Fish as a model in social neuroscience: conservation and diversity in the social brain network

Mechanisms for fish social behaviours involve a social brain network (SBN) which is evolutionarily conserved among vertebrates. However, considerable diversity is observed in the actual behaviour patterns amongst nearly 30000 fish species. The huge variation found in socio-sexual behaviours and strategies is likely generated by a morphologically and genetically well-conserved small forebrain system. Hence, teleost fish provide a useful model to study the fundamental mechanisms underlying social brain functions. Herein we review the foundations underlying fish social behaviours including sensory, hormonal, molecular and neuroanatomical features. Gonadotropin-releasing hormone neurons clearly play important roles, but the participation of vasotocin and isotocin is also highlighted. Genetic investigations of developing fish brain have revealed the molecular complexity of neural development of the SBN. In addition to straightforward social behaviours such as sex and aggression, new experiments have revealed higher order and unique phenomena such as social eavesdropping and social buffering in fish. Finally, observations interpreted as ‘collective cognition’ in fish can likely be explained by careful observation of sensory determinants and analyses using the dynamics of quantitative scaling. Understanding of the functions of the SBN in fish provide clues for understanding the origin and evolution of higher social functions in vertebrates.     

Gene expression in the social behavior network of the wire‐tailed manakin (Pipra filicauda) brain

The vertebrate basal forebrain and midbrain contain a set of interconnected nuclei that control social behavior. Conserved anatomical structures and functions of these nuclei have now been documented among fish, amphibians, reptiles, birds and mammals, and these brain regions have come to be known as the vertebrate social behavior network (SBN). While it is known that nuclei (nodes) of the SBN are rich in steroid and neuropeptide activity linked to behavior, simultaneous variation in the expression of neuroendocrine genes among several SBN nuclei has not yet been described in detail. In this study, we use RNA‐seq to profile gene expression across seven brain regions representing five nodes of the vertebrate SBN in a passerine bird, the wire‐tailed manakin Pipra filicauda. Using weighted gene co‐expression network analysis, we reconstructed sets of coregulated genes, showing striking patterns of variation in neuroendocrine gene expression across the SBN. We describe regional variation in gene networks comprising a broad set of hormone receptors, neuropeptides, steroidogenic enzymes, catecholamines and other neuroendocrine signaling molecules. Our findings show heterogeneous patterns of brain gene expression across nodes of the avian SBN and provide a foundation for future analyses of how the regulation of gene networks may mediate social behavior. These results highlight the importance of region‐specific sampling in studies of the mechanisms of behavior.     

Social behavior in context: Hormonal modulation of behavioral plasticity and social competence

In social species animals should fine-tune the expression of their social behavior to social environments in order to avoid the costs of engaging in costly social interactions. Therefore, social competence, defined as the ability of an animal to optimize the expression of its social behavior as a function of the available social information, should be considered as a performance trait that impacts on the Darwinian fitness of the animal. Social competence is based on behavioral plasticity which, in turn, can be achieved by different neural mechanisms of plasticity, namely by rewiring or by biochemically switching nodes of a putative neural network underlying social behavior. Since steroid hormones respond to social interactions and have receptors extensively expressed in the social behavioral neural network, it is proposed that steroids play a key role in the hormonal modulation of social plasticity. Here, we propose a reciprocal model for the action of androgens on short-term behavioral plasticity and review a set of studies conducted in our laboratory using an African cichlid fish (Oreochromis mossambicus) that provide support for it. Androgens are shown to be implicated as physiological mediators in a wide range of social phenomena that promote social competence, namely by adjusting the behavioral response to the nature of the intruder and the presence of third parties (dear enemy and audience effects), by anticipating territorial intrusions (bystander effect and conditioning of the territorial response), and by modifying future behavior according to prior experience of winning (winner effect). The rapid behavioral actions of socially induced short-term transient changes in androgens indicate that these effects are most likely mediated by nongenomic mechanisms. The fact that the modulation of rapid changes in behavior is open to the influence of circulating levels of androgens, and is not exclusively achieved by changes in central neuromodulators, suggests functional relevance of integrating body parameters in the behavioral response. Thus, the traditional view of seeing neural circuits as unique causal agents of behavior should be updated to a brain-body-environment perspective, in which these neural circuits are embodied and the behavioral performance (and outcomes as fitness) depends on a dynamic relationship between the different levels. In this view hormones play a major role as behavioral modulators.     

