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Sperm storage in the viviparous lizard Sceloporus bicanthalis (Squamata: Phrynosomatidae), a species with continuous spermatogenesis

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Abstract

Sceloporus bicanthalis inhabits the Nevado de Toluca, México, and the males exhibit continuous spermatogenesis with mature sperm available year round. Females were collected monthly to evaluate the morphology of the oviducts and the presence of sperm storage. Histological examination revealed that the oviductal structure in this lizard is similar to that described for other lacertilian species: anterior infundibulum, glandular uterus, and a posterior non-glandular uterus. The oviduct wall consists of a superficial visceral pleuroperitoneum, a middle layer of smooth muscle with outer longitudinal and inner circular fibers, and a deep mucosa or lamina propria deeply lined by an epithelium containing ciliated and non-ciliated secretory cells. Spermatozoa are stored at the base of the mucosal folds, in crypts and in sperm storage tubules at the transition between the glandular uterus and non-glandular uterus, as well as in the anterior non-glandular uterus of previtellogenic, vitellogenic, pregnant, and postpartum females. The sperm in the oviductal cavity or in retention sites is in contact with secretory products derived from non-ciliated epithelial cells. Spermatozoa usually assume an orderly distribution with their heads aligned and oriented toward the base of the folds or crypts. This study shows that females of S. bicanthalis exhibit prolonged sperm storage that corresponds with the continuous reproductive strategy employed by males.

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References

  • Ambriz-Rosales IA (2010) Actividad Reproductora de Sceloporus bicanthalis (Squamata: Phrynosomatidae) en el volcán Nevado de Toluca. Tesis de Licenciatura Universidad Autónoma del Estado de México, Estado de México

    Google Scholar 

  • Anjos LA, Rocha CFD (2008) Reproductive ecology of the invader species gekkonid lizard Hemidactylus mabouia in an area of southeastern Brazil. Iheringia Ser Zool 98:205–209

    Article  Google Scholar 

  • Bagwill A, Sever DM, Elsey RM (2009) Seasonal variation of the oviduct of the American alligator, Alligator mississippiensis (Reptilia: Crocodylia). J Morphol 270:702–713

    Article  PubMed  Google Scholar 

  • Birkhead TR, Moller AP (1993) Sexual selection and the temporal separation of reproductive events: sperm storage data from reptiles, birds and mammals. Boil J Linnean Soc 50:295–311

    Article  Google Scholar 

  • Blackburn DG (1998) Structure, function and evolution of the oviducts of squamate reptiles, with special reference to viviparity and placentation. J Exp Zool 282:560–617

    Article  CAS  PubMed  Google Scholar 

  • Botte V (1973) Some aspects of oviduct biochemistry in the lizard Lacerta sicula in relation to the annual cycle. Boll Zool 40:315–321

    Article  Google Scholar 

  • Bou-Resli MN, Bishhay LF, AL-Zaid NS (1981) Observations on the fine structure of the sperm storage crypts in the lizard Acanthodactylus scutellatus hardyi. Arch Biol 92:287–298

    Google Scholar 

  • Cuellar O (1966) Oviductual anatomy and sperm structures in lizards. J Morphol 19:7–20

    Article  Google Scholar 

  • Duffaure JP, Hubbert J (1961) Table de development du lezad vivipare: Lacerta (Zootoca) vivípara Jacquin. Arch Anat Microsc Morphol Exp 50:309–328

    Google Scholar 

  • Estrada FE, Peralta ZL, Rivas MP (1982) Manual de técnicas histológicas. AGT Editor S. A. México

  • Fox W (1963) Special tubules for sperm storage in female lizards. Nature 198:500–501

    Article  Google Scholar 

  • Fox W (1977) The urogenital system of reptiles. In: Gans C (ed) Biology of the Reptilia, vol 6. Academic Press, New York, pp 1–157

    Google Scholar 

  • Friesen CR, Kerns AR, Mason RT (2014) Factors influencing paternity in multiply mated female red-sided garter snakes and the persistent use of sperm stored over winter. Behav Ecol Sociobiol 68:1419–1430

    Article  Google Scholar 

  • Girling JE (2002) The reptilian oviduct: a review of structure and function and directions for future research. J Exp Zool 293:141–170

    Article  PubMed  Google Scholar 

  • Gist DH, Fischer EN (1993) Fine structure of the sperm storage tubules in the box turtle oviduct. J Reprod Fert 97:463–468

    Article  CAS  Google Scholar 

  • Gist DH, Bagwill A, Lance V, Sever DM, Elsey RM (2008) Sperm storage in the oviduct of the American Alligator. J Exp Zool 309A:1–7

