Sexually dichromatic protogynous angelfish Centropyge ferrugata (Pomacanthidae) males can change back to females

Protogynous hermaphroditism, female-to-male sex change, is well known among reef fishes where large males monopolize harems of females. When the dominant male disappears from a harem, the largest female may change sex within a few weeks. Recently, from experiments with some protogynous haremic fishes in which two males' cohabitated, it was confirmed that sexual behavior and gonads were completely reversible according to individual social status. However, the ability to reverse secondary-developed sexual body coloration has never been examined in any protogynous fish. We conducted two male cohabitation experiments with the protogynous haremic angelfish, Centropyge ferrugata, which has conspicuous sexual dichromatism on the dorsal fin. Smaller males of C. ferrugata soon performed female-specific mating behaviors when they became subordinated after losing a contest. They then completed gonadal sex change to females 47 or 89 d (n=2) after beginning cohabitation. In the course of the reversed gonadal sex change, male-specific coloration on the dorsal fin changed to that of a female. Thus, the sex of C. ferrugata, including secondary developed sexually dichromatic characteristics, can be completely reversible in accord with their social status.     

Alternative Contexts of Sex Change with Social Control in the Bucktooth Parrotfish, Sparisoma radians

Social control of sex change occurs in a variety of hermaphroditic fishes; upon removal of the dominant individual, the largest individual of the opposite sex typically changes sex and acquires mating priority with the remaining members of the social group. Social control may allow a phenotypically plastic response to social situations that convey cues about the relative advantages of functioning as one sex or the other, and should be advantageous in highly heterogeneous habitats such as coral reefs. Parrotfishes (family Scaridae) are dominant members of herbivorous coral reef fish assemblages, and numerous histological examinations of gonads have demonstrated the hermaphroditic life history of many species in the family. However, social control of sex change has never been conclusively demonstrated in the parrotfishes. To test a new version of the size-advantage model for sex change, we conducted removal experiments of dominant male bucktooth parrotfish, Sparisoma radians, in St. Croix, U.S. Virgin Islands. A total of seven females from five different reefs changed sex following removals, clearly demonstrating social control of sex change. In addition, all but one of those individuals changing sex were smaller than the largest females remaining in the harems, and this contrasts with nearly all previous studies of sex change in fishes. Sex change proceeds via a novel sequence of events when compared with previous studies. Rather than behavioral sex change preceding morphological sex change, the appearance of male coloration is followed by the development of male behavior that is fully expressed approximately 20 days after removal. We show how differing arrival rates of bachelor males at our study sites may facilitate alternative contexts of sex change, with sex change occurring within social groups in some locations and with bachelor males filling harem vacancies in other locations. Alternative contexts of sex change further illustrate the astonishing phenotypic plasticity in the social and mating behavior of parrotfishes.     

Physical interactions facilitate sex change in the protogynous orange-spotted grouper,Epinephelus coioides

Sex change in teleost fishes is commonly regulated by social factors. In species that exhibit protogynous sex change, such as the orange-spotted grouper Epinephelus coioides, when the dominant males are removed from the social group, the most dominant female initiates sex change. The aim of this study was to determine the regulatory mechanisms of socially controlled sex change in E. coioides. We investigated the seasonal variation in social behaviours and sex change throughout the reproductive cycle of E. coioides, and defined the behaviour pattern of this fish during the establishment of a dominance hierarchy. The social behaviours and sex change in this fish were affected by season, and only occurred during the prebreeding season and breeding season. Therefore, a series of sensory isolation experiments was conducted during the breeding season to determine the role of physical, visual and olfactory cues in mediating socially controlled sex change. The results demonstrated that physical interactions between individuals in the social groups were crucial for the initiation and completion of sex change, whereas visual and olfactory cues alone were insufficient in stimulating sex change in dominant females. In addition, we propose that the steroid hormones 11-ketotestosterone and cortisol are involved in regulating the initiation of socially controlled sex change.     