Exogenous vasotocin alters aggression during agonistic exchanges in male Amargosa River pupfish (Cyprinodon nevadensis amargosae)

Pupfishes in the Death Valley region have rapidly differentiated in social behaviors since their isolation in a series of desert streams, springs, and marshes less than 20,000 years ago. These habitats can show dramatic fluctuations in ecological conditions, and pupfish must cope with the changes by plastic physiological and behavioral responses. Recently, we showed differences among some Death Valley populations in brain expression of arginine vasotocin (AVT). As AVT regulates both hydromineral balance and social behaviors in other taxa, these population differences may indicate adaptive changes in osmoregulatory and/or behavioral processes. To test whether AVT is relevant for behavioral shifts in these fish, here we examined how manipulations to the AVT system affect agonistic and reproductive behaviors in Amargosa River pupfish (Cyprinodon nevadensis amargosae). We administered exogenous AVT (0.1, 1, and 10 microg/g body weight) and an AVP V1 receptor antagonist (Manning compound, 2.5 microg/g body weight) intraperitoneally to males in mixed-sex groups in the laboratory. We found that AVT reduced the initiation of aggressive social interactions with other pupfish but had no effect on courtship. The effects of AVT were confirmed in males in the wild where AVT (1 microg/g body weight) reduced the aggressive initiation of social interactions and decreased aggressive responses to the behavior of other males. Combined, these results show that AVT can modulate agonistic behaviors in male pupfish and support the idea that variation in AVT activity may underlie differences in aggression among Death Valley populations.     

From molecule to behavior: Brain aromatase (cyp19a1b) characterization,expression analysis and its relation with social status and male agonistic behavior in a Neotropical cichlid fish

The enzyme aromatase, responsible for the conversion of C19 androgens to C18 estrogens, exists as two paralogue copies in teleost fish: Cyp19a1a mostly expressed in the gonads, referred as gonadal aromatase, and Cyp19a1b, mostly expressed in the brain, accordingly known as brain aromatase. The neural localization of Cyp19a1b is greatly contained within the social behavior network and mesolimbic reward system in fish, suggesting a strong role of estrogen synthesis in the regulation of social behavior. In this work we aimed to analyze the variation in cyp19a1b expression in brain and pituitary of males of a highly social cichlid, Cichlasoma dimerus (locally known as chanchita), and its relation with inter-individual variability in agonistic behavior in a communal social environment. We first characterized chanchita's cyp19a1b mRNA and deduced amino acid sequence, which showed a high degree of conservation when compared to other teleost brain aromatase sequences, and its tissue expression patterns. Within the brain, Cyp19a1b was solely detected at putative radial glial cells of the forebrain, close to the brain ventricles. We then studied the relative expression levels of cyp19a1b by Real Time PCR in the brain and pituitary of males of different social status, territorial vs. non-territorial, and its relationship with an index of agonistic behavior. We found that even though, brain aromatase expression did not differ between types of males, pituitary cyp19a1b expression levels positively correlated with the index of agonistic behavior. This suggests a novel role of the pituitary in the regulation of social behavior by local estrogen synthesis.     

FUNCTIONAL INNOVATIONS AND MORPHOLOGICAL DIVERSIFICATION IN PARROTFISH

The association between diversification and evolutionary innovations has been well documented and tested in studies of taxonomic richness but the impact that such innovations have on the diversity of form and function is less well understood. Using phylogenetically rigorous techniques, we investigated the association between morphological diversity and two design breakthroughs within the jaws of parrotfish. Similar intramandibular joints and other modifications of the pharyngeal jaws have evolved repeatedly in teleost fish and are frequently hypothesized to promote diversity. We quantified morphological diversity within six functionally important oral jaw traits using the Brownian motion rate of evolution to correct for phylogenetic and time‐related biases and compared these rates across clades that did and did not possess the intramandibular joint and the parrotfish pharyngeal jaw. No change in morphological diversity was associated with the pharyngeal jaw modification alone but rates of oral jaw diversification were up to 8× faster in parrotfish species that possessed both innovations. Interestingly, this morphological diversity may not have led to differential resource uses as available data suggest that members of this clade show remarkable homogeneity of diet.     

Ecologically relevant genetic variation from a non-Arabidopsis perspective

Ecologically relevant genetic variation occurs in genes harbouring alleles that are adaptive in some environments but not in others. Analysis of this type of genetic variation in model organisms has made substantial progress, and is now being expanded to other species in order to better cover the diversity of plant life. Recent advances in connecting ecological and molecular studies in non-model species have been made with regard to edaphic and climatic adaptation, plant reproduction, life-history parameters and biotic interactions. New research avenues that increase biological complexity and ecological relevance by integrating ecological experiments with population genetic and functional genomic approaches provide new insights into the genetic basis of ecologically relevant variation.     

