1932

Abstract

Cloning as it relates to the animal kingdom generally refers to the production of genetically identical individuals. Because cloning is increasingly the subject of renewed attention as a tool for rescuing endangered or extinct species, it seems timely to dissect the role of the numerous reproductive techniques encompassed by this term in animal species conservation. Although cloning is typically associated with somatic cell nuclear transfer, the recent advent of additional techniques that allow genome replication without genetic recombination demands that the use of induced pluripotent stem cells to generate gametes or embryos, as well as older methods such as embryo splitting, all be included in this discussion. Additionally, the phenomenon of natural cloning (e.g., a subset of fish, birds, invertebrates, and reptilian species that reproduce via parthenogenesis) must also be pointed out. Beyond the biology of these techniques are practical considerations and the ethics of using cloning and associated procedures in endangered or extinct species. All of these must be examined in concert to determine whether cloning has a place in species conservation. Therefore, we synthesize progress in cloning and associated techniques and dissect the practical and ethical aspects of these methods as they pertain to endangered species conservation.

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2024-02-15
2024-04-12
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Literature Cited

  1. 1.
    Roth TL, Swanson WF. 2018. From petri dishes to politics—a multi-pronged approach is essential for saving endangered species. Nat. Commun. 9:2588
    [Google Scholar]
  2. 2.
    Swegen A, Appeltant R, Williams SA. 2023. Cloning in action: Can embryo splitting, induced pluripotency and somatic cell nuclear transfer contribute to endangered species conservation?. Biol. Rev. 98:41225–49
    [Google Scholar]
  3. 3.
    Loughry WJ, Prodöhl PA, McDonough CM, Avise JC. 1998. Polyembryony in armadillos. Am. Sci. 86:3274–79
    [Google Scholar]
  4. 4.
    Mullen RJ, Whitten W, Carter S. 1970. Studies on chimeric mice and half-embryos. Annu. Report Jackson Lab. 1970:67–68
    [Google Scholar]
  5. 5.
    Willadsen SM. 1979. A method for culture of micromanipulated sheep embryos and its use to produce monozygotic twins. Nature 277:5694298–300
    [Google Scholar]
  6. 6.
    Willadsen SM, Polge C. 1981. Attempts to produce monozygotic quadruplets in cattle by blastomere separation. Vet. Rec. 108:10211–13
    [Google Scholar]
  7. 7.
    Nagashima H, Kato Y, Ogawa S. 1989. Microsurgical bisection of porcine morulae and blastocysts to produce monozygotic twin pregnancy. Gamete Res 23:11–9
    [Google Scholar]
  8. 8.
    Ozil JP, Heyman Y, Renard JP. 1982. Production of monozygotic twins by micromanipulation and cervical transfer in the cow. Vet. Rec. 110:6126–27
    [Google Scholar]
  9. 9.
    Széll A, Hudson RHH. 1991. Factors affecting the survival of bisected sheep embryos in vivo. Theriogenology 36:3379–87
    [Google Scholar]
  10. 10.
    Udy GB. 1987. Commercial splitting of goat embryos. Theriogenology 28:6837–47
    [Google Scholar]
  11. 11.
    Williams TJ, Elsden RP, Seidel GE. 1984. Pregnancy rates with bisected bovine embryos. Theriogenology 22:5521–31
    [Google Scholar]
  12. 12.
    Fields AT, Feldheim KA, Poulakis GR, Chapman DD. 2015. Facultative parthenogenesis in a critically endangered wild vertebrate. Curr. Biol. 25:11R446–47
    [Google Scholar]
  13. 13.
    Ryder OA, Thomas S, Judson JM, Romanov MN, Dandekar S et al. 2021. Facultative parthenogenesis in California condors. J. Hered. 112:7569–74
    [Google Scholar]
  14. 14.
    Watts PC, Buley KR, Sanderson S, Boardman W, Ciofi C, Gibson R. 2006. Parthenogenesis in Komodo dragons. Nature 444:71221021–22
    [Google Scholar]
  15. 15.
    Wei Y, Yang R, Zhao Z. 2022. Viable offspring derived from single unfertilized mammalian oocytes. PNAS 12:e2115248119
    [Google Scholar]
  16. 16.
