Behavioral and energetic costs of group membership in a coral reef fish

Animals in social aggregations often spend more time foraging than solitary conspecifics. This may be a product of the relative safety afforded by aggregations: group members can devote more time to foraging and less time to antipredator behaviors than solitary animals (the “risk reduction” effect). All else being equal, risk reduction should result in higher food intake for grouped animals. However, intragroup competition may force group members to spend more time foraging in order to obtain the same food ration as solitary individuals (the “resource competition” effect). We compared these opposing explanations of foraging time allocation in a coral reef fish, bluehead wrasse (Thalassoma bifasciatum). Aggregations of juvenile bluehead wrasse experience safety-in-numbers, and preliminary observations suggested that juveniles in aggregations spent more time foraging for copepods in the water column than solitary juveniles. However, the risk reduction and resource competition hypotheses are indistinguishable on the basis of behavioral observations alone. Therefore, we collected behavioral, dietary, and growth data (using otolith growth rings) for bluehead wrasse at multiple reefs around a Caribbean island. Despite spending more time foraging in the water column, grouped fish did not capture more prey items and had slower growth rates than solitary fish. Thus, the increased foraging time of grouped fish appears to reflect resource competition, not risk reduction. This competition may limit the size and frequency of aggregations among juvenile bluehead wrasse, which have been shown to experience reduced mortality rates in larger groups. Bluehead wrasse recruits also spent less time foraging but grew faster at sites where planktonic copepod prey were more abundant. This suggests the possibility that large-scale spatiotemporal variability in the abundance of planktonic copepods over coral reefs may produce corresponding variability in the dynamics of reef fish populations. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Increased H-Y antigen levels associated with behaviorally induced, female-to-male sex reversal in a coral-reef fish

It has been proposed that H-Y antigen is the synthetic product of sex-determining genes, and that H-Y antigen controls ontogenetic differentiation of the heterogametic sex throughout vertebrates. The coral-reef fish Anthias squamipinnis is a protogynous hermaphrodite in which all individuals mature initially as females. Males result when adult females change sex as a consequence of alterations in behavioral interactions within social groups. Three assay methods were used to measure H-Y antigen levels in the spleens, gonads, and epidermal tissue of 16 adult females and in 16 males that had been induced to change sex from a prior female phase by the removal of a pre-existing male from each of 16 social groups. In 15 male-female pairs, the H-Y antigen levels were higher in male than in female spleen, gonad, and epidermis tissues. The precise temporal relationship between the onset of sex change and the increase in the H-Y antigen level was not examined. If, as we strongly suspect, the temporal relationship proves to be close, the inference will be that the behavioral cues inducing sex change also influence the synthetic activity of genes controlling H-Y antigen production.     

Post-settlement emigration affects mortality estimates for two Bahamian wrasses

Understanding the dynamics of open marine populations is inherently complex, and this complexity has led to decades of debate regarding the relative importance of pre- versus post-settlement processes in structuring these populations. Movement between patches may be an important modifier of patterns established at settlement, yet local immigration and emigration have received less attention than other demographic rates. I examined loss rates from tagged populations of juvenile wrasses (yellowhead wrasse Halichoeres garnoti and bluehead wrasse Thalassoma bifasciatum) at two sites in the Bahamas. Assuming that all losses were due solely to mortality would have significantly underestimated survivorship of yellowhead wrasse by 29% and bluehead wrasse by 14%. On average, per capita mortality and emigration rates were higher for yellowhead than bluehead wrasse, but neither demographic rate differed between sites for either species. With respect to within-species density, bluehead wrasse mortality was density-dependent at the patch reef site, but mortality rates of yellowhead wrasse were consistently density-independent. Evaluating the effects of between-species density, yellowhead wrasse mortality increased with a decrease in bluehead wrasse density, but this effect was limited to the patch reef site. Emigration rates were not a function of either within-species or between-species density, but instead varied inversely with isolation distance. Numerous previous studies of coral-reef fish, conducted on patch reefs separated by only a few meters of sand and often using untagged fish, may have confounded losses due to emigration with those due to mortality. A better understanding of the factors affecting emigration in marine fishes is important to their effective management using spatial tools such as marine protected areas.     

