Environmental Btology of Fishes 29: 81-93, 1990.

01990 Kluwer Academic Publishers. Printed in the Netherlands

The evolution of sex-change mechanisms in fishes

Robert M. Ross National Fish'fry Research and Development Laboratory, R.D.# 4, Box 63, Wellsboro, PA 16901, U.S.A.
Received 27.3.1989 Accepted 17.10.1989

Key words: Dominance hierarchy, Group size, Hermaphroditism, Mating system, Polygamy potential, Protandry, Protogyny, Sex ratio, Size ratio, Teleostei
Synopsis

Five distinct sex-change mechanisms are identified among sequentially hermaphroditic fishes based on socio-ecologicalcharacteristics. The primary determinants of the sex-change mechanisms appear to be social organization and mating system, which in turn depend on resource distribution in space and time. The ability of a single imdividual to control all mating in the social unit, which is related to the size of the social unit, differentiates three suppression mechanisms from two induction mechanisms. Sex-change suppression, which is characteristic of species with small group size and rigid dominance hierarchies, refers to inevitable sex change in the absence of group dominance. Ability to migrate between resource patches differentiates protogynous suppression (e.g. in Labroides dimidiatus) from protandrous suppression (e.g. in Amphiprion spp.). Early sex change appears to have evolved from protogynous suppression under special conditions involving the loss of mating control by a single dominant individual in certain species (e.g. Centropyge spp.). Sex-change induction, which is characteristic of species with large social groups lacking rigid dominance hierarchies, refers to the requirement that sex change must be induced by specific characteristics of (or changes in) the social group, regardless of dominance status. Ability to distinguish sex, or its importance, differentiates sex-ratio induction (e.g. Anthias squamipinnis) from size-ratio induction (e.g. Thalassoma spp.). Alternative models account for the possibility that all cases of sex change require stimulation from smaller conspecifics (universal induction-inhibition model) or that all fish have the genetic capacity to switch mechanisms. depending on changing ecological conditions and resulting changes in mating system (behavioral-scaling model). Neurophysiological models suggest that induction mechanisms, which require at least two categories of environmental stimuli, may have evolved from the simpler suppression mechanisms, which require only one kind of input from the environment.

Introduction

Hermaphroditism may be defined as the presence of both sex functions at some time during the life of an individual. Among teleost fishes, hermaphroditism occurs rather commonly in diverse taxa. An understanding of the biology of hermaphroditism in fishes has grown considerably since the initial descriptive work of Essenberg (1926), van Oordt

(1933), Kinoshita (1936), and others. Although neuroendocrine pathways have not been adequately identified in any species, investigators are beginning to understand some of the important control processes at higher levels of organization. Recent experimental analyses have moved the frontier of research to a point where the integration of neuroendocrine, behavioral, and ecological knowledge will soon be profitable.

Sequential hermaphroditism, or sex change, is also a common phenomenon among fishes. Many species from at least 14 families are known to be protogynous (female to male) hermaphrodites, and various species from at least eight families are protandrous (male to female) hermaphrodites (Warner 1978, 1984). The irreversibility of sex change, once it is completed, in all species investigated (Reinboth 1980) suggests that there are physiological, developmental, or perhaps even socioecological constraints on sexual lability. Many studies have shown that ecological variables play an important role in determining the type of social organization and mating system an animal exhibits. For example, the distribution and predictability of resources, including mates, directly affect the mating strategies of animals (Emlen & Oring 1977, Fricke 1980, Jones 1981). In this paper I review the importance of ecological factors in sequentially hermaphroditic species and argue that social and mating systems in turn determine the mechanism of sex change in those species. My thesis in this beginning effort to develop a comprehensive theory of sex change is that, given a set of ecological conditions and social organization, one can predict whether sex change is likely in a given fish species, and further, by what general mechanism the process of sex change will proceed. I start by describing a model with two fundamentally different processes from which five distinct mechanisms of sex change are identified. I then describe testable alternative models which account for observations not consistent with the first model.

