Effect of temperature, food availability, and estradiol injection on gametogenesis and gender in the pearl oyster Pinctada margaritifera

Abstract

The black-lip pearl oyster Pinctada margaritifera is a protandrous hermaphrodite species. Its economic value has led to the development of controlled hatchery reproduction techniques, although many aspects remain to be optimized. In order to understand reproductive mechanisms and their controlling factors, two independent experiments were designed to test hypotheses of gametogenesis and sex ratio control by environmental and hormonal factors. In one, pearl oysters were exposed under controlled conditions at different combinations of temperature (24 and 28°C) and food level (10,000 and 40,000 cells mL(-1) ); whereas in the other, pearl oysters were conditioned under natural conditions into the lagoon and subjected to successive 17β-estradiol injections (100 μg per injection). Gametogenesis and sex ratio were assessed by histology for each treatment. In parallel, mRNA expressions of nine marker genes of the sexual pathway (pmarg-foxl2, pmarg-c43476, pmarg-c45042, pmarg-c19309, pmarg-c54338, pmarg-vit6, pmarg-zglp1, pmarg-dmrt, and pmarg-fem1-like) were investigated. Maximum maturation was observed in the treatment combining the highest temperature (28°C) and the highest microalgae concentration (40,000 cells mL(-1) ), where the female sex tended to be maintained. Injection of 17β-estradiol induced a significant increase of undetermined stage proportion 2 weeks after the final injection. These results suggest that gametogenesis and gender in adult pearl oysters can be controlled by environmental factors and estrogens. While there were no significant effects on relative gene expression, the 3-gene-pair expression ratio model of the sexual pathway of P. margaritifera, suggest a probable dominance of genetic sex determinism without excluding a mixed sex determination mode (genetic + environmental). J. Exp. Zool. 325A:13-24, 2016. © 2015 Wiley Periodicals, Inc.

Population Connectivity and Genetic Assessment of Exploited and Natural Populations of Pearl Oysters within a French Polynesian Atoll Lagoon

“…Recently, concerns have been raised about common pearl farming practices that affect the global sex ratio of the exploited population [4,9]. P. margaritifera is a protandrous hermaphrodite, all oysters are male during the first two years of their life and slowly transition to the female sex, from which they will be able to go back and forth (multiple changes from female to male and male to female for a given individual) according to environmental conditions [10]. Globally, a cohort will contain 0% females at one year of age, 27% females at 6 years of age and 41% past 8 years of age [11].…”

Sex Determining Mechanisms in Bivalves

“…Their results showed a significant effect on sex ratio for oysters conditioned at high temperature and low food concentration with a significant proportion of females (50%) changing to males under those conditions (Teaniniuraitemoana et al 2016). The authors invoked an energetic deficit as the potential cause of the female-to-male sex change; they specifically argued that the increase in oxygen consumption and metabolic rate at high temperature depleted the energetic reserves required for the production of female gametes, which is hypothesized to be more energetically costly than the production of male gametes in mollusc species (Russell-Hunter 1979).…”

“…Owing to their importance in aquaculture and fisheries, the interest in bivalve genomics and transcriptomics to identify the genes involved in reproduction, sex differentiation and sex determination processes has significantly increased in recent years (e. Teaniniuraitemoana et al 2014Teaniniuraitemoana et al , 2016. However, because this is beyond the scope and goals of the present review, studies relating genes involved in reproduction or in later steps during sexual differentiation are not discussed.…”

“…Following the discovery of a role of sex hormones in the hormonal regulation of bivalve reproduction (Mackie 1984; Chávez-Villalba et al 2011; Teaniniuraitemoana et al 2016), a role that was suggested to be similar to that in vertebrate endocrine systems, several studies have attempted to control the reproductive state of cultured bivalves using exogenous steroids (see Croll and Wang 2007 for a review). However, only a small number of these studies demonstrated that the sex of bivalves can be affected by steroid hormones (i.e., by the demonstration of sex reversal of adult individuals) and none of them explored the underlying mechanisms (Table 1).…”

“…Similar patterns have also been demonstrated in laboratory reared and natural populations of Pacific oysters (Lango-Reynoso 1999; Chávez-Villalba et al 2011); i.e., a sex ratio in favor of females was noted when food availability conditions were favorable. Apparently, any situation that lowers body nutrient reserves and/or food intake (e.g., removal of gills, starvation, parasitic infections), always leads to a rise in the percentage of males in populations of bivalves capable of changing sex (Amemiya 1935 Teaniniuraitemoana et al (2016) also suggested that there is a mixed sex determination system in P. margaritifera that involves both genetic and environmental factors. However, because the latter work focused on sex change in adults, additional studies will need to be conducted on juvenile spat before expression of first signs of gonadic differentiation.…”