Sex-changing Fish Research Articles

Meta-analysis of gonadal transcriptome provides novel insights into sex change mechanism across protogynous fishes.

Protogyny, being capable of changing from female to male during their lifetime, is prevalent in 20 families of teleosts but is believed to have evolved within specific evolutionary lineages. Therefore, shared regulatory factors governing the sex change process are expected to be conserved across protogynous fishes. However, a comprehensive understanding of this mechanism remains elusive. To identify these factors, we conducted a meta-analysis using gonadal transcriptome data from seven species. We curated data pairs of ovarian tissue and transitional gonad, and employed ratios of expression level as a unified criterion for differential expression, enabling a meta-analysis across species. Our approach revealed that classical sex change-related genes exhibited differential expression levels between the ovary and transitional gonads, consistent with previous reports. These results validate our methodology's robustness. Additionally, we identified novel genes not previously linked to gonadal sex change in fish. Notably, changes in the expression levels of acetoacetyl-CoA synthetase and apolipoprotein Eb, which are involved in cholesterol synthesis and transport, respectively, suggest that the levels of cholesterol, a precursor of steroid hormones crucial for sex change, are decreased upon sex change onset in the gonads. This implies a potential universal influence of cholesterol dynamics on gonadal transformation in protogyny.

Transcriptomic signatures associated with underlying rapid changes in the early phase brain of bi-directional sex change in Trimma okinawae.

Teleost fish exhibit remarkable sexual plasticity and divergent developmental systems, including sequential hermaphroditism. One of the more fascinating models of sexual plasticity is socially controlled sex change, which is often observed in coral reef fish. The Okinawa rubble goby, Trimma okinawae, is a bi-directional sex-changing fish. It can rapidly change sex in either direction based on social circumstances. Although behavioural and neuroendocrine sex change occurs immediately and is believed to trigger gonadal changes, the underlying mechanisms remain poorly understood. In this study, we conducted a de novo transcriptome analysis of the T. okinawae brain and identified genes that are differentially expressed between the sexes and genes that were immediately controlled by social stimulation implicating sex change. Several genes showed concordant expression shifts regardless of the sex change direction and were associated with histone modification in nerve cells. These genes are known to function in the neuroendocrine control of reproduction in nerve cells. Overall, we identified genes associated with the initiation of sex change, which provides insight into the regulation of sex change and sexual plasticity.

Neuroanatomy of a sex changing fish: the New Zealand spotty wrasse (Notolabrus celidotus) brain atlas

ABSTRACT For most vertebrates, sexual fate is genetically determined and remains fixed throughout life. However, for some teleost fishes sex is more plastic. Significant progress has been made in characterising the cellular and molecular processes that underpin gonadal sex change. The brain-mediated mechanisms that underlie and initiate this transformation, however, remain poorly understood. One reason for this is the current lack of a neuroanatomical reference work for sex changing fishes. Here, we present a brain atlas for the New Zealand (NZ) spotty wrasse (Notolabrus celidotus), developed from 10 wild caught specimens (2 male and 8 female). From each fish, coronal cryosections were collected and stained with cresyl violet solution. Photomicrographs were taken of each section using an inverted bright field microscope and 3D reconstructions were rendered of each brain for annotation and volumetric comparison of specific brain regions. The brain atlas describes the general features of the NZ spotty wrasse brain as well as its specificities. This atlas provides the necessary foundation for further investigation of the brain mechanisms driving protogyny in this species.

