 108 saddle-backed tortoises known to have Floreana ancestry35 already residing at the breeding 109 center using information from ~700-bp of mitochondrial DNA sequence and diploid genotypes 110 from 12 nuclear microsatellite loci. These loci have previously been shown to accurately assign 111 individuals to tortoise species25–31. 112 Thirty-five of the 150 individuals analyzed had a mitochondrial DNA haplotype 113 diagnostic of the Floreana species (Supplementary Figure S1).