Behavioral flexibility in rats and mice: contributions of distinct frontocortical regions

Research examining the contribution of genetics to behavior is increasingly focused on higher order behavioral and cognitive processes including the ability to modify behaviors when environmental demands change. The frontal cortices of mammals, including rodents, subserve a diverse set of behavioral and cognitive functions including motor planning, social behavior, evaluation of expected outcomes and working memory, which may be particularly sensitive to genetic factors and interactions with experience (e.g. stress). Behavioral flexibility is a core attribute of these functions. This review orients readers to the current landscape of the literature on the frontocortical bases of behavioral flexibility in rodent laboratory experiments. Studies are divided into three broad categories: reversal learning, inhibitory learning and set‐shifting. Functional dissociations within the broader scope of behavioral flexibility are reviewed, followed by discussion of the associations between specific components of frontal cortex and specific aspects of relevant behavioral processes. Finally, the authors identify open questions that need to be addressed to better establish the constituents of frontal cortex underlying behavioral flexibility.     

Convergent evolution of cysteine residues in sperm protamines of one genus of marsupials, the Planigales

A characteristic feature of the sperm P1 protamines of eutherian mammals is the constant presence of six to nine cysteine residues per molecule. During spermiogenesis these residues become oxidized to form a three-dimensional network of disulfide bridges between, and within, protamine molecules in the sperm chromatin. This covalent cross linking strongly stabilizes eutherian sperm nuclei. In contrast, protamines sequenced from teleost fish, birds, monotremes, and marsupials all lack cysteine residues and their sperm nuclei, without the stabilizing cross links, are easily decondensed in vitro. We have now found that one genus of tiny, shrewlike dasyurid marsupials, the Planigales, possess P1 protamines containing five to six cysteine residues. These residues appear to have evolved since the divergence of Planigales from other members of the family Dasyuridae, such as the marsupial mouse, Sminthopsis crassicaudata. We believe this constitutes a case of convergent evolution in a subfamily of dasyurid marsupials toward the cysteine-rich eutherian form of sperm protamine P1.      

A Comparative Perspective on Brain Regeneration in Amphibians and Teleost Fish

Regeneration of lost cells in the central nervous system, especially the brain, is present to varying degrees in different species. In mammals, neuronal cell death often leads to glial cell hypertrophy, restricted proliferation, and formation of a gliotic scar, which prevents neuronal regeneration. Conversely, amphibians such as frogs and salamanders and teleost fish possess the astonishing capacity to regenerate lost cells in several regions of their brains. While frogs lose their regenerative abilities after metamorphosis, teleost fish and salamanders are known to possess regenerative competence even throughout adulthood. In the last decades, substantial progress has been made in our understanding of the cellular and molecular mechanisms of brain regeneration in amphibians and fish. But how similar are the means of brain regeneration in these different species? In this review, we provide an overview of common and distinct aspects of brain regeneration in frog, salamander, and teleost fish species: from the origin of regenerated cells to the functional recovery of behaviors.     

Stress coping style predicts aggression and social dominance in rainbow trout

Social stress is frequently used as a model for studying the neuroendocrine mechanisms underlying stress-induced behavioral inhibition, depression, and fear conditioning. It has previously been shown that social subordination may result in increased glucocorticoid release and changes in brain signaling systems. However, it is still an open question which neuroendocrine and behavioral differences are causes, and which are consequences of social status. Using juvenile rainbow trout of similar size and with no apparent differences in social history, we demonstrate that the ability to win fights for social dominance can be predicted from the duration of a behavioral response to stress, in this case appetite inhibition after transfer to a new environment. Moreover, stress responsiveness in terms of confinement-induced changes in plasma cortisol was negatively correlated to aggressive behavior. Fish that exhibited lower cortisol responses to a standardized confinement test were markedly more aggressive when being placed in a dominant social position later in the study. These findings support the view that distinct behavioral-physiological stress coping styles are present in teleost fish, and these coping characteristics influence both social rank and levels of aggression.     