Sex differences in aggressive intensities and brain steroids during status resolution in a sex changing fish, Lythrypnus dalli

For vertebrates living in social hierarchies, the neuroendocrine system regulates temporal aspects of aggressive interactions during status establishment. In teleost fishes, the sex steroids 17β-estradiol (E2) and 11-ketotestosterone (KT), and the glucocorticoid, cortisol (CORT) are associated with aggression in distinct phases of their life history. Bluebanded gobies, Lythrypnus dalli, exhibit bidirectional sexual plasticity by responding to changes in their social structure by escalating aggression associated with neural changes that precede gonadal reorganization to the opposite sex. Here, we used a novel experimental design to investigate systemic (waterborne) and neural steroids associated with the earliest behavioral changes associated with feminization and masculinization during protandrous and protogynous sex change respectively. In stable social groups of wild-caught L. dalli comprising of one male and two females, we disrupted hierarchy by adding or removing a male, providing a social context for intrasexual aggression. Within only 30 min, males exhibited high rates of physical aggression inside the nest to maintain their territory, while females exhibited high rates of chases outside the nest to reestablish social status. During this period of instability, while waterborne steroids were not affected, brain E2 was higher in all fish and CORT was lower in male brains. Brain KT was higher in males who emerged as dominant compared to dominant females. Overall, a combination of differences in brain E2, CORT, and KT were important in the regulation of hierarchy re-establishment and maintenance. Rapid responses during conspecific aggressive encounters are likely mediated by neural steroid synthesis that precede changes in systemic steroids.

Accelerated of Sex Reversal use 17α-methyltestosterone Induced Female, Orange-Spotted Grouper <I>Epinephelus coioides</I>

Highlight Research Sex reversal for orange-spotted grouper Epinephelus coioides The application of 17α-methyltestosterone induce sex change The stability of sex change need more investigation Abstract The occurance of hermaphrodites in grouper fish causes a scarcity of male parents, so an alternative is needed to accelerate sexchange to male at a young age. The present study was expected to scrutinize the mechanisms of sex-change in fish in the early change process, and whether the testis converted from immature ovary using 17α-methyltestosterone (MT) would recover after the termination of MT treatment. MT-induced sex-change and 5-aza-2’-deoxycytidine (5-Aza) were connected as DNA methylation inhibitors to comprehend the alternation of gonadal soma cells. The orange-spotted groupers were used at the developmental ages and fed a diet containing MT at 50 mg/kg for three months and then a normal diet for a month. In the first week and second week fish injected with 5-Aza intraperitoneally during the MT-oral administration. Most of the fishes in the control group had immature ovaries, but all the females fed with MT, had immature spermatogenesis. However, one month after the withdrawal of MT treatment, the sex of the fish returned to female-like even though the fish have undergone MT-induced masculinization. This outcome demonstrates precocious sex-change from under yearling, orange-spotted grouper utilizing oral MT treatment is impermanent. All the females of 5-aza treatments showed no spermatogenic cells. In this study, lower growth rates were demonstrated by the MT-treated groups. The impact of this metabolic change was clear after the end of the hormone oral administration since the decreased growth of the groups treated for three months.

Mechanisms of sex differentiation and sex reversal in hermaphrodite fish as revealed by the Epinephelus coioides genome.

Most grouper species are functional protogynous hermaphrodites, but the genetic basis and the molecular mechanisms underlying the regulation of this unique reproductive strategy remain enigmatic. In this study, we report a high-quality chromosome-level genome assembly of the representative orange-spotted grouper (Epinephelus coioides). No duplication or deletion of sex differentiation-related genes was found in the genome, suggesting that sex development in this grouper may be related to changes in regulatory sequences or environmental factors. Transcriptomic analyses showed that aromatase and retinoic acid are probably critical to promoting ovarian fate determination, and follicle-stimulating hormone triggers the female-to-male sex change. Socially controlled sex-change studies revealed that, in sex-changing fish, the brain's response to the social environment may be mediated by activation of the phototransduction cascade and the melatonin synthesis pathway. In summary, our genomic and experimental results provide novel insights into the molecular mechanisms of sex differentiation and sex change in the protogynous groupers.

