Semen Evaluation from Dominant Males of the Viviparous Mexican Lizard Sceloporus torquatus, Wiegmann, 1828 (Sauria: Phrynosomatidae)
Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. Organisms
2.2. Male Selection
2.3. Semen Collection
2.4. Semen Assessment
3. Results
4. Discussion
4.1. Dominant Male Characteristics
4.2. Semen Characteristics
4.3. Sperm Characteristics
4.4. Perspectives
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Anderson, M. Sexual Selection; Princeton University Press: Princeton, NJ, USA, 1994. [Google Scholar]
- Eberhard, W.G. Postcopulatory sexual selection: Darwin’s omission and its consequences. Proc. Natl. Acad. Sci. USA 2009, 106, 10025–10032. [Google Scholar] [CrossRef] [PubMed]
- Gomendio, M.; Malo, A.F.; Garde, J.; Roldan, E.R.S. Sperm traits and male fertility in natural populations. Reproduction 2007, 134, 19–29. [Google Scholar] [CrossRef] [PubMed]
- Tokarz, R.R. Mate choice in lizards: A review. Herpetol. Monogr. 1995, 9, 17–40. [Google Scholar] [CrossRef]
- Sinervo, B.; Méndez de la Cruz, F.; Miles, D.B.; Heulin, B.; Bastians, E.; Villagrán-Santa Cruz, M.; Lara-Resendiz, R.; Martínez-Méndez, N.; Calderón-Espinosa, M.L.; Meza-Lázaro, R.N.; et al. Erosion of lizard diversity by climate change and altered thermal niches. Science 2010, 328, 894–899. [Google Scholar] [CrossRef]
- Stapley, J.; Garcia, M.; Andrews, R.M. Long-term data reveal a population decline of the tropical lizard Anolis apletophallus, and a negative affect of El Niño years on population growth rate. PLoS ONE 2015, 10, e0115450. [Google Scholar] [CrossRef]
- Oliver, P.M.; Blom, M.P.K.; Cogger, H.G.; Fisher, R.N.; Richmond, J.Q.; Woinarski, J.C.Z. Insular biogeographic origins and high phylogenetic distinctiveness for a recently depleted lizard fauna from Christmas Island. Australia. Biol. Lett. 2018, 14, 20170696. [Google Scholar] [CrossRef] [PubMed]
- Diele-Viegas, L.M.; Werneck, F.P.; Rocha, C.F.D. Climate change effects on population dynamics of three species of Amazonian lizards. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2019, 236, 110530. [Google Scholar] [CrossRef]
- Young, C.; Ravida, N.; Curtis, M.; Mazzotti, F.; Durrant, B. Development of a sperm cryopreservation protocol for the Argentine black and white tegu (Tupinambis merianae). Theriogenology 2017, 87, 55–63. [Google Scholar] [CrossRef]
- Clulow, J.; Clulow, S. Cryopreservation and other assisted reproductive technologies for the conservation of threatened amphibians and reptiles: Bringing the ARTs up to speed. Reprod. Fertil. Devlop. 2016, 28, 1116–1132. [Google Scholar] [CrossRef] [PubMed]
- Martínez-Torres, M.; Sánchez-Rivera, U.Á.; Cruz-Cano, N.B.; Castro-Camacho, Y.J.; Luis, J.; Medrano, A. A non-invasive method for semen collection and evaluation in small and medium size lizards. Reprod. Dom. Anim. 2019, 54, 54–58. [Google Scholar] [CrossRef]
- Perry, S.M.; Mitchell, M.A. Reptile assisted reproductive technologies: Can ART help conserve 300 million years of evolution by preserving extant reptile biodiversity? Reprod. Fertil. Develop. 2022, 34, 385–400. [Google Scholar] [CrossRef] [PubMed]
- Martínez-Torres, M.; Álvarez-Rodríguez, C.; Luis, J.; Sánchez-Rivera, U.Á. Electroejaculation and semen evaluation of the viviparous lizard Sceloporus torquatus (Squamata: Phrynosomatidae). Zoo Biol. 2019, 38, 393–396. [Google Scholar] [CrossRef] [PubMed]
- IUCN. Available online: https://www.iucnredlist.org/species/64155/12749796 (accessed on 7 September 2020).
