1932

Abstract

Reproductive science in the context of conservation biology is often understood solely in terms of breeding threatened species. Although technologies developed primarily for agriculture or biomedicine have a potentially important role in species conservation, their effectiveness is limited if we regard the main objective of animal conservation as helping to support populations rather than to breed a small number of individuals. The global threats facing wild species include the consequences of climate change, population growth, urbanization, atmospheric and water pollution, and the release of chemicals into the environment, to cite but a few. Reproductive sciences provide important and often unexpected windows into many of these consequences, and our aim here is both to demonstrate the breadth of reproductive science and the importance of basic knowledge and to suggest where some of the insights might be useful in mitigating the problems.

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2022-02-15
2024-04-20
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Literature Cited

  1. 1. 
    Comizzoli P, Brown JL, Holt WV 2019. Reproductive Sciences in Animal Conservation, Vol. 1200 Cham, Switz.: Springer Int. Publ.
    [Google Scholar]
  2. 2. 
    Pilgrim KL, McKelvey KS, Riddle AE, Schwartz MK. 2005. Felid sex identification based on noninvasive genetic samples. Mol. Ecol. Notes 5:60–61
    [Google Scholar]
  3. 3. 
    Flasko A, Manseau M, Mastromonaco G, Bradley M, Neufeld L, Wilson P. 2017. Fecal DNA, hormones, and pellet morphometrics as a noninvasive method to estimate age class: an application to wild populations of Central Mountain and Boreal woodland caribou (Rangifer tarandus caribou). Can. J. Zool. 95:311–21
    [Google Scholar]
  4. 4. 
    Asa C, Moresco A 2019. Fertility control in wildlife: review of current status, including novel and future technologies. See Reference 1 507–43
  5. 5. 
    Cope HR, Hogg CJ, White PJ, Herbert CA. 2018. A role for selective contraception of individuals in conservation. Conserv. Biol. 32:546–58
    [Google Scholar]
  6. 6. 
    Mayer I. 2019. The role of reproductive sciences in the preservation and breeding of commercial and threatened teleost fish. See Reference 1 187–224
  7. 7. 
    Clulow J, Upton R, Trudeau VL, Clulow S. 2019. Amphibian assisted reproductive technologies: moving from technology to application. See Reference 1 413–63
  8. 8. 
    O'Brien JK, Steinman KJ, Montano GA, Dubach JM, Robeck TR. 2016. Chicks produced in the magellanic penguin (Spheniscus magellanicus) after cloacal insemination of frozen-thawed semen. Zoo Biol 35:326–38
    [Google Scholar]
  9. 9. 
    Hagedorn M, Spindler R, Daly J. 2019. Cryopreservation as a tool for reef restoration: 2019. See Reference 1 489–505
    [Google Scholar]
  10. 10. 
    Spindler R, Keeley T, Satake N 2014. Applied andrology in endangered, exotic and wildlife species. Animal Andrology: Theories and Applications PJ Chenoweth, SP Lorton 450–73 Wallingford, UK: CABI
    [Google Scholar]
  11. 11. 
    Prieto MT, Sanchez-Calabuig MJ, Hildebrandt TB, Santiago-Moreno J, Saragusty J. 2014. Sperm cryopreservation in wild animals. Eur. J. Wildl. Res. 60:851–64
    [Google Scholar]
  12. 12. 
    Findlay JK, Holland MK, Wong BBM. 2019. Reproductive science and the future of the planet. Reproduction 158:R91–R96
    [Google Scholar]
  13. 13. 
    Patrick J, Comizzoli P, Elliott G 2017. Dry preservation of spermatozoa: considerations for different species. Biopreserv. Biobank 15:158–68
    [Google Scholar]
  14. 14. 
    Saragusty J, Loi P. 2019. Exploring dry storage as an alternative biobanking strategy inspired by Nature. Theriogenology 126:17–27
    [Google Scholar]
  15. 15. 
    Minteer BA. 2018. The Fall of the Wild: Extinction, De-Extinction, and the Ethics of Conservation New York: Columbia Univ. Press
  16. 16. 
    Shapiro B. 2016. Pathways to de-extinction: How close can we get to resurrection of an extinct species?. Funct. Ecol. 31:996–1002
    [Google Scholar]
  17. 17. 
    Int. Union Conserv. Nat 2016. IUCN SSC Guiding principles on Creating Proxies of Extinct Species Gland, Switz.: Int. Union Conserv. Nat.
  18. 18. 
    Li D, Wintle NJP, Zhang G, Wang C, Luo B et al. 2017. Analyzing the past to understand the future: Natural mating yields better reproductive rates than artificial insemination in the giant panda. Biol. Conserv. 216:10–17
    [Google Scholar]
  19. 19. 