New cells added to the preoptic area during sex change in the common clownfish Amphiprion ocellaris

Sex differences in cell number in the preoptic area of the hypothalamus (POA) are documented across all major vertebrate lineages and contribute to differential regulation of the hypothalamic-pituitary-gonad axis and reproductive behavior between the sexes. Sex-changing fishes provide a unique opportunity to study mechanisms underlying sexual differentiation of the POA. In anemonefish (clownfish), which change sex from male to female, females have approximately twice the number of medium-sized cells in the anterior POA compared to males. This sex difference transitions from male-like to female-like during sex change. However, it is not known how this sex difference in POA cell number is established. This study tests the hypothesis that new cell addition plays a role. We initiated adult male-to-female sex change in 30 anemonefish (Amphiprion ocellaris) and administered BrdU to label new cells added to the POA at regular intervals throughout sex change. Sex-changing fish added more new cells to the anterior POA than non-changing fish, supporting the hypothesis. The observed effects could be accounted for by differences in POA volume, but they are also consistent with a steady trickle of new cells being gradually accumulated in the anterior POA before vitellogenic oocytes develop in the gonads. These results provide insight into the unique characteristics of protandrous sex change in anemonefish relative to other modes of sex change, and support the potential for future research in sex-changing fishes to provide a richer understanding of the mechanisms for sexual differentiation of the brain.

The ontogenic gonadal transcriptomes provide insights into sex change in the ricefield eel Monopterus albus

BackgroundThe ricefield eel is a freshwater protogynous hermaphrodite fish and has become an important aquaculture species in China. The sex change of ricefield eel is impeding its aquaculture practice, particularly the large-scale artificial breeding. Many studies including transcriptomes of mixed gonadal samples from different individuals have been aimed to elucidate mechanisms underlying the sex change. However, the key physiological factors involved in the initiation of sex change remain to be identified. ResultsThe present study performed transcriptomic analysis on gonadal samples of different sexual stages obtained through biopsy from the same fish undergoing sex change. A total of 539,764,816 high-quality reads were generated from twelve cDNA libraries of gonadal tissues at female (F), early intersexual (EI), mid-intersexual (MI), and late intersexual (LI) stages of three individual sex-changing fish. Pairwise comparisons between EI and F, MI and EI, and LI and MI identified 886, 319, and 10,767 differentially expressed genes (DEGs), respectively. Realtime quantitative PCR analysis of 12 representative DEGs showed similar expression profiles to those inferred from transcriptome data, suggesting the reliability of RNA-seq data for gene expression analysis. The expression of apoeb, csl2, and enpp2 was dramatically increased and peaked at EI while that of cyp19a1a, wnt4a, fgf16, and foxl2a significantly downregulated from F to EI and remained at very low levels during subsequent development until LI, which suggests that apoeb, csl2, enpp2, cyp19a1a, wnt4a, fgf16, and foxl2a may be closely associated with the initiation of sex change of ricefield eels.ConclusionsCollectively, results of the present study confirmed that the down-regulation of female-related genes, such as cyp19a1a, wnt4a, fgf16, and foxl2a, is important for the sex change of ricefield eels. More importantly, some novel genes, including apoeb, csl2, and enpp2, were shown to be expressed with peak values at EI, which are potentially involved in the initiation of sex change. The present transcriptomic data may provide an important research resource for further unraveling the mechanisms underlying the sex change and testicular development in ricefield eels as well as other teleosts.

Stable and persistent male-like behavior during male-to-female sex change in the common clownfish Amphiprion ocellaris