sion of sex change in protandrous species; i.e., a male in the group is suppressed from changing to female. In protogynous suppression a female fish is suppressed from changing into a male in a protogynous species. Early sex change has been used to describe sex change in a subdominant member of a social group with clear dominance relationships, but without the loss or removal of the dominant fish. Described only in protogynous species, it frequently results in the occurrence of 'bachelor' males without immediate mating status. Unfortunately, the term 'early sex change' connotes an aberrant or mal-adaptive condition, which is not the case (see below). Sex-change induction refers to a condition wherein sex change does not automatically occur when dominant or larger members of a group are lost or removed. Rather sex change must be induced by specific stimuli, social characteristics, or behavioral events. Sex-ratio induction refers to sex change caused by a change in the sex ratio of a social group through recruitment or mortality. Normally the largest single initial-sex individual changes sex, returning the group sex ratio to a sub-threshold value. In size-ratio induction, the relative-size ratio of a group, rather than the group sex ratio, is a cue for sex change. When a threshold ratio of the number of fish smaller than the sexchange candidate to the number of fish larger than the sex-change candidate in a social group is exceeded, a fish changes sex.

Ecological correlates of the sex-change mechanisms

Suppression versus induction model

Definitions of sex-change mechanisms Sex-change suppression occurs when one or more members of a social group prevent sex change in a candidate fish, normally through aggressive dominance. Sex change is initiated or completed only when the suppression condition is removed (disinhibition), normally when the single dominant terminal-sex individual dies or vacates the social group. Protandrous suppression refers to suppres-

Non-permeable social groups In this discussion I define social group or social unit as the set of conspecifics with which a given individual interacts routinely and repeatedly each day. Wilson (1975) further defines 'non-permeable' social groups as those that communicate little with nearby groups and seldom if ever accept adult immigrants. For reasons I discuss later, sex-changing fishes characterized by both the suppression mechanisms and early sex change live in small, nonpermeable social groups. Resource distribution can directly or indirectly

affect the size of a social group (Schoener 1971, Wilson 1975). For example, the protandrous anemonefishes (pomacentrids of the genus Amphiprion) are obligate commensals of sea anemones on Indo-Pacific coral reefs (Mariscal 1966, Allen 1972). Became of the low population densities and unpredictable distributions of sea anemones on many reefs, anemonefishes are unable to migrate between host anemones (Eibl-Eibesfeldt 1960, Mariscal 1970, Fricke & Fricke 1977). As a result, social groups of anemonefishes are also discontinuously distributed over reef habitats. Because anemones or anemone colonies are typically small (Allen 1972, Ross 1978b), the social groups of anemonefish are also small (usually a half-dozen or fewer individuals and only a single pair of adults). Such small, discontinuously distributed social groups may be described as 'non-permeable'. The predicted mating system given the abovenamed socio-ecological variables would be monogamy, because such conditions do not permit the acquisition o F multiple mates by individuals within social groups. Indeed, most anemonefishes are monogamous (Fricke & Fricke 1977, Moyer & Nakazono 1978b, Ross 1978a), though an exception has been described by both Moyer (1980) and Yanagisawa & Ochi (1986) wherein frequent, lengthy migration betwizen anemones does occur in Japanese populations of A. clarkii. Predictably, that species is sexually dlichromatic and occasionally polygamous, because some degree of competition for and acquisition of multiple mates is possible in those populations. Small, non-permeable social units also occur in protogynous cleaner wrasses, Labroides dimidiatus (Labridae), but for different reasons than in anemonefishes. Female cleaner wrasses use food resources (tissues of host fishes or their ectoparasites) that occur at fixed, predictable locations ('cleaning stations') that are apparently limiting (Robertson & Hoffman 1977). The food source may have led to permanent territoriality, enabling males to establish harems because of the lack of alternative feeding sites (and hence mobility) for females. Kuwamura (1984), however, suggested that female cleaner wrasses do not defend feeding sites, but rather merely establish dominance rela-

