Annual cycles in levels of pituitary and plasma gonadotropin, gonadal steroids, and thyroid activity in the Chinese cobra ( Naja naja)

Abstract

Adult Chinese cobras, Naja naja, were purchased monthly from a snake dealer in Hong Kong (6–8 animals per month for each sex, total of 290 snakes) and sacrificed after 1 day of acclimation in the laboratory. Pituitary and plasma gonadotropin (Gn), plasma thyroxine (T 4), sex steroids in plasma and testes, and ovarian Gn binding were examined in relation to the annual reproductive cycle. Changes in plasma Gn did not always correspond to pituitary Gn content, and a marked annual cycle in plasma T 4 was evident, despite a lack of change in thyroid weight or epithelial cell height. Although Gn levels were generally elevated during the reproductive season, gonadal activity did not always show the expected relationship to plasma Gn levels. In males, a winter peak in plasma Gn occurred despite low pituitary content; this increase in the plasma coincided with the initiation of testis growth. However, in summer, the testes showed full regression in weight, spermatogenesis, and testosterone (T) secretion, almost 2 months before a decline in plasma Gn was evident. Increased plasma T 4 might be implicated in this apparent dissociation between testis function and circulating Gn levels. Both plasma and testicular T increased only at the time of maximum testicular weight; they did not show the expected increase at the time when spermatogenesis was initiated. In females, plasma Gn showed a bimodal annual cycle but ovarian activity was compressed into a single relatively brief period of about 2 months in spring. A pronounced winter rise in plasma Gn, despite low pituitary Gn levels, was not reflected in detectable ovarian changes. Increases in plasma estradiol (E) and T occurred during the vitellogenic phase; plasma E dropped rapidly after ovulation, but T remained partially elevated until after oviposition. In contrast, plasma progesterone (PRO) did not rise until after ovulation; it then remained fully elevated until after oviposition. Thus, both T and PRO levels along with high Gn binding indicated that the corpora lutea remain functional until oviposition occurs. Steroid levels were reduced to baseline values in animals with atretic follicles. Plasma and pituitary Gn rose during the vitellogenic period and remained elevated until oviposition. Unlike the male, plasma T 4 levels were maximal during the active reproductive period (vitellogenesis and ovulation). The ability of ovarian tissues to bind radiolabeled gonadotropin was lowest in the previtellogenic stages, especially when plasma Gn was highest. Corpora atretica also had significantly reduced binding. We postulate that the ovarian cycle of this snake represents a progressive differentiation in the functional state of the ovary which is induced by relatively constant high levels of a single gonadotropin; thus, functional transitions in ovarian tissue rather than alterations in the nature or concentration of gonadotropins in the circulation are responsible for the changing pattern of ovarian steroid secretion.