- Feria-Ortiz, M.; Nieto-Montes de Oca, A.; Salgado-Ugarte, I.H. Diet and Reproductive Biology of the Viviparous Lizard Sceloporus torquatus torquatus (Squamata: Phrynosomatidae). J. Herpetol. 2001, 35, 104–112. [Google Scholar] [CrossRef]
- Sánchez-Rivera, U.A. Análisis hormonal y citológico de la espermatogénesis mediante biopsia testicular en Sceloporus torquatus (Sauria: Phrynosomatidae). BSc Dissertation, Universidad Nacional Autónoma de México, Mexico City, Mexico, 2017; p. 71. [Google Scholar]
- Martínez-Torres, M. Almacenamiento de espermatozoides en la vagina de la lagartija vivípara Sceloporus torquatus (Sauria: Prhynosomatidae). Acta Zoológica Mex. 2009, 25, 497–506. [Google Scholar] [CrossRef]
- Sánchez-Rivera, U.A.; Medrano, A.; Cruz-Cano, N.B.; Alcántar-Rodriguez ARCastro-Camacho, Y.J.; Martínez-Torres, M. Sperm cryopreservation of spiny collared lizard (Sceloporus torquatus). Reprod. Dom. Anim. 2019, 54 (Suppl. S4), 130–131. [Google Scholar]
- Sánchez-Rivera, U.A.; Medrano, A.; Cruz-Cano, N.B.; Alcantar-Rodríguez, A.; Dávila-Govantes, R.; Castro-Camacho, Y.J.; Martínez-Torres, M. Implementation of a method for sperm cryopreservation in sceloporine lizards. Conserv. Physiol. 2022, 10, coac068. [Google Scholar] [CrossRef]
- Smith, H.M. The Lizards of the Torquatus Group of the Genus Sceloporus Wiegmann, 1828. Kans. Univ. Sci. Bull. 1936, 24, 539–693. Available online: https://www.biodiversitylibrary.org/item/25856 (accessed on 11 February 2025).
- Castro-Franco, R.; Bustos-Sagal, G. List of reptiles of Morelos, México; and their distribution in relation to vegetation types. Southwest. Nat. 1994, 39, 171–213. [Google Scholar] [CrossRef]
- Carpenter, C.C. Patterns of social behavior of Merriam’s canyon lizard (Sceloporus m. merriami Iguanidae). Southwest. Nat. 1961, 6, 138–148. [Google Scholar] [CrossRef]
- Neal, J.K.; Wade, J. Courtship and copulation in the adult male green anole: Effects of season, hormone and female contact on reproductive behavior and morphology. Behav. Brain Res. 2007, 177, 177–185. [Google Scholar] [CrossRef]
- Guillette, L.J., Jr. A physiological (Ringer’s) solution for anoline lizard. Herpet. Rev. 1982, 13, 37–38. [Google Scholar]
- González-Urdiales, R.; Tejerina, F.; Domínguez, J.C.; Alegre, B.; Ferreras, A.; Peláez, J. Técnicas de Análisis Rutinario de la Calidad Espermática: Motilidad, Vitalidad Concentración, Resistencia Osmótica Y Morfología Espermática. In Manual de Técnicas de Reproducción Asistida en Porcino; Bonet, S., Martínez, E., Rodríguez, J.E., Barrera, X., Eds.; Universidad de Gerona y Red Temática Nacional de Reproducción Porcina: Girona, Spain, 2006; pp. 19–38. [Google Scholar]
- Organización Mundial de la Salud. Manual de Laboratorio de La OMS Para el Examen del Semen Humano y de La Interacción Entre el Semen y el Moco Cervical, 4th ed.; Médica Panamericana: Madrid, Spain, 2001; Available online: https://iris.who.int/handle/10665/343208 (accessed on 20 February 2020).