tionships in a given area. Regardless of the type of polygyny that occurs, the critical ecological factor is the predictability of location of resources (cleaning stations) and thus females (one per station). Group size is limited to the number of females a male can successfully interact and mate with, usually a half-dozen or fewer (Robertson 1972). Many protogynous angelfishes (genera Holacanthus and Centropyge) also live in small harems (Moyer et al. 1983, Thresher 1984). Such maledominated harems may be classified in terms of mating system as female-defense polygyny (Emlen & Oring 1977), although Moyer (1987) identified the Centropyge system as resource-defense polygyny. All anemonefish colonies as well as harems of cleaner wrasses and angelfishes are small and characterized by rigid dominance hierarchies (Robertson 1972, Fricke & Fricke 1977, Moyer & Nakazono 1978b; other references in Table 1). Permeable social groups Sex-changing fishes characterized by the induction mechanisms invariably live in large, permeable social groups. Large social groups (more than a dozen individuals) are frequently correlated with resources that are not fixed in location, unpredictable in distribution, or not limiting in abundance, though recruitment may also play a role in determining group size (Shapiro 1984). For example, the protogynous seabass Anthias squamipinnis (Serranidae) feeds on plankton, which is variable in occurrence in space and time but probably not limiting in abundance (Popper & Fishelson 1973, Reese 1978). Perhaps as a result, seabass form feeding swarms or schools over the reef substratum (Shapiro 1977). Subgroups develop and constitute the primary social unit in this species. Median subgroup size is about 19 fish, and individuals are free to migrate to and from such subgroups (Shapiro 1986b). Social groups of the species are therefore large and permeable, though structured inter-individual relations persist (Shapiro 1986a). The mating system of this fish is a form of male-dominance polygyny (Yogo 1985). The protogynous saddleback wrasse, Thalassoma duperrey (Labridae). lives in coral-reef habitat on extensively overlapping home ranges (Ross

1986). Saddleback wrasses interact with at least 25 conspecifics on their home ranges in Hawaii. These fish are generalist, even opportunistic, feeders, suggesting unpredictable and undefendable food resources. Social units of the saddleback wrasse are highly permeable, partly because both sexes are mobile. The mating system of this fish is resourcedefense polygyny (Ross 1986); the male-defended resources are favorable spawning sites for females. Increased permeability, as noted for social groups of seabass and saddleback wrasses, results in reduced stability (predictability of dominance relationship) within the dominance hierarchies (Wilson 1975). This effect, which has important implications for the mechanism of sex change in sequential hermaphrodites, is discussed later. All the examples already given demonstrate that social organization and mating system are correlated with, and probably determined by, specific ecological factors: the distribution, density, and predictability of resources as well as the size and permeability of social groups.

Social correlates and adaptive significance

Each sex-change mechanism may be viewed as adaptive in a social context imposed by ecological constraints. First, however, I offer a general theory of the adaptive significance of sex change. The most universally accepted tenet is the 'size- (or age-) advantage' hypothesis (Ghiselin 1969, Warner 1975, Charnov 1982). Here, sex change should occur whenever an individual's fitness increases with size (or age) at a faster rate through one sex function than through the other. The direction of sex change can be predicted primarily through polygamy potential, because female fertility often increases uniformly with size (or age, at least in species with indeterminate growth), regardless of species (Warner 1984). Despite recent challenges (e.g. Shapiro 1988), the hypothesis has stood the test of time and remains useful (Warner 1988). Each sexchange mechanism can be understood as a special case of this general theory.

