The ovary of the lobster, Homarus americanus: II. Structure of the mature follicle and origin of the chorion

doi:10.1016/S0022-5320(81)80056-1

Journal of Ultrastructure Research

Volume 76, Issue 3, September 1981, Pages 249-262

https://doi.org/10.1016/S0022-5320(81)80056-1 Get rights and content

We have analyzed the structure of the mature ovarian follicle from the lobster, Homarus americanus. Mature follicles are composed of five parts which from inside to outside are: (i) the oocyte, (ii) the chorion, (iii) the follicle cells, (iv) a thick basal lamina, and (v) cells associated with the follicle's surface. The oocyte comprises most of the mass of the follicle; it is packed with yolk and green in color due to the presence of ovoverdin. The oolemma forms thick microvilli which project into the perivitelline space and through the chorion or oocyte investing coat. The chorion is composed of two regions, an endochorion containing “bottlebrush” inclusions and a thinner exochorion. The chorion is completely surrounded by a single layer of follicle cells which are polygonal in shape. The follicle cells exhibit at least four types of synthetic activity. The components of the endochorion are synthesized in smooth vesicles in the supranuclear region of follicle cells. Rough endoplasmic reticulum, Golgi bodies, and associated electron-dense granules are present throughout the cells; the granules appeared to be released at the cell's basal surface and contribute to chorion formation. An extensive network of tubular smooth endoplasmic reticulum and associated vesicles containing moderately electron-dense material was present in the subnuclear zone; the organization of this network suggests the follicle cells are active in steroid synthesis. Lamellar bodies composed of alternating electron-dense and lucid bands were common, especially in the basal cytoplasm; their function is not yet known. The entire follicle is surrounded by a thick basal lamina. Often this basal lamina forms the outermost surface of the follicle. However, in some regions it was covered by surface cells including fibroblasts, blood vessels, muscle cells, hemocytes, and epithelial cells. This description of the ultrastructure of the lobster ovarian follicle will provide a framework for future investigations on ovarian physiology.

References (55)

AikenD. et al.
CruickshankW.J.
J. Insect. Physiol.
(1971)
GoudeauM. et al.
Tissue Cell
(1980)
GoudeauM. et al.
Tissue Cell
(1980)
HinschG.
J. Ultrastruct. Res.
(1971)
HinschG. et al.
Tissue Cell
(1979)
JengS.S. et al.
Gen. Comp. Endocrinol.
(1978)
MoralesT.I. et al.
Biochim. Biophys. Acta
(1978)
TalbotP.
J. Ultrastruct. Res.
(1981)
TalbotP. et al.
J. Ultrastruct. Res.
(1980)

TalbotP. et al.

J. Ultrastruct. Res.

(1980)

BeamsH.W. et al.

J. Cell Biol.

(1962)

BeamsH.W. et al.

J. Cell Biol.

(1963)

BeamsH.W. et al.

J. Cell Sci.

(1969)

BumpusH.C.

J. Morphol.

(1891)

BlanchetteE.J.

J. Cell Biol.

(1966)

CeccaldiH.J. et al.

C. R. Soc. Biol.

(1966)

Charniaux-CottonH.

Ann. Biol. Anim. Bioch. Biophys.

(1975)

CheungT.S.

J. Mar. Biol.

(1966)

ChristensenA.K. et al.

J. Biol. Phys. Biol. Chem. Cytol.

(1961)

ChristensenA.K. et al.

Amer. J. Anat.

(1966)

ClarkW.H. et al.

J. Exp. Zool.

(1977)

ClarkeK.U.

The Biology of Arthropoda

(1973)

DhainautA. et al.

Arch. Biol. (Bruxelles)

(1976)

DonahueJ.K.

Bull. Dep. Sea Shore Fish.

(1957)

EndersA.C.

J. Cell Biol.

(1962)

EspeyL.L. et al.

Biol. Reprod.

(1976)

Cited by (33)

