Detailed analysis of the male reproductive system in a potential bio-indicator species - The marine invertebrate Galeolaria caespitosa (Polychaeta: Serpulidae)

• Published in: PloS one 2017-04, Vol.12 (4), p.e0174907-e0174907
• Main Authors: Lu, Yonggang, Aitken, Robert John, Lin, Minjie
• Format: Article
• Language: English
• Subjects: Abdomen - anatomy & histology; Acidification; Animal reproductive organs; Animals; Arteries - anatomy & histology; Bioassays; Bioindicators; Biology and Life Sciences; Cell differentiation; Chemical analysis; Coastal environments; Compartments; Differentiation (biology); Embryos; Epithelial Cells - cytology; Epithelial Cells - ultrastructure; Epithelium; Gene expression; Genitalia, Male - anatomy & histology; Genitalia, Male - ultrastructure; Growth; Hazardous materials; Hazardous substances; Identification and classification; In vitro methods and tests; Indicator species; Intestines - anatomy & histology; Invertebrates; Laboratories; Life sciences; Male; Males; Marine invertebrates; Marine pollution; Medicine and Health Sciences; Microscopy, Electron, Scanning; Microscopy, Electron, Transmission; Morphology; Physiological aspects; Pollutants; Pollution indicators; Polychaeta; Polychaeta - anatomy & histology; Polychaeta - ultrastructure; Polychaetes; Reproductive system; Researchers; Seawater; Spawning; Sperm; Spermatocytes; Spermatogenesis; Spermatozoa; Spermatozoa - cytology; Spermatozoa - ultrastructure; Success; Vertebrates; Water analysis
• ISSN: 1932-6203; 1932-6203
• DOI: 10.1371/journal.pone.0174907

For the first time, this study has systemically investigated the male reproductive system in a sessile broadcast-spawning marine invertebrate, Galeolaria caespitosa (Polychaeta: Serpulidae), which has significant potential as a bio-indicator species of coastal marine pollution. The abdomen of G. caespitosa was divided by intersegmental septa into over 80 trunk segments. Each segment served as a germinal chamber with a C-shaped gonadal arrangement consisting of several distinct compartments: a seminiferous epithelium (SE) compartment located in the centre of the chamber, with each of its two ends connecting to a nurse cell (NC) compartment and then an efferent duct (ED) compartment. The SE compartment contained a multilayered seminiferous epithelium where spermatogenesis was initiated. Spermatids were released in pairs into the lumen of the SE compartment and then transported to the NC compartment where they underwent spermiogenesis with the support of secretory vesicles released by the nurse cells. Spermatozoa were stored in the ED compartment and subsequently released into the seawater through the vas deferens. Unlike vertebrates where germ cells differentiated in close proximity to the nurse cell population (i.e. Sertoli cells), the spermatogenic cells of G. caespitosa exhibited no direct contact with supporting cells at any spermatogenic stage. This finding suggested that the spermatogenesis in G. caespitosa was more dependent on intrinsic developmental programming than most species. Notwithstanding such differences, there were clear parallels between the male reproductive system of G. caespitosa and mammals, in terms of the structure and function. The independence of spermatogenic cells from supporting cells in G. caespitosa raised the possibility of inducing spermiogenesis in vitro, which would provide a useful tool to dissect the mechanisms underlying this complex cell differentiation process in invertebrates and other higher order animals.