Reversed Sex Change in The Haremic Protogynous Hawkfish Cirrhitichthys falco in Natural Conditions

Bi‐directional sex change has recently been reported in a range of reef fishes, including haremic species that were earlier thought to be protogynous (female to male). However, the occurrence of this phenomenon and the social conditions driving the reversion of males to females (reversed sex change) have been poorly documented under natural conditions. Reversed sex change is predicted to occur in low‐density populations where facultative monogamy is common. However, few studies have evaluated this over a long period in such populations. We documented the occurrence of bi‐directional sex change during a 3‐yr demographic survey of a population characterised by small harem sizes in haremic hawkfish Cirrhitichthys falco. New males were derived following a change in sex of functional females (secondary males; n = 3) and juveniles always matured first as females (n = 3). Thus, C. falco exhibited a typical protogynous sexual pattern, consistent with a range of haremic fish species. We observed reversed sex change in two males. In both cases, all the females disappeared from their harems and the neighbouring males expanded their territories to encompass the territories of the sex changers. However, bachelor males did not always revert to females. A dominant male experienced bachelor status twice but regained mating opportunities following the immigration of a female into his territory or by taking a female from a neighbouring harem. Thus, we conclude that bachelor males use reversed sex change as a facultative tactic to regain reproductive status in a haremic mating system. In addition, we discuss the influence of harem size upon occurrence of reversed sex change.     

Territorial behaviour reflects sexual status in groups of false clown anemonefish (Amphiprion ocellaris) under laboratory conditions

Anemonefishes (genus Amphiprion) are well known as protandrous sex-changing fish. They live symbiotically with sea anemones and form a social unit that consists of a breeding pair and several sexually immature individuals with ambisexual gonads. In general, the hierarchy of the social rank is strictly maintained in a group, and this hierarchy is considered to be one of the critical factors that induce sex change or sex differentiation in anemonefishes. Field observations have shown that behavioural characteristics of anemonefishes vary depending on the environment. In this study we examined the differences in territorial aggression directed at conspecific intruders according to sexual status in the false clown anemonefish, Amphiprion ocellaris, under laboratory conditions. Resident–intruder tests were conducted on groups consisting of three anemonefish: a dominant female, a second-ranked male and a subordinate ambisexual individual. Females and males showed more aggressive behaviour than did ambisexual individuals, and behaviours were specifically directed at intruders of the same sexual status, not at those of the opposite sex. Notably, the female residents displayed fierce aggressive behaviours particularly toward female intruders, whereas male residents engaged more often in side-by-side swimming with male intruders than with female or ambisexual intruders. Ambisexual intruders were threatened by all residents, rarely attacked. We observed only few aggressive acts towards tank mates. These results suggest that sexually mature resident anemonefish in a confined space, such as under laboratory conditions, perceive intruders of the same sexual status as competitors for reproductive status and thus, dominant social rank.     

Reversed Sex-Change in the Protogynous Reef Fish Labroides dimidiatus

Protogynous hermaphroditism, or female-to-male sex change, is known for many reef fishes including wrasses (family Labridae) in which large males monopolize mating. When the dominant male disappears from a polygynous group, the largest female may change sex within a few weeks. Such social control of sex change was first documented in harems of the cleaner wrasse Labroides dimidiatus almost 30 yr ago. To examine whether change of social status would induce males of L. dimidiatus to perform reversed sex-change, we conducted experiments: (i) releasing single males near lone males whose mates have been removed in the field; and (ii) keeping two males in a tank. Smaller males changed back to females when they became subordinate: it took 53–77 d (n=3) for them to complete gonadal sex change and release eggs in the aquarium. The male–male pairs performed spawning behavior, with the smaller male in the female role already 5–58 d before completion of gonadal sex change. This is the first report of reversed sex-change among protogynous wrasses. Moreover, we conducted another experiment, keeping a pair of a male and a larger female in a tank (n=1). We found sex change by both mates, which has not been reported from any fishes. Thus, the sex of L. dimidiatus is strictly determined by social status whenever it changes after mate loss.     

Gonad development in Midas cichlids and the evolution of sex change in fishes

Some fishes mature and function as one sex and later transform to the other sex in response to social interactions. Previous evidence suggested that a change in developmental timing may be involved in the evolution of adult sex change in fishes. The most recent support for this idea came from reports that sex in the Midas cichlid, Amphilophus citrinellus, was determined by social conditions experienced at the juvenile stage. Differentiation as a male was reported to be dependent on large body size relative to group-mates, and thought to be mediated through aggressive interactions. Here I demonstrate that socially controlled sex determination does not occur as was originally reported. Previously, I found that sex was not associated with body size in juveniles either in nature or in captivity. Similarly, I found no association between aggressive behavior and sex in juveniles. I later demonstrated that socially controlled sex determination does not typically occur in the Midas cichlid and closely related species and supported an alternative mechanism to explain large body size in adult males. Finally, in the current study I analyze gonad histology of fish from the same population used by the original authors and lay to rest the idea of socially controlled sex determination in this species. Recent observations of socially controlled sex determination in juveniles of species that typically change sex at the adult stage are examples of phenotypic plasticity, not genetic variation. Therefore, juvenile socially controlled sex determination does not support a theory that a change in developmental timing is involved in the evolution of adult sex change in fishes.     