Many fish species exhibit natural sex change as part of their life, providing unique opportunities to study sexually-differentiated social behaviors and their plasticity. Past research has shown that behavioral sex change in the female-to-male (protogynous) direction occurs rapidly and well before gonadal sex change. However, little is known about the timecourse of behavioral sex change in male-to-female (protandrous) sex-changing species, limiting our ability to compare patterns of behavioral sex change across species and identify conserved or divergent underlying mechanisms. Using the protandrous sex changing anemonefish Amphiprion ocellaris, we assessed behavior (aggression and parental care) and hormones (estradiol and 11-ketotestosterone) in fish over six months of sex change, and compared those fish against their non-changing partners as well as control males and females. Contrary to expectations, we found that sex-changing fish displayed behavior that was persistently male-like, and that their behavior did not become progressively female-like as sex change progressed. Hormones shifted to an intermediate profile between males and females and remained stable until gonads changed. These results support a new perspective that the timecourse for protandrous sex change in anemonefish is completely distinct from other well-established models, such that behavioral sex change does not occur until after gonadal sex change is complete, and that sex-changing fish have a stable and unique behavioral and hormonal phenotype that is distinct from a male-typical or female-typical phenotype. The results also identify aspects of sex change that may fundamentally differ between protandrous and protogynous modes, motivating further research into these remarkable examples of phenotypic plasticity.

Demographic Consequences of Small-Scale Fisheries for Two Sex-Changing Groupers of the Tropical Eastern Pacific

The effects of fishing on the demography and population ecology of sex-changing fishes are largely unknown, despite the fact that their fisheries provide important economic and nutritional resources in coastal communities throughout the tropics, especially in Latin America. Species with female-first sex change often have naturally skewed sex ratios in the adult population, and fishing pressure can alter this natural bias, limiting egg production and fertilization success. How fishing alters demography and population vital rates depends on which sizes and sexes are selected. We consider two types of fishery selectivity “asymptotic (selecting the largest fish) and plate-sized (selecting fish between in a narrow, but small, size range)” that to represent fisheries for two important fish species of the Tropical Eastern Pacific, the Pacific goliath grouper (Epinephelus quinquefasciatus) and the endemic sailfin grouper (Mycteroperca olfax) of the Galapagos Islands, known locally as bacalao. Each of these large, long-lived species support small scale fisheries of significant value, but there is limited information on fishing effort, selectivity, or population trends. Using a population model, we estimate how the biology of these species contributes to their risk of overexploitation under different possible scenarios of fishing and reproductive biology. Specifically, we consider how variation in growth rates and fertilization rates interact with selectivity to affect age structure and sex ratios. We compare two metrics of population status: the spawning potential ratio (SPR), and the relative standing biomass after fishing (BF/B0). In our modeled populations, when fertilization rates were reduced, fishing rapidly decreased the spawning potential of both species, but did not affect biomass at moderate levels of fishing mortality. However, we predict low fertilization success, fast somatic growth, and asymptotic selectivity of fisheries for sex-changing species decreases both spawning potential and biomass, even at low levels of exploitation, suggesting these factors can cause rapid depletion of sex-changing species. Our findings highlight key gaps in our knowledge of spawning behavior and fertilization success of sex-changing fishes that must be filled if we are to sustainably manage these culturally and economically significant fisheries.

On the role of eviction in group living sex changers

In most sex-changing fishes in coral reefs, a dominant male and multiple females form a mating group (harem). In a few species, the subordinates are simultaneous hermaphrodites that may act as sneakers. In this paper, we ask whether the subordinates in most sex changers choose to be female or whether they are forced to give up their male function to avoid eviction by the harem holder. We consider a game model in which (1) the dominant male evicts some hermaphroditic subordinates if the risk of sperm competition in regard to fertilizing eggs is high, and (2) each subordinate individual chooses its own sex allocation considering the risk of being evicted. In the evolutionarily stable state, the dominant male evicts subordinates only when the subordinates vary greatly in their reproductive resources. All the subordinate individuals are female if the summed male function of the subordinates is smaller than that of the dominant male. Otherwise, all the subordinates are hermaphrodites, and the large individuals have the same male investment but a greatly different female investment, while small individuals have a reduced male investment to avoid eviction risk. We conclude that situations in which the sex allocation of subordinates is affected by the possibility of eviction by the harem holder are rather limitedSignificance statementWe studied the role of eviction in social evolution. In most sex-changing fishes in coral reefs, a dominant male and multiple females form a mating group. In a few species, subordinates are simultaneous hermaphrodites. We asked whether the subordinates are forced to give up their male function to avoid eviction by the harem holder. We examined a game model in which the dominant male evicts hermaphroditic subordinates with a high risk of sperm competition, and each subordinate chooses its own sex allocation considering the eviction risk. We derived mathematical conditions for when subordinates are females or hermaphrodites in the ESS. The model demonstrated that the control by the dominant over subordinate reproductive decisions is rather limited.