    Campbell KHS, McWhir J, Ritchie WA, Wilmut I. 1996. Sheep cloned by nuclear transfer from a cultured cell line. Nature 380:656964–66
    [Google Scholar]
  17. 17.
    Wilmut I, Schnieke AE, McWhir J, Kind AJ, Campbell KHS. 1997. Viable offspring derived from fetal and adult mammalian cells. Nature 385:6619810–13
    [Google Scholar]
  18. 18.
    Keefer CL. 2015. Artificial cloning of domestic animals. PNAS 112:298874–78
    [Google Scholar]
  19. 19.
    Cohen J. 2016. Six cloned horses help rider win prestigious polo match. Science Dec. 13. https://www.science.org/content/article/six-cloned-horses-help-rider-win-prestigious-polo-match
    [Google Scholar]
  20. 20.
    Takahashi K, Yamanaka S. 2006. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126:4663–76
    [Google Scholar]
  21. 21.
    Hayashi K, Ogushi S, Kurimoto K, Shimamoto S, Ohta H, Saitou M. 2012. Offspring from oocytes derived from in vitro primordial germ cell-like cells in mice. Science 338:6109971–75
    [Google Scholar]
  22. 22.
    Hamazaki N, Kyogoku H, Araki H, Miura F, Horikawa C et al. 2020. Reconstitution of the oocyte transcriptional network with transcription factors. Nature 589:7841264–69
    [Google Scholar]
  23. 23.
    Hikabe O, Hamazaki N, Nagamatsu G, Obata Y, Hirao Y et al. 2016. Reconstitution in vitro of the entire cycle of the mouse female germ line. Nature 539:7628299–303
    [Google Scholar]
  24. 24.
    Hildebrandt TB, Hermes R, Goeritz F, Appeltant R, Colleoni S et al. 2021. The ART of bringing extinction to a freeze—history and future of species conservation, exemplified by rhinos. Theriogenology 169:76–88
    [Google Scholar]
  25. 25.
    Dicks N, Bordingnon V, Mastromonaco G. 2021. Induced pluripotent stem cells in species conservation: advantages, applications, and the road ahead. iPSCs from Diverse Species A Birbrair 221–45 London: Academic
    [Google Scholar]
  26. 26.
    Ishikura Y, Ohta H, Sato T, Yamamoto T, Murase Y et al. 2021. In vitro reconstitution of the whole male germ-cell development from mouse pluripotent stem cells. Cell Stem Cell 28:2167–79
    [Google Scholar]
  27. 27.
    Hayashi K, Ohta H, Kurimoto K, Aramaki S, Saitou M. 2011. Reconstitution of the mouse germ cell specification pathway in culture by pluripotent stem cells. Cell 146:4519–32
    [Google Scholar]
  28. 28.
    Shepard A, Kissil JL. 2020. The use of non-traditional models in the study of cancer resistance—the case of the naked mole rat. Oncogene 39:285083–97
    [Google Scholar]
  29. 29.
    Hedrick PW, Fredrickson R. 2010. Genetic rescue guidelines with examples from Mexican wolves and Florida panthers. Conserv. Genet. 11:2615–26
    [Google Scholar]
  30. 30.
    Wildt DE, Rall WF, Critser JK, Monfort SL, Seal US. 1997. Genome resource banks. BioScience 47:10689–98
    [Google Scholar]
  31. 31.
    Azevedo Borges A, Pereira De Oliveira Lira G, Nascimento LE, De Oliveira Santos MV, De Oliveira MF et al. 2020. Isolation, characterization, and cryopreservation of collared peccary skin-derived fibroblast cell lines. PeerJ 8:e9136
    [Google Scholar]
  32. 32.
    Fukuda T, Eitsuka T, Donai K, Kurita M, Saito T et al. 2018. Expression of human mutant cyclin dependent kinase 4, Cyclin D and telomerase extends the life span but does not immortalize fibroblasts derived from loggerhead sea turtle (Caretta caretta). Sci. Rep. 8:9229
    [Google Scholar]
  33. 33.
    Harper JM, Salmon AB, Leiser SF, Galecki AT, Miller RA. 2007. Skin-derived fibroblasts from long-lived species are resistant to some, but not all, lethal stresses and to the mitochondrial inhibitor rotenone. Aging Cell 6:11–13
    [Google Scholar]
  34. 34.