Sex-change suppression Given the ecological constraints, suppression of sex change, in which the aggressive dominance of one individual prevents sex change of group members (Robertson 1972, Fricke & Fricke 1977, Moyer & Nakazono 1978a), is apparently advantageous to all group members. The reason for this advantage is that the mechanism allows for rapid sex change in breeding individuals upon loss of the dominant group member. Rapid sex change is critical because (1) a reproductive windfall (all or none) awaits the successful sex changer and (2) a neighbor terminal-sex individual has the potential of taking over the harem if the largest initial-sex individual does not rapidly change sex. Loss of the dominant individual results in sex change of the ranking individual, regardless of the number of subdominants. The advantage of not changing sex, to fish at the bottom of the hierarchy, is that premature sex change might well result in their inability to compete against much larger males or females and result in a loss of feeding sites or possibly death. Thus, a minimum of informational input is required by any individual in the social group to enable the mechanism to operate: either the individual receives or does not receive aggressive dominance. The rapidity of sex change is facilitated through the bisexual maintenance of gametocytes in pre-inversion individuals (e.g. Robertson 1972, Fricke & Fricke 1977). What determines whether a population of fishes exhibits protogynous or protandrous suppression, i.e., the direction of sex change? Apparently the polygamy potential within the population is important. Protogyny occurs when multiple mates are simultaneously obtainable (see Warner 1975 and 1984 for theoretical explanation). If they are not obtainable (as in anemonefishes) protandry is favored because members of a monogamous pair produce more zygotes if the larger fish is a female. Numerous fish species appear to change sex under the above-described conditions (Table 1). Early sex change Another mechanism, 'early sex change', has recently been discovered. Moyer & Zaiser (1984), Hourigan & Kelley (l985), and Aldenhoven (1986)

have described haremic species of angelfishes in which a ranking female changes sex without the loss of the dominant male. The best proximate explanation of this phenomenon is that the female (apparently always the highest-ranking female) in some way circumvents the aggressive dominance of the male, changes sex, and becomes a 'bachelor male'. A baclhelor male may later establish its own territory and harem. Hourigan & Kelley (1985) suggested that candidates for early sex change circumvent aggressive dominance by remaining sheltered and visually isolated from the dominant male. One could expect early sex change in any haremic system where opportunities exist for more than one male to acquire mates and where conditions permit the loss of mating monopoly. Though such 'bachelor males' temporarily lose reproductive function in either sex, they remain poised to immediately take advantage of opportunities in their own or in neighboring harems, should a dominant male in either location disappear. In fishes with early sex change, fitness also appears to increase more rapidly with size through male than through female function due to polygamy potential, especially when population densities exceed a threshold value (Aldenhoven 1986). Early sex change ma) also confer a long-term advantage through growth acceleration when size affects reproductive success greatly (Hoffman et al. 1985, Ross 1987, Warner 1988).

Table 1.Proposed list of fishes with sex-change mechanisms described in the present work.
Sex-change mechanism and candidate species Protandrous suppression Amphiprion frenatus A. clarkii A. polymnus A. perideraion A. sandracinos A . ocellaris .4. bicinctus A. akallopisos A . melanopus Protogynous suppression Labroides dimidiatus Bodianus rufus Coris dorsomaculata Paragobiodon spp. Dascvllus aruanus D. marginatus Early sex change Centropyge interruptus C. tibicen C. bicolor Holacanthus tricolor Labroides dimidiatus Sex-ratio induction Anthias squamipinnis Size-ratio induction Tkalassoma duperrey (Unknown) induction 7: bifasciatum 7: lucasanum Clepticus parrae Pseudolabrus celidotus Rodianu~eclancheri Coris julis Corypkopterus personatus References*'

13 13 13 13 13 13 3.4,s 3, 5 20 10. 15, 18, 19 7, 17. 28 26 II 6. 25 25 14 14

1 X

16 23. 24 21.22 29 27 19 9 7 12 2

Sex-change induction Species with large permeable social units, on the other hand, usually lack stable dominance relationships. Here. a strategy of sex change in response to the loss of a single dominant individual would be too rigid to adopt. Since reproduction is normally shared by more than one individual in such societies, too little information about opportunities for reproduction in the terminal sex is transmitted by such an event. In such species, a sex-change mechanism of induction or stimulation apparently has evolved wherein sex change must be induced by the presence of' other group members or specific behavioral changes in them. In such fishes, a gradual increase in the number of smaller conspecifics (which tend to induce sex change) provides better

