Gamete cryopreservation in the recovery program of Mexican gray wolf (Canis lupus baylei): Results of reproductive season of 2018 in Mexico

Contenido principal del artículo

Raúl Eduardo Piña-Aguilar
Patricia Zúñiga-Sánchez
Rosa María Díaz-Salazar
Claudia González-Ortega
Beatriz Santamaria-Jiménez
Laura Elena Gómez-Montes
Herbe Monrroy-Jacobo
José de Jesús Barroso-Padilla
Alvar Alonso Cruz-Tamayo
Antonio Martin Gutiérrez-Gutiérrez

Resumen

Abstract

The Mexican grey wolf (Canis lupus baileyi) is a subspecies of grey wolf with unique morphologic, genetic and historical features. The Mexican grey wolf faced near-extinction during the 70s after decades of predator eradication actions. A binational, United States-Mexico, ex situ management program relying primarily on zoos has enabled a slow recovery for the population. The current population includes approximately two hundred fifty animals in captivity and more than a hundred that have been returned to the wild. One of the components of the recovery program is cryobanking gonadal tissue: initially sperm, and more recently, ovaries and oocytes. During the reproductive season of 2018 our Mexican team cryopreserved sperm obtained by electrojaculation from five males maintained in three facilities (Zoológico San Juan de Aragón, Parque Zoológico de León and Zoológico El Ocotal) and vitrified oocytes and cryopreserved ovaran tissue obtained by ovariohysterectomy in a female maintained at Zoológico de Zacango. Improved methods were introduced, such as the use of a commercial dog sperm extender that enabled superior post-thaw survival and motility rates, the measurement of testosterone and the use of ovary and oocyte cryopreservation techniques based on human procedures. We report the the successful cryopreservation of Mexican grey wolf gametes based only in local resources and expertise contributing, which will impact the population management program’s long-standing efforts to recover a flagship species of Mexican natural richness, the grey wolf.

 Keywords

Biobank, Oocyte vitrification, ovary cryopreservation, sperm freezing, testis, vitrification.

 

Resumen

El lobo mexicano (Canis lupus baileyi) es una subespecie del lobo gris con características morfológicas, genéticas e históricas únicas. El lobo gris mexicano estuvo cerca de la extinción durante los años 70 después de décadas de acciones para la erradicación de predadores. El programa binacional Estados Unidos-México de manejo ex situ, dependiente principalmente de los zoológicos, ha provisto de una recuperación lenta de la población actualmente con aproximadamente doscientos cincuenta animales en cautiverio y más de una centena de regreso a la vida libre. Uno de los componentes del programa de recuperación es la criopreservación de tejido gonadal, inicialmente espermatozoides y más recientemente ovario y ovocitos. Durante la temporada reproductiva 2018 nuestro equipo en México criopreservó espermatozoides obtenidos por electroeyaculación en tres instituciones (Zoológico San Juan de Aragón, Parque Zoológico de León y Zoológico El Ocotal) y vitrificó ovocitos y criopreservó tejido ovárico después de una ovariohisterectomía en una hembra mantenida en el Zoológico de Zacango. Métodos mejorados fueron introducidos, como el uso de un diluyente comercial para perros con mejores resultados en las tasas de viabilidad y motilidad postcongelación, y el uso de técnicas de criopreservación para ovarios y ovocitos basadas en procedimientos para humanos. Reportamos la criopreservación exitosa de gametos basados solamente en recursos y conocimiento local que impactaran en el programa de manejo de la población con acciones importantes en los esfuerzos de recuperación de una especie emblemática de la riqueza natural mexicana como el lobo gris mexicano.

Palabras clave

Biobanco, congelación de esperma, criopreservación de ovario, vitrificación de ovocitos, testículos, vitrificación.