    Siengdee P, Klinhom S, Thitaram C, Nganvongpanit K. 2018. Isolation and culture of primary adult skin fibroblasts from the Asian elephant (Elephas maximus). PeerJ 6:e4302
    [Google Scholar]
  35. 35.
    Yajing S, Rajput IR, Ying H, Fei Y, Sanganyado E et al. 2018. Establishment and characterization of pygmy killer whale (Feresa attenuata) dermal fibroblast cell line. PLOS ONE 13:3e0195128
    [Google Scholar]
  36. 36.
    Bolton RL, Mooney A, Pettit MT, Bolton AE, Morgan L et al. 2022. Resurrecting biodiversity: advanced assisted reproductive technologies and biobanking. Reprod. Fertil. 3:3R121–46
    [Google Scholar]
  37. 37.
    Comizzoli P. 2015. Biotechnologies for wildlife fertility preservation. Anim. Front. 5:173–78
    [Google Scholar]
  38. 38.
    Hermes R, Göritz F, Streich WJ, Hildebrandt TB. 2007. Assisted reproduction in female rhinoceros and elephants—current status and future perspective. Reprod. Domest. Anim. 42:Suppl. 233–44
    [Google Scholar]
  39. 39.
    Hermes R, Göritz F, Portas TJ, Bryant BR, Kelly JM et al. 2009. Ovarian superstimulation, transrectal ultrasound-guided oocyte recovery, and IVF in rhinoceros. Theriogenology 72:7958–68
    [Google Scholar]
  40. 40.
    Biasetti P, Hildebrandt TB, Göritz F, Hermes R, Holtze S et al. 2022. Ethical analysis of the application of assisted reproduction technologies in biodiversity conservation and the case of white rhinoceros (Ceratotherium simum) ovum pick-up procedures. Front. Vet. Sci. 9:831675
    [Google Scholar]
  41. 41.
    Holt W, Brown J, Comizzoli P 2014. Reproductive Sciences in Animal Conservation: Progress and Prospects Adv. Exp. Med. Biol. 753 New York: Springer
  42. 42.
    Mitchell RT, Williams SA. 2022. A fertile future: fertility preservation special series. Reprod. Fertil. 3:1C1–3
    [Google Scholar]
  43. 43.
    Cox RT, Pouton J, Williams S. 2021. The role of mitophagy during oocyte aging in human, mouse, and Drosophila: implications for oocyte quality and mitochondrial disease. Reprod. Fertil. 2:4R113–29
    [Google Scholar]
  44. 44.
    Katayama M, Fukuda T, Kaneko T, Nakagawa Y, Tajima A et al. 2022. Induced pluripotent stem cells of endangered avian species. Commun. Biol. 5:1049
    [Google Scholar]
  45. 45.
    Geuder J, Wange LE, Janjic A, Radmer J, Janssen P et al. 2021. A non-invasive method to generate induced pluripotent stem cells from primate urine. Sci. Rep. 11:13516
    [Google Scholar]
  46. 46.
    Nakajima M, Yoshimatsu S, Sato T, Nakamura M, Okahara J et al. 2019. Establishment of induced pluripotent stem cells from common marmoset fibroblasts by RNA-based reprogramming. Biochem. Biophys. Res. Commun. 515:4593–99
    [Google Scholar]
  47. 47.
    Korody ML, Ford SM, Nguyen TD, Pivaroff CG, Valiente-Alandi I et al. 2021. Rewinding extinction in the northern white rhinoceros: genetically diverse induced pluripotent stem cell bank for genetic rescue. Stem Cells Dev 30:4177–89
    [Google Scholar]
  48. 48.
    Zywitza V, Rusha E, Shaposhnikov D, Ruiz-Orera J, Telugu N et al. 2022. Naïve-like pluripotency to pave the way for saving the northern white rhinoceros from extinction. Sci. Rep. 12:3100
    [Google Scholar]
  49. 49.
    Verma R, Holland MK, Temple-Smith P, Verma PJ. 2012. Inducing pluripotency in somatic cells from the snow leopard (Panthera uncia), an endangered felid. Theriogenology 77:1220–228.e2
    [Google Scholar]
  50. 50.
