Social control of primary sex differentiation in the Midas cichlid.

Abstract

Sexual differentiation in teleost fishes is characteristically labile. The most dramatic form of sexual lability is postmaturational sex change, which is common among teleosts although rare In birds and mammals sex is determined at conception by a gene or genes residing on distinct sex chromosomes. Much research on other vertebrate taxa has been guided by the assumption that sex differentiation is initiated by similar genetic factors. An increased number of cases of environmental sex determination have been documented (1, 2), however, especially among reptiles (3-5). To date, studies of environmental sex determination in vertebrates have focused on the physical environment. In teleost fishes the social environment also plays an important role in sex differentiation (6), most notably in many sequential hermaphrodites in which size-mediated dominance interactions regulate sex change (7-9).The size-advantage model (10, 11) provides a functional explanation for this labile form of sex differentiation, based on a consideration of factors that could maximize lifetime fecundity. This model is particularly effective in accounting for postmaturational, protogynous sex change among teleosts in which a few large males can monopolize mating within a population. The model is less clear in its predictions about monogamous species. In this type of mating system, for reasons first elucidated by Fisher (12), we would expect selection for sex-determining mechanisms that would tend to generate 1:1 sex ratios. The surest mechanism would be a two-factor genetic system. However, postzygotic means of achieving this are also possible. Such a mechanism would be desirable if two conditions are met: (i) the size-fitness trajectories of the two sexes are sufficiently divergent; and (ii) size differences result from factors other than gender itself. We provide evidence for a postzygotic mechanism of sex determination in a monogamous fish, one in which social interactions play an important role.The publication costs of this article were defrayed in part by page charge payment. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. §1734 solely to indicate this fact.The Midas cichlid, Cichlasoma citrinellum, is monogamous and biparental (13). Within a cohort of Midas cichlids, as in many teleosts, pronounced variation in growth rate is apparent from an early age. The larger fish differentiate as males, and the smaller fish differentiate as females (14). A longitudinal study demonstrated that size ranks within a group are stable from an early juvenile stage through sexual maturity (14). Moreover, size ranges of males and females reared together overlap little. Because adult sex ratios in this species approximate 1.0 both in nature (13) and in the laboratory, the sex of a Midas cichlid can be reliably predicted from its relative size as a juvenile.In a typical group of siblings, juveniles above the median size rank differentiate as males; those below the median size rank differentiate as females. The...

Otolith-check formation and accelerated growth associated with sex change in an annual protogynous tropical fish

“…It is this growth-spurt that leads to males monopolising the largest size classes in the population. In contrast, the growth trajectories of males and females were found to diverge well before sex change in the coral trout Plectropomus maculatus (Adams & Williams 2001), and before female maturation in the freshwater cichlid Cichlasoma citrinellum (Francis & Barlow 1993). In these species, individuals that establish relatively superior growth early in life are the ones that change sex (Fig.…”

“…1). The second hypothesis, the 'juvenile growth hypothesis', states that sex-specific size-at-age differences are the result of growth trajectories established early in life (Francis & Barlow 1993, Adams & Williams 2001) (2 in Fig. 1).…”

Environmental Effects on Fish Sex Determination and Differentiation

“…A social control of sex determination has been evidenced in only 2 species, the paradise fish, Macropodus opercularis (Anabantidae) and the Midas cichlid, Amphilophus citrinellus [Francis, 1984[Francis, , 1990Francis and Barlow, 1993]. In the paradise fish, isolated individuals became male, whereas female proportion was correlated with density.…”

Sex-specific growth effects in protogynous hermaphrodites

“…There is increasing evidence that growth rates during the early life history can influence primary sex determination (Francis and Barlow 1993) and the expression of alternative male reproductive behaviours (Metcalfe et al 1989) in fishes. Early life history growth rates might also influence patterns of sex change in hermaphroditic species, especially where sex change is socially controlled and only the largest individual(s) in a social group or cohort change sex (Francis 1992).…”