    Article  Google Scholar 

  • Goldberg SR (1970) Seasonal ovarian histology of the ovoviviparous iguanid Sceloporus jarrovi Cope. J Morphol 132:265–276

    Article  CAS  PubMed  Google Scholar 

  • Gribbins K, Anzalone M, Collier M, Granados-González G, Villagrán-SantaCruz M, Hernández-Gallegos O (2011) Temporal germ cell development strategy during continuous spermatogenesis within the montane lizard, Sceloporus bicanthalis (Squamata: Phrynosomatidae). Theriogenology 76:1090–1099

    Article  PubMed  Google Scholar 

  • Guillette JL Jr (1981) On the occurrence of oviparous and viviparous forms of the Mexican lizard Sceloporus aeneus. Herpetologica 37:11–15

    Google Scholar 

  • Guillette JL Jr, Casas-Andreu G (1981) Seasonal variation in fat body weights of the Mexican high elevation lizard Sceloporus grammicus microlepidotus. J Herpetol 15:366–371

    Article  Google Scholar 

  • Guillette JL Jr, Guillette RE (1985) Ovarian, oviductual, and placental morphology of the reproductively bimodal lizard Sceloporus aeneus. J Morphol 184:85–98

    Article  Google Scholar 

  • Hernández-Gallegos O (1995) Estudio comparativo del patrón reproductor de los machos de dos especies de lagartijas emparentadas con distinto modo reproductor: Sceloporus aeneus y S.bicanthalis. Tesis de Licenciatura en Biología, Facultad de Ciencias, Universidad Nacional Autónoma de México, México

  • Hernández-Gallegos O, Méndez-de la Cruz FR, Villagrán-Santa Cruz M, Andrews RM (2002) Continuos spermatogenesis in the lizard Sceloporus bicanthalis (Sauria: Phrynosomatidae) from high elevation habitat of central México. Herpetologica 58:415–421

    Article  Google Scholar 

  • Kiernan JA (1981) Histochemical and histochemical methods: theory and practice. Pergamon, Oxford

    Google Scholar 

  • Leache AD (2010) Species trees for spiny lizards (genus Sceloporus): identifying points of concordance and conflict between nuclear and mitochondrial data. Mol Phylogenet Evol 54:162–171

    Article  CAS  PubMed  Google Scholar 

  • Manríquez-Morán NL (1995) Estrategias reproductoras en las hembras de dos especies hermanas de lacetilios: Scelporus aeneus y S. bicanthalis. Tesis de icenciatura en Biología. Facultad de Ciencias. Universidad Nacional Autónoma de México, México

  • Mendoza-Cruz E (2006) Morfología del oviducto y formación de la membrana de la cáscara en el lacertilio vivíparo Sceloporus bicanthalis (Sauria: Phrynosomatidae). Tesis de Maestría en Ciencias. Facultad de Ciencias, Universidad Nacional Autónoma de México, México

    Google Scholar 

  • Mendoza-Cruz and Villagrán-Santa Cruz M (2007) Participación del oviducto en la formación y estructura de la membrana de la cáscara en la lagartija vivípara Sceloporus bicanthalis. S3-BYQ16 Memorias del IV encuentro Participación de la Mujer en la Ciencia, León Guanajuato, México

  • Murphy KS, Hudson S, Shea G (2006) Reproductive seasonality of three cold-temperate viviparous skinks from Southeastern Australia. J Herpetol 40:454–464

    Article  Google Scholar 

  • Nogueira KOPC (2008) Morfologia e ultra-estructura de oviducto de Hemidactylus mabouia (Moreau de Jonnès, 1818) (Reptilia, Squamata, Sauria, Gekkonidae) durante o ciclo reproductivo. Dissertação. Universidade Federal de Viçosa, MG 

  • Nogueira KOPC, Souza-Rodrígues S, Alvano-Araújo V, Andrade Neves C (2011) Oviductal structure and ultrastructure of the oviparous gecko, Hemidactylus mabouia (Moreau De Jonnés, 1818). Anat Rec 294:883–892

    Article  Google Scholar 

  • Olsson M, Madsen T (1998) Sexual selection and sperm competition in reptiles. In: Birkhead TR, Moller AP (eds) Sperm competition and sexual selection. Academic Press, London, pp 503–564

    Chapter  Google Scholar 

  • Ortega-León A, Villagrán-Santa Cruz M, Zúñiga-Vega JJ, Cueva del Castillo R, Méndez-de la Cruz FR (2009) Sperm viability in the reproductive tract of females in a population of Sceloporus mucronatus exhibiting asynchronous reproduction. West North Am Nat 69:96–104

    Article  Google Scholar 

  • Palmer BD, DeMarco VC, Guillette JL Jr (1993) Oviductal morphology and the eggshell formation in the lizard, Sceloporus woodi. J Morphol 217:205–217