    Martin-Wintle MS, Kersey DC, Wintle NJP, Aitken-Palmer C, Owen MA, Swaisgood RR 2019. Comprehensive breeding techniques for the giant panda. See Reference 1 275–308
  20. 20. 
    Howard JG, Lynch C, Santymire RM, Marinari PE, Wildt DE. 2016. Recovery of gene diversity using long-term cryopreserved spermatozoa and artificial insemination in the endangered black-footed ferret: black-footed ferret gene restoration. Anim. Conserv. 19:102–11
    [Google Scholar]
  21. 21. 
    Santymire RM, Livieri TM, Branvold-Faber H, Marinari PE 2014. The black-footed ferret: On the brink of recovery?. Reproductive Sciences in Animal Conservation WV Holt, JL Brown, P Comizzoli 119–34 New York: Springer-Verlag
    [Google Scholar]
  22. 22. 
    Keller LF, Waller DM. 2002. Inbreeding effects in wild populations. Trends Ecol. Evol. 17:230–41
    [Google Scholar]
  23. 23. 
    Ralls K, Sunnucks P, Lacy RC, Frankham R 2020. Genetic rescue: A critique of the evidence supports maximizing genetic diversity rather than minimizing the introduction of putatively harmful genetic variation. Biol. Conserv. 251:108784
    [Google Scholar]
  24. 24. 
    Taylor AC 2003. Assessing the consequences of inbreeding for population fitness: past challenges and future prospects. Reproductive Science and Integrated Conservation WV Holt, AR Pickard, JC Rodger, DE Wildt 67–81 Cambridge, UK: Cambridge Univ. Press
    [Google Scholar]
  25. 25. 
    Frankham R, Ballou JD, Ralls K, Eldridge MD, Dudash MR et al. 2019. Inbreeding and loss of genetic diversity increase extinction risk. A Practical Guide for Genetic Management of Fragmented Animal and Plant Populations31–48 Oxford, UK: Oxford Univ. Press
    [Google Scholar]
  26. 26. 
    Della Togna G, Howell LG, Clulow J, Langhorne CJ, Marcec-Greaves R, Calatayud NE 2020. Evaluating amphibian biobanking and reproduction for captive breeding programs according to the Amphibian Conservation Action Plan objectives. Theriogenology 150:412–31
    [Google Scholar]
  27. 27. 
    Zahmel J, Fernandez-Gonzalez L, Jewgenow K, Müller K 2019. Felid-gamete-rescue within EAZA - efforts and results in biobanking felid oocytes and sperm. J. Zoo Aquar. Res. 7:15–24
    [Google Scholar]
  28. 28. 
    Mara L, Casu S, Carta A, Dattena M 2013. Cryobanking of farm animal gametes and embryos as a means of conserving livestock genetics. Anim. Reprod. Sci. 138:25–38
    [Google Scholar]
  29. 29. 
    Lermen D, Blomeke B, Browne R, Clarke A, Dyce PW et al. 2009. Cryobanking of viable biomaterials: implementation of new strategies for conservation purposes. Mol. Ecol. 18:1030–33
    [Google Scholar]
  30. 30. 
    Halbert ND, Grant WE, Derr JN 2005. Genetic and demographic consequences of importing animals into a small population: a simulation model of the Texas State Bison Herd (USA). Ecol. Model. 181:263–76
    [Google Scholar]
  31. 31. 
    Halbert ND, Raudsepp T, Chowdhary BP, Derr JN. 2004. Conservation genetic analysis of the Texas State Bison Herd. J. Mammal. 85:924–31
    [Google Scholar]
  32. 32. 
    Harnal VK, Wildt DE, Bird DM, Monfort SL, Ballou JD. 2002. Computer simulations to determine the efficacy of different genome resource banking strategies for maintaining genetic diversity. Cryobiology 44:122–31
    [Google Scholar]
  33. 33. 
    Williams SE, Hoffman EA. 2009. Minimizing genetic adaptation in captive breeding programs: a review. Biol. Conserv. 142:2388–400
    [Google Scholar]
  34. 34. 
    Gooley RM, Hogg CJ, Fox S, Pemberton D, Belov K, Grueber CE. 2020. Inbreeding depression in one of the last DFTD-free wild populations of Tasmanian devils. PeerJ 8:e9220
    [Google Scholar]
  35. 35. 
    McLennan EA, Grueber CE, Wise P, Belov K, Hogg CJ. 2020. Mixing genetically differentiated populations successfully boosts diversity of an endangered carnivore. Anim. Conserv. 23:700–12
    [Google Scholar]
  36. 36. 
    Brandies PA, Wright BR, Hogg CJ, Grueber CE, Belov K. 2020. Characterization of reproductive gene diversity in the endangered Tasmanian devil. Mol. Ecol. Resour. 21:721–32
    [Google Scholar]
  37. 37. 