*' References follow: 1, Aldenhoven 1986;2, Cole & Robertson

1988; 3, Fricke 1979; 4, Fricke 1983; 5, Fricke & Fricke 1977; 6, Fricke & Holzberg 1974; 7, Hoffman 1985; 8, Hourigan & Kelley 1985; 9, Jones 1981; 10, Kuwamura 1981; 11. Lassig 1977; 12. Lejeune 1987; 13, Moyer & Nakazono 1978b; 14, Moyer & Zaiser 1984; 15, Robertson 1972; 16, Robertson 1974; 17, Robertson 1981; 18, Robertson & Choat 1974; 19, Robertson & Hoffman 1977; 20, Ross 1978a; 21, Ross et al. 1983; 22, Ross et al. 1990; 23, Shapiro 1979; 24, Shapiro 1980a; 25. Shpigel & Fishelson 1986; 26, Tribble 1982; 27, Warner 1982; 28, Warner & Robertson 1978; 29, Warner et al. 1975.

information on the appropriate time to change sex. In one type of induction studied in detail, group size and group sex ratio may be the proximate determinants of sex change (Shapiro 1979, 1980). In another type, sex-change stimulation or inhibition depends on relative-size ratios within the social unit (Ross et al. 1983, 1990). The former (sexratio induction) occurs in a monandric, sexually dimorphic species and the latter (size-ratio induction) in a species that is diandric and sexually monomorphic over half the adult size range. In the goby Coryphopterus personatus, sex change appears to be controlled by the net balance of inhibitory cues from larger conspecifics and stimulatory cues from smaller conspecifics (Cole & Robertson 1988). The multiply triggered sex changes observed in this fish suggest sex change by size-ratio rather than sex-ratio induction. Size-ratio induction has been verified experimentally (Ross et al. 1990). Both sex-ratio induction and size-ratio induction were described as 'behavioral induction' by Shapiro (1984), though the role of behavior in the sex-change mechanism of T. duperrey remains undetermined (Ross et al. 1983). Shapiro (1988) recently challenged the conclusions reached by Ross et al. (1983) by reasoning that, since all experimental females were removed from unknown social groups on the reef, all experimentally observed sex changes may well have been due to 'male removal'. However, the premise of his lengthy argument is based on a single statement involving flawed reasoning: '(...)if a female changes sex following separation of the sexes, then it was the separation that triggered sex change' (p. 284). Separation of the sexes, or male removal, was precluded as a variable in those experiments by the very nature of the experimental design. Different sex-change results were still obtained when both experimental and control groups were 'male removed'. Clearly female 7: duperrey change sex in response to prevailing social conditions they are exposed to, not the sudden change or removal in itself. This fact in no way invalidates the importance of male removal for certain species of hermaphroditic fishes. Further testing of the above model of sex-change mechanisms is needed. The kinds of ecological data

lacking include social-group size and organization as well as mating-system knowledge, particularly in the damselfishes, wrasses, and gobies, where some work has already been done. Such knowledge should be followed by field removal studies to determine whether smaller conspecifics are needed, which fish change sex, and how many fish change sex. At the behavioral level, laboratory analyses are needed to determine whether specific kinds of behavior (e.g. displays that reinforce dominance order in social groups) are necessary to either suppress sex change or to induce it, particularly in wrasses (other than cleaner wrasses) and angelfishes, where mating systems are already known. Robertson (1972) and Fricke & Fricke (1977) showed the importance of aggressive dominance in mediating sex-change suppression, while Shapiro (1979) showed that changes in the proportion of rushes received mediates sex-change induction in seabass. Further similar studies are needed in other species to determine if there is a fundamental difference in the way suppression and induction are mediated behaviorally.