    Verma R, Liu J, Holland MK, Temple-Smith P, Williamson M, Verma PJ. 2013. Nanog is an essential factor for induction of pluripotency in somatic cells from endangered felids. Biores. Open Access 2:172–76
    [Google Scholar]
  51. 51.
    Yoshino T, Suzuki T, Nagamatsu G, Yabukami H, Ikegaya M et al. 2021. Generation of ovarian follicles from mouse pluripotent stem cells. Science 373:6552eabe0237
    [Google Scholar]
  52. 52.
    Yamashiro C, Sasaki K, Yabuta Y, Kojima Y, Nakamura T et al. 2018. Generation of human oogonia from induced pluripotent stem cells in vitro. Science 362:6412356–60
    [Google Scholar]
  53. 53.
    Leemans B, Gadella BM, Stout TAE, De Schauwer C, Nelis H et al. 2016. Why doesn't conventional IVF work in the horse? The equine oviduct as a microenvironment for capacitation/fertilization. Reproduction 152:6R233–45
    [Google Scholar]
  54. 54.
    Herrick JR. 2019. Assisted reproductive technologies for endangered species conservation: developing sophisticated protocols with limited access to animals with unique reproductive mechanisms. Biol. Reprod. 100:51158–70
    [Google Scholar]
  55. 55.
    Behboodi E, Anderson GB, BonDurant RH, Cargill SL, Kreuscher BR et al. 1995. Birth of large calves that developed from in vitro-derived bovine embryos. Theriogenology 44:2227–32
    [Google Scholar]
  56. 56.
    Young LE, Fernandes K, McEvoy TG, Butterwith SC, Gutierrez CG et al. 2001. Epigenetic change in IGF2R is associated with fetal overgrowth after sheep embryo culture. Nat. Genet. 27:2153–54
    [Google Scholar]
  57. 57.
    Rodriguez-Caro H, Williams SA. 2018. Strategies to reduce non-communicable diseases in the offspring: negative and positive in utero programming. J. Dev. Orig. Health Dis. 9:6642–52
    [Google Scholar]
  58. 58.
    Crosier AE, Lamy J, Bapodra P, Rapp S, Maly M et al. 2020. First birth of cheetah cubs from in vitro fertilization and embryo transfer. Animals 10:101811
    [Google Scholar]
  59. 59.
    Fjeldstad HE, Johnsen GM, Staff AC. 2020. Fetal microchimerism and implications for maternal health. Obstet. Med. 13:3112–19
    [Google Scholar]
  60. 60.
    Browne RK, Silla AJ, Upton R, Della-Togna G, Narcec-Greaves R et al. 2019. Sperm collection and storage for the sustainable management of amphibian biodiversity. Theriogenology 133:187–200
    [Google Scholar]
  61. 61.
    Kouba CK, Julien AR. 2022. Linking in situ and ex situ populations of threatened amphibian species using genome resource banks. Reproductive Technologies and Biobanking for the Conservation of Amphibians AJ Silla, AJ Kouba, H Heatwole 188–203 London: CSIRO Publ.
    [Google Scholar]
  62. 62.
    Hu T, Taylor L, Sherman A, Tiambo CK, Kemp SJ et al. 2022. A low-tech, cost-effective and efficient method for safeguarding genetic diversity by direct cryopreservation of poultry embryonic reproductive cells. eLife 11:74036
    [Google Scholar]
  63. 63.
    Kaurova S, Nikitina L, Uteshev V, Gakhova E 1998. Cryopreservation of totipotent embryo cells and their use in reconstruction of enucleated eggs. Proceedings of the XV Working Meeting, Pushchino, Oct. 13–15, EN Gakhova, VN Karnaukhov 206–8 Pushchino, Russ.: Pushchino
    [Google Scholar]
  64. 64.
    Uteshev V, Melnikova E, Kaurova S, Nikitin V, Gakhova E, Karnaukhov V. 2002. Fluorescent analysis of cryopreserved totipotent cells of amphibian embryos. Biofizika 47:3539–45
    [Google Scholar]
  65. 65.
    Uteshev VK, Gakhova EN, Kramarova LI, Shishova NV, Kaurova SA et al. 2023. Russian collaborative development of reproduction technologies for the sustainable management of amphibian biodiversity. Asian Herpetol. Res. 14:1103–15
    [Google Scholar]
  66. 66.