    Farquharson KA, Gooley RM, Fox S, Huxtable SJ, Belov K et al. 2018. Are any populations “safe”? Unexpected reproductive decline in a population of Tasmanian devils free of devil facial tumour disease. Wildl. Res. 45:31–37
    [Google Scholar]
  38. 38. 
    Johnston SD, Lopez-Fernandez C, Arroyo F, Roy R, Holt WV, Gosalvez J 2019. Protamine composition of koala and wombat spermatozoa provides new insights into DNA stability following cryopreservation. Reprod. Fertil. Dev. 31:1558–66
    [Google Scholar]
  39. 39. 
    Rodger JC. 2019. Marsupials: progress and prospects. See Reference 1 309–25
  40. 40. 
    Dicks N, Bordignon V, Mastromonaco GF 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]
  41. 41. 
    Johnston SD, Holt WV. 2019. Using the koala (Phascolarctos cinereus) as a case study to illustrate the development of artificial breeding technology in marsupials: an update. Adv. Exp. Med. Biol. 1200:327–62
    [Google Scholar]
  42. 42. 
    Allen CD, Burridge M, Mulhall S, Chafer ML, Nicolson VN et al. 2008. Successful artificial insemination in the koala (Phascolarctos cinereus) using extended and extended-chilled semen collected by electroejaculation. Biol. Reprod. 78:661–66
    [Google Scholar]
  43. 43. 
    Johnston SD, O'Callaghan P, Nilsson K, Tzipori G, Curlewis JD 2004. Semen-induced luteal phase and identification of a LH surge in the koala (Phascolarctos cinereus). Reproduction 128:629–34
    [Google Scholar]
  44. 44. 
    Saint Jalme M, Lecoq R, Seigneurin F, Blesbois E, Plouzeau E 2003. Cryopreservation of semen from endangered pheasants: the first step towards a cryobank for endangered avian species. Theriogenology 59:875–88
    [Google Scholar]
  45. 45. 
    Blesbois E, Seigneurin F, Grasseau I, Limouzin C, Besnard J et al. 2007. Semen cryopreservation for ex situ management of genetic diversity in chicken: creation of the French avian cryobank. Poult. Sci. 86:555–64
    [Google Scholar]
  46. 46. 
    Morrell JM, Mayer I. 2017. Reproduction biotechnologies in germplasm banking of livestock species: a review. Zygote 25:545–57
    [Google Scholar]
  47. 47. 
    Uteshev VK, Gakhova EN, Kramarova LI, Shishova NV, Kaurova SA, Browne RK. 2019. Cryobanking of amphibian genetic recourses in Russia: past and future. Russ. J. Herpetol. 26:319–24
    [Google Scholar]
  48. 48. 
    Kouba AJ, Lloyd RE, Houck ML, Silla AJ, Calatayud N et al. 2013. Emerging trends for biobanking amphibian genetic resources: the hope, reality and challenges for the next decade. Biol. Conserv. 164:10–21
    [Google Scholar]
  49. 49. 
    Strand J, Thomsen H, Jensen JB, Marcussen C, Nicolajsen TB et al. 2020. Biobanking in amphibian and reptilian conservation and management: opportunities and challenges. Conserv. Genet. Resour. 12:709–25
    [Google Scholar]
  50. 50. 
    Birkhead T, Møller A. 1993. Female control of paternity. Trends Ecol. Evol. 8:100–4
    [Google Scholar]
  51. 51. 
    Holt WV, Fazeli A. 2016. Sperm storage in the female reproductive tract. Annu. Rev. Anim. Biosci. 4:291–310
    [Google Scholar]
  52. 52. 
    Orr TJ, Zuk M. 2014. Reproductive delays in mammals: an unexplored avenue for post-copulatory sexual selection. Biol. Rev. Cambridge Philos. Soc. 89:889–912
    [Google Scholar]
  53. 53. 
    Fischer D, Schneider H, Meinecke-Tillmann S, Wehrend A, Lierz M 2020. Semen analysis and successful artificial insemination in the St. Vincent amazon (Amazona guildingii). Theriogenology 148:132–39
    [Google Scholar]
  54. 54. 
    Blanco JM, Gee GF, Wildt DE, Donoghue AM. 2002. Producing progeny from endangered birds of prey: treatment of urine-contaminated semen and a novel intramagnal insemination approach. J. Zoo Wildl. Med. 33:1–7
    [Google Scholar]
  55. 55. 
    Villaverde-Morcillo S, García-Sánchez R, Castaño C, Rodríguez E, Gonzalez F et al. 2015. Characterization of natural ejaculates and sperm cryopreservation in a golden eagle (Aquila chrysaetus). J. Zoo Wildl. Med. 46:335–38
    [Google Scholar]
  56. 56. 
    Dogliero A, Rota A, Lofiego R, von Degerfeld MM, Quaranta G. 2016. Semen evaluation in four autochthonous wild raptor species using computer-aided sperm analyzer. Theriogenology 85:1113–17
    [Google Scholar]
  57. 57. 
