Advancements in assisted reproductive technologies for the conservation of endangered mammalian species - A review

Sajad Ali Laghari; Qudratullah Kalwar; Hidayatullah Soomro; Baby Yasmeen; Sheikh Muhammad Usman; Kewal Das Bheel

doi:10.53992/njns.v11i1.310

Authors

Sajad Ali Laghari Department of Theriogenology, Faculty of Veterinary Sciences, Shaheed Benazir Bhutto University of Veterinary and Animal Sciences Sakrand, Pakistan
Qudratullah Kalwar Department of Theriogenology, Faculty of Veterinary Sciences, Shaheed Benazir Bhutto University of Veterinary and Animal Sciences Sakrand, Pakistan
Hidayatullah Soomro Department of Veterinary Medicine, Faculty of Veterinary Sciences, Shaheed Benazir Bhutto University of Veterinary and Animal Sciences Sakrand, Pakistan
Baby Yasmeen Department of Veterinary Pharmacology, Faculty of Animal Husbandry and Veterinary Sciences, Sindh Agriculture University Tandojam, Pakistan
Sheikh Muhammad Usman Department of Anatomy, Faculty of Veterinary Sciences, University of Agriculture Faisalabad, Pakistan
Kewal Das Bheel Department of Theriogenology, Faculty of Veterinary Sciences, Shaheed Benazir Bhutto University of Veterinary and Animal Sciences Sakrand, Pakistan

DOI:

https://doi.org/10.53992/njns.v11i1.310

Keywords:

Animals, Conservation, Mammals, Reproductive Technologies

Abstract

The protection of endangered mammal species has emerged as an urgent issue because of habitat destruction, climate change, and threats caused by human activities. Advanced assisted reproductive technologies (ARTs) offer innovative solutions to counter declining population trends. Methods like in vitro fertilization, embryo transfer, artificial insemination, and gamete cryopreservation have demonstrated their potential in overcoming reproductive challenges in these species. Additionally, emerging approaches like cloning and stem cell technology provide avenues for preserving genetic diversity and even reviving species that are facing extinction. These technologies enable the rescue of genetic material from deceased or infertile individuals, facilitate cross-institutional breeding programs, and minimize the risks of inbreeding in small populations. However, their application faces ethical, logistical, and species-specific challenges, requiring interdisciplinary collaboration among conservationists, veterinarians, and reproductive biologists. Despite these challenges, ARTs represent a promising tool in the global effort to safeguard biodiversity and restore balance to fragile ecosystems. This abstract underscores the importance of integrating scientific advancements with conservation strategies to secure the future of endangered mammalian species.

References

Comizzoli P, Crosier AE, Songsasen N, Gunther MS, Howard JG, Wildt DE. Advances in reproductive science for wild carnivore conservation. Reprod Domest Anim. 2009; 44(Suppl 2):47-52.

Holt WV, Pickard AR. Role of reproductive technologies and genetic resource banks in animal conservation. Rev Reprod. 1999; 4(3):143-150.

Andrabi SMH, Maxwell WMC. A review on reproductive biotechnologies for conservation of endangered mammalian species. Anim Reprod Sci. 2007; 99(3-4):223-243.

Loskutoff NM, Bartels P, Meintjes M, Godke RA, Schiewe MC. Assisted reproductive technology in nondo-mestic ungulates: a model approach to preserving and managing genetic diversity. Theriogenology. 1995; 43(1):3-12.

International Union for Conservation of Nature (IUCN). The IUCN Red List of Threatened Species. Version 2014.2 [Internet]. Gland: IUCN; 2014 [cited 2025 Jan 19]. Available from: http://www.iucnredlist.org

Wildt DE, Comizzoli P, Pukazhenthi B, Songsasen N. Lessons from biodiversity the value of nontraditional species to advance reproductive science, conservation, and human health. Mol Reprod Dev. 2010; 77(5): 397-409.