- Freshman, J.L. Semen Collection and Evaluation. Clin. Tech. Small Anim. Pract. 2002, 17, 104–107. [Google Scholar] [CrossRef] [PubMed]
- Barth, A.D.; Oko, R.J. Abnormal morphology of bovine spermatozoa; Iowa State University Press: Ames, IA, USA, 1989; p. 285. [Google Scholar]
- Garner, D.L. Johnson LA. Viability assessment of mammalian sperm using SYBR-14 and propidium iodide. Biol. Reprod. 1995, 53, 276–284. [Google Scholar] [CrossRef] [PubMed]
- Harrison, R.A.; Ashworth, P.J.; Miller, N.G. Bicarbonate/CO2, an effector of capacitation, induces a rapid and reversible change in the lipid architecture of boar sperm plasma membranes. Mol. Reprod. Develop. 1996, 45, 378–391. [Google Scholar] [CrossRef]
- Rathi, R.; Colenbrander, B.; Bevers, M.M.; Gadella, B.M. Evaluation of in vitro capacitation of stallion spermatozoa. Biol. Reprod. 2001, 65, 462–470. [Google Scholar] [CrossRef]
- Green, C.E.; Watson, P.F. Comparison of the capacitation-like state of cooled boar spermatozoa with true capacitation. Reproduction 2001, 122, 889–898. [Google Scholar] [CrossRef]
- Medrano, A.; Holt, W.V.; Watson, P.F. Controlled freezing studies on boar sperm cryopreservation. Andrologia 2009, 41, 246–250. [Google Scholar] [CrossRef]
- Ruby, D. The function of the shudder displays in the lizard Sceloporus jarrovi. Copeia 1977, 1977, 110–114. [Google Scholar] [CrossRef]
- Trivers, R.L. Sexual selection and resource-accruing abilities in Anolis garmani. Evolution 1976, 30, 253–269. [Google Scholar] [CrossRef]
- Andrews, R.M. Mate choice by females of the lizard, Anolis carolinensis. J. Herpetol. 1985, 19, 284–289. [Google Scholar] [CrossRef]
- Tokarz, R.R. Body size as a factor determining dominance in staged agonistic encounters between male brown anoles (Anolis sagrei). Anim. Behav. 1985, 33, 746–753. [Google Scholar] [CrossRef]
- Sacchi, R.; Pupin, F.; Gentilli, A.; Rubolini, D.; Scali, S.; Fasola, M.; Galeotti, P. Male-male combats in a polymorphic lizard: Residency and size, but not color, affect fighting rules and contest outcome. Aggress. Behav. 2009, 35, 274–283. [Google Scholar] [CrossRef]
- Johnson, M.A.; Kamath, A.; Kirby, R.; Fresquez, C.C.; Wang, S.; Stehle, C.M.; Templeton, A.R.; Losos, J. What determines paternity in wild lizards? A spatiotemporal analysis of behavior and morphology. Integr. Comp. Biol. 2021, 61, 634–642. [Google Scholar] [CrossRef]
- Zimmerman, D.M.; Mitchell, M.A.; Perry, B.H. Collection and characterization of semen from green iguanas (Iguana iguana). Am. J. Vet. Res. 2013, 74, 1536–1541. [Google Scholar] [CrossRef]
- López-Juri, G.; Chiaraviglio, M.; Cardozo, G. Electrostimulation is an effective and safe method for semen collection in medium sized lizards. Theriogenology 2018, 118, 40–45. [Google Scholar] [CrossRef]
- Kahrl, A.F.; Cox, R.M. Diet affects ejaculate traits in a lizard with condition-dependent fertilization success. Behav. Ecol. 2015, 26, 1502–1511. [Google Scholar] [CrossRef]