    Mattson JK, DeVries AT, McGuire SM, Krebs J, Louis EE, Loskutoff NM 2007. Successful artificial insemination in the corn snake (Elaphe gutatta), using fresh and cooled semen. Reprod. Fertil. Dev. 19:240
    [Google Scholar]
  58. 58. 
    Zacariotti RL, Grego KF, Fernandes W, Sant'Anna SS, Guimaraes M. 2007. Semen collection and evaluation in free-ranging Brazilian rattlesnakes (Crotalus durissus terrificus). Zoo Biol 26:155–60
    [Google Scholar]
  59. 59. 
    Oliveri M, Bartoskova A, Spadola F, Morici M, di Giuseppe M, Knotek Z. 2018. Method of semen collection and artificial insemination in snakes. J. Exot. Pet. Med. 27:75–80
    [Google Scholar]
  60. 60. 
    Racey PA 1975. The prolonged survival of spermatozoa in bats. The Biology of the Male Gamete JG Duckett, PA Racey 385–416 London: Academic
    [Google Scholar]
  61. 61. 
    Racey PA, Suzuki F, Medway L. 1973. The relationship between stored spermatozoa and the oviductal epithelium in bats of the genus Tylonycteris. Colloq. Inst. Natl. Sante Rech. Med. 26:283–94
    [Google Scholar]
  62. 62. 
    Hunter RHF. 1981. Sperm transport and reservoirs in the pig oviduct in relation to the time of ovulation. J. Reprod. Fertil. 63:109–17
    [Google Scholar]
  63. 63. 
    Hunter RH, Nichol R. 1983. Transport of spermatozoa in the sheep oviduct: preovulatory sequestering of cells in the caudal isthmus. J. Exp. Zool. 228:121–28
    [Google Scholar]
  64. 64. 
    Holt WV, Elliott RM, Fazeli A, Sostaric E, Georgiou AS et al. 2006. Harnessing the biology of the oviduct for the benefit of artificial insemination. Soc. Reprod. Fertil. Suppl. 62:247–59
    [Google Scholar]
  65. 65. 
    Aldarmahi A, Elliott S, Russell J, Fazeli A 2014. Effects of spermatozoa-oviductal cell coincubation time and oviductal cell age on spermatozoa-oviduct interactions. Reprod. Fertil. Dev. 26:358–65
    [Google Scholar]
  66. 66. 
    Elliott RM, Lloyd RE, Fazeli A, Sostaric E, Georgiou AS et al. 2009. Effects of HSPA8, an evolutionarily conserved oviductal protein, on boar and bull spermatozoa. Reproduction 137:191–203
    [Google Scholar]
  67. 67. 
    Holt WV, Del Valle I, Fazeli A 2015. Heat shock protein A8 stabilizes the bull sperm plasma membrane during cryopreservation: effects of breed, protein concentration, and mode of use. Theriogenology 84:693–701
    [Google Scholar]
  68. 68. 
    Moein-Vaziri N, Phillips I, Smith S, Almiñana C, Maside C et al. 2014. Heat shock protein A8 restores sperm membrane integrity by increasing plasma membrane fluidity. Reproduction 147:719–32
    [Google Scholar]
  69. 69. 
    Lloyd RE, Elliott RM, Fazeli A, Watson PF, Holt WV. 2009. Effects of oviductal proteins, including heat shock 70 kDa protein 8, on survival of ram spermatozoa over 48 h in vitro. Reprod. Fertil. Dev. 21:408–18
    [Google Scholar]
  70. 70. 
    Alvarez-Rodríguez M, Alvarez M, Borragan S, Martinez-Pastor F, Holt WV et al. 2013. The addition of heat shock protein HSPA8 to cryoprotective media improves the survival of brown bear (Ursus arctos) spermatozoa during chilling and after cryopreservation. Theriogenology 79:541–50
    [Google Scholar]
  71. 71. 
    Roy VK, Krishna A. 2011. Sperm storage in the female reproductive tract of Scotophilus heathii: role of androgen. Mol. Reprod. Dev. 78:477–87
    [Google Scholar]
  72. 72. 
    Roy VK, Krishna A. 2012. Changes in the expression of HSL and OCTN2 in the female reproductive tract of the bat, Scotophilus heathii in relation to sperm storage. Acta Histochem 114:358–62
    [Google Scholar]
  73. 73. 
    Chen H, Liu T, Holt WV, Yang P, Zhang L et al. 2020. Advances in understanding mechanisms of long-term sperm storage-the soft-shelled turtle model. Histol. Histopathol. 35:1–23
    [Google Scholar]
  74. 74. 
    Brown JL, Wildt DE. 1997. Assessing reproductive status in wild felids by non-invasive faecal steroid monitoring. Int. Zoo Yearb. 35:173–91
    [Google Scholar]
  75. 75. 
