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The reproductive system of Osedax (Annelida, Siboglinidae): ovary structure, sperm ultrastructure, and fertilization mode.

Katz S, Rouse GW - Invertebr. Biol. (2013)

Bottom Line: Transmission electron microscopy and fluorescence microscopy allowed detection of sperm associated with ovarian tissue of the female ovisac of four different Osedax species.A heart body was found in the circulatory system, as seen in other siboglinids and some other annelids.These morphological features provide new insights for comparing the regionalization of Osedax females in relation to other siboglinids.

View Article: PubMed Central - PubMed

Affiliation: Scripps Institution of Oceanography, University of California San Diego La Jolla, California, 92093-0202, USA.

ABSTRACT

Osedax is a genus of siboglinid annelids in which the females live on dead vertebrate bones on the seafloor. These females have a posterior end that lies within the bone and contains the ovarian tissue, as well as the "roots" involved with bone degradation and nutrition. The males are microscopic and live as "harems" in the lumen of the gelatinous tube that surrounds the female trunk, well away from the ovary. Females are known to spawn fertilized primary oocytes, suggesting internal fertilization. However, little is known about sperm transfer, sperm storage, or the location of fertilization, and the morphology of the female reproductive system has not been described and compared with the reproductive systems of other siboglinids. A 3D-reconstruction of the ovisac of Osedax showed ovarian tissue with multiple lobes and mature oocytes stored in a "uterus" before being released through the single oviduct. The oviduct emerges as a gonopore on the trunk and travels along the trunk to finally open to the seawater as a thin cylindrical tube among the crown of palps. Light and transmission electron microscopy of mature Osedax sperm revealed elongate heads consisting of a nucleus with helical grooves occupied by mitochondria. In contrast to other Siboglinidae, Osedax sperm are not packaged into spermatophores or spermatozeugmata, and Osedax females lack a discrete region for sperm storage. Transmission electron microscopy and fluorescence microscopy allowed detection of sperm associated with ovarian tissue of the female ovisac of four different Osedax species. This provides the first evidence for the site of internal fertilization in Osedax. A heart body was found in the circulatory system, as seen in other siboglinids and some other annelids. The possible presence of nephridia in the anterior ovisac region was also documented. These morphological features provide new insights for comparing the regionalization of Osedax females in relation to other siboglinids.

No MeSH data available.


AMIRA® reconstruction of ovisac region of Osedax frankpressi. A. 3D model of entire reconstructed ovisac region of O. frankpressi. B. Near sagittal section through 3D model of O. frankpressi ovisac region, showing oviduct in anterior ovisac that becomes the uterus region posteriorly before branching into ovarian ducts that go into the lobes of ovarian tissue. C. Dorso-lateral view of the ovisac region without the body wall, showing dorsal blood vessel and oviduct running in close association in the center and the ovarian tissue arranged in lobes on the periphery. Oocytes (yellow) are passing from the ovarian tissue to the ovarian ducts. D. Sagittal section through 3D model of O. frankpressi ovisac showing large dorsal vessel, oviduct running in close association with it and branching out as ovarian ducts to the ovarian lobes. Late vitellogenic or mature oocytes, scattered through the ovarian tissue, are collected into the ovarian ducts. E. Lateral view of the ovisac region of O. frankpressi showing reproductive structures only. Note the oviduct running in the center, ovarian ducts leading to the uterus, and the ovarian tissue arranged in lobes on the periphery. bw, body wall (light blue); dbv, dorsal blood vessel (red); ov, ovarian lobes (green); oc, oocytes (yellow); od, oviduct branching into the ovarian ducts (purple); vbv, ventral blood vessel (dark blue).
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fig05: AMIRA® reconstruction of ovisac region of Osedax frankpressi. A. 3D model of entire reconstructed ovisac region of O. frankpressi. B. Near sagittal section through 3D model of O. frankpressi ovisac region, showing oviduct in anterior ovisac that becomes the uterus region posteriorly before branching into ovarian ducts that go into the lobes of ovarian tissue. C. Dorso-lateral view of the ovisac region without the body wall, showing dorsal blood vessel and oviduct running in close association in the center and the ovarian tissue arranged in lobes on the periphery. Oocytes (yellow) are passing from the ovarian tissue to the ovarian ducts. D. Sagittal section through 3D model of O. frankpressi ovisac showing large dorsal vessel, oviduct running in close association with it and branching out as ovarian ducts to the ovarian lobes. Late vitellogenic or mature oocytes, scattered through the ovarian tissue, are collected into the ovarian ducts. E. Lateral view of the ovisac region of O. frankpressi showing reproductive structures only. Note the oviduct running in the center, ovarian ducts leading to the uterus, and the ovarian tissue arranged in lobes on the periphery. bw, body wall (light blue); dbv, dorsal blood vessel (red); ov, ovarian lobes (green); oc, oocytes (yellow); od, oviduct branching into the ovarian ducts (purple); vbv, ventral blood vessel (dark blue).

