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New insights in Cercopithecinae spermatozoa

Published online by Cambridge University Press:  18 March 2021

Guillaume Martinez Open the ORCID record for Guillaume Martinez [Opens in a new window] ,
Cécile Garcia ,
Céline Francois-Brazier ,
Sylvie Laidebeure ,
Antoine Leclerc ,
Alexis Lecu ,
Baptiste Mulot ,
Thierry Petit ,
Benoit Quintard  and
Sophie Brouillet
...Show all authors
Guillaume Martinez*
Affiliation:
Hôpital Couple-Enfant, Centre Hospitalier Universitaire de Grenoble, UM de Génétique Chromosomique, 38000Grenoble, France Genetic Epigenetic and Therapies of Infertility, Institute for Advanced Biosciences INSERM U1209, CNRS UMR5309, 38000Grenoble, France
Cécile Garcia
Affiliation:
UMR 7206 Eco-anthropologie, CNRS – MNHN – Université de Paris, Musée de l’Homme, 75016Paris, France
Céline Francois-Brazier
Affiliation:
Parc Zoologique et Botanique de Mulhouse, 68100Mulhouse, France
Sylvie Laidebeure
Affiliation:
Parc zoologique de Paris-Muséum national d’Histoire naturelle, 53 avenue de Saint Maurice, 75012Paris, France
Antoine Leclerc
Affiliation:
ZooParc de Beauval & Beauval Nature, 41110St Aignan, France
Alexis Lecu
Affiliation:
Parc zoologique de Paris-Muséum national d’Histoire naturelle, 53 avenue de Saint Maurice, 75012Paris, France
Baptiste Mulot
Affiliation:
ZooParc de Beauval & Beauval Nature, 41110St Aignan, France
Thierry Petit
Affiliation:
Zoo de la Palmyre, Avenue de Royan, 17570Les Mathes, France
Benoit Quintard
Affiliation:
Parc Zoologique et Botanique de Mulhouse, 68100Mulhouse, France
Sophie Brouillet
Affiliation:
Université de Montpellier, EmbryoPluripotency, DEFE, INSERM 1203, Hôpital Arnaud de Villeneuve, CHRU Saint-Eloi, 80 Avenue Augustin Fliche, 34295Montpellier Cedex 5, France
Christophe Arnoult
Affiliation:
Genetic Epigenetic and Therapies of Infertility, Institute for Advanced Biosciences INSERM U1209, CNRS UMR5309, 38000Grenoble, France Station de Primatologie, UPS 846, CNRS, 13790Rousset, France
Charles Coutton
Affiliation:
Hôpital Couple-Enfant, Centre Hospitalier Universitaire de Grenoble, UM de Génétique Chromosomique, 38000Grenoble, France Genetic Epigenetic and Therapies of Infertility, Institute for Advanced Biosciences INSERM U1209, CNRS UMR5309, 38000Grenoble, France
Romain Lacoste
Affiliation:
Station de Primatologie, UPS 846, CNRS, 13790Rousset, France
*
Author for correspondence: Guillaume Martinez. Hôpital Couple-Enfant, Centre Hospitalier Universitaire de Grenoble, UM de Génétique Chromosomique, 38000Grenoble, France. E-mail: [email protected]
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Summary

Sperm morphometric and morphologic data have been shown to represent useful tools for monitoring fertility, improving assisted reproduction techniques and conservation of genetic material as well as detecting inbreeding of endangered primates. We provide here for the first time sperm morphologic and morphometric data from Cercopithecus neglectus, Cercopithecus cephus, Papio papio and critically endangered Cercopithecus roloway, as well as comparative data from other Cercopithecinae species, i.e. Allochrocebus lhoesti, Mandrillus sphinx and Papio anubis. Following collection from the epididymis, spermatozoa were measured for each species for the following parameters: head length, head width, head perimeter, head area, midpiece length and total flagellum length, and the head volume, ellipticity, elongation, roughness and regularity were then calculated. Our data are consistent with both the general morphology and the morphometric proportions of Cercopithecinae sperm. Some specificities were observed, with C. cephus displaying a narrow head (width = 2.76 ± 0.26 µM) and C. roloway displaying a short midpiece (6.65 ± 0.61 µM). This data set represents an important contribution, especially for Cercopithecus roloway, one of the most endangered monkeys in the world, and further data on additional specimens coupled to data on mating systems and reproductive ecology should allow a better understanding of the mechanisms underlying these morphological differences across primate species.