    Schwarzenberger F, Mostl E, Palme R, Bamberg E 1996. Faecal steroid analysis for non-invasive monitoring of reproductive status in farm, wild and zoo animals. Anim. Reprod. Sci. 42:515–26
    [Google Scholar]
  76. 76. 
    Ganswindt A, Brown JL, Freeman EW, Kouba AJ, Penfold LM et al. 2012. International Society for Wildlife Endocrinology: the future of endocrine measures for reproductive science, animal welfare and conservation biology. Biol. Lett. 8:695–97
    [Google Scholar]
  77. 77. 
    Creel S, Christianson D, Schuette P. 2013. Glucocorticoid stress responses of lions in relationship to group composition, human land use, and proximity to people. Conserv. Physiol. 1:cot021
    [Google Scholar]
  78. 78. 
    Ezenwa VO, Ekernas LS, Creel S. 2012. Unravelling complex associations between testosterone and parasite infection in the wild. Funct. Ecol. 26:123–33
    [Google Scholar]
  79. 79. 
    De La Peña E, Martín J, Barja I, Pérez-Caballero R, Acosta I, Carranza J 2020. Immune challenge of mating effort: steroid hormone profile, dark ventral patch and parasite burden in relation to intrasexual competition in male Iberian red deer. Integr. Zool. 15:262–75
    [Google Scholar]
  80. 80. 
    Habig B, Archie EA. 2015. Social status, immune response and parasitism in males: a meta-analysis. Philos. Trans. R. Soc. Lond. B 370:20140109
    [Google Scholar]
  81. 81. 
    Lanyon JM, Burgess EA. 2019. Reproductive science methods for wild, fully-marine mammals: current approaches and future applications. See Reference 1 363–411
  82. 82. 
    Hunt KE, Robbins J, Rolland RM. 2016. Development of fecal hormone techniques for assessment of reproduction and stress in humpback whales (Megaptera novaeangliae). Integr. Comp. Biol. 56:E98
    [Google Scholar]
  83. 83. 
    Valenzuela-Molina M, Atkinson S, Mashburn K, Gendron D, Brownell RL Jr 2018. Fecal steroid hormones reveal reproductive state in female blue whales sampled in the Gulf of California, Mexico. Gen. Comp. Endocrinol. 261:127–35
    [Google Scholar]
  84. 84. 
    Lemos LS, Olsen A, Smith A, Chandler TE, Larson S et al. 2020. Assessment of fecal steroid and thyroid hormone metabolites in eastern North Pacific gray whales. Conserv. Physiol. 8:coaa110
    [Google Scholar]
  85. 85. 
    Pereira RJG, Christofoletti MD, Blank MH, Duarte JMB. 2018. Urofecal steroid profiles of captive Blue-fronted parrots (Amazona aestiva) with different reproductive outcomes. Gen. Comp. Endocrinol. 260:1–8
    [Google Scholar]
  86. 86. 
    Young AM, Hallford DM. 2013. Validation of a fecal glucocorticoid metabolite assay to assess stress in the budgerigar (Melopsittacus undulatus). Zoo Biol 32:112–16
    [Google Scholar]
  87. 87. 
    Penfold LM, Hallager S, Boylan J, de Wit M, Metrione LC, Oliva M 2013. Differences in fecal androgen patterns of breeding and nonbreeding kori bustards (Ardeotis kori). Zoo Biol 32:54–62
    [Google Scholar]
  88. 88. 
    Zuberi A, Ali S, Brown C 2011. A non-invasive assay for monitoring stress responses: a comparison between wild and captive-reared rainbowfish (Melanoteania duboulayi). Aquaculture 321:267–72
    [Google Scholar]
  89. 89. 
    Lupica SJ, Turner JW. 2009. Validation of enzyme-linked immunosorbent assay for measurement of faecal cortisol in fish. Aquac. Res. 40:437–41
    [Google Scholar]
  90. 90. 
    Scott AP, Ellis T. 2007. Measurement of fish steroids in water—a review. Gen. Comp. Endocrinol. 153:392–400
    [Google Scholar]
  91. 91. 
    Makaras T, Razumiene J, Gureviciene V, Sakinyte I, Stankeviciute M, Kazlauskiene N. 2020. A new approach of stress evaluation in fish using β-d-glucose measurement in fish holding-water. Ecol. Indic. 109:105829
    [Google Scholar]
  92. 92. 
    Khanwalker M, Johns J, Honikel MM, Smith V, Maxwell S et al. 2019. Electrochemical detection of fertility hormones. Crit. Rev. Biomed. Eng. 47:235–47
    [Google Scholar]
  93. 93. 
    Kappel ND, Proll F, Gauglitz G 2007. Development of a TIRF-based biosensor for sensitive detection of progesterone in bovine milk. Biosens. Bioelectron. 22:2295–300
    [Google Scholar]
  94. 94. 
