Ecology meets endocrinology: environmental sex determination in fishes

Van Valen (1973) characterized evolution as the control of development by ecology. Sex determination in fishes provides some clear examples of this “control” in operation. Teleost fishes show a remarkable variety of sex determination and differentiation patterns. These range from systems in which sex is determined by sex chromosomes, as in birds and mammals, to simultaneous hermaphrodites that alternate spawning as a female and male on a second to second basis. This extraordinary flexibility may result from a combined lack of developmental constraint on reproductive structures in many lineages and selection for sexual lability in the face of environmental unpredictability. This review addresses environmental influences on sex determination and differentiation in fishes. There is a variety of documented environmental influences on sex determination (ESD) in fishes. We focus here on two classes of examples where the key environmental cues are of clear ecological relevance, the effects appear especially likely to be important as a normal part of the life history, and where there is evidence suggesting the sexual patterns observed represent adaptations that increase individual fitness. These classes are sex determination that is controlled by social interactions (behavioral sex determination [BSD]) (Crews 1993) and temperaturedependent sex determination (TSD). Sex determination controlled by social influences can occur before or after sexual maturation but appears to maximize the expected reproductive success of individuals in both cases. Here we first address BSD and then TSD in fishes. For each pattern of sex determination, we discuss selection pressures that appear to favor these patterns, examples of each, and what is known regarding the underlying physiological mechanisms. For more comprehensive and general reviews of patterns and mechanisms of sex determination in fishes, the reader is referred to several excellent reviews (Nakamura et al. 1998; Baroiller et al. 1999; Baroiller and D’Cotta 2001; Piferrer 2001). The major focus in studies of physiological mediation of teleost sex determination is what is referred to by endocrinologists as the hypothalamo-pituitary-gonadal (HPG) axis (Fig. 1). This axis consists primarily of hypothalamic neurosecretory neurons producing gonadotropin-releasing hormone (GnRH), gonadotropins produced in and released from the pituitary gland (GtH I and GtH II), and the gonad as the major site of steroid biosynthesis with its steroid metabolizing enzymes, steroid hormone receptors, and a variety of other proteins that mediate steroid hormone action. One steroid biosynthetic enzyme that has been a particularly fruitful focus in correlative and manipulative studies of vertebrate sex determination is cytochrome P-450 aromatase. This enzyme catalyzes the conversion of androgens to estrogens (primarily testosterone to estradiol-17 ). Aromatase expression correlates with female determination in a variety of vertebrates, and aromatasespecific antagonists can block female development in fishes, amphibians, reptiles, and birds (Elbrecht and Smith 1992; Lance and Bogart 1992; Crews et al. 1994; Wennstrom and Crews 1995; Kitano et al. 1999; D’Cotta et al. 2001). Estradiol-17 plays a central role in female reproductive physiology in fishes, whereas the androgen 11-ketotestosterone (11-KT) is crucial to gamete maturation and the expression of secondary sexual characteristics in males (Borg 1994; Brantley et al. 1993). Importantly, testosterone levels often do not differ between male and female fishes or are higher in females (Borg 1994). Because of the central role of aromatase in the biosynthesis of estrogens, it will be a focus in consideration of mechanisms by which environmental information leads to sex determination responses. More generally, our understanding of vertebrate sexual function indicates the HPG axis plays the key role in transducing environmental information into gonadal determination, differentiation, and maturation events. A general theme of this review is where and how this transduction may occur in the HPG axis.