Ovarian development in swimming crabs: Comparative histochemistry and ultrastructure of Callinectes ornatus and Arenaeus cribrarius (Brachyura, Portunidae)
2020, Tissue and Cell
Citation Excerpt :
Ultrastructurally, the least electron-dense layer, i.e., the endochorion, increases in thickness, while the more electron-dense outer layer, i.e., the exochorion, undergoes little alteration. The chorion is composed of layers of different electron density, which has also been reported for the majoids Libinia emarginata (Hinsch, 1971), Mithrax hispidus (Herbst, 1790), Mithrax tortugae Rathbun, 1920, Mithraculus forceps A Milne-Edwards, 1875, and Omalacantha bicornuta (Latreille 1825) (Mollenberg et al., 2017) and for the lobster Homarus americanus H. Milne Edwards, 1837 by Talbot (1981). As also proposed by Charniaux-Cotton (1980), the microvilli of both portunids are significantly reduced at the mature stage, and pinocytic vesicles are no longer observed in the oocyte cortex, which indicates the end of the exogenous phase.
The ovarian development of Callinectes ornatus and Arenaeus cribrarius was described using histochemistry and ultrastructure. Both species shows the same ovarian stages, which are the juvenile (JUV), adult rudimentary (RUD), developing (DEV), intermediary (INT), mature (MAT), and spent (OV) stages. The JUV and RUD stages showed similar characteristics, and previtellogenesis is characterized by meiotic prophase chromosomes. In the primary vitellogenesis, the oocyte cytoplasm shows many small and large cytoplasmic glycoprotein vesicles. These vesicles correspond to the dilated cisternae of the rough endoplasmic reticulum (RER), which produces the immature (endogenous) yolk. Secondary vitellogenesis (exogenous phase) begins at the DEV stage with the fusion of pinocytic vesicles and vesicles with immature yolks to form mature yolk granules. At the INT stage, the formation of the chorion begins, and the mature yolks increase in size and number, while the RER diminishes. In the MAT stage, the oocytes are completely formed, and the cytoplasm is filled with mature yolk, lipid droplets, and glycogen. There are no significant variations between the gonadosomatic and hepatosomatic indices, which allows us to infer that the transfer of reserves from the hepatopancreas is nearly constant during ovarian development, since we observed primiparous and multiparous females in the same sampled population.
Research frontiers in penaeid shrimp reproduction: Future trends to improve commercial production
2019, Aquaculture
Citation Excerpt :
The role of steroid hormones in crustaceans may be similar to fish and amphibia, where estrogens stimulate vitellogenesis and progestagens induce oocyte maturation (Fairs et al., 1990). In the lobster, Homarus americanus, steroidogenesis is associated with the follicle cells (Talbot, 1981). Merlin et al. (2016) suggested that the hepatopancreas could be the major organ responsible for progesterone and estradiol synthesis in P. monodon; progesterone levels seem to increase in hemolymph and ovary for advanced vitellogenic stages.
Shrimp farming worldwide is based on a similar technological package, characterized by three phases: Controlled Reproduction, Larvae Culture, and Grow-out Culture. This basic aquaculture package uses broodstock animals, with different levels of fundamental genetic selection, induced to mature and reproduce based on unilateral eyestalk ablation. This review identified ten reproduction-related research subjects that can improve the shrimp industry based on basic scientific knowledge and four levels of application: eyestalk ablation alternatives, larvae production, product protection, and grow-out yield improvement. Species-specificity must be considered in developing biotechnology solutions. Alternatives to eyestalk ablation for controlling ovarian maturation are based on neurotransmitter regulation in Litopenaeus; however, the environmental impact of this approach has to be evaluated. Maturation by RNAi requires further evaluation, and maturation pheromones have not been explored. Sex reversal, hybridization, in vitro fertilization, and seedstock cryopreservation of penaeids require fundamental research. Triploid culture and genetic selection can be applied to some species for product protection; however, for L. vannamei, triploidization is not practical yet.
Relationship between hatching rate and the outer egg membranes of the in vitro artificially fertilized eggs of the Japanese mitten crab Eriocheir japonica
2009, Aquaculture
This study shows that by removing the outer membranes of the in vitro artificially fertilized eggs of the Japanese mitten crab Eriocheir japonica, the normal zoea hatching rate of the eggs can be raised from 10% up to over 90%. This finding suggests that the normal zoea hatching rate is strongly influenced by the outer egg membranes of the in vitro artificially fertilized eggs. In addition, observations by transmission electron microscopy indicate that the outer egg membranes of the in vitro artificially fertilized eggs are 1.5 to 3 times thicker than those of the naturally spawned eggs. Discussion focuses on the role these thick outer egg membranes play in the normal zoea hatching rate of in vitro artificially fertilized eggs.
Molecular cloning and characterization of cortical rod protein in the giant freshwater prawn Macrobrachium rosenbergii, a species not forming cortical rod structures in the oocytes