    Conley AJ, Loux SC, Legacki EL, Stoops MA, Pukazhenthi B et al. 2021. The steroid metabolome of pregnancy, insights into the maintenance of pregnancy and evolution of reproductive traits. Mol. Cell. Endocrinol. 528:111241
    [Google Scholar]
  95. 95. 
    Rivers N, Daly J, Jones R, Temple-Smith P. 2020. Cryopreservation of testicular tissue from Murray River Rainbowfish, Melanotaenia fluviatilis. Sci. Rep. 10:19355
    [Google Scholar]
  96. 96. 
    Comizzoli P, Holt WV. 2019. Breakthroughs and new horizons in reproductive biology of rare and endangered animal species. Biol. Reprod. 101:514–25
    [Google Scholar]
  97. 97. 
    Rollins-Smith LA. 2020. Global amphibian declines, disease, and the ongoing battle between Batrachochytrium fungi and the immune system. Herpetologica 76:178–88
    [Google Scholar]
  98. 98. 
    Daszak P, Berger L, Cunningham AA, Hyatt AD, Green DE, Speare R. 1999. Emerging infectious diseases and amphibian population declines. Emerg. Infect. Dis. 5:735–48
    [Google Scholar]
  99. 99. 
    Fisher MC, Garner TWJ. 2020. Chytrid fungi and global amphibian declines. Nat. Rev. Microbiol. 18:332–43
    [Google Scholar]
  100. 100. 
    Kouba AJ, Vance CK. 2009. Applied reproductive technologies and genetic resource banking for amphibian conservation. Reprod. Fertil. Dev. 21:719–37
    [Google Scholar]
  101. 101. 
    Campbell L, Cafe SL, Upton R, Doody JS, Nixon B et al. 2020. A model protocol for the cryopreservation and recovery of motile lizard sperm using the phosphodiesterase inhibitor caffeine. Conserv. Physiol. 8:coaa044
    [Google Scholar]
  102. 102. 
    Browne RK, Silla AJ, Upton R, Della-Togna G, Marcec-Greaves R et al. 2019. Sperm collection and storage for the sustainable management of amphibian biodiversity. Theriogenology 133:187–200
    [Google Scholar]
  103. 103. 
    Clulow J, Clulow S. 2016. Cryopreservation and other assisted reproductive technologies for the conservation of threatened amphibians and reptiles: bringing the ARTs up to speed. Reprod. Fertil. Dev. 28:1116–32
    [Google Scholar]
  104. 104. 
    Graham KM, Kouba AJ, Langhorne CJ, Marcec RM, Willard ST. 2016. Biological sex identification in the endangered dusky gopher frog (Lithobates sevosa): a comparison of body size measurements, secondary sex characteristics, ultrasound imaging, and urinary hormone analysis methods. Reprod. Biol. Endocrinol. 14:41
    [Google Scholar]
  105. 105. 
    Silla AJ, Byrne PG. 2019. The role of reproductive technologies in amphibian conservation breeding programs. Annu. Rev. Anim. Biosci. 7:499–519
    [Google Scholar]
  106. 106. 
    Howell LG, Frankham R, Rodger JC, Witt RR, Clulow S et al. 2020. Integrating biobanking minimises inbreeding and produces significant cost benefits for a threatened frog captive breeding programme. Conserv. Lett. 14:2e12776
    [Google Scholar]
  107. 107. 
    Poo S, Hinkson KM. 2020. Amphibian conservation using assisted reproductive technologies: Cryopreserved sperm affects offspring morphology, but not behavior, in a toad. Glob. Ecol. Conserv. 21:e00809
    [Google Scholar]
  108. 108. 
    Garner TWJ, Schmidt BR, Martel A, Pasmans F, Muths E et al. 2016. Mitigating amphibian chytridiomycoses in nature. Philos. Trans. R. Soc. Lond. B 371:20160207
    [Google Scholar]
  109. 109. 
    Venesky MD, Mendelson JR III, Sears BF, Stiling P, Rohr JR. 2012. Selecting for tolerance against pathogens and herbivores to enhance success of reintroduction and translocation. Conserv. Biol. 26:586–92
    [Google Scholar]
  110. 110. 
    Smith C, Wootton RJ 2016. The remarkable reproductive diversity of teleost fishes. Fish Fish 17:1208–15
    [Google Scholar]
  111. 111. 
    Int. Union Conserv. Nat 2020. IUCN 2020. The IUCN Red List of Threatened Species Version 2020–2 Cambridge, UK: Int. Union Conserv. Nat https://www.iucnredlist.org
  112. 112. 
    Tiersch TR, Yang H, Hu E 2011. Outlook for development of high-throughput cryopreservation for small-bodied biomedical model fishes. Comp. Biochem. Physiol. C 154:76–81
    [Google Scholar]
  113. 113. 