Detalles del artículo

Compartir en:

Métricas de PLUMX

Citas

Ackermann, C.L., C.S. Asa, R. Krisher, K. Bauman, S. Casey and M.D. Lopes. 2017. Evaluation of follicular growth and tissue viability in vitrified/warmed domestic dog ovaries after in vitro culture. Reproduction in Domestic Animals, 52:77-81.

Asa, C., P. Miller, M. Agnew, J.A. Rebolledo, S.L. Lindsey, M. Callahan and K. Bauman. 2007. Relationship of inbreeding with sperm quality and reproductive success in Mexican gray wolves. Animal Conservation ,10:326-331.

Boutelle, S., K. Lenahan, R. Krisher, K.L. Bauman, C.S. Asa and S. Silber. 2011. Vitrification of oocytes from endangered Mexican gray wolves (Canis lupus baileyi). Theriogenology, 75:647-654.

CEPANAF. 2018a. Zoológico El Ocotal. Available at: http://cepanaf.edomex.gob.mx/zoologico_el_ocotal [Accessed on December 30, 2018].

CEPANAF. 2018b. Parque Ecológico de Zacango. Available at

http://cepanaf.edomex.gob.mx/parque_ecologico_zacango [Accessed on December 30, 2018].

Christensen, B.W., C.S. Asa, C. Wang, K. Bauman, M.K. Agnew, S.P. Lorton and M. Callahan. 2013. Kinematic activity of gray wolf (Canis lupus) sperm in different extenders, added before or after centrifugation. Theriogenology, 79:953-960.

Comizzoli P., E.E. Paulson, L.K and McGinnis LK. (2018). The mutual benefits of research in wild animal species and human-assisted reproduction. Journal of Assisted Reproduction and Genetics 35:551-560.

Fitak, R.R., S.E. Rinkevich and M. Culver. 2018. Genome-wide analysis of SNPs is consistent with no domestic dog ancestry in the endangered Mexican wolf (Canis lupus baileyi). Journal of Heredity, 109:372-383.

Fossum, T. 2013. Small Animal Surgery 4th Edition. Elsevier Mosby: Missouri

Heffelfinger, J. R., Nowak, R. M. and D. Paetkau. 2017. Clarifying historical range to aid recovery of the Mexican wolf. Journal and Wildlife Management, 81:766-777.

Howard, J.G., C. Lynch, R.M. Santymire, P.E. Marinari and D.E., Wildt. 2016. Black‐footed ferret gene restoration. Animal Conservation, 19:102-111.

Kim, M.K., G. Jang, H.J. Oh, F. Yuda, H.J., Kim, W.S. Hwang, M.S. Hossein, J.J. Kim, N.S. Shin, S.K. Kang, and B.C. Lee. 2007. Endangered wolves cloned from adult somatic cells. Cloning Stem Cells, 9:130-137.

Kuwayama, M. 2007. Highly efficient vitrification for cryopreservation of human oocytes and embryos: the Cryotop method. Theriogenology, 67:73-80.

Lara-Díaz, N.E., C.A. López-González, H. Coronel-Arellano and J.L. Cruz-Romo. 2015. Nacidos libres: en el camino a la recuperación del lobo mexicano. CONABIO. Biodiversitas, 119:1-6.

Lee, B.C., M.K. Kim, G. Jang, H.J. Oh, F. Yuda, H.J. Kim, M.S. Hossein, J.J. Kim, S.K. Kang, G. Schatten and W.S. Hwang. 2006. Dogs cloned from adult somatic cells. Nature, 436:641.

López-Saucedo, J.L., J.P. Ramon-Ugalde and R.E. Piña-Aguilar. 2010. ¿Es posible la recuperación de especies silvestres extintas a través de la transferencia somática nuclear? Revista Mexicana de Biodiversidad, 81:587-589.

López-Saucedo, J., J.P. Ramón-Ugalde, J. Jesús, A.M. Gutiérrez-Gutiérrez, R. Fierro and R.E. Piña-Aguilar. 2013. Superovulation, in vivo embryo recovery and cryopreservation for Aoudad (Ammotragus lervia) females using osmotic pumps and vitrification: A preliminary experience and its implications for conservation. Tropical Conservation Science, 6:149-157.