Lasley BL, Loskutoff NM, Anderson GB. The limitation of conventional breeding programs and the need and promise of assisted reproduction in nondomestic species. Theriogenology. 1994; 41(1):119-132.

Holt WV, Lloyd RE. Artificial insemination for the propagation of CANDES: the reality! Theriogenology. 2009; 71(1):228-235.

Mastromonaco GF, Songsasen N. Reproductive technologies for the conservation of wildlife and endangered species. In: Reproductive Technologies in Animals. London: Academic Press; 2020. p. 99-117.

Comizzoli P, Mermillod P, Mauget R. Reproductive biotechnologies for endangered mammalian species. Reprod Nutr Dev. 2000; 40(5):493-504.

Comizzoli P, Songsasen N, Hagedorn M, Wildt DE. Comparative cryobiological traits and requirements for gametes and gonadal tissues collected from wildlife species. Theriogenology. 2012; 78(8):1666-1681.

Hildebrandt TB, Holtze S. Advanced assisted reproduction technologies in endangered mammalian species. Reprod Domest Anim. 2024; 59(Suppl 2):e14700.

Hildebrandt TB, Holtze S, Colleoni S, Hermes R, Stejskal J, Lekolool I, Ndeereh D, Ngulu S, Iwajomo S, Mutisya S, Omondi P, Galatowitsch M, Diecke S, Göritz F, Galli C. In vitro fertilization program in white rhinoceros. Reproduction. 2023; 166(6): 383-399.

Hildebrandt TB, Hermes R, Colleoni S, Diecke S, Holtze S, Renfree MB, Stejskal J, Galli C, Göritz F. Embryos and embryonic stem cells from the white rhinoceros. Nat Commun. 2018; 9(1):2589.

Howard JG, Lynch C, Santymire RM, Marinari PE, Wildt DE. Recovery of gene diversity using long-term cryopreserved spermatozoa and artificial insemination in the endangered black-footed ferret. Anim Conserv. 2016; 19(2):102-111.

Comizzoli P. Birth of a giant panda cub after artificial insemination with frozen-thawed semen. Biopreserv Biobank. 2020;1 8(5):349-350.

Santymire R. Implementing the use of a biobank in the endangered black-footed ferret (Mustela nigripes). Reprod Fertil

Dev. 2016; 28(8):1097-1104.

Hildebrandt TB, Hermes R, Göritz F, Appeltant R, Colleoni S, de Mori B, Diecke S, Drukker M, Galli C, Hayashi K, Lazzari G, Loi P, Payne J, Stejskal J, Walzer C, Williams SA, Zalewski A, Holtze S. The ART of bringing extinction to a freeze-history and future of species conservation, exemplified by rhinos. Theriogenology. 2021; 169:76-88.

Zywitza V, Frahm S, Krüger N, Weise A, Göritz F, Hermes R, Holtze S, Hildebrandt TB, Diecke S. Induced pluripotent stem cells and cerebral organoids from the critically endangered Sumatran rhinoceros. iScience. 2022; 25(11):105414.

Hayashi M, Zywitza V, Naitou Y, Hamazaki N, Göritz F, Hermes R, Holtze S, Lazzari G, Galli C, Stejskal J, Diecke S, Hildebrandt TB, Hayashi K. Robust induction of primordial germ cells of white rhinoceros on the brink of extinction. Sci Adv. 2022; 8(49): eabp9683.

Zywitza V, Rusha E, Shaposhnikov D, Ruiz-Orera J, Telugu N, Rishko V, Göritz F, Hermes R, Holtze S, Lazzari G, Galli C, Stejskal J, Petrakis S, Sebbe J, Hubner N, Hildebrandt TB, Drukker M, Diecke S. Naïve-like pluripotency to pave the way for saving the northern white rhinoceros from extinction. Sci Rep. 2022; 12(1):3100.

Hermes R, Saragusty J, Göritz F, Bartels P, Potier R, Baker B, Streich WJ, Hildebrandt TB. Freezing African elephant semen as a new population management tool. PLoS One. 2013; 8(3):e57616.