Mentions: The ovarian tissue lies in the coelom of the ovisac region and comprises a large proportion of the female body (Fig. 1D–F). Proliferative germinal epithelia are scattered throughout the ovisac resulting in several ovarian lobes (Figs. 1D–F, 2A). The discrete ovarian lobes were numerous, but could not be counted for this study (Figs. 1D–F, 2A). It is not clear if the ovarian tissue represents multiple ovaries or a single large ovary. The germinal epithelium inside each ovarian lobe grows toward the lumen, forming several stalks (Figs. 3C–E,G,I, 4A,B). Oocytes develop at the distal end of these stalks (Fig. 4A,B). As the oocytes mature, with thin follicle cells surrounding them, they show yolk droplets and increase in size (Fig. 4B,C). Mature oocytes lie at the distal end of the stalks and move into the ovarian ducts, which are present in each lobe (Fig. 3I,J). Each ovarian lobe is surrounded by peritoneal tissue and shows intermingling connective tissue (Fig. 3C–E). The short ovarian ducts are composed of a thick-walled, single cell-layered, nonciliated epithelium surrounded by musculature and embedded in connective tissue (Fig. 4D). The ovarian ducts lead to what we term here as a uterus, an enlarged, thin-walled proximal end portion of the terminal oviduct (Figs. 1D, 2A, 3E–J). The uterus is not surrounded by musculature and lacks cilia. The uterus holds mature oocytes that are likely to be already fertilized (Fig. 1D). From the uterus, the oocytes pass further along to a nonciliated part of the oviduct proper in the lower trunk (Figs. 2A,C,D 3E–J, 4A). As outlined above, the oviduct then emerges at the lower to upper trunk border (at what we interpret as the gonopore, see Discussion) and runs as the exterior oviduct, visible on the dorsal side of the upper trunk (Figs. 1A,B, 2D). The spatial relations of the ovarian lobes, the ovarian ducts, and the oviduct (including the uterus region) with each other, as well as their spatial relation with the dorsal and ventral blood vessels, are shown in a 3-D reconstruction (Fig. 5A–E). Different sagittal views from this reconstruction illustrate the branching system of the reproductive ducts (ovarian ducts, uterus, and oviduct) (Fig. 5B) and the wide dorsal blood vessel and the thinner ventral blood vessel running in close association with each other through the center of the ovisac (Fig. 5D). The female reproductive system only, with the vascular system removed, is shown in Fig. 5E. It resembles a bunch of grapes, with the ovarian lobes arranged on the periphery and the duct system, composed of the ovarian ducts, uterus, and oviduct in the center, corresponding to the stems of the grape cluster.


The reproductive system of Osedax (Annelida, Siboglinidae): ovary structure, sperm ultrastructure, and fertilization mode.

Katz S, Rouse GW - Invertebr. Biol. (2013)