Nagashima, J.B., S.R. Sylvester, J.L. Nelson, S.H. Cheong, C. Mukai, C. Lambo, J.A. Flanders, V.N. Meyers-Wallen, N. Songsasen and A.J. Travis. 2015. Live births from domestic dog (Canis familiaris) embryos produced by in vitro fertilization. PLoS One, 10:e0143930.

Oh, H.J., M.K. Kim, G. Jang, H.J. Kim, S.G. Hong, J.E. Park, K. Park, C. Park, S.H. Sohn, D.Y. Kim, N.S. Shin and B.C. Lee. 2008. Cloning endangered gray wolves (Canis lupus) from somatic cells collected postmortem. Theriogenology, 70:638-647.

Oktay, K., H. Newton and R.G. Gosden. 2000. Transplantation of cryopreserved human ovarian tissue results in follicle growth initiation in SCID mice. Fertil Steril, 73:599-603.

Oktay, K, and O. Oktem. 2010. Ovarian cryopreservation and transplantation for fertility preservation for medical indications: report of an ongoing experience. Fertil Steril, 93:762-768.

Parque Zoológico de León. 2018. Parque Zoológico de León: Available at: http://www.zooleon.org.mx. [Accesed on December 30, 2018].

Piña-Aguilar, R.E., J. Lopez-Saucedo, R. Sheffield, L.I. Ruiz-Galaz, J. de J. Barroso-Padilla and A. Gutiérrez-Gutiérrez. 2009. Revival of extinct species using nuclear transfer: hope for the mammoth, true for the Pyrenean ibex, but is it time for "conservation cloning"? Cloning Stem Cells, 11:341-6.

Piña-Aguilar, R.E., J. López-Saucedo, L.I. Ruiz-Galaz, J.J. Barroso-Padilla, M.C. Gallegos-Rivas, C. González-Ortega and A.M. Gutiérrez-Gutiérrez. 2016. A human reproductive approach to the study of infertility in chimpanzees: An experience at Leon's Zoological Park, Mexico. Veterinary Research Forum, 7:255-259.

SEDEMA. 2018. Zoológico de Aragón. Available at: http://data.sedema.cdmx.gob.mx/zoo_aragon/ [Accessed on December 30, 2018].

Silber, S.J., N. Barbey, K. Lenahan and D.Z. Silber. 2013. Applying clinically proven human techniques for contraception and fertility to endangered species and zoo animals: a review. Journal of Zoo and Wildlife Medicine, 44:S111-122.

Siminski, D.P. 2017. Mexican Wolf, Canis lupus baileyi, International Studbook, 2017. The Living Desert, Palm Desert, California, USA.

Siminski, P. and E. Spevak. 2017. Mexican Wolf (Canis lupus baileyi) Population Analysis & Breeding and Transfer Plan. Association of Zoos and Aquariums. USA.

U.S. Fish and Wildlife Service. 2017. Mexican Wolf Biological Report: Version 2. Region 2, Albuquerque, New Mexico, USA.

Wisely, S.M., O.A. Ryder and R.M. Santymire, J.F. Engelhardt and B.J. Novak. 2015. A Road Map for 21st Century Genetic Restoration: Gene Pool Enrichment of the Black-Footed Ferret. Journal of Heredity, 106:581-592.

WHO (World Health Organization). 2010. WHO laboratory manual for the examination and processing of human semen. Fifth edition, Geneva, Switzerland

Zindl, C., C.S. Asa and A.R. Günzel-Apel. 2006. Influence of cooling rates and addition of Equex pasta on cooled and frozen-thawed semen of generic gray (Canis lupus) and Mexican gray wolves (C. l. baileyi). Theriogenology, 66:1797-1802.