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Reproductive System in the Male Phase of a Parasitic Isopod (Crustacea) - Morphological, Histological and Ultrastructural Evidence for Sequential Protandrous Hermaphroditic Changes

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Reproductive System in the Male Phase of a Parasitic Isopod (Crustacea) - Morphological, Histological and Ultrastructural Evidence for Sequential Protandrous Hermaphroditic Changes

Helna Ameri Kottarathil et al. Zool Stud.

Abstract

This paper reports the protandric hermaphroditic changes in the reproductive system of the male-phased Norileca indica, a cymothoid that parasitizes the scombrid fish Rastrelliger kanagurta. Each part of N. indica's paired reproductive system lies on either side of the gut. This study considers the three successive size classes of the male phase - designated as M1, M2 and M3 - using light microscopy and ultrastructural methods. The testis comprises of three bulged sac-like lobes labelled t1, t2 and t3, all of which open into the ovary of their respective side. The vas deferens, which emerges as a posterior extension of the ovary, opens into the penis and the distal end of each oviduct leads to a sealed gonopore on their respective sides. Each testis lobe (t1/t2/t3) displays clusters of germ cells undergoing stage-specific differentiation. Spermatids undergoing sequential changes associated with spermiogenesis keep close proximity to somatic accessory cells. The characteristic histological changes associated with protandric hermaphroditism are visible in the ovaries of sequential size classes (M1, M2 and M3). In early M1, besides spermatophores, the ovary has abundant polymorphic nuclei; in the mid/late M1, the posterior ovary has abundant spermatophores, anterior displayed oogonia, previtellogenic oocytes and two distinct forms of follicle cells. In M2, the anterior ovary shows compactly arranged oocytes while the posterior region accommodates spermatophores - fewer, however, than during M1. The entire ovary during M3 is crowded with previtellogenic oocytes, which marginalize the spermatophore passage. The vas deferens of the smallest M1 lack spermatophores. As the size class progresses through late M1 into M2 and M3, the posterior vas deferens is filled with spermatophores, which closely associate with the glandular epithelial lining.

Keywords: Male reproductive system; Norelica indica; Ovary; Protandric hermaphroditism; Spermatogenesis; Spermiogenesis; Testis.