- Hall, J.M.; Warner, D.A. Body size and reproduction of a non-native lizard are enhanced in an urban environment. Biol. J. Linn. Society 2017, 122, 860–871. [Google Scholar] [CrossRef]
- Hall, J.M.; Warner, D.A. Thermal spikes from the urban heat island increase mortality and alter physiology of lizard embryos. J. Exp. Biol. 2018, 221, jeb181552. [Google Scholar] [CrossRef]
- Jorge-Neto, P.N.; de Moraes Francisco, F.; Carneiro, M.D.D.; Santos, S.R.B.; Requena, L.A.; Ramos, S.D.; de Goés, M.F.; Valle, R.F.; Padilha, F.L.A.; Colbachini, H.; et al. Specific setup and methodology for computer assisted sperm analysis (CASA) in evaluating elasmobranch sperm. Theriogenol. Meth. 2024, 4, 100091. [Google Scholar] [CrossRef]
- Baqir, S.; Orabah, A.B.; AL-Zeheimi, N.; AL-Shakaili, Y.; AL-Rasbi, K.; Gartley, C.J.; Mastromonaco, G. Computer assisted sperm analysis (CASA) in the critically endangered captive Arabian leopard (Panthera pardus nimr): A multivariate clustering analysis. J. Vet. Sci. Technol. 2018, 9, 526. [Google Scholar] [CrossRef]
- Berger, T. Anderson DL. Penedo MCT. Porcine sperm fertilizing potential in relationship to sperm functional capacities. Anim. Reprod. Sci. 1996, 44, 231–239. [Google Scholar] [CrossRef]
- Brito, L.F.C.; Barth, A.D. Bilodeau-Goeseels S, Panich PL, Kastelic J P. Comparison of methods to evaluate the plasmalemma of bovine sperm and their relationship with in vitro fertilization rate. Theriogenology 2003, 60, 1539–1551. [Google Scholar] [CrossRef] [PubMed]
- Rigssellaere, T.; Van Soom, A.; Tanghe, S.; Coryn, M.; Maes, D.; de Kruif, A. 2005. New techniques for the assessment of canine semen quality: A review. Theriogenology 2005, 64, 706–719. [Google Scholar] [CrossRef]
- Salinas, P.; Pezo, F.; Sánchez, R.; Risopatrón, J. Validation of SYBR-14 and 6-CFDA to evaluate the viability and plasma membrane integrity in sperm of chihuahua canine breed. Int. J. Morph. 2014, 32, 16–21. [Google Scholar] [CrossRef]
- Tartaglionea, C.M.; Rittaa, M.N. Prognostic value of spermatological parameters as predictors of in vitro fertility of frozen-thawed bull semen. Theriogenology 2004, 62, 1245–1252. [Google Scholar] [CrossRef]
- Ladha, S. Lipid heterogeneity and membrane fluidity in a highly polarized cell, the mammalian spermatozoon. J. Membr. Biol. 1998, 165, 1–10. [Google Scholar] [CrossRef]
- Companyó, M.; Iborra, A.; Villaverde, J.; Martínez, P.; Morros, A. Membrane fluidity changes in goat sperm induced by cholesterol depletion using beta-cyclodextrin. Bioch. Biophys. Acta Biomembr. 2007, 1768, 2246–2255. [Google Scholar] [CrossRef] [PubMed]
- Buffone, M.G.; Doncel, G.F.; Calamera, J.C.; Verstraeten, S.V. Capacitation-associated changes in membrane fluidity in asthenozoospermic human spermatozoa. Int. J. Androl. 2009, 32, 360–375. [Google Scholar] [CrossRef]
