Assembly of ovarian follicles in the caeciliansIchthyophis tricolorandGegeneophis ramaswamii:light and transmission electron microscopic study

Abstract

Though much is known about various aspects of reproductive biology of amphibia, there is little information on the cellular and mechanistic basis of assembly of ovarian follicles in this group. This is especially true of the caecilians. Therefore, taking advantage of the abundant distribution of caecilians in the Western Ghats of India, two species of caecilians, Ichthyophis tricolor and Gegeneophis ramaswamii, were subjected to light and transmission electron microscopic analysis to trace the sequential changes during the assembly of ovarian follicles. The paired ovaries of these caecilians are elongated sac-like structures each including numerous vitellogenic follicles. The follicles are connected by a connective tissue stroma. This stroma contains nests of oogonia, primary oocytes and pregranulosa cells as spatially separated nests. During assembly of follicles the oocytes increase in size and enter the meiotic prophase when the number of nucleoli in the nucleus increases. The mitochondrial cloud or Balbiani vitelline body, initially localized at one pole of the nucleus, disperses through out the cytoplasm subsequently. Synaptonemal complexes are prominent in the pachytene stage oocytes. The pregranulosa cells migrate through the connective tissue fibrils of the stroma and arrive at the vicinity of the meiotic prophase oocytes. On contacting the oocyte, the pregranulosa cells become cuboidal in shape, wrap the diplotene stage oocyte as a discontinuous layer and increase the content of cytoplasmic organelles and inclusions. The oocytes increase in size and are arrested in diplotene when the granulosa cells become flat and form a continuous layer. Soon a perivitelline space appears between the oolemma and granulosa cells, completing the process of assembly of follicles. Thus, the events in the establishment of follicles in the caecilian ovary are described.

Stages in follicle cell/oocyte interface during vitellogenesis in caecilians Ichthyophis tricolor and Gegeneophis ramaswamii: a transmission electron-microscopic study

“…The sequential cytological changes in the two caecilians from these perspectives are believed to be comparable with those known for the anurans X. laevis (Dumont 1972;Wallace and Bergink 1974;Wallace 1985;Wallace and Selman 1990), Rana esculenta (Wartenberg and Gusek 1960), Rana pipiens (Ward 1962) and Rana tigrina (Sretarugsa et al 2001) and the urodeles Notophthalmus viridescens (Hope et al 1963) and Necturus maculosus (Kessel and Ganion 1980). The formation of the vitelline envelope in X. laevis (Dumont 1972) and R. tigrina (Sretarugsa et al 2001) is first detectable in stage II oocytes as is the case in the caecilians (Beyo et al 2007a(Beyo et al , 2007b. However, a study in X. laevis (Yamaguchi et al 1989) has indicated that the cytoplasm of oocytes as early as stage I contains components reacting to anti-vitelline coat antibodies, suggesting that the oocyte plays a role in synthesizing its own vitelline envelope.…”

“…The two caecilians, which overlap in their distribution in the Western Ghats of Southern India, differ little in their reproductive cyclicity, structural changes in the ovarian follicles and dependence on environmental factors (Beyo et al 2007a(Beyo et al , 2007b. Hence, we have traced the developmental sequence of the follicle cell/oocyte interface for these two species together.…”

“…c Dense granules (dg), oocyte cortex (oc) and extension of the follicle cell (fc) cytoplasm into the tunnel (tl) of the vitelline envelope. Bar 0.31 μm the first arrival of the material of the vitelline envelope in the perivitelline space (Beyo et al 2007a(Beyo et al , 2007b.…”

“…Among the urodeles the salamander Notophthalmus viridescens (Hope et al 1963) and the newt Necturus maculosus (Kessel and Ganion 1980) are two species that have been studied in adequate detail. No reports of TEM analysis of caecilian ovarian follicles exist, except for our description of the previtellogenic follicles of Ichthyophis tricolor and Gegeneophis ramaswamii of the Western Ghats of India (Beyo et al 2007a(Beyo et al , 2007b. However, the light-microscopic morphology of the ovarian changes in relation to follicular dynamics is known for Ichthyophis beddomei Nadkarni 1993a, 1993b) and Typhlonectes compressicauda (Exbrayat 2006).…”

“…The TEM analysis of the follicle cell/oocyte interface of I. tricolor and G. ramaswamii involved the same basic methodology as described earlier (Beyo et al 2007a(Beyo et al , 2007b. I. tricolor (Ichthyophiidae) and G. ramaswamii (Caeciliidae) were collected from terraced plantations of mixed coconut and rubber from Thekkada (08°37′N, 76°57′E) in the Trivandrum district of Kerala and Maramalai (08°26′N, 77°24′E) in the Kanyakumari district of Tamil Nadu, Southern India, from June 2004 to June 2005.…”