Keywords

ARTNon-human primatesSperm morphologySperm morphometrySperm parameters
Type
Research Article
Information
Zygote , Volume 29 , Issue 5 , October 2021 , pp. 401 - 409
Copyright
© The Author(s), 2021. Published by Cambridge University Press

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References

Ackerman, DR and Roussel, JD (1968). Fructose, lactic acid and citric acid content of the semen of eleven subhuman primate species and of man. Reproduction 17, 563–6.CrossRefGoogle Scholar
Anderson, MJ, Nyholt, J and Dixson, AF (2005). Sperm competition and the evolution of sperm midpiece volume in mammals. J Zool 267, 135–42.CrossRefGoogle Scholar
Andrabi, SMH and Maxwell, WMC (2007). A review on reproductive biotechnologies for conservation of endangered mammalian species. Anim Reprod Sci 99(3–4), 223–43.CrossRefGoogle ScholarPubMed
Bedford, JM (1967). Observations on the fine structure of spermatozoa of the bush baby (Galago senegalensis), the African green monkey (Cercopithecus aethiops) and man. Am J Anat 121, 443–59.CrossRefGoogle ScholarPubMed
Bedford, JM and Hoskins, DD (1990). The mammalian spermatozoon: morphology, biochemistry and physiology. In Lamming, G.E. (ed.). Marshall’s Physiology of Reproduction, pp. 379–568. Edinburgh, London, Melbourne, New York: Churchill Livingstone.Google Scholar
Carrick, FN and Hughes, RL (1982). Aspects of the structure and development of monotreme spermatozoa and their relevance to the evolution of mammalian sperm morphology. Cell Tiss Res 222, 127–41.CrossRefGoogle ScholarPubMed
Chan, P, Cseh, S, Corselli, J and Bailey, L (1999). Sperm characteristics after sequential semen collection and pentoxifylline treatment in the baboon (Papio anubis). Theriogenology 51, 340.CrossRefGoogle Scholar
Cooper, TG, Noonan, E, Von Eckardstein, S, Auger, J, Baker, HW, Behre, HM, & Vogelsong, KM (2010). World Health Organization reference values for human semen characteristics. Hum Reprod Update 16, 231–45.CrossRefGoogle ScholarPubMed
Cranfield, MR, Kempske, SE and Schaffer, N (1988). The use of in vitro fertilisation and embryo transfer techniques for the enhancement of genetic diversity in the captive population of the lion-tailed macaque Macaca silenus . International Zoo Yearbook 27, 149–59.CrossRefGoogle Scholar
Cseh, S, Chan, PJ, Corselli, J and Bailey, LL (2000). Electroejaculated baboon (Papio anubis) sperm requires a higher dosage of pentoxifylline to enhance motility. J Assist Reprod Genet 17, 449–53.CrossRefGoogle ScholarPubMed
Cummins, JM and Woodall, PF (1985). On mammalian sperm dimensions. Reproduction 75, 153–75.CrossRefGoogle ScholarPubMed
de Villiers, C (2018). A comparison between the semen and sperm parameters from the captive-bred Vervet monkey (Chlorocebus aethiops) and Rhesus monkey (Macaca mulatta). J Med Primatol 47, 211–6.CrossRefGoogle Scholar
Estrada, A, Garber, PA, Rylands, AB, Roos, C, Fernandez-Duque, E, Di Fiore, A et al. (2017). Impending extinction crisis of the world’s primates: why primates matter. Sci Adv 3, e1600946.CrossRefGoogle ScholarPubMed
Flećhon, JE and Hafez, ES (1975). Spermiation and epididymal maturation of spermatozoa in the bonnet macaque (Macaca radiata) as viewed by scanning electron microscopy. Fertil Steril 26, 1219–27.Google ScholarPubMed
Flećhon, JE, Kraemer, DC and Hafez, ESE (1976). Scanning electron microscopy of baboon spermatozoa. Fol Primatol 26, 24–35.Google ScholarPubMed
Gadea, J, Toledano-Díaz, A, Navarro-Serna, S, Jiménez-Movilla, M, Soriano, P, Matás, C and Santiago-Moreno, J (2019). Assessment and preservation of liquid and frozen–thawed Black crested mangabey (Lophocebus aterrimus) spermatozoa obtained by transrectal ultrasonic-guided massage of the accessory sex glands and electroejaculation. Anim Reprod Sci 210, 106176.CrossRefGoogle ScholarPubMed
