Abstract
Simultaneous or functional hermaphrodites possessing both ovary and testis at the same time are good materials for studying sexual development. However, previous research on sex determination and differentiation was mainly conducted in gonochoristic species and studies on simultaneous hermaphrodites are still limited. In this study, we conducted a combined morphological, endocrine and molecular study on the gonadal development of a hermaphroditic scallop Argopecten irradians aged 2–10 month old. Morphological analysis showed that sex differentiation occurred at 6 months of age. By examining the dynamic changes of progesterone, testosterone and estradiol, we found testosterone and estradiol were significantly different between the ovaries and testes almost throughout the whole process, suggesting the two hormones may be involved in scallop sex differentiation. In addition, we identified two critical sex-related genes FoxL2 and Dmrt1L, and investigated their spatiotemporal expression patterns. Results showed that FoxL2 and Dmrt1L were female- and male-biased, respectively, and mainly localized in the germ cells and follicular cells, indicating their feasibility as molecular markers for early identification of sex. Further analysis on the changes of FoxL2 and Dmrt1L expression in juveniles showed that significant sexual dimorphic expression of FoxL2 occurred at 2 months of age, earlier than that of Dmrt1L. Moreover, FoxL2 expression was significantly correlated with estradiol/testosterone ratio (E2/T). All these results indicated that molecular sex differentiation occurs earlier than morphological sex differentiation, and FoxL2 may be a key driver that functions through regulating sex steroid hormones in the scallop. This study will deepen our understanding of the molecular mechanism underlying sex differentiation and development in spiralians.
Highlights
We found sexual dimorphic expression of FoxL2 occurred earlier than Dmrt1L, suggesting that FoxL2 may be the key driving factor of sex differentiation in A. irradians, and further research on the molecular mechanism underlying sex differentiation should be conducted in 2-month-old or even younger individuals
We found significantly higher levels of testosterone and lower levels of estradiol in the testes than in the ovaries almost during the whole developmental process in A. irradians, suggesting the two hormones likely participate in sex differentiation and subsequent gametogenesis
The expression of FoxL2 was significantly correlated with E2/T, suggesting FoxL2 may function by regulating the enzyme that converts androgen to estrogen
Summary
Sexual reproduction has long been the focus of research in the life sciences, and extensive research has been carried out in various taxa, such as mammals (Sinclair et al, 1990; Warr and Greenfield, 2012; Andersen et al, 2017), birds (Smith et al, 2009; Wang et al, 2017), fishes (Sandra and Norma, 2003; Parzefall et al, 2008; Desjardins and Fernald, 2009), and insects (Hales et al, 2002; Sexual Development of a Hermaphroditic ScallopErickson and Quintero, 2008). Sex is genetically determined by the gene on the sex chromosome, which in turn activates downstream genes or pathways for sex differentiation and maintenance. In mammals, sex is determined by the SRY gene on the Y chromosome, which activates SOX9 and inhibits female pathway. Mollusca represents the second largest phylum of invertebrates after Arthropoda. It contains several subgroups, including cephalopods, gastropods, bivalves, monoplacophorans, etc. These animals exhibit a diversity of sexual systems, including gonochorism, simultaneous hermaphroditism, and sequential hermaphroditism (Collin, 2013). There is a great potential for understanding the molecular mechanisms underlying gonochorism and hermaphroditism within bivalvia or gastropoda
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