    Nikitina L. 1996. Nuclear heterotransplantation in fish and amphibians. Russ. J. Dev. Biol. 5:267–80
    [Google Scholar]
  67. 67.
    Strand J, Fraser B, Houch M, Clulow S. 2022. Culturing and biobanking of amphibian cell lines for conservation applications. Reproductive Technologies and Biobanking for the Conservation of Amphibians AJ Silla, AJ Kouba, H Heatwole 166–87 London: CSIRO Publ.
    [Google Scholar]
  68. 68.
    Malin K, Witkowska-Piłaszewicz O, Papis K. 2022. The many problems of somatic cell nuclear transfer in reproductive cloning of mammals. Theriogenology 189:246–54
    [Google Scholar]
  69. 69.
    Mastromonaco GF, King WA. 2007. Cloning in companion animal, non-domestic and endangered species: Can the technology become a practical reality?. Reprod. Fertil. Dev. 19:748–61
    [Google Scholar]
  70. 70.
    Olsson PO, Jeong YW, Jeong Y, Kang M, Park GB et al. 2022. Insights from one thousand cloned dogs. Sci. Rep. 12:11209
    [Google Scholar]
  71. 71.
    Gamborg C 2014. What's so special about reconstructing a mammoth? Ethics of breeding and biotechnology in re-creating extinct species. The Ethics of Animal Re-creation and Modification M Oksanen, H Siipi 60–76 London: Palgrave Macmillan
    [Google Scholar]
  72. 72.
    Campbell MLH. 2018. Is cloning horses ethical?. Equine Vet. Educ. 30:5268–73
    [Google Scholar]
  73. 73.
    Hong IH, Jeong YW, Shin T, Hyun SH, Park JK et al. 2011. Morphological abnormalities, impaired fetal development and decrease in myostatin expression following somatic cell nuclear transfer in dogs. Mol. Reprod. Dev. 78:5337–46
    [Google Scholar]
  74. 74.
    Srirattana K, Imsoonthornruksa S, Laowtammathron C, Sangmalee A, Tunwattana W et al. 2012. Full-term development of gaur-bovine interspecies somatic cell nuclear transfer embryos: effect of trichostatin A treatment. Cell. Reprogr. 14:3248–57
    [Google Scholar]
  75. 75.
    Hradecky P, Stover J, Stott G. 1988. Histology of a heifer placentome after interspecies transfer of a gaur embryo. Theriogenology 30:593–604
    [Google Scholar]
  76. 76.
    Heyman Y, Chavatte-Palmer P, Berthelot V, Fromentin G, Hocquette JF et al. 2007. Assessing the quality of products from cloned cattle: an integrative approach. Theriogenology 67:1134–41
    [Google Scholar]
  77. 77.
    Heyman Y, Chavatte-Palmer P, Fromentin G, Berthelot V, Jurie C et al. 2007. Quality and safety of bovine clones and their products. Animal 1:7963–72
    [Google Scholar]
  78. 78.
    Burgstaller JP, Brem G. 2017. Aging of cloned animals: a mini-review. Gerontology 63:5417–25
    [Google Scholar]
  79. 79.
    Kim MJ, Oh HJ, Kim GA, Park JE, Park EJ et al. 2012. Lessons learned from cloning dogs. Reprod. Domest. Anim. 47:Suppl. 4115–19
    [Google Scholar]
  80. 80.
    Kim MJ, Oh HJ, Hwang SY, Hur TY, Lee BC. 2018. Health and temperaments of cloned working dogs. J. Vet. Sci. 19:5585–91
    [Google Scholar]
  81. 81.
    Browning H. 2018. Won't somebody please think of the mammoths? De-extinction and animal welfare. J. Agric. Environ. Ethics 31:6785–803
    [Google Scholar]
  82. 82.
    Conde DA, Colchero F, Gusset M, Pearce-Kelly P, Byers O et al. 2013. Zoos through the lens of the IUCN Red List: a global metapopulation approach to support conservation breeding programs. PLOS ONE 8:12e80311
    [Google Scholar]
  83. 83.
    Powell DM, Meyer TG, Duncan M. 2023. By bits and pieces: the contributions of zoos and aquariums to science and society via biomaterials. J. Zool. Bot. Gard. 4:1277–87
    [Google Scholar]
  84. 84.
