Ultrastructure of spermatogenesis in lion’s paw scallop Nodipecten subnodosus (G. B. Sowerby I, 1835), with some implications in the systematics of the Pectinidae

Autores/as

Marco Antonio Ángel-Dapa Instituto Politécnico Nacional, Centro Interdisciplinario de Ciencias Marinas (CICIMAR), Av. Instituto Politécnico Nacional s/n Col. Playa Palo de Santa Rita. C.P. 23096, La Paz, B.C.S. México. https://orcid.org/0000-0002-5147-9424
Marcial Arellano-Martínez Instituto Politécnico Nacional, Centro Interdisciplinario de Ciencias Marinas (CICIMAR), Av. Instituto Politécnico Nacional s/n Col. Playa Palo de Santa Rita. C.P. 23096, La Paz, B.C.S. México. https://orcid.org/0000-0002-9344-2128
Esther Uría-Galicia Instituto Politécnico Nacional, Escuela Nacional de Ciencias Biológicas. Unidad Profesional Lázaro Cárdenas, Prolongación de Carpio y Plan de Ayala s/n, Col. Santo Tomas, C.P. 11340, Delegación Miguel Hidalgo, Ciudad de México. https://orcid.org/0000-0003-1255-8522
Edgar Oliver López Villegas Instituto Politécnico Nacional, Escuela Nacional de Ciencias Biológicas. Unidad Profesional Lázaro Cárdenas, Prolongación de Carpio y Plan de Ayala s/n, Col. Santo Tomas, C.P. 11340, Delegación Miguel Hidalgo, Ciudad de México. https://orcid.org/0000-0002-9995-2145
Bertha Patricia Ceballos Vázquez Instituto Politécnico Nacional, Centro Interdisciplinario de Ciencias Marinas (CICIMAR), Av. Instituto Politécnico Nacional s/n Col. Playa Palo de Santa Rita. C.P. 23096, La Paz, B.C.S. México. https://orcid.org/0000-0002-9995-2145
Pedro Saucedo Centro de Investigaciones Biológicas del Noroeste (CIBNOR). Av. Instituto Politécnico Nacional 195, Col. Playa Palo de Santa Rita Sur, La Paz, B.C.S., 23096, México. https://orcid.org/0000-0002-2155-9677

DOI:

https://doi.org/10.33936/at.v6i2.6893

Palabras clave:

Scallops, Reproduction, Spermatogenesis, taxonomy, Vieira, reproducción, espermatogénesis, taxonomía

Resumen

ABSTRACT | This is the first study to characterize the ultrastructure of spermatogenesis in the lion’s paw scallop Nodipecten subnodosus, discussing some implications of cell morphology and function in the systematics of the family Pectinidae. Gonad samples were collected on a monthly basis during an annual cycle and processed using conventional TEM techniques. The number and area of developing cells occurring throughout spermatocytogenesis, meiosis, and spermiogenesis were determined. Overall, the arrangement of developing cells was concentric and most cellular changes comprising the transition from spermatogonia to spermatid matched the general pattern of marine bivalves undergoing external fertilization. The main features included a primitive-type, tailed sperm with four spherical mitochondria located in the midpiece, and the typical 9+2 arrangement of microtubules surrounding the centriole. During spermatogenesis, the key changes in cell morphology occurred up to the spermatozoon stage, including the appearance of a bullet-shaped nucleus, a conical acrosome, a small oval-shaped proacrosomal vesicle, and two lateral satellite fibers linked to the centriole. The flagellum also formed up to the sperm stage. Taxonomically, these features appear to be family-specific or species-specific and suggest that N. subodosus may be closely related to the hermaphrodite scallops Patinopecten yessoensis, Chlamys farreri farreri, C. swiftii, and Argopecten irradians within the family Pectinidae.

Citas

Angel-Dapa M.A., Arellano-Martínez M., Ceballos-Vázquez B.P., Acosta-Salmón H., Saucedo, P.E. (2015). Comparative analysis of the reproductive strategy of lion’s paw scallop Nodipecten subnodosus in Baja California Sur, Mexico. Lat Am J Aquatic Res. 43: 616–620.

Arellano-Martínez M., Ceballos-Vázquez B.P., Villalejo-Fuerte M., García-Domínguez F., Elorduy-Garay J.F., Esliman-Salgado A., Racotta, I.S. (2004a). Reproduction of the lion’s paw scallop Nodipecten subnodosus Sowerby, 1835 (Bivalvia: Pectinidae) from Laguna Ojo de Liebre, B.C.S., Mexico. J Shellfish Res. 23: 723–729.

Arellano-Martínez M., Racotta I.S., Ceballos-Vázquez B.P., Elorduy-Garay J.F. (2004b). Biochemical composition, reproductive activity and food availability of the lion’s paw scallop Nodipecten subnodosus in the Laguna Ojo de Liebre, Baja California Sur, Mexico. J Shellfish Res. 23: 15–23.

Beltrán-Lugo A.I., Maeda-Martínez A., Pacheco-Aguilar R., Nolasco-Soria H. (2006). Seasonal variations in chemical, physical, textural, and microstructural properties of adductor muscles of Pacific lions-paw scallop (Nodipecten subnodosus). Aquaculture 258: 619–632.

Camacho-Mondragón M.A., Ceballos-Vázquez B.P., Uría-Galicia E., López-Villegas E.O, Arellano-Martínez M. (2014). Ultraestructure of the spermatogenic process in the penshell Atrina maura (Bivalvia: Pinnidae). Malacologia 57: 329–339.