Idea paper: Effects of gonad type and body mass on the time required for sex change in fishes

AbstractSex change is a well‐known phenomenon in teleost fishes, and it takes several days to a few months depending on the species and direction of sex change. However, the underlying factors influencing the time required for sex change (TS) remain unclear. Given that the time for producing a new gonad largely determines TS, the gonad type (i.e., whether fish retain the gonad of opposite sex or not [delimited or non‐delimited]) and metabolic rate may affect TS. This study sought to test two hypotheses: (1) the delimited gonad shortens TS and (2) TS scales with mass0.1−0.2, because the metabolic scaling exponent (β) in fishes is 0.8–0.9 and biological times scale with mass1−β in general. We compiled data on TS for 12 female‐to‐male and 14 male‐to‐female sex‐changing species from the literature. Results of individual examinations of the effects of gonad type and mass were consistent with our hypotheses. However, upon simultaneous examination of the effects of gonad type and mass, these effects became unclear because of their strong multicollinearity. The compiled data for delimited and non‐delimited gonads were biased toward the smaller and larger species, respectively, precluding us from being able to statistically distinguish between these effects. Small species with non‐delimited gonads and large species with delimited gonads exist; however, their TS has not been measured with high temporal resolution thus far. Therefore, additional experiments on these species are required to statistically distinguish between, as well as to better understand, the effects of gonad type and mass on TS.

Epigenetics underpins phenotypic plasticity of protandrous sex change in fish.

Phenotypic plasticity is an important driver of species resilience. Often mediated by epigenetic changes, phenotypic plasticity enables individual genotypes to express variable phenotypes in response to environmental change. Barramundi (Lates calcarifer) are a protandrous (male‐first) sequential hermaphrodite that exhibits plasticity in length‐at‐sex change between geographic regions. This plasticity is likely to be mediated by changes in DNA methylation (DNAm), a well‐studied epigenetic modification. To investigate the relationships between length, sex, and DNAm in a sequential hermaphrodite, here, we compare DNAm in four conserved vertebrate sex‐determining genes in male and female barramundi of differing lengths from three geographic regions of northern Australia. Barramundi first mature as male and later sex change to female upon the attainment of a larger body size; however, a general pattern of increasing female‐specific DNAm markers with increasing length was not observed. Significant differences in DNAm between males and females of similar lengths suggest that female‐specific DNAm arises rapidly during sex change, rather than gradually with fish growth. The findings also reveal that region‐specific differences in length‐at‐sex change are accompanied by differences in DNAm and are consistent with variability in remotely sensed sea temperature and salinity. Together, these findings provide the first in situ evidence for epigenetically and environmentally mediated sex change in a protandrous hermaphrodite and offer significant insight into the molecular and ecological processes governing the marked and unique plasticity of sex in fish.

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.

Sex determination, gonadal sex differentiation, and plasticity in vertebrate species.

