Oogonia proliferate by mitosis to become primary oocytes. In these cells the chromosomes are arrested in the diplotene stage of the first meiotic prophase. The oocytes then enter a period of growth that varies from species to species, enlarging chiefly by accumulating yolk. As they grow and mature, various intracellular and extracellular changes occur. Initially the follicular cells form a simple squamous epithelium around each oocyte but, as development proceeds, the cells enlarge and may become cuboidal and even columnar. In cyclostomes and teleosts the follicular epithelium remains single layered but, in Chondrich-thyes, it may be composed of several layers (Franchi, 1962). As is typical of many epithelia, desmosomes connect adjacent follicular cells. Follicular cells may also produce ovarian hormones. The follicular epithelium is surrounded by its own basal lamina which separates it from a sheath of condensed vascular connective tissue, the theca folliculi. As the follicle differentiates, the theca becomes more distinct and may be divided into a theca interna and theca externa. The theca contains fibroblasts, collagenous fibres and capillaries and, in some species, special thecal steroid-producing cells (Figure 2.1).
During development, a thick, translucent, acellular zona pellucida, or vitelline envelope, develops between the oocyte and follicular cells. After hatching, when a simple plasma membrane would be inadequate for such a large cell to withstand the rigours of independent existence, this sheath serves as a tough enclosure for the egg. Even in viviparous forms, where the embryos develop within the body of the female, this envelope is formed during oogenesis (Flegler, 1977). During growth of the oocyte, the zona pellucida becomes perforated by pore canals, enabling an exchange of materials between the oocyte and follicular cells; these channels contain microvilli that extend from the surfaces of both the oocyte and the follicular cells (Figure 2.2).
Polarity is laid down within the oocyte of the me-daka Oryzias latipes during formation of the zona pellucida, before yolk production begins (Iwamatsu and Nakashima, 1996). This animal-vegetal axis consists of an animal pole of the most active protoplasm that develops diametrically opposite a vegetal pole of yolky, relatively inert protoplasm. It is suggested that this axis is established during development by reciprocal interactions of the oocyte with the adjacent follicular cells where a group of compactly clustered follicular cells determines the position of the vegetal pole area. A follicular cell at the opposite side of the oocyte differentiates into a micropylar cell, thereby determining the position of the micropyle (point of sperm entry) at the animal pole. Indeed, the micropyle is a convenient marker for identifying the animal pole.
In lampreys, possibly all elasmobranchs, and some bony fishes, oogonial proliferation is limited to the larval or embryonic period (Tokarz, 1978). Successive generations of oocytes appear to develop from oogonia in the germinal ridge of adult hagfish Myxine glutinosa; these oocytes enter a resting phase while they await ovulation of the previous generation of oocytes (Patzner, 1974). In most bony fishes, oogonial proliferation is found in the adult animal. There is a limited period of peak oogonial division in species with circumscribed annual breeding cycles; in species which do not have restricted breeding cycles, oogonial proliferation occurs either in waves or continuously throughout the year.
At the end of oogonial proliferation, the secondary oogonia become primary oocytes and enter a protracted early prophase. A primary oocyte is surrounded by a single layer of follicular cells to form a primordial follicle (Tokarz, 1978). This process is similar in all non-mammalian vertebrates and begins at approximately the same stage of meiotic prophase. A scheme of follicular development in the medaka Oryzias latipes is shown in Figure 2.3.
Because of the accessiblity of initial stages in the syngnathids — the pipefish and the seahorse — extensive descriptions of folliculogenesis have been carried out on these species, providing much of the information used here (Begovac and Wallace, 1987,1988; Sel-man, Wallace, and Player, 1991). Their germinal ridge is well-defined and contains oogonia, early prophase I oocytes, and somatic prefollicular cells as well as occasional degenerating cells (Figure 2.4). Oogonia of the germinal ridge divide by mitosis. As the daughter cells move away they are enveloped by follicular cells which are derived from the proliferation of prefollicular cells that extend processes between contiguous meiotic oocytes. This results in the isolation of the germ cells from other cells, thereby forming a follicle consisting of an oocyte surrounded by a follicular epithelium enclosed by its own basal lamina (Figure 2.5A). Prefollicular and follicular cells contain cytoplasmic filaments that distinguish them from early meiotic oocytes which contain no filaments. Newly formed follicles are surrounded by a thin theca of connective tissue elements.