- Macías-García BGonzález-Fernández, L.; Ortega-Ferrusola, C.; Salazar-Sandoval, C.; Morillo-Rodríguez, A.; Rodríguez-Martinez, H.; Tapia, J.A.; Morcuende, D.; Peña, F.J. Membrane lipids of the stallion spermatozoon in relation to sperm quality and susceptibility to lipid peroxidation. Reprod. Domes. Anim. 2011, 46, 141–148. [Google Scholar] [CrossRef]
- Guthrie, H.D.; Welch, G.R. Effects of reactive oxygen species on sperm function. Theriogenology 2012, 78, 1700–1708. [Google Scholar] [CrossRef]
- Holt, W.V.; Fazeli, A. Sperm storage in the female reproductive tract. Annu. Rev. Anim. Biosci. 2016, 4, 291–310. [Google Scholar] [CrossRef] [PubMed]
- Roberts, K.D. Sterol sulfates in the epididymis; synthesis and possible function in the reproduction process. J. Steroids Biochem. 1987, 27, 337–341. [Google Scholar] [CrossRef] [PubMed]
- Suarez, S.S. Regulation of sperm storage and movement in the mammalian oviduct. Int. J. Dev. Biol. 2008, 52, 455–462. [Google Scholar] [CrossRef]
- Ghersevich, S.; Massa, E.; Zumoffen, C. Oviductal secretion and gamete interaction. Reproduction 2015, 149, R1–R14. [Google Scholar] [CrossRef] [PubMed]
- Mirihagalle, S.; Hughes, J.R.; Miller, D.J. Progesterone-induced sperm release from the oviduct sperm reservoir. Cells 2022, 11, 1622. [Google Scholar] [CrossRef]
- DasGupta, S.; Mills, C.L.; Fraser, L.R. Ca2-related changes in the capacitation state of human spermatozoa assessed by a chlortetracycline fluorescence assay. J. Reprod. Fertil. 1993, 88, 135–143. [Google Scholar] [CrossRef]
- Fraser, L.R.; Herod, J.E. Expression of capacitation-dependent changes in chlortetracycline fluorescence patterns in mouse spermatozoa requires a suitable glycosable substrate. J. Reprod. Fertil. 1990, 88, 611–621. [Google Scholar] [CrossRef]
- Vaidya, R.A.; Bedford, J.M.; Glass, R.H.; Morris, M.c.L. Evaluation of the removal of tetracycline fluorescence from spermatozoa as a test for capacitation in the rabbit. J. Reprod. Fertil. 1969, 19, 483–489. [Google Scholar] [CrossRef]
- Witte, T.S.; Schäfer-Somi, S. Involvement of cholesterol, calcium and progesterone in the induction of capacitation and acrosome reaction of mammalian spermatozoa. Anim. Reprod. Sci. 2007, 102, 181–193. [Google Scholar] [CrossRef]
- Esponda, P.; Bedford, J.M. Post-testicular change in the reptile sperm surface with particular reference to the snake, Natrix fasciata. J. Exp. Zool. 1987, 241, 123–132. [Google Scholar] [CrossRef]
- Sánchez-Rivera, U.A.; Cruz-Cano, N.B.; Medrano, A.; Álvarez-Rodríguez, C.; Martínez-Torres, M. Sperm incubation in Biggers–Whitten–Whittingham medium induces capacitation-related changes in the lizard Sceloporus torquatus. Animals 2024, 14, 1388. [Google Scholar] [CrossRef] [PubMed]