Alternative models
Universal induction-inhibition model
Fricke (1983) suggested that, even in the small social groups of certain anemonefishes, smaller conspecifics may need to be present to induce a complete functional sex change. J. T. Moyer (personal communication) observed the same phenomenon in Amphiprion clarkii in Japan, where isolated solitary males have apparently remained male for periods of a year or more. These observations call to question the distinction between, or at least the exclusive operation of, suppression and induction mechanisms. However, smaller conspecifics are apparently necessary only for the completion (not the initiation) of the process in Amphiprion bicinctus. Two other phenomena point to fundamental differences in the processes of suppression and induction. First, pre-inversion individuals in species showing suppression of sex change maintain clearly identifiable bisexual gonads (Table 2).

Second, hom,osexual pairs are not formed in Amphiprion bicinctus, as they are in Thalassoma duperrey, when size and sex are reversed in pairing experiments (Table 3). Homosexual-pair formation in wrasses may simply reflect the importance of relative size as a cue for sex change. In any case, the contrasting results of these experiments point to the need for further evaluation of both sexualrecognition :systems and dominance relationships in these and related species. Other studies point to the need for a model combining elements of both the suppression and induction processes. Robertson's (1974) work with Labroides was the first to suggest that the sexchange process is accelerated when smaller females are present. More recently, Moyer (1987) reported evidence of both suppression and induction in three species of angelfishes of the genus Centropyge. In vie*wof these recent findings, a universal induction-inhibition model may well explain all forms of sex change in fishes. Under such a model, all sex change in teleosts would depend on induction by smaller or subdominant conspecifics; however, the induction process may affect only the rate or completeness of sex change in some species. It might be reasoned, for example, that if there are no

or few other female cleaner wrasses in a vacated harem, the urgency to change sex would be less than if there were many females present. Future work should center on determining (1) the specific kinds of social stimuli (present in smaller conspecifics) needed to induce sex change, (2) the kinds of stimuli (present in larger or more dominant conspecifics) needed to suppress or inhibit sex change, and (3) factors (if any) affecting the rate of the sex-change process.

Behavioral-scalingmodel Because of the preceding observations and the occurrence of the same or similar sex-change mechanisms in disparate families of teleosts, the possibility of a form of behavioral-physiologicalscaling (as in Wilson 1975) must also be entertained. Individual fish may well be genetically programmed for more than one sex-change mechanism, determined ultimately by environmental conditions. In support of this hypothesis, it is known that different populations of the same species of fish have different mating systems under different ecological conditions. Dascyllus marginatus, for example, switches

Table 2. Proximate causes and socio-ecological attributes of sex-change mechanisms. See Table 1 for references. Proximate cause or socio-ecological attribute Sex-change mechanism Protandrous suppression Size of social unit Stability of dominance hierarchies No. simultane,ms egg clutches per social unit (polygamy potential) Female vagilit y Direction of sex change Maintenance of gametocytes in pre-inversion fish Function of aggressive dominance*' Minimum no. smaller conspecifics needed for sex change to be initiated Sexual dimorphism over size range where sex change (occurs small stable single low to female bisexual suppression 0 no Protogynous suppression small stable multiple low to male bisexual suppression 0 sometimes Early sex change small moderately stable multiple moderate to male unisexual suppression
1

Sex-ratio induction large unstable multiple high to male unisexual inhibition 3or4 Yes

Size-ratio induction large unstable multiple high to male unisexual inhibition 1 no

yes
-

*' In suppression, the removal of aggressive dominance automatically results in sex change (or at least the activation of heterologous
gamete develc~pment) in ranking fish; in inhibition, sex change does not necessarily occur after removal of aggressive dominance (nor is heterologous :amete development necessarily activated).

from multimale polygyny to harem-defense polygyny to monogamy as coral habitat, and hence group size, becomes increasingly restricted (Fricke 1980). Similarly, Halichoeres maculipinna is a resourcedefense polygynist on reef-top habitat where preferred spawning sites are concentrated, but is a harem-defense polygynist on deep reefs (Robertson 1981). Large female Labroides dimidiatus may also undergo 'early sex change' under certain social conditions (Robertson 1974). These and related species are excellent candidates for testing the behavioral-scaling model.