    Ceballos G, Ehrlich PR, Barnosky AD, Garcia A, Pringle RM, Palmer TM. 2015. Accelerated modern human-induced species losses: entering the sixth mass extinction. Sci. Adv. 1:5e1400253
    [Google Scholar]
  85. 85.
    Hoffmann M, Hilton-Taylor C, Angulo A, Böhm M, Brooks TM et al. 2010. The impact of conservation on the status of the world's vertebrates. Science 330:60101503–9
    [Google Scholar]
  86. 86.
    Wood JR, Perry GLW, Wilmshurst JM. 2017. Using palaeoecology to determine baseline ecological requirements and interaction networks for de-extinction candidate species. Funct. Ecol. 31:51012–20
    [Google Scholar]
  87. 87.
    Seddon PJ, Moehrenschlager A, Ewen J. 2014. Reintroducing resurrected species: selecting DeExtinction candidates. Trends Ecol. Evol. 29:3140–47
    [Google Scholar]
  88. 88.
    Deinet S, Ieronymidou C, McRae L, Burfield IJ, Foppen RP et al. 2022. Wildlife comeback in Europe: the recovery of selected mammal and bird species Rep., Rewild. Eur., ZSL, BirdLife Int., Eur. Bird Census Counc. London: ZSL
  89. 89.
    Kothmann KH, Jons A, Wilhelmi B, Kasozi N, Graham L et al. 2022. Non-invasive assessment of fecal glucocorticoid, progesterone, and androgen metabolites and microbiome in free-ranging southern white rhinoceros (Ceratotherium simum simum) in South Africa. Gen. Comp. Endocrinol. 329:114099
    [Google Scholar]
  90. 90.
    Wang Y, Kasper LH. 2013. The role of microbiome in central nervous system disorders. Brain Behav. Immun. 38:1–12
    [Google Scholar]
  91. 91.
    Zheng D, Liwinski T, Elinav E. 2020. Interaction between microbiota and immunity in health and disease. Cell Res 30:6492–506
    [Google Scholar]
  92. 92.
    Challender D, Cooney R. 2016. Informing decisions on trophy hunting Brief. Pap. Int. Union Conserv. Nat. Gland, Switz.:
  93. 93.
    Arney DR. 2021. Animal welfare and morality of the use of cloned animals. Scand. J. Lab. Anim. Sci. 47:425–30
    [Google Scholar]
  94. 94.
    Long CR, Walker SC, Tang RT, Westhusin ME. 2003. New commercial opportunities for advanced reproductive technologies in horses, wildlife, and companion animals. Theriogenology 59:139–49
    [Google Scholar]
  95. 95.
    De Mori B, Spiriti MM, Pollastri I, Normando S, Biasetti P et al. 2021. An ethical assessment tool (ETHAS) to evaluate the application of assisted reproductive technologies in mammals’ conservation: the case of the northern white rhinoceros (Ceratotherium simum cottoni). Animals 11:2312
    [Google Scholar]
  96. 96.
    Sandler RL, Moses L, Wisely SM. 2021. An ethical analysis of cloning for genetic rescue: case study of the black-footed ferret. Biol. Conserv. 257:109118
    [Google Scholar]
  97. 97.
    Devolder K. 2010. Complicity in stem cell research: the case of induced pluripotent stem cells. Hum. Reprod. 25:92175–80
    [Google Scholar]
  98. 98.
    Segers S, Mertes H, de Wert G, Dondorp W, Pennings G. 2017. Balancing ethical pros and cons of stem cell derived gametes. Ann. Biomed. Eng. 45:71620–32
    [Google Scholar]
  99. 99.
    Moradi S, Mahdizadeh H, Šarić T, Kim J, Harati J et al. 2019. Research and therapy with induced pluripotent stem cells (iPSCs): social, legal, and ethical considerations. Stem Cell Res. Ther. 10:341
    [Google Scholar]
  100. 100.
    Colossal 2023. The Mammoth https://colossal.com/mammoth/
  101. 101.
    Revive & Restore 2022. The black-footed ferret project. https://reviverestore.org/projects/black-footed-ferret/
  102. 102.