    Billard R, Zhang T 2001. Techniques of genetic resource banking in fish. Cryobanking the Genetic Resource: Wildlife Conservation for the Future? PF Watson, WV Holt 143–70 London, UK: Taylor & Francis
    [Google Scholar]
  114. 114. 
    Liu Y, Blackburn H, Taylor SS, Tiersch TR 2019. Development of germplasm repositories to assist conservation of endangered fishes: examples from small-bodied livebearing fishes. Theriogenology 135:138–51
    [Google Scholar]
  115. 115. 
    Maceda-Veiga A. 2013. Towards the conservation of freshwater fish: Iberian Rivers as an example of threats and management practices. Rev. Fish Biol. Fish. 23:1–22
    [Google Scholar]
  116. 116. 
    Yang H, Tiersch TR 2009. Current status of sperm cryopreservation in biomedical research fish models: zebrafish, medaka, and Xiphophorus. Comp. Biochem. Physiol. C 149:224–32
    [Google Scholar]
  117. 117. 
    Liu Y, Grier H, Tiersch TR 2018. Production of live young with cryopreserved sperm from the endangered livebearing fish redtail splitfin (Xenotoca eiseni, Rutter, 1896). Anim. Reprod. Sci. 196:77–90
    [Google Scholar]
  118. 118. 
    Iida A, Nomura J, Hondo E. 2021. Histological observation of the reproductive system in a viviparous teleost Xenotoca eiseni Rutter 1896 (Cyprinodontiformes: Goodeidae). Anat. Histol. Embryol. 50:161–68
    [Google Scholar]
  119. 119. 
    Yang H, Hazlewood L, Walter RB, Tiersch TR. 2009. Sperm cryopreservation of a live-bearing fish, Xiphophorus couchianus: male-to-male variation in post-thaw motility and production of F1 hybrid offspring. Comp. Biochem. Physiol. C 149:233–39
    [Google Scholar]
  120. 120. 
    Yanagimachi R, Cherr G, Matsubara T, Andoh T, Harumi T et al. 2013. Sperm attractant in the micropyle region of fish and insect eggs. Biol. Reprod. 88:47–51
    [Google Scholar]
  121. 121. 
    Hagedorn M, Hsu E, Kleinhans FW, Wildt DE. 1997. New approaches for studying the permeability of fish embryos: toward successful cryopreservation. Cryobiology 34:335–47
    [Google Scholar]
  122. 122. 
    Hagedorn M, Kleinhans FW, Freitas R, Liu J, Hsu EW et al. 1997. Water distribution and permeability of zebrafish embryos, Brachydanio rerio. J. Exp. Zool. 278:356–67
    [Google Scholar]
  123. 123. 
    Litscher ES, Wassarman PM. 2014. Evolution, structure, and synthesis of vertebrate egg-coat proteins. Trends Dev. Biol. 8:65–76
    [Google Scholar]
  124. 124. 
    Diwan AD, Harke SN,Gopalkrishna Panche AN. 2020. Cryobanking of fish and shellfish egg, embryos and larvae: an overview. Front. Mar. Sci. 7:251
    [Google Scholar]
  125. 125. 
    Rivers N, Daly J, Temple-Smith P. 2020. New directions in assisted breeding techniques for fish conservation. Reprod. Fertil. Dev. 32:807–21
    [Google Scholar]
  126. 126. 
    Saito T, Goto-Kazeto R, Fujimoto T, Kawakami Y, Arai K, Yamaha E. 2010. Inter-species transplantation and migration of primordial germ cells in cyprinid fish. Int. J. Dev. Biol. 54:1481–86
    [Google Scholar]
  127. 127. 
    Kawakami Y, Goto-Kazeto R, Saito T, Fujimoto T, Higaki S et al. 2010. Generation of germ-line chimera zebrafish using primordial germ cells isolated from cultured blastomeres and cryopreserved embryoids. Int. J. Dev. Biol. 54:1493–501
    [Google Scholar]
  128. 128. 
    Kobayashi T, Takeuchi Y, Takeuchi T, Yoshizaki G. 2007. Generation of viable fish from cryopreserved primordial germ cells. Mol. Reprod. Dev. 74:207–13
    [Google Scholar]
  129. 129. 
    Okutsu T, Suzuki K, Takeuchi Y, Takeuchi T, Yoshizaki G. 2006. Testicular germ cells can colonize sexually undifferentiated embryonic gonad and produce functional eggs in fish. PNAS 103:2725–29
    [Google Scholar]
  130. 130. 
    Jonsson B, Jonsson N. 2014. Early environment influences later performance in fishes. J. Fish. Biol. 85:151–88
    [Google Scholar]
  131. 131. 
    Hare AJ, Zimmer AM, LePabic R, Morgan AL, Gilmour KM 2021. Early-life stress influences ion balance in developing zebrafish (Danio rerio). J. Comp. Physiol. B 191:69–84
    [Google Scholar]
  132. 132. 