Oogonia of the pipefish — the stem cells of the germ cell lineage — are oval to spherical cells, about lOpmin diameter, which occur in the luminal epithelium, near the germinal ridge, and within the germinal ridge itself (Begovac and Wallace, 1988) (Figure 2.6). They are contiguous with other germ cells and somatic cells but are not in contact with the basal lamina of the luminal epithelium. They are the only germ cells within the germinal ridge that incorporate [3H] thymidine, indicating that they are the only germ cells capable of nuclear division; somatic cells, including follicular cells and connective tissue cells incorporate the label as well. Oogonia have the largest nuclear/cy-toplasmic ratio of any cells of the germ cell line. The oval nuclei contain one to three nucleoli. Dense-cored granules of unknown composition within the nucleus are specific to nuclei of the germ cell line and are also present in larger oocytes. Oogonial chromatin is more electron-dense than that of meiotic oocytes. Oogonial cytoplasm contains mitochondria, ribosomes, and scant endoplasmic reticulum but appears to lack a Golgi complex. Aggregates of nuage material are frequently associated with mitochondria; this is an electron-dense, membraneless organelle consisting of a spongelike aggregation of fine granular material. The function and composition of nuage are uncertain but its presence is a reliable marker of germ cells. Oogonia of the sea lamprey Petromyzon marinus appear to be similar to those of teleosts (Okkelberg, 1921; Lewis and McMillan, 1965).
The process of transformation of oogonia to oocytes is oogenesis (Selman and Wallace, 1989). It is generally accepted that the chromosomes become arrested at diplotene of the first meiotic prophase and the initial follicle is established (Wallace and Selman, 1981). It is unclear how oogonial daughter cells are transformed into prophase I meiotic oocytes and whether the oogonial division that produces the oocytes is symmetrical (Begovac and Wallace, 1988). Although it is difficult to distinguish the earliest meiotic oocytes from oogonia, some features are said to characterize newly formed oocytes in the sequentially arranged ovaries of syngnathids: an increase in size along with a decrease in nuclear/cytoplasmic ratio; loss of the perinuclear ring of mitochondria; proliferation of other organelles, especially Golgi complexes; and changes in nuclear morphology, especially condensation of chromatin (Begovac and Wallace, 1988; Selman, Wallace, and Player, 1991) (Figures 2.5B and 2.7A). The most obvious sign of transformation of oogonia to oocytes in the sea lamprey is the increase in the size of the nucleus and the appearance of a prominent nucleolus (Lewis and McMillan, 1965).
Cytoplasmic bridges have been described between oogonia and oocytes of some teleosts (Figure 2.8) (Brusle and Brusle, 1978; Grandi and Colombo, 1997); these bridges were no longer observed when follicular cells had enveloped the oocyte (Brusle, 1980). On the other hand, intercellular bridges were never observed between oogonia or oocytes of the syngnathids (Begovac and Wallace, 1987; Selman, Wallace, and Player, 1991).
An increase in size is the most obvious manifestation of oocyte development (Figure 2.9). The oocyte grows both by an enlargement of the nucleus and the addition of cytoplasm. Later, most growth is due to an increase in the amount of cytoplasm and, in the final stages of maturation, the oocyte has its full complement of yolk and is ready to be ovulated. Four principal stages of oocyte development, as outlined below, have been described in several teleosts (Wallace and Selman, 1981). The major cellular and physiological processes occurring at each stage of the zebrafish Brachydanio rerio are outlined by Selman et al. (1993). Average diameters of follicles (oocytes
TABLE 2.1. Average diameters of ovarian follicles in Fundulus heteroclitus during the stages of oocyte development (Data from Selman and Wallace, 1986)
IA. Chromatin nucleolus phase 8 — 20 pm
IB. Perinucleolus phase 20 — 175 pm
2. Cortical alveolus stage 175 — 550 pm
4A.Earlymaturation 1.35 — 1.7 mm
4B. Late maturation 1.7 — 1.9 mm in early stages), recorded for Fundulus heteroclitus, are shown in Table 2.1. Four similar stages have been outlined in the lamprey Lampetra planeri (Busson-Mabillot, 1967c). Similar development in the red sea bream Pagrus major (Matsuyama, Nagahama, and Matsuura, 1991), the rainbow trout Salmo gairdneri (van den Hurk and Peute, 1979), and the summer flounder Paralichthys dentatus (Merson et al., 2000) have been assigned to seven stages, nine stages in the medaka Oryzias latipes (Figure 2.53) (Iwamatsu et al., 1988) and, in the blenny Blenniuspholis, eleven (Figure 2.5) (Shackley and King, 1977).
Classification of stages of ovarian maturity by macroscopic observation are useful in fecundity studies (Bagenal and Braum, 1971); these have been adapted, using histological criteria, for the perch Percafluviati-lis and pike Esox lucius (Figure 2.10) (Treasurer and Holliday, 1981; Treasurer, 1990) and for the bass Dicentrarchus labrax (Mayer, Shackley, and Ryland, 1988).
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