Encounter-rate model Finally, Marvin Lutnesky (1989, unpublished) has developed a set of models for sex-change proximate causation which predict that sex change is stimulated or inhibited by threshold levels of encounters between social-group members. The models suggest that patterns of contact may vary with population density, and therefore so may patterns of sex change. He has tested the model with the Hawaiian angelfish Centropygepotteri, but the model has the potential for broad applicability to sequential hermaphrodites. Whether any or all of the above models can be supplanted by a model potentially as simple as one based on group encounter rates seems worthy of pursuit.

Evolutionary relationships among sex-change mechanisms Analyses of both the proximate causes of sex

change and socio-ecological attributes support the hypothesis that two separate but related groups of sex-change mechanisms exist: suppression and induction (Table 2). Social-group size and degree of permeability appear to be the primary determinants in their evolution. An alternative model (suppression-induction), which is also testable, incorporates both suppression and induction by holding that any sex change must be induced or stimulated by the presence of smaller or subdominant individuals. Evolutionary pathways are illustrated in Figure 1, which shows the ecological and social conditions that may give rise to each of the proposed sex-change mechanisms. Phylogeny and the occurrence of particular sexchange mechanisms seem not to be correlated (Fig. 2). In looking for evolutionary relationships, one must consider the range of social and mating systems characteristic of the members of the lineage in question. This range reflects the constraints imposed on the group of related species by its evolutionary history. Some groups show a broad range of mating systems and sexual strategies. The Pomacentridae, for example, include gonochoristic species, protandrous hermaphrodites, and protogynous hermaphrodites (Fricke & Holzberg 1974, Shpigel & Fishelson 1986). Certainly these related species have very different ecologies, the anemonefishes being restricted to sporadically occurring sea anemones and the species of Dascyllus being in no such way restricted. Alternatively, not a single species of Thalassoma forms harems, undoubtedly for ecological reasons discussed earlier. Hence, suppression of sex change is not expected to be found within this genus (though it certainly is within the family Labridae). Sex-change mecha-

Table 3. Summary of sex-change experiments involving pairings with relative size and sex as variables.
Larger fish terminal initial initial terminal Smaller fish initial initial terminal terminal

Amphiprion bicinctus (#IN)*'

not tested sex change (717) no sex change (616) no sex change (717)

Thalassorna duperrey (#IN)*'

no sex change (12112) sex change (21126) sex change (617) not tested

*' From Fricke (1983) and Fricke & Fricke (1977).

*2

From Ross et al. (1983).

Evolution of teleost sociality

Small social units

r 12 individuals rigid dominance hierarchy
suppression of sex change

> 12 individuals unstable dominance hierarchy

induction of'sex change

polygamy potential low

polygamy potential high

sex identifiable and important

sex ambiguous or unimportant

suppression

suppression
loss of mating control

induction

induction

Early sexchange

Fig. 1. Proposed evolutionary pathway for sex-change mechanisms identified among teleosts. Primary socio-ecological determinants are given at each level.

nisms have undoubtedly evolved many times independently, as have forms of hermaphroditism among teleost fishes (Smith 1975).

Neurophysiological models

The simplest neurophysiological model of sexchange suppression has only a single category of input stimuli from the environment: any behavior or behaviors that mediate aggressive dominance (Fig. 3a). Such a model predicts sex change when it is 'disinhibited' . It can also explain early sex change when aggressive dominance becomes subthreshold or if the sex-change candidate is able to avoid aggressive stimuli. This model is simpler than, though essentially similar to, the disinhibition model proposed by Shapiro (1988: Fig. 1). Sex-change induction, on the other hand, requires at least two categories of environmental stimuli: promoting stimuli (of one or more types) and inhibiting :stimuli (at least in size-ratio induction; Fig. 3b). Here the 'CNS link' must be preceded by an 'Analyzer' capable of integrating the two or more categories of environmental information and