Genetic basis and biotechnological manipulation of sexual dimorphism and sex determination in fish

Aquaculture has made an enormous contribution to the world food production,especially to the sustainable supply of animal proteins.The utility of diverse reproduction strategies in fish,such as the exploiting use of unisexual gynogenesis,has created a typical case of fish genetic breeding.A number of fish species show substantial sexual dimorphism that is closely linked to multiple economic traits including growth rate and body size,and the efficient development of sex-linked genetic markers and sex control biotechnologies has provided significant approaches to increase the production and value for commercial purposes.Along with the rapid development of genomics and molecular genetic techniques,the genetic basis of sexual dimorphism has been gradually deciphered,and great progress has been made in the mechanisms of fish sex determination and identification of sex-determining genes.This review summarizes the progress to provide some directive and objective thinking for further research in this field.     

Sexual determination and differentiation in teleost fish

The present work reviews the latest information on the cellular, molecular and physiological aspects of sexual determination and differentiation in teleost fish. The group exhibits a large variety of mechanisms of sexual determination. These may be genetic, or depend on environmental conditions such as temperature, pH, and social factors, all of which can influence the proportion of the sexes. Additionally, sex steroids play an important role in the regulation of sexual differentiation. The patterns of gonadal sexual differentiation are diverse, and species may be hermaphroditic or gonochoristic, some of the latter displaying juvenile hermaphroditism. In recent years, several genes involved in the sexual determination and differentiation pathways in vertebrates, particularly in mammals, have also been characterized in teleosts. Conserved as well as diversified functions have been proposed.     

The joy of sex pheromones

Sex pheromones provide an important means of communication to unite individuals for successful reproduction. Although sex pheromones are highly diverse across animals, these signals fulfil common fundamental roles in enabling identification of a mating partner of the opposite sex, the appropriate species and of optimal fecundity. In this review, we synthesize both classic and recent investigations on sex pheromones in a range of species, spanning nematode worms, insects and mammals. These studies reveal comparable strategies in how these chemical signals are produced, detected and processed in the brain to regulate sexual behaviours. Elucidation of sex pheromone communication mechanisms both defines outstanding models to understand the molecular and neuronal basis of chemosensory behaviours, and reveals how similar evolutionary selection pressures yield convergent solutions in distinct animal nervous systems.EMBO reports advance online publication 13 September 2013; doi:10.1038/embor.2013.140     

Arginine vasotocin regulation of interspecific cooperative behaviour in a cleaner fish

In an interspecific cooperative context, individuals must be prepared to tolerate close interactive proximity to other species but also need to be able to respond to relevant social stimuli in the most appropriate manner. The neuropeptides vasopressin and oxytocin and their non-mammalian homologues have been implicated in the evolution of sociality and in the regulation of social behaviour across vertebrates. However, little is known about the underlying physiological mechanisms of interspecific cooperative interactions. In interspecific cleaning mutualisms, interactions functionally resemble most intraspecific social interactions. Here we provide the first empirical evidence that arginine vasotocin (AVT), a non-mammalian homologue of arginine vasopressin (AVP), plays a critical role as moderator of interspecific behaviour in the best studied and ubiquitous marine cleaning mutualism involving the Indo-Pacific bluestreak cleaner wrasse Labroides dimidiatus. Exogenous administration of AVT caused a substantial decrease of most interspecific cleaning activities, without similarly affecting the expression of conspecific directed behaviour, which suggests a differential effect of AVT on cleaning behaviour and not a general effect on social behaviour. Furthermore, the AVP-V1a receptor antagonist (manning compound) induced a higher likelihood for cleaners to engage in cleaning interactions and also to increase their levels of dishonesty towards clients. The present findings extend the knowledge of neuropeptide effects on social interactions beyond the study of their influence on conspecific social behaviour. Our evidence demonstrates that AVT pathways might play a pivotal role in the regulation of interspecific cooperative behaviour and conspecific social behaviour among stabilized pairs of cleaner fish. Moreover, our results suggest that the role of AVT as a neurochemical regulator of social behaviour may have been co-opted in the evolution of cooperative behaviour in an interspecific context, a hypothesis that is amenable to further testing on the potential direct central mechanism involved.     

Cellular calcium and redox regulation: the mediator of vertebrate environmental sex determination?