    Laing LV, Viana J, Dempster EL, Webster TMU, van Aerle R et al. 2018. Sex-specific transcription and DNA methylation profiles of reproductive and epigenetic associated genes in the gonads and livers of breeding zebrafish. Comp. Biochem. Phys. A 222:16–25
    [Google Scholar]
  133. 133. 
    Todd EV, Ortega-Recalde O, Liu H, Lamm MS, Rutherford KM et al. 2019. Stress, novel sex genes, and epigenetic reprogramming orchestrate socially controlled sex change. Sci. Adv. 5:eaaw7006
    [Google Scholar]
  134. 134. 
    Fargeot L, Loot G, Prunier JMG, Rey O, Veyssiere C, Blanchet S 2021. Patterns of epigenetic diversity in two sympatric fish species: genetic versus environmental determinants. Genes 12:107
    [Google Scholar]
  135. 135. 
    Siripattarapravat K, Prukudom S, Cibelli J 2016. Method for somatic cell nuclear transfer in zebrafish. Zebrafish: Genetics, Genomics, and Transcriptomics, Vol. 135 HW Detrich, M Westerfield, LI Zon 245–57 Cambridge, MA: Academic. , 4th ed..
    [Google Scholar]
  136. 136. 
    Fatira E, Havelka M, Labbé C, Depince A, Iegorova V et al. 2018. Application of interspecific Somatic Cell Nuclear Transfer (ISCNT) in sturgeons and an unexpectedly produced gynogenetic sterlet with homozygous quadruple haploid. Sci. Rep. 8:5997
    [Google Scholar]
  137. 137. 
    Fatira E, Havelka M, Labbé C, Depince A, Psenicka M, Saito T. 2019. A newly developed cloning technique in sturgeons; an important step towards recovering endangered species. Sci. Rep. 9:10453
    [Google Scholar]
  138. 138. 
    Rouillon C, Depince A, Chenais N, Le Bail P-Y, Labbé C 2019. Somatic cell nuclear transfer in non-enucleated goldfish oocytes: understanding DNA fate during oocyte activation and first cellular division. Sci. Rep. 9:12462
    [Google Scholar]
  139. 139. 
    Chenais N, Depince A, Le Bail P-Y, Labbé C 2014. Fin cell cryopreservation and fish reconstruction by nuclear transfer stand as promising technologies for preservation of finfish genetic resources. Aquacult. Int. 22:63–76
    [Google Scholar]
  140. 140. 
    Wiedemann C, Hribal R, Ringleb J, Bertelsen MF, Rasmusen K et al. 2012. Preservation of primordial follicles from lions by slow freezing and xenotransplantation of ovarian cortex into an immunodeficient mouse. Reprod. Domest. Anim. 47:300–4
    [Google Scholar]
  141. 141. 
    Landi M, Everitt J, Berridge B. 2021. Bioethical, reproducibility, and translational challenges of animal models. ILAR J. 2021:ilaa027
    [Google Scholar]
  142. 142. 
    Mrowiec P, Bugno-Poniewierska M, Mlodawska W. 2021. The perspective of the incompatible of nucleus and mitochondria in interspecies somatic cell nuclear transfer for endangered species. Reprod. Domest. Anim. 56:199–207
    [Google Scholar]
  143. 143. 
    Zhao X-Y, Li W, Lv Z, Liu L, Tong M et al. 2010. Viable fertile mice generated from fully pluripotent IPS cells derived from adult somatic cells. Stem. Cell Rev. Rep. 6:390–97
    [Google Scholar]
  144. 144. 
    Diagne C, Leroy B, Vaissière A-C, Gozlan RE, Roiz D et al. 2021. High and rising economic costs of biological invasions worldwide. Nature 592:571–76
    [Google Scholar]
  145. 145. 
    Robertson BC, Elliott GP, Eason DK, Clout MN, Gemmell NJ. 2006. Sex allocation theory aids species conservation. Biol. Lett. 2:229–31
    [Google Scholar]
  146. 146. 
    Trivers RL, Willard DE. 1973. Natural-selection of parental ability to vary sex-ratio of offspring. Science 179:90–92
    [Google Scholar]
  147. 147. 
    Bateson P, Gluckman P, Hanson M 2014. The biology of developmental plasticity and the Predictive Adaptive Response hypothesis. J. Physiol. 592:2357–68
    [Google Scholar]
  148. 148. 
    Watkins AJ, Rubini E, Hosier ED, Morgan HL. 2020. Paternal programming of offspring health. Early Hum. Dev. 150:105185
    [Google Scholar]
  149. 149. 
    Burggren WW, Crews D. 2014. Epigenetics in comparative biology: why we should pay attention. Integr. Comp. Biol. 54:7–20
    [Google Scholar]
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