2007, Comparative Biochemistry and Physiology - B Biochemistry and Molecular Biology
The formation of cortical rod structures is a characteristic of fully mature oocytes in penaeid prawns, but such structures are absent from oocytes of giant freshwater prawn Macrobrachium rosenbergii. In the present study, we first demonstrated the presence of a 30-kDa protein, which was immunologically related to kuruma prawn cortical rod protein (CRP), in the ovary of giant freshwater prawn, and subsequently purified this protein. Furthermore, a cDNA encoding the CRP-like protein was isolated. Based on the high homology (98%) in the amino acid sequence with kuruma prawn CRP, the 30-kDa protein has been identified as a CRP homologue of giant freshwater prawn, designated mrCRP. The RT-PCR analysis revealed that mrCRP mRNA was present in the ovary from a prawn with a gonadosomatic index (GSI) of 0.2. Western blot analysis revealed the presence of a CRP-immunoreactive band of 30kDa in the ovary with GSI of 1.6. By immunocytochemistry, CRP-immunopositive signals were detected in the ovary with GSI of 0.9, that had started to accumulate considerable amounts of vitellins and lipids in the peripheral cytoplasm. With progress of vitellogenesis, mrCRP was apparently accumulated in the mature oocytes, although it was not detectable, presumably because a relatively small amount of mrCRP was masked with large amounts of vitellin and lipids. In giant freshwater prawn without forming cortical rod structures, our findings indicate that the oocytes produce mrCRP, a homologue of CRP found in penaeid prawns.
Morphological characterization of the ovary and oocytes vitellogenesis of the tick Rhipicephalus sanguineus (Latreille, 1806) (Acari: Ixodidae)
2005, Experimental Parasitology
This study presents the morphology of the ovary, as well as the process of the vitellogenesis in oocytes of the tick Rhipicephalus sanguineus. The ovary of these individuals is of the panoistic type; therefore, it lacks nurse cells. This organ consists of a single tubular structure, continuous, and composed of a wall formed by small epithelial cells with rounded nuclei which delimit the lumen. The oocytes in the different developmental stages in this tick species were classified into five stages (I–V). They remain attached to the ovary during vitellogenesis by a cellular pedicel and afterwards the mature oocytes (stage V) are released into the ovary lumen.
Gamete interactions during in vitro fertilization of lobster (Homarus americanus) Oocytes
1991, Journal of Structural Biology
Preovulatory lobster oocytes were mechanically removed from follicles and fertilized in vitro with sperm from the vas deferens of males or the seminal receptacle of females. Oocytes were fixed for ultrastructural analysis at various times after insemination. Stages in gamete interaction beginning with sperm binding to envelope 1A and extending through nuclear envelope breakdown of the fertilizing sperm were examined microscopically. Numerous sperm bind to envelope 1A of mature oocytes. Only properly oriented sperm undergoing normal acrosome reactions penetrate envelopes 1A and 1B (together these form the vitelline envelope). During the acrosome reaction, the inner acrosomal material comes in direct contact with envelope 1B and does not appear to release a lysin for penetration of envelopes 1A and 1B. The acrosomal membrane overlying the acrosomal filament appears to be the first membrane of the sperm to contact the oolemma and is probably the initial site of gamete membrane fusion. Following fusion, egg cytoplasm flows around the sperm nucleus forming a small fertilization cone. The acrosomal contents are left outside the oocyte in the pervitelline space. Once gamete membrane fusion has occurred, the nuclear envelope fragments, and by 120 min after insemination, it has completely disappeared around some sperm nuclei. As sperm are incorporated into the ooplasm, the microtubules associated with the membrane/microtubule complex of the nucleus depolymerize, and the membranes of this complex are less frequently observed. After gamete membrane fusion, the acrosomal filament is contiguous with oocyte cytoplasm, and it remains structurally unchanged by 120 min after insemination. It is probable that the oocyte releases some high density cortical granules within the first 120 min of insemination; however, there was no evidence for the release of low density vesicles, ring vesicles, and moderately dense vesicles during this time.

View all citing articles on Scopus

: Supported by a Sea Grant from NOAA and an Intercampus Travel Grant from the University of California.

¹: Present address: Department of Biology, University of California, Riverside, Calif. 92521.

View full text

The ovary of the lobster, Homarus americanus: II. Structure of the mature follicle and origin of the chorion

J. Insect. Physiol.

Tissue Cell

Tissue Cell

J. Ultrastruct. Res.

Tissue Cell

Gen. Comp. Endocrinol.

Biochim. Biophys. Acta

J. Ultrastruct. Res.

J. Ultrastruct. Res.

J. Ultrastruct. Res.

J. Cell Biol.

J. Cell Biol.

J. Cell Sci.

J. Morphol.

J. Cell Biol.

C. R. Soc. Biol.

Ann. Biol. Anim. Bioch. Biophys.

J. Mar. Biol.

J. Biol. Phys. Biol. Chem. Cytol.

Amer. J. Anat.

J. Exp. Zool.

The Biology of Arthropoda

Arch. Biol. (Bruxelles)

Bull. Dep. Sea Shore Fish.

J. Cell Biol.

Biol. Reprod.