comparing their summed or fractional value with a pre-programmed value. The neurophysiological models of Shapiro (1985) distinguished between and illustrated the two types of induction illustrated in a single model here. The models are useful because of their simplicity and their ability to account for the evolution of one type of mechanism from another type by the addition (or loss) of only a single integrative center in the CNS. Candidate brain integrative centers are currently being identified and will become the focus of future experimental studies in saddleback wrasses and other species. An alternative model for sex-change suppression involves the positive stimulation of the CNS link by behavior(s) mediating aggressive dominance (Fig. 4). The difference between this model and that in Figure 3a focuses on the kind of hormones playing a role in sex change. In model a (Fig. 4) either initial-sex hormones are or are not secreted, whereas model b involves the (lack of) secretion of sex-change inhibiting hormones. The same principles can be applied to the induction mechanisms (Fig. 3b). Integration need not even be limited to the CNS. Separate stimulatory or inhibitory mess-

Pomacanthidae Serranidae
Anthiinae

Labridae Gobiidae

Pomacentridae

Suppression
I

Suppression lnduction

Induction I Early sex change Sex-ratio induction Early sex change

Perciformes Labridae
I

Gobiidae

Pomacentridae
Thalassorna

1
Protogyno~ ~uppressic

1
Coryphopterus lnductio~

Amphiprion

Bodianus

suppression

Protandrous suppression
I

Protogynous " s e x Protogynous wwression

change I
J

Suppression Induction

Fig.2. Comparison of phylogentic relationships and sex-change mechanisms for some perciform families that have been studied to date: a - overview; b - detailed for families where several species have been studied. Phylogenetic data from Smith (1975) and Greenwood et al. (1966). No phylogenetic significance is implied by the illustrated branching pattern below the level of family. Not all species within a given taxon are necessarily described by the indicated sex-change mechanism.

ages may act directly on the gonads with resultant feedback to the brain, thus affecting behavior. Recent endocrine studies by Nakamura et al. (1989) showed rising levels of 11-keto-testosterone concomitant with the sex-change process in Thalassoma duperrey. Though CNS integrative centers were not identified, these results support neuroen-

docrine model b (Fig. 3) among the four presented here (Fig. 3 , 4 ) . The usefulness of these models lies in their application to the testing of sex-change mechanisms at the neurophysiological level. Such tests are under way in various laboratories and will undoubtedly constitute the most productive line of research in the field of sex-change mechanisms for the near

Environment p -

Organism

--

=-m-Aggressive

hormones

change

rT--13--1
Aggressive dominance

Sex-change sex lnhlbit~ v ' change hormones

-I

Fig. 3. Neuroghysiological models of sex-change suppression (a) and sex-chsnge induction (b). Double slashes indicate negative influence. CNS = central nervous system.

Fig. 4. Alternative models of sex-change suppression involving assumptions different from those in Figure 3: a - specific sexchange hormones are not produced; b - sex-change inhibiting hormones are produced. CNS = central nervous system.

future. Ultimately, these kinds of studies will enable investigators to view sex change as an integrative, multi-level phenomenon caused by specific environmer~tal stimuli, reaching certain neuroendocrine patlhways, and resulting in predictable anatomical changes in the reproductive system of a hermaphroditic fish.

References cited
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Acknowledgements

I thank E. Reese, G. Losey, J. Stimson, and M. Diamond f'or stimulating me to pursue this work; D. Shapiro for fostering the critical examination of existing hypotheses; J. Moyer for giving me a reason to complete this analysis; and J. Bull, P. Eschmeyer, M. Hixon, S. Hoffman, T. Hourigan, R. Robertson and several anonymous referees for making valuable comments that led to substantial improvemcmts. I acknowledge the research facilities and staffs of the University of Guam Marine Laboratory, the University of Hawaii Zoology Department, and the Hawaii Institute of Marine Biology for their support, as well as ASIH-NSF for a travel grant. Finally, I thank D. Enderle for help with the figures and S. Bencus for typing the manuscript.

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