Size,sex and social experience: Experimental tests of multiple factors mediating contest behaviour in a rockpool fish

Aggressive contests amongst conspecifics are important to understand from an ecological and evolutionary perspective as contest dynamics can directly influence individual fitness. For some species, individual attributes such as relative body size closely predict the outcome, intensity and duration of contests, whereas for others, prior social experiences play a key role. However, disentangling the relative effects of individual attributes and social experiences is challenging from an experimental perspective, and because of this, few studies have investigated relative effects of multiple factors. Rockpool fishes have been well studied in terms of factors governing abundance, distribution and community structure, but much less so in terms of contest behaviour. This is surprising because contest dynamics are likely to directly affect the distribution of fishes along the rocky shore, and hence indirectly govern population and community composition. Here, we explored multiple factors potentially influencing contest behaviour in a numerically dominant, resident intertidal fish species, Bathygobius cocosensis (Gobiidae). Using a series of staged pairwise contest trials, we investigated the effect of size, sex and social experiences (namely prior residency and winner–loser experiences) on contest dynamics. We found no evidence that prior residency influenced contest outcome, suggesting social experiences play a minor role in contest dynamics. Previous winner/loser experience also did not influence contest outcome, although this is likely a product of low sample size. In addition, the likelihood of winning was unrelated to contestant sex, and the combination of sexes in paired contests did not influence contest intensity or duration. Instead, body size was related to contest outcome, intensity and duration in the majority of experimental trials. These results suggest that body size rather than sex or social experiences is the key determinant of contest dynamics in this species. We suggest that the dynamic biotic and abiotic environment inhabited by intertidal fish may reduce the influence of prior social experiences in modulating contest dynamics.     

Multiple mechanisms of phenotype development in the bluehead wrasse

Despite having detailed information on mechanisms mediating sex-typical behavior in many species, we have little understanding of whether the same mechanisms regulate these behaviors when they are performed in the same species under different social contexts. In the five field experiments of this study of bluehead wrasses (Thalassoma bifasciatum), a sex-changing fish, we examined the roles of arginine vasotocin (AVT) and the potent teleost androgen 11-ketotestosterone (11KT) in mediating sexual and aggressive behaviors typical of dominant males. We demonstrated that AVT appears necessary for the assumption of dominant territorial status in males and females, but is sufficient only in the socially dominant terminal phase (TP) male phenotype. Specifically, an AVP V(1) receptor antagonist prevented both TP males and females from gaining dominance over recently vacated territories. However, unlike TP males in a previous study, neither females nor initial phase males responded to AVT treatment with increases in display of TP male typical behaviors when under social conditions that inhibit sex change. Treating females with 11KT did not alter responsiveness to AVT, but did induce male coloration and courtship behavior that was not observed in oil-treated females. Combined with the results of a previous study, these results indicate that the ability of AVT to induce male-typical behavior differs among sexual phenotypes and that this differential responsiveness appears to be dependent on social context and not directly on exposure to 11KT. Furthermore, since 11KT can induce courtship behavior in females that is not affected by AVT, there may be different hormonal mechanisms mediating courtship behavior under different social contexts.     

Growth acceleration,behaviour and otolith check marks associated with sex change in the wrasse <Emphasis Type="Italic">Halichoeres miniatus</Emphasis>

In protogynous sex-changing fishes, females are expected to compete for the opportunity to change sex following the loss of a dominant male and may exhibit growth and behavioural traits that help them maintain their dominant status after sex change. A male removal experiment was used to examine changes in female growth and behaviour associated with sex change in the haremic wrasse Halichoeres miniatus and to test whether any changes in growth associated with sex change were recorded in otolith microstructure. Dominant females began displaying male-characteristic behaviour almost immediately after the harem male was removed. The frequency of interactions between females increased following male removal. In contrast, feeding frequency of females decreased. The largest one to three females in each social group changed sex following male removal and exhibited an increase in growth associated with sex change. Sex changers grew more than twice as fast as non-sex changers during the experimental period. This growth acceleration may enable new sex-changed males to rapidly reach a size where they can defend the remaining harem from other males. An optical discontinuity (check mark) was present in the otoliths of sex-changed fish, and otolith accretion rate increased significantly after the check mark, corresponding with the increased growth rate of sex-changing females. Wild caught males, but not females, exhibited an analogous check mark in their otoliths and similar increases in otolith increment widths after the check. This indicates that an increase in growth rate is a regular feature of sex-change dynamics of H. miniatus. Communicated by Environment Editor Prof. Rob van Woesik