Gestational morphogenesis of the uterine epithelium of the gummy shark (Mustelus antarcticus)

Abstract

Developing embryos of the non-placental, viviparous gummy shark (Mustelus antarcticus) are supplied with yolk from external and internal yolk sacs throughout the initial stages of gestation. Yolk supplies are exhausted by the 7th month of an 11-12 month gestation. During embryonic development, there is an approximate 800% gain in dry mass. These factors suggest nutrients are transferred from the mother to the young. The results of the present study provide some insights into how this is occurring. The uteri are paired and both are functional. Using both light and transmission electron microscopy, regions of the uterus were examined throughout maturation and gestation. The layers of the uterine wall throughout the entire length are similar to the uteri of other chondrichthyans previously examined. The uterine epithelium of the body of the uterus is smooth contoured, does not form villi, and undergoes cyclical and secretory changes throughout maturity and gestation. In immature uteri, the epithelium is simple columnar with minimal periodic acid-Schiff-positive and Alcian blue-positive secretory vesicles. In mature uteri, the epithelium is highly stratified with cuboidal cells containing numerous Alcian blue-positive and periodic acid-Schiff-positive vesicles. With pregnancy, prominent changes include a reduction in the number of cell layers, a reduction in cell size, a reduction in the connective tissue intervening between epithelium and blood vessel endothelium, and an increase in blood vessel number and size, so that at term, the uterine compartment consists of a single layer of squamous cells immediately underlain by sinusoidal-like blood vessels. These features along with a small number of secretory vesicles, dilated intercellular spaces, and clear transport vesicles suggest the transepithelial transfer of water and minerals from the maternal to embryonic environment, supplemented by minimal uterine secretions. This is defined as minimal histotrophy and this article represents the first detailed description of this reproductive mode.

Quantification of the maternal–embryonal nutritional relationship of elasmobranchs: case study of wobbegong sharks (genus Orectolobus)

“…A combination of methods, e.g. mass changes (present study; Guallart & Vicent, 2001), histology and electron microscopy of the uterus (Storrie et al , 2009), radio‐tracer assay (Riesch et al , 2010) and uterine fluid analysis (Kormanik, 1988) throughout gestation, is crucial to discern between these two reproductive modes and is the only way to confirm the production of histotroph.…”

Histological Remarks of the Uterus of Sympterygia acuta (Garman, 1877) and Sympterygia bonapartii (Müller & Henle, 1841) (Chondrichthyes; Rajidae)

“…As in all studied Chondrichthyes, each uterus independently joins a common urogenital sinus and it is common to find a sphincter-like muscular structure at the ends of the uterus of viviparous species (Galíndez et al, 2010b;Hamlett & Hysell;McMillan;Storrie et al, 2009). However, it seems to be no such structure limiting the uterine lumen in oviparous species, like S. acuta, S. bonapartii and R. asterias (Koob & Hamlett).…”

Atlantic Multidecadal Oscillation (AMO) and sea surface temperature in the Bay of Biscay and adjacent regions

“…On the contrary, any value higher than -20% (and naturally all weight gain) is considered matrotrophy (Hamlett et al, 2005;Storrie et al, 2009). On the contrary, any value higher than -20% (and naturally all weight gain) is considered matrotrophy (Hamlett et al, 2005;Storrie et al, 2009).…”