Endocrine mechanisms,behavioral phenotypes and plasticity: known relationships and open questions

Behavior of wild vertebrate individuals can vary in response to environmental or social factors. Such within-individual behavioral variation is often mediated by hormonal mechanisms. Hormones also serve as a basis for among-individual variations in behavior including animal personalities and the degree of responsiveness to environmental and social stimuli. How do relationships between hormones and behavioral traits evolve to produce such behavioral diversity within and among individuals? Answering questions about evolutionary processes generating among-individual variation requires characterizing how specific hormones are related to variation in specific behavioral traits, whether observed hormonal variation is related to individual fitness and, whether hormonal traits are consistent (repeatable) aspects of an individual's phenotype. With respect to within-individual variation, we need to improve our insight into the nature of the quantitative relationships between hormones and the traits they regulate, which in turn will determine how they may mediate behavioral plasticity of individuals. To address these questions, we review the actions of two steroid hormones, corticosterone and testosterone, in mediating changes in vertebrate behavior, focusing primarily on birds. In the first part, we concentrate on among-individual variation and present examples for how variation in corticosterone concentrations can relate to behaviors such as exploration of novel environments and parental care. We then review studies on correlations between corticosterone variation and fitness, and on the repeatability over time of corticosterone concentrations. At the end of this section, we suggest that further progress in our understanding of evolutionary patterns in the hormonal regulation of behavior may require, as one major tool, reaction norm approaches to characterize hormonal phenotypes as well as their responses to environments.In the second part, we discuss types of quantitative relationships between hormones and behavioral traits within individuals, using testosterone as an example. We review conceptual models for testosterone-behavior relationships and discuss the relevance of these models for within-individual plasticity in behavior. Next, we discuss approaches for testing the nature of quantitative relationships between testosterone and behavior, concluding that again reaction norm approaches might be a fruitful way forward.We propose that an integration of new tools, especially of reaction norm approaches into the field of behavioral endocrinology will allow us to make significant progress in our understanding of the mechanisms, the functional implications and the evolution of hormone–behavior relationships that mediate variation both within and among individuals. This knowledge will be crucial in light of already ongoing habitat alterations due to global change, as it will allow us to evaluate the mechanisms as well as the capacity of wild populations to adjust hormonally-mediated behaviors to altered environmental conditions.     

Genetic diversity within vertebrate species is greater at lower latitudes

The latitudinal gradient of species diversity is one of the oldest recognized patterns in biology. While the cause of the pattern remains debated, the global signal of greater diversity toward the tropics is widely established. Whether the pattern holds for genetic diversity within species, however, has received much less attention. We examine latitudinal variation of intraspecific genetic diversity by contrasting nucleotide distance within low- and high-latitude animal groups. Using mitochondrial DNA markers across 72 vertebrate species that together span six continents, two oceans, and 129 degrees of latitude, we found significantly greater genetic diversity at low latitudes within mammalian species, and trends consistent with this pattern in reptiles, amphibians, fish, and birds. The signal held even after removing species whose current geographic ranges include areas recently covered by glaciers during the late Pleistocene and which presumably have experienced colonization bottlenecks in high latitudes. Higher genetic diversity within species was found at low latitudes also for genera that do not possess higher species richness toward the tropics. Moreover, examination of a subset of species with sufficient sampling across a broad geographic range revealed that genetic variation demonstrates a typical gradient, with mid-latitude populations intermediate in genetic diversity between high and low latitude ones. These results broaden the pattern of the global latitudinal diversity gradient, to now include variation within species. These results are also concordant with other studies indicating that low latitude populations and species are on different evolutionary trajectories than high latitude ones, and we speculate that higher rates of evolution toward the equator are driving the pattern for genetic diversity within species.     

Does geography or ecology best explain 'cultural' variation among chimpanzee communities?

Much attention has been paid to geographic variation in chimpanzee behavior, but few studies have applied quantitative techniques to explain this variation. Here, we apply methods typically utilized in macroecology to explain variation in the putative cultural traits of chimpanzees. We analyzed published data containing 39 behavioral traits from nine chimpanzee communities. We used a canonical correspondence analysis to examine the relative importance of environmental characteristics and geography, which may be a proxy for inter-community gene flow and/or social transmission, for explaining geographic variation in chimpanzee behavior. We found that geography, and longitude in particular, was the best predictor of behavioral variation. Chimpanzee communities in close longitudinal proximity to each other exhibit similar behavioral repertoires, independent of local ecological factors. No ecological variables were significantly related to behavioral variation. These results support the idea that inter-community dispersal patterns have played a major role in structuring behavioral variation. We cannot be certain whether behavioral variation has a genetic basis, is the result of innovation and diffusion, or a combination of the two.     

