Sex Steroid Metabolism in the Antarctic Pteropod Clione antarctica (Mollusca: Gastropoda)

Abstract

The ability of the antarctic pteropod Clione antarctica (Mollusca: Gastropoda) to synthesize sex from radiolabeled steroids from radiolabeled steroid precursors was examined in individuals sampled near the end of their observed reproductive season from McMurdo Sound, Antarctica. The precursors, 3H-progesterone and 3H-androstenedione, were absorbed and subsequently metabolized to produce several progestin and androgen metabolites, including 5a-pregnane-3,20dione, 3p-hydroxy-5oL-pregnan-20-one, 3 3-hydroxy-4-pregnen-20-one, 5o-androstane-3,17-dione, 3 B-hydroxy-5x-androstan-17-one (androsterone), and 3p3-hydroxy-5a-androstan-17-one (epiandrosterone). Synthesis or accumulation of testosterone and estradiol was not observed. At least 2 unidentified, water-soluble progestin metabolites were synthesized, as well as an unidentified esterified steroid. The metabolic accumulation of these steroidal compounds indicates that C. antarctica can produce potentially bioactive steroids. The activity of steroid metabolic enzymes in a polar species further indicates the universal capacity of invertebrates from various geographic regions to metabolize biologically relevant steroids. Additional key words: androgen, progesterone, invertebrate, polar, endocrinology The potential for endocrine regulation of physiological processes within the Mollusca was recognized several decades ago with classic ablation experiments conducted on the cephalopod Octopus vulgaris. These studies demonstrated the dependency of gonadal development on neuroendocrine signals from the optic glands (Wells & Wells 1959; Wells 1960). Further studies noted the involvement of several organs (particularly the optic tentacles, brain, and gonads) and certain neuronal peptides in the regulation of specific physiological processes such as ovulation (Geraerts et al. 1983), vitellogenesis (Geraerts & Joosse 1975), and growth and differentiation (Feral et al. 1987) in molluscs. The majority of reports on molluscan endocrinology have been concerned with neuroendocrine aspects (reviewed by Joosse 1979). The role of other (potentially) endocrine components such as the sex steroids has not been examined extensively. Early investigations of the giant land slug Ariolimax californicus (see Lehoux & Sandor 1970) revealed the presence of steroids and steroid metabolizing enzymes, suggesting that a class of vertebrate hormones was present in representatives of the Mollusca. Subsequent reports noted the presence of sex steroids (progestins, androgens, and estrogens) in at least three molluscan aTo whom correspondence should be addressed. classes: cephalopods (Carreau & Drosdowsky 1977), pelecypods (De Longcamp et al. 1974; Reis-Henriques & Coimbra 1990), and gastropods (De Jong-Brink et al. 1981; Le Guellec et al. 1987). Variations in the quantity and quality of these steroids were correlated with reproduction, growth, and development, suggesting that steroids are regulators of physiological processes in molluscs. Pteropods are pelagic opisthobranch gastropods and are divided into two orders, thecosomes and gymnosomes. Thecosomatous pteropods possess a shell, feed on algae, and are often protandrous hermaphrodites. In contrast, gymnosomatous pteropods lack a shell, feed exclusively on thecosomatous pteropods, and may occur as simultaneous hermaphrodites (Lalli & Gilmer 1989). Clione antarctica (SMITH 1902), a gymnosomatous pteropod, has a circumpolar distribution around Antarctica (Gilmer & Lalli 1990). Reports concerning the reproductive physiology of C. antarctica are limited to a description of the simultaneous hermaphroditic condition of mature individuals (Lalli & Gilmer 1989) and field observations on mate attraction and copulation (M. Slattery, pers. comm.). The long term goals of this study are to evaluate the endocrine regulation of behavior and reproduction in antarctic pteropods. In this paper we report the ability of C. antarctica to metabolize C21 (progesterone) and C19 (androstenedione) steroids. This content downloaded from 207.46.13.50 on Sat, 09 Apr 2016 06:47:22 UTC All use subject to http://about.jstor.org/terms Hines, Bryan, Wasson, McClintock, & Watts