De Gaulejac B., Henry M., Vicente N. (1995). An ultrastructural study of gametogenesis of the marine bivalve Pinna nobilis (Linnaeus 1758). II. Spermatogenesis. J. Mollusc Stud. 61: 393–403.

Dimitri P., Caizzi R., Giordano E., Accardo M.C., Lattanzi G., Biamonti G. (2009). Constitutive heterochromatin: a surprising variety of expressed sequences. Chromosoma 118: 419–435.

Dorange G. and Le Pennec M. (1989). Ultrastructural characteristics of spermatogenesis in Pecten maximus (Mollusca, Bivalvia). Invert Repro Dev. 15: 109–117.

Eckelbarger K.J. and Davis C.V. (1996). Ultrastructure of the gonad and gametogenesis in the eastern oyster, Crassostrea virginica. II. Testis and spermatogenesis. Mar Biol. 127: 89–96.

Franzen A. (1970). Phylogenetic aspects of the morphology of spermatozoa and spermiogenesis. In: Baccetti, B., Karp, G., Berrill, N.J. (eds.), Comparative Spermatology. McGraw-Hill, New York, pp. 3–46.

Gutiérrez-Villaseñor C.E., Chi-Barragán G. (1997). Effect of temperature and feeding ratio on the conditioning of Lyropecten subnodosus (Sowerby, 1835). In: Book of Abstracts. Proceedings 11th International Pectinid Workshop, CICIMAR, La Paz, Baja California Sur, Mexico, pp. 73–75.

Healy J.M. (1995). Spermatozoa and spermatogenesis in a monoplacophoran mollusk, Leavipilina antartica: ultrastructure and comparison with other Mollusca. Mar. Biol. 122: 53-65.

Healy J.M., Keys J.L., Daddow L.Y.M. (2000). Comparative sperm ultrastructure in pteriomorphian bivalves with special reference to phylogenetic and taxonomic implications. In: Harper, E.M., Taylor, J.D., Crame, J.A. (eds.), The evolutionary Biology of the Bivalvia. Special Publications Geological Society, London, UK, pp. 169–190.

Jun J.C, Kim J.H., Park Y.J., Kang H.W., Chung J.S., Chung E.Y. (2012). Morphology and taxonomic values of the sperm in male Chlamys (Swiftopecten) swiftii (Pteriomorphia: Pectinidae) in Western Korea. Korean J. Malacol. 28: 165–174.

Kang H.W., Chung E.Y., Kim J.H., Chung J.S., Lee K.Y. (2012). Germ cell differentiations during spermatogenesis and taxonomic values of mature sperm morphology of Atrina (Servatrina) pectinata (Bivalvia, Pteriomorphia, Pinnidae). Dev Repro. 16: 19–29.

Kim J.H. (2001). Spermatogenesis and comparative ultrastructure of spermatozoa in several species of Korean economic bivalves (13 families, 34 species). Ph.D. Thesis, Pukyung National University, Daeyeon, South Korea.

Kim J.H., Chung J.S., Lee K.Y. (2013). Ultraestructural characteristics of the testis, spermatogenesis and taxonomic values of sperm morphology in male Ruditapes philippinarum in Western Korea. Dev Repro. 17: 121–132.

López-Sánchez J.A., Maeda-Martínez A.N., Croll R.P., Acosta-Salmón H. (2009). Monoamine fluctuations during the reproductive cycle of the Pacific lion’s paw scallop Nodipecten subnodosus. Comp Biochem Physiol. A. 154: 425–428.

Maeda-Martínez A.N. and Lodeiros C. (2011). Biología y cultivo de moluscos pectinidos del género Nodipecten. Ed. Limusa, México City, 398 p.

Ortíz E., Uría-Galicia E., Silva-Olivares A., Tsutsumi V., Shybayama M. (2003). Estudio de la ultraestructura de la espermatogénesis de Anadara tuberculosa (Sowerby, 1833) (Mollusca: Pelicipoda: Arcidae). Hidrobiológica 13: 145–150.

Ortíz E., Uría-Galicia E., Silva-Olivares A., Tsutsumi V., Shybayama M. (2006). Ultraestructure of spermatogenesis in the white clam Chione californiensis (Broderip, 1835) (Mollusca: Pelecipoda). J Shellfish Res. 25: 399–401.

Palacios E., Racotta I.S., Kraffe E., Marty Y., Moal J., Samain J.F. (2005). Lipid composition of the giant lion’s paw scallop (Nodipecten subnodosus) in relation to gametogenesis: I. Fatty acids. Aquaculture 250: 270–282.

Palacios E., Racotta I.S., Arjona O., Marty Y., Coz J.R., Moal J., Samain J.F. (2007). Lipid composition of the pacific lion’s paw scallop, Nodipecten subnodosus, in relation to gametogenesis. 2. Lipid classes and sterols. Aquaculture 266: 266–273.

Suwanrajat J. and Parnrong S. (1999). Reproductive cycles of Anadara granosa L. in Jebilung Satun Province. Warasan Songkhanakarin 12: 341–351.

Thielley M., Weppe M., Herbaut C. (1993). Ultrastructural study of gametogenesis in the French Polynesian black pearl oyster Pinctada margaritifera (Mollusca, Bivalvia). I. Spermatogenesis. J Shellfish Res. 12:41–47.

Villalejo-Fuerte M., Camacho-Mondragón M.A., Ceballos-Vázquez B.P., López-Villegas E.O., Uría-Galicia E., Arellano-Martínez M. (2018). Ultrastructure of sperm development and mature sperm morphology in Spondylus calcifer and S. princeps (Bivalvia: Spondylidae). Malacologia 62: 1–10.