Ovarian structure and oogenesis of the extremophile viviparous teleostPoecilia mexicana(Poeciliidae) from an active sulfur spring cave inSouthernMexico

Abstract

The structure of the ovary and oogenesis of Poecilia mexicana from an active sulfur spring cave is documented. Poecilia mexicana is the only poeciliid adapted to a subterranean environment with high hydrogen sulfide levels and extreme hypoxic conditions. Twenty females were captured throughout one year at Cueva del Azufre, located in the State of Tabasco in Southern Mexico. Ovaries were processed with histological techniques. P. mexicana has a single, ovoid ovary with ovigerous lamella that project to the ovarian lumen. The ovarian wall presents abundant loose connective tissue, numerous melanomacrophage centers and large blood vessels, possibly associated with hypoxic conditions. The germinal epithelium bordering the ovarian lumen contains somatic and germ cells forming cell nests projecting into the stroma. P. mexicana stores sperm in ovarian folds associated with follicles at different developmental phases. Oogenesis in P. mexicana consisted of the following stages: (i) oogonial proliferation, (ii) chromatin nucleolus, (iii) primary growth, subdivided into: (a) one nucleolus, (b) multiple nucleoli, (c) droplet oils-cortical alveoli steps; (iv) secondary growth, subdivided in: (a) early secondary growth, (b) late secondary growth, and (c) full grown. Follicular atresia was present in all stages of follicular development; it was characterized by oocyte degeneration, where follicle cells hypertrophy and differentiate in phagocytes. The ovary and oogenesis are similar to these seen in other poeciliids, but we found frequent atretic follicles, melanomacrophage centers, reduced fecundity and increased of offspring size.

Structure of the testis and spermatogenesis of the viviparous teleost Poecilia mexicana (Poeciliidae) from an active sulfur spring cave in Southern Mexico

“…It is known that females have reduced fecundity (Riesch, Tobler, Plath, & Schlupp, ) and reproduce continuously, with a cycle of 28 days (Parzefall, ). The oogenesis of this ecotype is similar to other poeciliids, but females produce exceptionally large eggs (Torres‐Martínez, Hernández‐Franyutti, Uribe, & Contreras‐Sánchez, ). Only one study exists documenting that sperm volumes are significantly lower in P. mexicana compared with surface dwelling ecotypes (Franssen, Tobler, Riesch, León, Tiedemann, Schlupp, & Plath, ).…”

“…All specimens of P. mexicana analyzed in this study showed maximum spermatogenic activity, even at sizes as small as 2.2 cm. This means that males are spermatogenetically active around the year as reported in females, where vitellogenic and pregnant ovaries were found across all the sampled seasons (Torres‐Martínez et al, ). We suggest that reproduction at early ages and year round guarantee the reproductive success of P. mexicana in the Cueva del Azufre.…”

“…It is not a coincidence that almost all species living in environments with H 2 S are viviparous (Riesch et al, ). Viviparity in P. mexicana has also favored the colonization of extreme environments, because embryos develop inside the ovarian follicles, in such a way that maternal tissues protect the offspring during the development from the systemic and deleterious effect of H 2 S (Torres‐Martínez et al, ).…”

“…MMCs were described previously in the ovary of P. reticulata (Campuzano‐Caballero & Uribe ), where they might be involved in the protection of the embryos by immunological functions. In P. mexicana , Torres‐Martínez et al () considered that MMCs may play a role in recycling materials from degenerating oocytes and in the detoxification of heavy metals and/or sulfur‐derived compounds present in the sulfur spring cave where this ecotype inhabits. The MMCs identified in the testes of P. mexicana may play a similar role as in females, that is, to be involved in immunological functions and recycling compounds of degenerating spermatocysts and/or in the detoxification of sulfurous compounds or other toxins present in the Cueva del Azufre.…”

Morphology of yolk and pericardial sacs in lecithotrophic and matrotrophic nutrition in poeciliid fishes

“…transfer from maternal tissues to the embryo (Blackburn, 2015;Marsh-Matthews & Deaton, 2006;Thibault & Schultz, 1978;Torres-Martínez et al, 2017;Turner, 1940a;Uribe et al, 2010Uribe et al, , 2019Wourms, 1991). These two ways of nutrient transfer are not mutually excluding.…”