A diverse array of sex determination (SD) mechanisms, encompassing environmental to genetic, have been found to exist among vertebrates, covering a spectrum from fixed SD mechanisms (mammals) to functional sex change in fishes (sequential hermaphroditic fishes). A major landmark in vertebrate SD was the discovery of the SRY gene in 1990. Since that time, many attempts to clone an SRY ortholog from nonmammalian vertebrates remained unsuccessful, until 2002, when DMY/dmrt1by was discovered as the SD gene of a small fish, medaka. Surprisingly, however, DMY/dmrt1by was found in only 2 species among more than 20 species of medaka, suggesting a large diversity of SD genes among vertebrates. Considerable progress has been made over the last 3 decades, such that it is now possible to formulate reasonable paradigms of how SD and gonadal sex differentiation may work in some model vertebrate species. This review outlines our current understanding of vertebrate SD and gonadal sex differentiation, with a focus on the molecular and cellular mechanisms involved. An impressive number of genes and factors have been discovered that play important roles in testicular and ovarian differentiation. An antagonism between the male and female pathway genes exists in gonads during both sex differentiation and, surprisingly, even as adults, suggesting that, in addition to sex-changing fishes, gonochoristic vertebrates including mice maintain some degree of gonadal sexual plasticity into adulthood. Importantly, a review of various SD mechanisms among vertebrates suggests that this is the ideal biological event that can make us understand the evolutionary conundrums underlying speciation and species diversity.

An in vitro ovarian explant culture system to examine sex change in a hermaphroditic fish.

Many teleost fishes undergo natural sex change, and elucidating the physiological and molecular controls of this process offers unique opportunities not only to develop methods of controlling sex in aquaculture settings, but to better understand vertebrate sexual development more broadly. Induction of sex change in some sequentially hermaphroditic or gonochoristic fish can be achieved in vivo through social manipulation, inhibition of aromatase activity, or steroid treatment. However, the induction of sex change in vitro has been largely unexplored. In this study, we established an in vitro culture system for ovarian explants in serum-free medium for a model sequential hermaphrodite, the New Zealand spotty wrasse (Notolabrus celidotus). This culture technique enabled evaluating the effect of various treatments with 17β-estradiol (E2), 11-ketotestosterone (11KT) or cortisol (CORT) on spotty wrasse ovarian architecture for 21 days. A quantitative approach to measuring the degree of ovarian atresia within histological images was also developed, using pixel-based machine learning software. Ovarian atresia likely due to culture was observed across all treatments including no-hormone controls, but was minimised with treatment of at least 10 ng/mL E2. Neither 11KT nor CORT administration induced proliferation of spermatogonia (i.e., sex change) in the cultured ovaries indicating culture beyond 21 days may be needed to induce sex change in vitro. The in vitro gonadal culture and analysis systems established here enable future studies investigating the paracrine role of sex steroids, glucocorticoids and a variety of other factors during gonadal sex change in fish.

Behavioural differences between breeding and nonbreeding pairs of protandry monogamous false clown anemonefish Amphiprion ocellaris

Anemonefishes are some of the most popular marine ornamental fishes. Due to the adverse impacts of commercial fishing on the wild populations of anemonefishes, a more suitable and efficient captive breeding programme must be promoted. In the wild, anemonefishes are protandrous sex-changing fish, but when two immature individuals with ambisexual gonads are raised together in captivity, the two differentiate directly into a male and a female, to form a breeding pair. However, not all the formed pairs spawn, explaining the great care required in captive breeding. This behaviour appears to be counter-adaptative, as anemonefish social groups form randomly in the wild, and such phenomenon would disturb their breeding success. This study evaluated the behavioural and physiological differences between breeding and nonbreeding pairs of false clown anemonefish Amphiprion ocellaris under captive conditions. Behavioural observations revealed that nonbreeding females monopolized the shelter provided, whereas breeding females allowed breeding males to use the shelter and the pair frequently stayed together in the shelter. Both nonbreeding and breeding females possessed mature ovarian tissue and similar level of plasma estradiol concentrations, but nonbreeding males had a smaller amount of testicular tissue and lower plasma 11-ketotestosterone levels compared to breeding males.