Many reptiles and some fish determine offspring sex by environmental cues such as incubation temperature. The mechanism by which environmental signals are captured and transduced into specific sexual phenotypes has remained unexplained for over 50 years. Indeed, environmental sex determination (ESD) has been viewed as an intractable problem because sex determination is influenced by a myriad of genes that may be subject to environmental influence. Recent demonstrations of ancient, conserved epigenetic processes in the regulatory response to environmental cues suggest that the mechanisms of ESD have a previously unsuspected level of commonality, but the proximal sensor of temperature that ultimately gives rise to one sexual phenotype or the other remains unidentified. Here, we propose that in ESD species, environmental cues are sensed by the cell through highly conserved ancestral elements of calcium and redox (CaRe) status, then transduced to activate ubiquitous signal transduction pathways, or influence epigenetic processes, ultimately to drive the differential expression of sex genes. The early evolutionary origins of CaRe regulation, and its essential role in eukaryotic cell function, gives CaRe a propensity to be independently recruited for diverse roles as a ‘cellular sensor’ of environmental conditions. Our synthesis provides the first cohesive mechanistic model connecting environmental signals and sex determination pathways in vertebrates, providing direction and a framework for developing targeted experimentation.     

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.     

Decoding sex: Elucidating sex determination and how high-quality genome assemblies are untangling the evolutionary dynamics of sex chromosomes

Sexual reproduction is a diverse and widespread process. In gonochoristic species, the differentiation of sexes occurs through diverse mechanisms, influenced by environmental and genetic factors. In most vertebrates, a master-switch gene is responsible for triggering a sex determination network. However, only a few genes have acquired master-switch functions, and this process is associated with the evolution of sex-chromosomes, which have a significant influence in evolution. Additionally, their highly repetitive regions impose challenges for high-quality sequencing, even using high-throughput, state-of-the-art techniques. Here, we review the mechanisms involved in sex determination and their role in the evolution of species, particularly vertebrates, focusing on sex chromosomes and the challenges involved in sequencing these genomic elements. We also address the improvements provided by the growth of sequencing projects, by generating a massive number of near-gapless, telomere-to-telomere, chromosome-level, phased assemblies, increasing the number and quality of sex-chromosome sequences available for further studies.     

Visual sex discrimination in goldfish: seasonal, sexual, and androgenic influences

The olfactory signals used by goldfish for sexual and aggressive communication have been studied extensively, but little work has addressed the role of other sensory modalities in social communication in this species. We therefore investigated the role that visual stimuli play in sex discrimination and the ability of androgens, which masculinize courtship behavior, to affect behavioral responses toward female visual stimuli. We found that males selectively orient toward female visual stimuli during the breeding season but not outside it, whereas prostaglandin F2-alpha (PGF2alpha)-injected females do not differentially approach male and female visual stimuli, even during the breeding season. Implanting adult females with testosterone (T) and 11-ketotestosterone (KT), however, induced orientation responses toward female visual stimuli similar to those observed in males. These results indicate that visual sexual stimuli are likely important for reproductive signaling in goldfish, potentially helping males identify ovulating females from a distance in a shoal of fish, and that androgens can influence mechanisms associated with orientation responses toward such stimuli.     

The effect of local stock density on social behavior and sex change in the Mediterranean labrid Coris julis

Synopsis Two stocks of Coris julis, a protogynous hermaphrodite labrid fish, were studied in the field in Corsica (France) to observe the effect of stock density variations on the timing of sex change. A higher density was associated with lower terminal phase male's territory size and an earlier sex change whilst the proportion of terminal phase males in the stock increased. As well, the average number of females courted per terminal phase male and the percentage of spawning with non-territorial male interferences remained similar in the two situations. These results indicate that territory availability should be considered as an important cue for wrasse sex change.     

Evolution of fungal sex chromosomes

Sexual reproduction enables organisms to shuffle two parental genomes to produce recombinant progeny, and to purge the genome of deleterious mutations. Sex is conserved in virtually all organisms, from bacteria and fungi to plants and animals, and yet the mechanisms by which sexual identity are established share both conserved general features and are remarkably diverse. In animals, sexual identity is established by dimorphic sex chromosomes, whereas in fungi a specialized region of the genome, known as the mating-type locus, governs the establishment of cell type identity and differs in DNA sequence between cells of different mating-types. Recent studies on the mating-type loci of fungi and algae reveal features shared with the mammalian X and Y chromosomes, suggesting that these represent early steps in the evolution of sex chromosomes.     