- Nixon, B.; Anderson, A.L.; Smith, N.D.; McLeod, R.; Johnston, S.D. The Australian saltwater crocodile (Crocodylus porosus) provides evidence that the capacitation of spermatozoa may extend beyond the mammalian lineage. Proc. R. Soc. B. 2016, 283, 20160495. [Google Scholar] [CrossRef] [PubMed]
- Nixon, B.; Johnston, S.D.; Skerrett-Byrne, D.A.; Anderson, A.L.; Stanger, S.J.; Bromfield, E.G.; Martin, J.H.; Hansbro, P.H.; Dun, M.D. Modification of crocodile spermatozoa refutes the tenet that post-testicular sperm maturation is restricted to mammals. Mol. Cell. Proteom. 2019, 18, S59–S76. [Google Scholar] [CrossRef] [PubMed]
Characteristics | Mean ± SD | Interval | |
---|---|---|---|
Ejaculates (n) | 3.2 ± 0.8 | 2–4 | |
Volume 1 (µL) | 14.0 ± 5.4 | 7.0–27.0 | |
Wave motility (1–3) | 2.7 ± 0.4 | 2–4 | |
Total motility (%) | 87.8 ± 9.8 | 72.0–96.5 | |
Sperm concentration (×106 cells/mL) | 125.7 ± 62.2 | 51.1–179.3 | |
Sperm viability (%) | 89.0 ± 7.2 | 72.0–96.5 | |
Plasma membrane integrity (%) | 87.7 ± 8.1 | 70.0–98.0 | |
Plasma membrane fluidity (%) | Low | 94.9 ± 2.9 | 89.0–98.0 |
High | 5.0 ± 2.9 | 2.0–11.0 | |
Acrosome integrity (%) | 88.8 ± 7.7 | 70.0–97.0 | |
Sperm morphology (%) | Normal | 88.8 ± 8.5 | 70.5–98.0 |
Primary 2 | 5.5 ± 4.8 | 1–15 | |
Secondary 2 | 5.6 ± 5.0 | 1–17 | |
Sperm capacitation status (%) | F | 90.5 ± 5.2 | 80.0–98.0 |
B | 7.7 ± 5.4 | 1.0–19.0 | |
AR | 2.2 ± 1.3 | 1.0–5.0 |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2025 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Martínez-Torres, M.; Sánchez-Rivera, U.Á.; Medrano, A.; Hernández-Gónzalez, E.O.; Dávila-Govantes, R.; Castro-Camacho, Y.J.; Cruz-Cano, N.B. Semen Evaluation from Dominant Males of the Viviparous Mexican Lizard Sceloporus torquatus, Wiegmann, 1828 (Sauria: Phrynosomatidae). Vet. Sci. 2025, 12, 363. https://doi.org/10.3390/vetsci12040363
Martínez-Torres M, Sánchez-Rivera UÁ, Medrano A, Hernández-Gónzalez EO, Dávila-Govantes R, Castro-Camacho YJ, Cruz-Cano NB. Semen Evaluation from Dominant Males of the Viviparous Mexican Lizard Sceloporus torquatus, Wiegmann, 1828 (Sauria: Phrynosomatidae). Veterinary Sciences. 2025; 12(4):363. https://doi.org/10.3390/vetsci12040363
Chicago/Turabian StyleMartínez-Torres, Martín, Uriel Ángel Sánchez-Rivera, Alfredo Medrano, Enrique Othón Hernández-Gónzalez, Rodrigo Dávila-Govantes, Yabín Josué Castro-Camacho, and Norma Berenice Cruz-Cano. 2025. "Semen Evaluation from Dominant Males of the Viviparous Mexican Lizard Sceloporus torquatus, Wiegmann, 1828 (Sauria: Phrynosomatidae)" Veterinary Sciences 12, no. 4: 363. https://doi.org/10.3390/vetsci12040363
APA StyleMartínez-Torres, M., Sánchez-Rivera, U. Á., Medrano, A., Hernández-Gónzalez, E. O., Dávila-Govantes, R., Castro-Camacho, Y. J., & Cruz-Cano, N. B. (2025). Semen Evaluation from Dominant Males of the Viviparous Mexican Lizard Sceloporus torquatus, Wiegmann, 1828 (Sauria: Phrynosomatidae). Veterinary Sciences, 12(4), 363. https://doi.org/10.3390/vetsci12040363