Population Dynamics of Sex‐Changing Fish Species in Marine Protected Areas

Easter et al. used population models to analyze the expected pattern of recovery of sex-changing fish populations inside marine protected areas (MPAs). Many fishes begin life female and then change to male when older. In these female-first (protogynous) species, harvest tends to selectively remove males, shifting sex ratios and impairing reproduction. Setting expectations for population recovery inside MPAs requires understanding how quickly sex ratios (and reproduction) rebound. Easter et al. show that whether sex-changing populations recover faster or slower than non-sex-changing species depends on how many males a population needs for successful reproduction. This quantity can be estimated using field experiments. These photographs illustrate the article “Influence of protogynous sex change on recovery of fish populations within marine protected areas” by E. E. Easter, M. S. Adreani, S. L. Hamilton, M. S. Steele, S. Pang, and J. W. White published in Ecological Applications. https://doi.org/10.1002/eap.2070

Steroidal regulation of the aromatase gene and dominant behavior in the false clown anemonefish Amphiprion ocellaris

The interaction between cortisol and aromatase may be a critical factor in sex determination or sex changes in teleost species. High cortisol concentrations inhibit transcription of the aromatase gene, resulting in masculinization. Anemonefish (Amphiprion spp.) are socially controlled, protandrous sex-changing fish, with a monogamous mating system. Females are the largest and most dominant members of social groups, second-ranking individuals become males, and other individuals remain nonreproductive. Individuals that change from male to female display high plasma cortisol concentrations, contrary to a previously established mechanism of masculinization. We investigated the effects of exogenous steroids on gene expression in the brain and gonads and on the occurrence of dominant behavior in the sexually immature ambisexual false clown anemonefish Amphiprion ocellaris. Transcription of the cyp19a1a aromatase gene increased in the gonads of estradiol pellet-fed fish but decreased in cortisol pellet-fed fish. Dominant behavior intensity significantly increased in estradiol pellet-fed fish, but decreased in cortisol pellet-fed fish. Methyltestosterone had no apparent effect on gene transcription or behavior. These results suggest that the masculinization mechanism induced by cortisol is common among teleost species, including protandrous sex-changing fish, and that behavioral changes induced by steroid supplements reflect social status in A. ocellaris.

Influence of protogynous sex change on recovery of fish populations within marine protected areas.

Marine protected areas (MPAs) are increasingly implemented as a conservation tool worldwide. In many cases, they are managed adaptively: the abundance of target species is monitored, and observations are compared to some model-based expectation for the trajectory of population recovery to ensure that the MPA is achieving its goals. Most previous analyses of the transient (short-term) response of populations to the cessation of fishing inside MPAs have dealt only with gonochore (fixed-sex) species. However, many important fishery species are protogynous hermaphrodites (female-to-male sex-changing). Because size-selective harvest will predominantly target males in these species, harvesting not only reduces abundance but also skews the sex ratio toward females. Thus the response to MPA implementation will involve changes in both survival and sex ratio, and ultimately reproductive output. We used an age-structured model of a generic sex-changing fish population to compare transient population dynamics after MPA implementation to those of an otherwise similar gonochore population and examine how different features of sex-changing life history affect those dynamics. We examined both demographically open (most larval recruitment comes from outside the MPA) and demographically closed (most larval recruitment is locally produced) dynamics. Under both scenarios, population recovery of protogynous species takes longer when fishing was more intense pre-MPA (as in gonochores), but also depends heavily on the mating function, the degree to which the sex ratio affects reproduction. If few males are needed and reproduction is not affected by a highly female-biased sex ratio, then population recovery is much faster; if males are a limiting resource, then increases in abundance after MPA implementation are much slower than for gonochores. Unfortunately, the mating function is largely unknown for fishes. In general, we expect that most protogynous species with haremic mating systems will be in the first category (few males needed), though there is at least one example of a fish species (though not a sex-changing species) for which males are limiting. Thus a better understanding of the importance of male fish to population dynamics is needed for the adaptive management of MPAs.