A social basis for the development of primary males in a sex-changing fish

An example of alternative male strategies is seen in diandric protogynous (female first) hermaphrodites, where individuals either mature directly as male (primary males) or first reproduce as female and then change sex to male (secondary males). In some sex-changing fishes, the testes of primary males appear anatomically similar to those of non-sex-changing species, whereas the testes of secondary males have anatomical evidence of their former ovarian function. Here, we provide evidence that in the bluehead wrasse, Thalassoma bifasciatum, these strikingly different male phenotypes arise from differences in the ontogenetic timing of environmental sex determination, timing that can be experimentally altered through changes in the social circumstances. Juveniles differentiated almost exclusively as females when reared in isolation, regardless of whether they were collected from a reef with a high proportion of primary males or from a reef with a low proportion of primary males. In contrast, one individual usually differentiated as a primary male when reared in groups of three. Our results indicate that primary males of the bluehead wrasse are an environmentally sensitive developmental strategy that has probably evolved in response to variation in the reproductive success of primary males in populations of different sizes.     

Aromatase pathway mediates sex change in each direction

The enzyme aromatase controls the androgen/oestrogen ratio by catalysing the irreversible conversion of testosterone into oestradiol (E2). Therefore, the regulation of E2 synthesis by aromatase is thought to be critical in sexual development and differentiation. Here, we demonstrate for the first time that experimental manipulation of E2 levels via the aromatase pathway induces adult sex change in each direction in a hermaphroditic fish that naturally exhibits bidirectional sex change. Our results demonstrate that a single enzymatic pathway can regulate both female and male sexual differentiation, and that aromatase may be the key enzyme that transduces environmental, including social, cues to functional sex differentiation in species with environmental sex determination.     

Experimentally induced variation in neuroendocrine processes affects male reproductive behaviour,sperm characteristics and social interactions

While extensive research has focused on how social interactions evolve, the fitness consequences of the neuroendocrine mechanisms underlying these interactions have rarely been documented, especially in the wild. Here, we measure how the neuroendocrine mechanisms underlying male behaviour affect mating success and sperm competition in the ocellated wrasse (Symphodus ocellatus). In this species, males exhibit three alternative reproductive types. “Nesting males” provide parental care, defend territories and form cooperative associations with unrelated “satellites,” who cheat by sneaking fertilizations but help by reducing sperm competition from “sneakers” who do not cooperate or provide care. To measure the fitness consequences of the mechanisms underlying these social interactions, we used “phenotypic engineering” that involved administering an androgen receptor antagonist (flutamide) to wild, free‐living fish. Nesting males treated with flutamide shifted their aggression from sneakers to satellite males and experienced decreased submissiveness by sneaker males (which correlated with decreased nesting male mating success). The preoptic area (POA), a region controlling male reproductive behaviours, exhibited dramatic down‐regulation of androgen receptor (AR) and vasotocin 1a receptor (V1aR) mRNA following experimental manipulation of androgen signalling. We did not find a direct effect of the manipulation on male mating success, paternity or larval production. However, variation in neuroendocrine mechanisms generated by the experimental manipulation was significantly correlated with changes in behaviour and mating success: V1aR expression was negatively correlated with satellite‐directed aggression, and expression of its ligand arginine vasotocin (AVT) was positively correlated with courtship and mating success, thus revealing the potential for sexual selection on these mechanisms.     

Regain of sex determination system and sexual reproduction ability in a synthetic octoploid male fish

Polyploids in vertebrates are generally associated with unisexual reproduction, but the direct consequences of polyploidy on sex determination system and reproduction mode remain unknown. Here, we synthesized a group of artificial octoploids between unisexual gynogenetic hexaploid Carassius gibelio and sexual tetraploid Carassius auratus. The synthetic octoploids were revealed to have more than 200 chromosomes, in which 50 chromosomes including the X/Y sex determination system were identified to transfer from sexual tetraploid C. auratus into the unisexual gynogenetic hexaploid C. gibelio. Significantly, a few synthetic octoploid males were found to be fertile, and one octoploid male was confirmed to regain sexual reproduction ability,which exhibits characteristics that are the same to sexual reproduction tetraploid males, such as 1:1 sex ratio occurrence, meiosis completion and euploid sperm formation in spermatogenesis, as well as normal embryo development and gene expression pattern during embryogenesis. Therefore, the current finding provides a unique case to explore the effect of sex determination system incorporation on reproduction mode transition from unisexual gynogenesis to sexual reproduction along with genome synthesis of recurrent polyploidy in vertebrates.