Gage, MJ (1998). Mammalian sperm morphometry. Proc R Soc Lond B Biol Sci 265(1391), 97–103.CrossRefGoogle ScholarPubMed
Gago, C, Perez-Sanchez, F, Yeung, CH, Tablado, L, Cooper, TG and Soler, C (1998). Standardization of sampling and staining methods for the morphometric evaluation of sperm heads in the cynomolgus monkey (Macaca fascicularis) using computer-assisted image analysis. Int J Androl 21, 169–76.CrossRefGoogle ScholarPubMed
Gago, C, Pérez-Sánchez, F, Yeung, CH, Tablado, L, Cooper, TG and Soler, C (1999). Morphological characterization of ejaculated cynomolgus monkey (Macaca fascicularis) sperm. Am J Primatol 47, 105–15.3.0.CO;2-L>CrossRefGoogle ScholarPubMed
García-Vázquez, FA, Gadea, J, Matás, C and Holt, WV (2016). Importance of sperm morphology during sperm transport and fertilization in mammals. Asian J Androl 18, 844.Google ScholarPubMed
Gomendio, M, Cassinello, J and Roldan, ERS (2000). A comparative study of ejaculate traits in three endangered ungulates with different levels of inbreeding: fluctuating asymmetry as an indicator of reproductive and genetic stress. Proc R Soc Lond B Biol Sci 267(1446), 875–82.CrossRefGoogle ScholarPubMed
Gould, KG (1980). Scanning electron microscopy of the primate sperm. Int Rev Cytol 63, 323–55.CrossRefGoogle ScholarPubMed
Gould, KG and Martin, DE (1978). Comparative morphology of primate spermatozoa using scanning electron microscopy. II. Families Cercopithecidae, Lorisidae, Lemuridae. J Hum Evol 7, 637–42.CrossRefGoogle Scholar
Gould, KG, Young, LG, Smithwick, EB and Phythyon, SR (1993). Semen characteristics of the adult male chimpanzee (Pan troglodytes). Am J Primatol 29, 221–32.CrossRefGoogle Scholar
Hedrick, PW and Kalinowski, ST (2000). Inbreeding depression in conservation biology. Annu Rev Ecol Syst 31, 139–62.CrossRefGoogle Scholar
Hernández-López, L, Parra, GC, Cerda-Molina, AL, Pérez-Bolaños, SC, Sánchez, VD and Mondragón-Ceballos, R (2002). Sperm quality differences between the rainy and dry seasons in captive black-handed spider monkeys (Ateles geoffroyi). Am J Primatol 57, 35–41.CrossRefGoogle Scholar
Kholkute, SD, Gopalkrishnan, K and Puri, CP (2000). Variations in seminal parameters over a 12-month period in captive bonnet monkeys. Primates 41, 393–405.CrossRefGoogle Scholar
Koné, I, Oates, JF, Dempsey, A, Gonedelé, BiS, McGraw, S and Wiafe, E (2019). Cercopithecus roloway. The IUCN Red List of Threatened Species: e.T4232A92384429.Google Scholar
Kyaligonza, JK (1998). Semen analysis and induction of acrosome reaction in spermatozoa of Tana mangabey (Cercocebus galeritus) and De Brazza’s Cercopilhecus monkeys (Doctoral dissertation, University of Nairobi).Google Scholar
Leão, DL, Sampaio, WV, Sousa, PC, Moura, AA, Oskam, IC, Santos, RR and Domingues, SF (2020). Micromorphological and ultrastructural description of spermatozoa from squirrel monkeys (Saimiri collinsi Osgood, 1916). Zygote, 28, 203–7.CrossRefGoogle Scholar
Maree, L (2011). Sperm Mitochondria: Species Specificity and Relationships to Sperm Morphometric Features and Sperm Function in Selected Mammalian Species. Thesis.Google Scholar
Martin, DE, Gould, KG and Warner, H (1975). Comparative morphology of primate spermatozoa using scanning electron microscopy. I. Families Hominidae, Pongidae, Cercopithecidae and Cebidae. J Hum Evol 4, 287–92.CrossRefGoogle Scholar
Martinez, G and Garcia, C (2020). Sexual selection and sperm diversity in primates. Mol Cell Endocrinol, 110974.CrossRefGoogle ScholarPubMed
Mastroianni, L Jr and Manson, WA Jr (1963). Collection of monkey semen by electroejaculation. Proc Soc Exp Biol Med 112, 1025–7.CrossRefGoogle ScholarPubMed