Saragusty J, Hermes R, Göritz F, Hildebrandt TB. Mammalian reproduction out of cryopreserved cells and tissues. Int Zoo Yearb. 2011; 45(1): 133-153.

Saragusty J, Hildebrandt TB, Behr B, Knieriem A, Kruse J, Hermes R. Successful cryopreservation of Asian elephant spermatozoa. Anim Reprod

Sci. 2009; 115(1-4):255-266.

Saragusty J, Hildebrandt TB, Bouts T, Göritz F, Hermes R. Collection and preservation of pygmy hippopotamus semen. Theriogenology. 2010; 74(4): 652-657.

Schiewe MC, Anderson RE. Vitrification: the pioneering past to current trends and perspectives. J Biorepository Sci Appl Med. 2017; 5:57-68.

Rienzi L, Cobo A, Paffoni A, Scarduelli C, Capalbo A, Vajta G, Ubaldi FM. Consistent delivery rates after oocyte vitrification. Hum Reprod. 2012; 27(6):1606-1612.

Rienzi L, Gracia C, Maggiulli R, LaBarbera AR, Kaser DJ, Ubaldi FM, Vanderpoel S, Racowsky C. Cryopreservation in ART: systematic review and meta-analysis. Hum Reprod Update. 2017; 23(2):139-155.

Zahmel J, Jänsch S, Jewgenow K, Sandgreen DM, Simonsen KS, Colombo M. Maturation and fertilization of African lion oocytes after vitrification. Cryobiology. 2021; 98:146-151.

Simone R, Čižmár D, Holtze S, Mulot B, Lamglait B, Knauf-Witzens T, Göritz F, Hildebrandt TB. Cryopreservation of okapi oocytes following in vitro maturation. Theriogenology Wild. 2024; 4:100088.

Simone R, Čižmár D, Holtze S, Michel G, Sporbert A, Okolo C, Schoneberg J, Göritz F, Hildebrandt TB. In vitro production of naked mole-rat blastocysts. Sci Rep. 2023; 13(1): 22355.

Nava-Trujillo H, Rivera RM. Large offspring syndrome in ruminants. Animal. 2023; 17(Suppl 1):100740.

Bolton RL, Mooney A, Pettit MT, Bolton AE, Morgan L, Drake GJ, Appeltant R, Walker SL, Gillis JD, Hvilsom C. Resurrecting biodiversity. Reprod Fertil. 2022; 3(3):R121-R146.

Sandler RL, Moses L, Wisely SM. Ethical analysis of cloning for genetic rescue. Biol Conserv. 2021; 257:109118.

Novak BJ, Ryder OA, Houck ML, Walker K, Russell L, Russell B, Walker S, Arenivas SS, Aston L, Veneklasen G, Ivy JA, Koepfli KP, Rusnak A, Simek J, Zhuk A, Putnam AS, Phelan R. Endangered Przewalski’s horse (Equus przewalskii) cloned from historically cryopreserved cells. Animals (Basel). 2025; 15(5):613.

Teem JL, Alphey L, Descamps S, Edgington MP, Edwards O, Gemmell N, Harvey-Samuel T, Melnick DJ, Oh KP, Piaggio AJ, Saah JR, Schill D, Thomas P, Wong A, Roberts AJ. Genetic biocontrol for invasive species. Front Bioeng Biotechnol. 2020; 8:452.

Chen Y, He ZX, Liu A, Wang K, Mao WW, Chu JX, Zhu JH, Xu LX, Sun SY. Embryonic stem cells generated by nuclear transfer. Cell Res. 2003; 13(4):251-263.

Adams L, Liu Y, Polejaeva IA. Interspecies somatic cell nuclear transfer. Mammal Rev. 2024; 54(4): 387-403.

Vendramini OM, Bruyas JF, Fieni F, Battut I, Tainturier D. Embryo transfer in Poitou donkeys. Theriogenology. 1997; 47(1):409.