Figures

Fig. 1.
Fig. 1.
Fig. 1. Norileca indica and its protandrous hermaphroditic reproductive system. A. Norileca indica – male; B. paired structure of gonad (20 X); C-E. Gonad in different male stages (C: M1, D: M2, E: M3) (40 X); F. testes lobes showing different staged cells and germarium. t1, t2, t3- testis lobes 1-3, o- ovary, od- oviduct, vd- vas deferens, avd- anterior vas deferens, pvd- posterior vas deferens, Oo- oocytes, sp- spermatophore, ag- androgenic gland.
Fig. 2.
Fig. 2.
Fig. 2. Norileca indica – hermaphroditic gonad in male stages. A. anterior gonad showing the connection between the testis lobes and the ovary (200 X); B. testis (M1) showing spermatogonia (1000 X); C. testis (M2) showing spermatocytes at equatorial plate forming stage of meiosis and somatic accessory cells (1000 X); D. spermatocytes at different meiotic stages (1000 X) (semithin LS: 1 μm; Methylene blue). Testes showing E. regionalization of germ cells undergoing spermatogenesis and spermiogenesis (M3) (200 X); F. spermiogenesis (arrow showing elongation of spermatid nucleus) (1000 X); G. somatic accessory cell types (1000 X); H. somatic accessory cell, spermatophores and spermatozoa (400 X). t1, t2, t3 - testis lobes 1-3, Oo- oocyte, w- wall, psg- primary spermatogonia, ssg- secondary spermatogonia, sc- spermatocyte, sac- somatic accessory cell, o- ovary, fc- follicle cell, sac- somatic accessory cell, sd- spermatid, sc- spermatocyte, n- nucleus, sp- spermatophore, s- spermatozoa, sac 1, sac 2, sac 3 - somatic accessory cell types 1-3, w- wall, M- muscle.
Fig. 3.
Fig. 3.
Fig. 3. Histological section of testicular lobes (t1, t2, t3) of male N. indica (LS: 3 μm, Haematoxylin-Eosin) depicting asynchrony in spermatogenesis (1000 X) A. t1 showing spermatocytes and spermatophores; B. t1 showing the association between spermatophores and somatic accessory cells; C. t2 showing spermatocytes at pachytene stage and spermatogonia; D. t3 showing spermatocytes at equatorial plate forming stage of meiosis (arrow), spermatid and somatic accessory cells. sp - spermatophore, sc- spermatocytes, sac- somatic accessory cells, sg- spermatogonia, sd- spermatid.
Fig. 4.
Fig. 4.
Fig. 4. N. indica male A. spermatophores (unstained) (100 X); B. methylene blue stained single spermatophore (200 X); C. spermatophore heads showing positivity to methylene blue (1000 X); D. spermatophore (unstained) (1000 X); E. spermatozoon showing distinct nucleus, acrosome and tail (1000 X); F. spermatophores (Haematoxylin-Eosin) (400 X); G. spermatophore heads showing positivity to basic fuchsin (1000 X); H. spermatophore showing positivity to bromophenol blue (1000 X); I. spermatophore heads showing positivity to Sudan Black (1000 X). sp- spermatophore, t- tail, a- acrosome, n- nucleus, h- head.
Fig. 5.
Fig. 5.
Fig. 5. Electron micrographs of testis in male stage of N. indica showing A. spermatocyte (arrow) at meiotic stage (equatorial plate formation) (2900 X), B. somatic accessory cells (2900 X), C extracellular tubules and nuclei of spermatozoa (6800 X), D. tails of spermatozoa showing striations and central lumen (13000 X), E. clustered spermatophore tails (13000 X), F. spermatophore associated with somatic accessory cells (4800 X), G. somatic accessory cell cytoplasm showing cell organelles (30000 X), H. head of spermatozoon (13000 X). sac- somatic accessory cell, sc- spermatocyte, c- somatic accessory cell cytoplasm, n- somatic accessory cell nucleus, n- somatic accessory cell nucleus, t- spermatophore tail, ts- transverse striations, m- mitochondria, RER- Rough endoplasmic reticulum, l- lumen, n- nucleus, l- lumen, h- head, cr- chromatin, ect- extracellular tubules, a- acrosome.
Fig. 6.
Fig. 6.
Fig. 6. Histology of ovary in male stages (M1, M2, M3). A. prestaged M1 ovary B. M1 ovary.
Fig. 7.
Fig. 7.
Fig. 7. Histological and histochemical observation of ovarian germ cells and oocytes (N. indica) during male phase of N. indica. (LS: 4 μm; Haematoxylin-Eosin; 1000 X) A. germ cells (in M1); B. spermatophore and germ cells (in M1); C. follicle cells enveloping the oocytes (in M2); D. oocytes (in late M3); semithin LS: 1 μm; methylene blue showing E. spermatophores (M1) (400 X); F. follicle cells, previtellogenic oocytes and spermatophores (M2 1000 X); G. bulged ovarian wall (arrow) (400 X); H. ovarian wall showing involution (M2) (arrow) (400 X). g- germ cells, sp- spermatophore, Oo- oocytes, fc- follicle cells. sp- spermatophore, t- tail, Oo- oocytes, fc1- follicle cell type 1, fc2- follicle cell type 2, n- nucleus, s- sperm, w- wall.
Fig. 8.
Fig. 8.
Fig. 8. Electron micrographs of ovary during male stages of N. indica A. previtellogenic oocytes associated with follicle cells (1900 X); B. previtellogenic oocytes showing ribosome associated nuclear membrane (6800 X); C. different types of follicle cells (1900 X); D. follicle cell cytoplasm showing RER and protruded plasma membrane (arrow) (23000 X); E. follicle cell cytoplasmic vesicle fused with the plasma membrane (23000 X); F. Wall of the ovary at male stage. Oo- oocytes, fc- follicle cell, n- nucleus, nl- nucleolus, r- ribosomes, m- mitochondria, nm- nuclear membrane, ol- oolemma fc1- follicle cell type 1, fc2- follicle cell type 2, n- follicle cell nucleus, c- follicle cell cytoplasm, sv- secretory vesicle, g- golgi.
Fig. 9.
Fig. 9.
Fig. 9. Vas deferens of male staged N. indica showing A. spermatophores and secretory epithelial wall (CS: 3 μm; Haematoxylin-Eosin) (1000 X), B. spermatophores (LS: 3 μm; Haematoxylin-Eosin) (400 X), C. association of spermatophore tails with the secretory epithelial layer (1000 X) (inset- enlarged view); semithin section D. (1000 X) and electron micrograph E. showing concentric layered fibrous tissue associated with the wall of the vas deferens (arrow) (1400 X). F. Oviduct. sp- spermatophore, t- tail, Oo- oocytes, t1- type 1 epithelial cell, t2- type 2 epithelial cell, n- epithelial cell nucleus, w- epithelial wall.

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