The hagfish oocyte at late stages of oogenesis: Structural and metabolic events at the micropylar region

Abstract

The hagfishes (Class Agnatha), primitive vertebrates and massive secretors of mucus, occupy a unique niche in a marine benthic environment and exists in abundance despite an infrequent ovulation of a low number (12–45) of notably large, prolate ellipsoidal (~8 mm × 28 mm. width × length, respectively) eggs. To establish factors that might contribute to survivability of one species ( Eptatretus stouti), we examined three groups of mature females and document structural events characteristic of oocytes at late developmental stages: attached to the gonad, after ovulation into the body cavity, and after deposition on aquaria substrata. Quantitative autoradiographic analyses following administration in vivo of [ 3H]-leucine was useful to confirm post-vitellogenic stages and late metabolic events at the micropylar region located at one end of each egg. After egg disassembly, a combination of light microscopy and scanning electron microscopy was used to delineate structural features and 3-D relationships in juxtaposition to the micropylar cup and canal. A thick (~200μm) complex tripartite chorion surrounds a large micropylar cup (~300μm, width at base) consisting of fused polygonal (mainly hexagonal) substructural units (3–4 μm, width) and collectively serves to stabilize the micropylar canal (of size to prevent polyspermy) that penetrates the ooplasm near the germinal vesicle. A tuft composed of numerous chorionic appendages (‘anchor filaments’, ~2–3 mm length) is enmeshed in a gel matrix and surrounds the cup. When the eggs are deposited, intermediate filament aggregates (IFA) from slime gland mucus become interspersed in the tuft/gel complex. A similar IFA/tuft/gel region found on the vegetal pole-end facilitates firm egg-end attachments and possibly assists localization of egg clutches to a favorable substratum. Although the mode of fertilization is as yet unknown, the collective structural characteristies of the hagfish egg arc indicative of physical strength and are markedly different from eggs of the other group of cyclostomes (lampreys) and from tcleosts. The hagfish produces fewer but larger eggs which are prolate ellipsoidal rather than spherical and have a thicker chorion, a greater chorion to egg width ratio, a much larger micropylar cup with a unique substructure, larger and more localized chorionic appendages, and appendage tufts interspersed with adhesive substances derived not only from the follicular epithelium but also from the slime glands.