Mdhluli, MC, Seier, JV and van der Horst, G (2004). The male vervet monkey: sperm characteristics and use in reproductive research. Gynecol Obstet Invest 57, 17–8.Google ScholarPubMed
Nakazato, C, Yoshizawa, M, Isobe, K, Kusakabe, KT, Kuraishi, T, Hattori, S and Kai, C (2015). Morphological characterization of spermatozoa of the night monkey. J Mamm Ova Res 32, 37–40.CrossRefGoogle Scholar
Nyachieo, A, Spiessens, C, Chai, DC, Kiulia, NM, Mwenda, JM and D’Hooghe, TM (2012). Baboon spermatology: basic assessment and reproducibility in olive baboons (Papio anubis). J Med Primatol 41, 297–303.CrossRefGoogle Scholar
Oliveira, KG, Santos, RR, Leão, DL, Brito, AB, Lima, JS, Sampaio, WV and Domingues, SF (2016). Cooling and freezing of sperm from captive, free-living and endangered squirrel monkey species. Cryobiology, 72, 283–9.CrossRefGoogle ScholarPubMed
Piña-Aguilar, RE, López-Saucedo, J, Ruiz-Galaz, LI, de Jesús Barroso-Padilla, J, Gallegos-Rivas, MC, González-Ortega, C and Gutiérrez-Gutiérrez, AM (2016). A human reproductive approach to the study of infertility in chimpanzees: an experience at Leon’s Zoological Park, Mexico. Vet Res Forum 7, 255–9.Google Scholar
Pukazhenthi, B, Comizzoli, P, Travis, AJ and Wildt, DE (2005). Applications of emerging technologies to the study and conservation of threatened and endangered species. Reprod Fertil Dev 18, 77–90.CrossRefGoogle Scholar
Robson, SK, Rouse, GW and Pettigrew, JD (1997). Sperm ultrastructure of Tarsius bancanus (Tarsiidae, Primates): implications for primate phylogeny and the use of sperm in systematics. Act Zool 78, 269–78.CrossRefGoogle Scholar
Sampaio, WV, Oliveira, KG, Leão, DL, Caldas-Bussiere, M, Queiroz, HL, Paim, FP and Domingues, SF (2017). Morphologic analysis of sperm from two neotropical primate species: comparisons between the squirrel monkeys Saimiri collinsi and Saimiri vanzolinii Zygote 25, 141–8.CrossRefGoogle Scholar
San Diego Zoo Global Library Sperm Atlas (2020). San Diego Zoo Global. Last updated: 31 December 2019 https://ielc.libguides.com/c.php?g=692908&p=4909133 Google Scholar
Schaffer, N, Cranfield, M, Meehan, T and Kempske, S (1989). Semen collection and analysis in the conservation of endangered nonhuman primates. Zoo Biol 8(S1), 47–60.CrossRefGoogle Scholar
Seier, JV, Conradie, E, Oettle, EE and Fincham, JE (1993). Cryopreservation of vervet monkey semen and recovery of progressively motile spermatozoa. J Med Primatol 22, 355–9.CrossRefGoogle ScholarPubMed
Shang, EY, Ji, WZ, Yang, SC, Chen, JC and Zou, RJ (1993). Electron microscopical study of Tibetan macaque (Macaca thibetana) sperm. Zool Res 14, 1–4.Google Scholar
Steinberg, ER, Nieves, M, Ascunce, MS, Palermo, AM and Mudry, MD (2009). Morphological and genetic characterization of Saimiri boliviensis . Int J Primatol 30, 29–41.CrossRefGoogle Scholar
Thomson, JA, Iliff-Sizemore, SA, Gliessman, PM and Wolf, DP (1992). Collection and fertilization potential of sperm from the Sulawesi crested black macaque (Macaca nigra). Am J Primatol 28, 289–97.CrossRefGoogle Scholar
Thomsen, R (2014). Non-invasive collection and analysis of semen in wild macaques. Primates 55, 231–7.CrossRefGoogle ScholarPubMed
World Health Organization (2010). WHO Laboratory Manual for the Examination and Processing of Human Semen, 5th edn. Google Scholar
Wickings, EJ and Nieschlag, E (1980). Seasonality in endocrine and exocrine testicular function of the adult rhesus monkey (Macaca mulatta) maintained in a controlled laboratory environment. Int J Androl 3(1–6), 87–104.CrossRefGoogle Scholar
Zainuddin, Z, Kang, YC, Tarmizi, MRM, Ahmad, AH and Payne, JB (2019). Seminal evaluation and cryopreservation of sperms from the pig-tailed macaque, Macaca nemestrina . J Sust Sci Manag 14, 92–9.Google Scholar