Differences in the behavior and diet between shoaling and solitary surgeonfish (Acanthurus triostegus)

Variation in behavior within marine and terrestrial species can influence the functioning of the ecosystems they inhabit. However, the contribution of social behavior to ecosystem function remains underexplored. Many coral reef fish species provide potentially insightful models for exploring how social behavior shapes ecological function because they exhibit radical intraspecific variation in sociality within a shared habitat. Here, we provide an empirical exploration on how the ecological function of a shoaling surgeonfish (Acanthurus triostegus) may differ from that of solitary conspecifics on two Pacific coral reefs combining insight from behavioral observations, stable isotope analysis, and macronutrient analysis of gut and fecal matter. We detected important differences in how the social mode of A. triostegus affected its spatial and feeding ecology, as well as that of other reef fish species. Specifically, we found increased distance traveled and area covered by shoaling fish relative to solitary A. triostegus. Additionally, shoaling A. triostegus primarily grazed within territories of other herbivorous fish and had piscivorous and nonpiscivorous heterospecific fish associated with the shoal, while solitary A. triostegus grazed largely grazed outside of any territories and did not have any such interactions with heterospecific fish. Results from stable isotope analysis show a difference in δ15N isotopes between shoaling and solitary fish, which suggests that these different social modes are persistent. Further, we found a strong interaction between social behavior and site and carbohydrate and protein percentages in the macronutrient analysis, indicating that these differences in sociality are associated with measurable differences in both the feeding ecology and nutrient excretion patterns. Our study suggests that the social behavior of individuals may play an important and underappreciated role in mediating their ecological function.     

鱼类特异的基因组复制

辐鳍鱼类是脊椎动物中种类最多、分布最广的类群,其基因组大小不等。过去的观点认为,在脊椎动物进化历程中曾发生了两次基因组复制。近期的系统基因组学研究资料进一步提出,在大约350百万年,辐鳍鱼还发生了第三次基因组复制,即鱼类特异的基因组复制(fish-specificgenomeduplication,FSGD),且发生的时间正处在“物种极度丰富”的硬骨鱼谱系(真骨总目)和“物种贫乏”的谱系(辐鳍鱼纲基部的类群)出现分歧的时间点,表明FSGD与硬骨鱼物种和生物多样性的增加有关。进一步开展鱼类比较基因组学和功能基因组学研究将进一步验证FSGD这一假说。     

Subfunction partitioning, the teleost radiation and the annotation of the human genome

Half of all vertebrate species are teleost fish. What accounts for this explosion of biodiversity? Recent evidence and advances in evolutionary theory suggest that genomic features could have played a significant role in the teleost radiation. This review examines evidence for an ancient whole-genome duplication (tetraploidization) event that probably occurred just before the teleost radiation. The partitioning of ancestral subfunctions between gene copies arising from this duplication could have contributed to the genetic isolation of populations, to lineage-specific diversification of developmental programs, and ultimately to phenotypic variation among teleost fish. Beyond its importance for understanding mechanisms that generate biodiversity, the partitioning of subfunctions between teleost co-orthologs of human genes can facilitate the identification of tissue-specific conserved noncoding regions and can simplify the analysis of ancestral gene functions obscured by pleiotropy or haploinsufficiency. Applying these principles on a genomic scale can accelerate the functional annotation of the human genome and understanding of the roles of human genes in health and disease.     

Identification of protein kinase C (PKC) isoforms in teleostean, amphibian and avian pigment cells

The beta isoform of protein kinase C (PKC) has been described as the main isoform involved in the stimulation of melanogenesis in mammalian skin melanocytes. Little is known about PKC isoforms in non-mammalian pigment cells. In neopterigian fish (holostei and teleostei), PKC is associated with pigment granule aggregation within the pigment cells (skin lightening), whereas in elasmobranchs and tetrapods, the activation of PKC leads to pigment granule dispersion (skin darkening). In an attempt to a better understanding of this distinct functional behavior upon PKC activation, we decided to investigate the PKC isoforms expressed in pigment cell lines of teleost fish, amphibians and birds, using RT-PCR followed by cloning and sequencing. Our results demonstrate the presence of messenger RNA (mRNA) for the following PKC isoforms: beta 1, lambda and iota in GEM-81 cells (Carassius auratus erythrophoroma), beta 1, beta 2 and zeta in Xenopus laevis (amphibian) melanophores; beta 1 and lambda in Gallus gallus (chicken) primary melanocytes. Beta 1 PKC seems to be conserved throughout phylogeny, but the diversity of the other isoforms in the different groups may account for the functional differences after PKC activation, which are observed between teleost and tetrapod pigment cells.