AMIRA® reconstruction of ovisac region of Osedax frankpressi. A. 3D model of entire reconstructed ovisac region of O. frankpressi. B. Near sagittal section through 3D model of O. frankpressi ovisac region, showing oviduct in anterior ovisac that becomes the uterus region posteriorly before branching into ovarian ducts that go into the lobes of ovarian tissue. C. Dorso-lateral view of the ovisac region without the body wall, showing dorsal blood vessel and oviduct running in close association in the center and the ovarian tissue arranged in lobes on the periphery. Oocytes (yellow) are passing from the ovarian tissue to the ovarian ducts. D. Sagittal section through 3D model of O. frankpressi ovisac showing large dorsal vessel, oviduct running in close association with it and branching out as ovarian ducts to the ovarian lobes. Late vitellogenic or mature oocytes, scattered through the ovarian tissue, are collected into the ovarian ducts. E. Lateral view of the ovisac region of O. frankpressi showing reproductive structures only. Note the oviduct running in the center, ovarian ducts leading to the uterus, and the ovarian tissue arranged in lobes on the periphery. bw, body wall (light blue); dbv, dorsal blood vessel (red); ov, ovarian lobes (green); oc, oocytes (yellow); od, oviduct branching into the ovarian ducts (purple); vbv, ventral blood vessel (dark blue).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
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fig05: AMIRA® reconstruction of ovisac region of Osedax frankpressi. A. 3D model of entire reconstructed ovisac region of O. frankpressi. B. Near sagittal section through 3D model of O. frankpressi ovisac region, showing oviduct in anterior ovisac that becomes the uterus region posteriorly before branching into ovarian ducts that go into the lobes of ovarian tissue. C. Dorso-lateral view of the ovisac region without the body wall, showing dorsal blood vessel and oviduct running in close association in the center and the ovarian tissue arranged in lobes on the periphery. Oocytes (yellow) are passing from the ovarian tissue to the ovarian ducts. D. Sagittal section through 3D model of O. frankpressi ovisac showing large dorsal vessel, oviduct running in close association with it and branching out as ovarian ducts to the ovarian lobes. Late vitellogenic or mature oocytes, scattered through the ovarian tissue, are collected into the ovarian ducts. E. Lateral view of the ovisac region of O. frankpressi showing reproductive structures only. Note the oviduct running in the center, ovarian ducts leading to the uterus, and the ovarian tissue arranged in lobes on the periphery. bw, body wall (light blue); dbv, dorsal blood vessel (red); ov, ovarian lobes (green); oc, oocytes (yellow); od, oviduct branching into the ovarian ducts (purple); vbv, ventral blood vessel (dark blue).
Mentions: The ovarian tissue lies in the coelom of the ovisac region and comprises a large proportion of the female body (Fig. 1D–F). Proliferative germinal epithelia are scattered throughout the ovisac resulting in several ovarian lobes (Figs. 1D–F, 2A). The discrete ovarian lobes were numerous, but could not be counted for this study (Figs. 1D–F, 2A). It is not clear if the ovarian tissue represents multiple ovaries or a single large ovary. The germinal epithelium inside each ovarian lobe grows toward the lumen, forming several stalks (Figs. 3C–E,G,I, 4A,B). Oocytes develop at the distal end of these stalks (Fig. 4A,B). As the oocytes mature, with thin follicle cells surrounding them, they show yolk droplets and increase in size (Fig. 4B,C). Mature oocytes lie at the distal end of the stalks and move into the ovarian ducts, which are present in each lobe (Fig. 3I,J). Each ovarian lobe is surrounded by peritoneal tissue and shows intermingling connective tissue (Fig. 3C–E). The short ovarian ducts are composed of a thick-walled, single cell-layered, nonciliated epithelium surrounded by musculature and embedded in connective tissue (Fig. 4D). The ovarian ducts lead to what we term here as a uterus, an enlarged, thin-walled proximal end portion of the terminal oviduct (Figs. 1D, 2A, 3E–J). The uterus is not surrounded by musculature and lacks cilia. The uterus holds mature oocytes that are likely to be already fertilized (Fig. 1D). From the uterus, the oocytes pass further along to a nonciliated part of the oviduct proper in the lower trunk (Figs. 2A,C,D 3E–J, 4A). As outlined above, the oviduct then emerges at the lower to upper trunk border (at what we interpret as the gonopore, see Discussion) and runs as the exterior oviduct, visible on the dorsal side of the upper trunk (Figs. 1A,B, 2D). The spatial relations of the ovarian lobes, the ovarian ducts, and the oviduct (including the uterus region) with each other, as well as their spatial relation with the dorsal and ventral blood vessels, are shown in a 3-D reconstruction (Fig. 5A–E). Different sagittal views from this reconstruction illustrate the branching system of the reproductive ducts (ovarian ducts, uterus, and oviduct) (Fig. 5B) and the wide dorsal blood vessel and the thinner ventral blood vessel running in close association with each other through the center of the ovisac (Fig. 5D). The female reproductive system only, with the vascular system removed, is shown in Fig. 5E. It resembles a bunch of grapes, with the ovarian lobes arranged on the periphery and the duct system, composed of the ovarian ducts, uterus, and oviduct in the center, corresponding to the stems of the grape cluster.

Bottom Line: Transmission electron microscopy and fluorescence microscopy allowed detection of sperm associated with ovarian tissue of the female ovisac of four different Osedax species.A heart body was found in the circulatory system, as seen in other siboglinids and some other annelids.These morphological features provide new insights for comparing the regionalization of Osedax females in relation to other siboglinids.

View Article: PubMed Central - PubMed

Affiliation: Scripps Institution of Oceanography, University of California San Diego La Jolla, California, 92093-0202, USA.

ABSTRACT

Osedax is a genus of siboglinid annelids in which the females live on dead vertebrate bones on the seafloor. These females have a posterior end that lies within the bone and contains the ovarian tissue, as well as the "roots" involved with bone degradation and nutrition. The males are microscopic and live as "harems" in the lumen of the gelatinous tube that surrounds the female trunk, well away from the ovary. Females are known to spawn fertilized primary oocytes, suggesting internal fertilization. However, little is known about sperm transfer, sperm storage, or the location of fertilization, and the morphology of the female reproductive system has not been described and compared with the reproductive systems of other siboglinids. A 3D-reconstruction of the ovisac of Osedax showed ovarian tissue with multiple lobes and mature oocytes stored in a "uterus" before being released through the single oviduct. The oviduct emerges as a gonopore on the trunk and travels along the trunk to finally open to the seawater as a thin cylindrical tube among the crown of palps. Light and transmission electron microscopy of mature Osedax sperm revealed elongate heads consisting of a nucleus with helical grooves occupied by mitochondria. In contrast to other Siboglinidae, Osedax sperm are not packaged into spermatophores or spermatozeugmata, and Osedax females lack a discrete region for sperm storage. Transmission electron microscopy and fluorescence microscopy allowed detection of sperm associated with ovarian tissue of the female ovisac of four different Osedax species. This provides the first evidence for the site of internal fertilization in Osedax. A heart body was found in the circulatory system, as seen in other siboglinids and some other annelids. The possible presence of nephridia in the anterior ovisac region was also documented. These morphological features provide new insights for comparing the regionalization of Osedax females in relation to other siboglinids.

No MeSH data available.