    Article  Google Scholar 

  • Rheubert JL, Touzinsky K, Hernández-Gallegos O, Granados-González G, Gribbins KM (2012) Ontogenic development of spermatids during spermiogenesis in the high altitude bunchgrass lizard (Sceloporus bicanthalis). Spermatogenesis 2:1–10

    Article  Google Scholar 

  • Rodríguez-Romero F, Smith GR, Méndez-Sánchez F, Hernández-Gallegos O, Sánchez-Nava P, Méndez-de la Cruz FR (2011) Demography of a semelparous, high-elevation population of Sceloporus bicanthalis (Lacertilia: Phrynosomatidae) from the Nevado de Toluca Volcano, México. Southwest Nat 56:71–77

    Article  Google Scholar 

  • Saint-Girons H (1962) Presence de receptacles seminaux chez les cameleons. Beaufortia 9:165–172

    Google Scholar 

  • Saint-Girons H (1973) Sperm survival and transport in the female genital tract of reptiles. In: Hafez ESE, Thibault CG (eds) The biology of spermatozoa. Karger, Basel, pp 105–113

    Google Scholar 

  • Schuett GW (1992) Is long-term sperm storage an important component of the reproductive biology of temperate pitvipers? In: Campbell JA, Brodic ED Jr (eds) Biology of the Pitvipers. Selva, Austin, pp 169–184

    Google Scholar 

  • Sever DM, Hamlett WC (2002) Female sperm storage in reptiles. J Exp Zool 292:187–199

    Article  PubMed  Google Scholar 

  • Sever DM, Hopkins WA (2004) Oviductal sperm storage in the ground skink Scincella laterale Holbrood (Reptilia: Scincidae). J Exp Zool 301A:599–611

    Article  Google Scholar 

  • Sever DM, Ryan TJ (1999) Ultrastructure of the reproductive system of the black swamp snake (Seminatrix pygaea). Part I Evidence for oviductal sperm storage. J Morphol 241:1–18

    Article  CAS  PubMed  Google Scholar 

  • Sever DM, Ryan TJ, Morris T, Patton D, Swafford S (2000) Ultrastructure of the reproductive system of the black snake (Seminatrix pygaea). Part II annual oviductal cycle. J Morphol 245:146–160

    Article  CAS  PubMed  Google Scholar 

  • Siegel DS, Miralles A, Chabarria RE, Aldridge RD (2011) Female reproductive anatomy: cloaca, oviducts, and sperm storage. In: Aldridge RD, Sever DM (eds) Reproductive biology and phylogeny of snakes. CRC Press, Florida

    Google Scholar 

  • Siegel DS, Miralles A, Rheubert JL, Sever DM (2015) Female reproductive anatomy: cloaca, oviduct and sperm storage. In: Rheubert JL (ed) Reproductive biology and phylogeny of lizards and tuatara. Taylor & Francis Group, Oxfordshire, pp 144–195

    Google Scholar 

  • Villagrán-Santa Cruz M, Méndez-de la Cruz FR, Cuellar O (1992) Obligatory sperm storage in the lizard Sceloporus grammicus. Acta Zool Mex 49:23–31

    Google Scholar 

  • Villagrán-Santa Cruz M, Hernández-Gallegos O, Méndez-de la Cruz FR (2009) Reproductive cycle of the lizard Sceloporus mucronatus with comments on intraspecific geographic variation. West North Am Nat 69:437–446

    Article  Google Scholar 

  • Vitt LJ (1986) Reproductive tactic of sympatric gekkonid lizards with a comment on the evolutionary and ecological consequences of invariant clutch size. Copeia 1986:773–786

    Article  Google Scholar 

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Acknowledgments

We thank Teresa F López for the histological processing; Misol-ja Méndez and Dzilam Méndez for their help with the graphic design and digital preparation of the figures. The Posgrado en Ciencias Biológicas, Universidad Nacional Autónoma de México (UNAM), provided financial support through a fellowship granted to Mendoza-Cruz E.

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Correspondence to Maricela Villagrán-SantaCruz.

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All laboratory procedures were undertaken following ethical norms for animal experiments, and the study met the relevant legal regulations as well as institutional procedures for research of the Universidad Nacional Autónoma de México, and Ley de protección a los animales del Distrito Federal, México.

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Villagrán-SantaCruz, M., Mendoza-Cruz, E., Granados-González, G. et al. Sperm storage in the viviparous lizard Sceloporus bicanthalis (Squamata: Phrynosomatidae), a species with continuous spermatogenesis. Zoomorphology 136, 85–93 (2017). https://doi.org/10.1007/s00435-016-0327-6

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  • DOI: https://doi.org/10.1007/s00435-016-0327-6

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