Schiewe MC, Bush M, Phillips LG, Citino S, Wildt DE. Estrus synchronization and embryo cryopreservation in antelopes. J Exp Zool. 1991; 258(1):75-88.

Swanson WF. Laparoscopic embryo transfer and AI in felids. Reprod Domest Anim. 2012; 47(Suppl 6):136-140.

Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell. 2006; 126(4):663-676.

Ben-Nun IF, Montague SC, Houck ML, Tran HT, Garitaonandia I, Leonardo TR, Wang YC, Charter LC, Laurent LC, Harkness NM, Wong CC, Andreadis ST, Nosrati M, Choi J, Faulknier B, Gutzmann S, Ryder OA, Loring JF. iPS cells from endangered species. Nat Methods. 2011; 8(10):829- 831.

Hayashi K, Galli C, Diecke S, Hildebrandt TB. Artificially produced gametes: a new tool for wildlife conservation? Reprod Fertil Dev. 2021; 33(2):91-101.

Hayashi K, Ohta H, Kurimoto K, Aramaki S, Saitou M. Reconstitution of the mouse germ cell specification pathway in culture by pluripotent stem cells. Cell. 2011; 146(4):519-532.

Hikabe O, Hamazaki N, Nagamatsu G, Obata Y, Hirao Y, Hamada N, Shimamoto S, Imamura T, Nakashima K, Saitou M, Hayashi K. Reconstitution in vitro of the entire female germ cell cycle in mice. Nature. 2016; 539(7628): 299-303.

Ishikura Y, Ohta H, Sato T, Murase Y, Yabuta Y, Kojima Y, Yamashiro C, Nakamura T, Yamamoto T, Ogawa T, Saitou M. In vitro reconstitution of the whole male germ-cell development from mouse pluripotent stem cells. Cell Stem Cell. 2021; 28(12):2167-2179.

Sakai YS, Nakamura T, Okamoto I, Gyobu-Motani S, Ohta H, Yabuta Y, Tsukiyama T, Iwatani C, Tsuchiya H, Ema M, Saitou M. Induction of the germ cell fate from pluripotent stem cells in cynomolgus monkeys. Biol Reprod. 2020; 102(3):620-638.

Seita Y, Cheng K, McCarrey JR, Yadu N, Cheeseman IH, Bagwell A, Sreerattana K, Little CA, Gagneux P, Orwig KE. Efficient induction of primordial germ cell-like cells from common marmoset embryonic stem

cells. eLife. 2023; 12: e82263.

Yoshino T, Suzuki T, Nagamatsu G, Yabukami H, Ikegaya M, Kishima M, Kita H, Imamura T, Nakashima K, Nishinakamura R, Beppu H, Shiojima I, Hayashi K. Generation of ovarian follicles from mouse induced pluripotent stem cells. Science. 2021; 373(6552): eabe0237.

Doudna JA, Charpentier E. Genome engineering. The new frontier of genome engineering with CRISPR-Cas9. Science. 2014; 346(6213): 1258096.

Hayashi M, Zywitza V, Naitou Y, Hamazaki N, Göritz F, Hermes R, Holtze S, Lazzari G, Galli C, Stejskal J, Diecke S, Hildebrandt TB, Hayashi K. Robust induction of primordial germ cells of white rhinoceros on the brink of extinction. Sci Adv. 2022; 8(49): eabp9683.

Frankham R, Ballou JD, Briscoe DA. Introduction to Conservation Genetics. 2nd ed. Cambridge: Cambridge University Press; 2010.

Swanson WF. Assisted reproduction for wild felids: successes and challenges. Theriogenology. 2022; 197:133-138.

Huijsmans TERG, Hassan HA, Smits K, Van Soom A. Postmortem gamete collection in endangered mammals: a review. Animals (Basel). 2023; 13(8):1360.

Wildt DE, Wemmer C, Chakraborty PK, Bush M. Comparative reproductive biology and artificial insemination in the rhinoceros and other nondomestic species. Proc Natl Acad Sci U S A. 1993; 90(24):11431-11434.