    IUCN Species Surviv. Comm 2016. IUCN SSC Guiding Principles on Creating Proxies of Extinct Species for Conservation Benefit Gland, Switz.: IUCN Species Surviv. Comm.
  103. 103.
    Shapiro B. 2017. Pathways to de-extinction: How close can we get to resurrection of an extinct species?. Funct. Ecol. 31:5996–1002
    [Google Scholar]
  104. 104.
    Aguilar-Cucurachi MAS, Dias PAD, Rangel-Negrín A, Chavira R, Boeck L, Canales-Espinosa D. 2010. Preliminary evidence of accumulation of stress during translocation in mantled howlers. Am. J. Primatol. 72:9805–10
    [Google Scholar]
  105. 105.
    Folch J, Cocero MJ, Chesné P, Alabart JL, Domínguez V et al. 2009. First birth of an animal from an extinct subspecies (Capra pyrenaica pyrenaica) by cloning. Theriogenology 71:61026–34
    [Google Scholar]
  106. 106.
    Novak BJ. 2018. De-extinction. Genes 9:11548
    [Google Scholar]
  107. 107.
    Dolman PM, Collar NJ, Scotland KM, Burnside RJ. 2015. Ark or park: the need to predict relative effectiveness of ex situ and in situ conservation before attempting captive breeding. J. Appl. Ecol. 52:4841–50
    [Google Scholar]
  108. 108.
    Gibbons E, Durrant B. 1987. Behavior and development in offspring from interspecies embryo transfer: theoretical issues. Appl. Anim. Behav. Sci. 18:1105–18
    [Google Scholar]
  109. 109.
    McCauley DJ, Hardesty-Moore M, Halpern BS, Young HS. 2017. A mammoth undertaking: harnessing insight from functional ecology to shape de-extinction priority setting. Funct. Ecol. 31:51003–11
    [Google Scholar]
  110. 110.
    Zimov SA. 2005. Pleistocene Park: return of the mammoth's ecosystem. Science 308:5723796–98
    [Google Scholar]
  111. 111.
    Steeves TE, Johnson JA, Hale ML. 2017. Maximising evolutionary potential in functional proxies for extinct species: a conservation genetic perspective on de-extinction. Funct. Ecol. 31:51032–40
    [Google Scholar]
  112. 112.
    Camacho AE. 2015. Going the way of the dodo: de-extinction, dualisms, and reframing conservation. Harvard Law Rev. 92:4849–906
    [Google Scholar]
  113. 113.
    Sherkow JS, Greely HT. 2013. What if extinction is not forever?. Science 340:612832–33
    [Google Scholar]
  114. 114.
    Robert A, Thévenin C, Princé K, Sarrazin F, Clavel J. 2017. De-extinction and evolution. Funct. Ecol. 31:51021–31
    [Google Scholar]
  115. 115.
    Jones KE. 2014. From dinosaurs to dodos: Who could and should we de-extinct?. Front. Biogeogr. 6:1 https://doi.org/10.21425/F5FBG19431
    [Crossref] [Google Scholar]
  116. 116.
    Richmond DJ, Sinding M-HS, Thomas M, Gilbert P, Richmond DJ et al. 2016. The potential and pitfalls of de-extinction. Zool. Scr. 45:22–36
    [Google Scholar]
  117. 117.
    Ricketts TH, Dinerstein E, Boucher T, Brooks TM, Butchart SHM et al. 2005. Pinpointing and preventing imminent extinctions. PNAS 102:5118497–501
    [Google Scholar]
  118. 118.
    Isaac NJB, Turvey ST, Collen B, Waterman C, Baillie JEM 2007. Mammals on the EDGE: conservation priorities based on threat and phylogeny. PLOS ONE 2:3e296
    [Google Scholar]
  119. 119.
    Comizzoli P, Holt WV. 2019. Breakthroughs and new horizons in reproductive biology of rare and endangered animal species. Biol. Reprod. 101:3514–25
    [Google Scholar]
  120. 120.
    Santymire RM, Livieri TM, Branvold-Faber H, Marinari PE. 2014. The black-footed ferret: On the brink of recovery?. See Reference 41 119–34
/content/journals/10.1146/annurev-animal-071423-093523
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/content/journals/10.1146/annurev-animal-071423-093523
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  • Article Type: Review Article
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