The correlation between subordinate fish eye colour and received attacks: a negative social feedback mechanism for the reduction of aggression during the formation of dominance hierarchies

Eye darkening has been linked to social status in fish. The subordinate's eyes darken, while the eyes of the dominant fish become pale. Although this phenomenon has been described in salmonid fishes and in the African cichlid Nile tilapia Oreochromis niloticus, it is unclear whether eye darkening correlates with a reduction in aggressive behaviour. Thus, we evaluated the link between social status and eye darkening. We evaluated whether the eye colours of subordinate fish correlate with the frequency of received attacks in a neotropical fish, the pearl cichlid Geophagus brasiliensis. We paired pearl cichlids and quantified both the aggressive behaviour and the eye darkening of each fish. As has been described for Nile tilapia and Atlantic salmon, a clear-cut hierarchical relationship formed, where dominance and subordination were associated with pale and dark eye colours, respectively. Initially, eye colour darkening was positively correlated with the frequency of received attacks; however, a negative association occurred following eye darkening, in which the intensity of aggressive interactions decreased. Thus, fish that initially received a high number of attacks signalled subordination more rapidly and intensely (rapid and dramatic eye darkening), thereby inducing a negative social feedback mechanism that led to reduced aggression.     

The relationship between dominance behaviour and growth as a function of habitat stability and community complexity: a test using salmon and trout

Predation shortly after release is the main source of mortality among hatchery‐reared fish used to restore or enhance endangered salmonid populations. We found, that hatchery‐reared salmonid young originating from endangered stocks have weak innate responses to their natural fish predators. The ability to avoid predation in fish can be improved through social learning from experienced to naïve individuals. Huge benefits would be achieved, if social learning processes could be successfully applied on a large scale to enhance viability of hatchery fish prior to release into the wild. By using model predators together with chemical cues from real predators we tested if social learning could be used to train hatchery‐reared salmonid young to avoid fish predators. As there are clear differences in social behaviour among the salmonid species, we first examined whether these differences affect the probability and efficiency of learning anti‐predator skills from trained demonstrators. We compared anti‐predator responses of observers (fish trained by using experienced fish as demonstrators) with those of control fish, which had been 'trained' by untrained naïve conspecifics. We also examined how the efficiency of social learning depends on the ratio of experienced to naïve fish involved in social transmission trials. The results of these experiments will give guidelines how social learning could be utilized in developing hatchery scale training protocols.     

Social Interactions through the Eyes of Macaques and Humans

Group-living primates frequently interact with each other to maintain social bonds as well as to compete for valuable resources. Observing such social interactions between group members provides individuals with essential information (e.g. on the fighting ability or altruistic attitude of group companions) to guide their social tactics and choice of social partners. This process requires individuals to selectively attend to the most informative content within a social scene. It is unclear how non-human primates allocate attention to social interactions in different contexts, and whether they share similar patterns of social attention to humans. Here we compared the gaze behaviour of rhesus macaques and humans when free-viewing the same set of naturalistic images. The images contained positive or negative social interactions between two conspecifics of different phylogenetic distance from the observer; i.e. affiliation or aggression exchanged by two humans, rhesus macaques, Barbary macaques, baboons or lions. Monkeys directed a variable amount of gaze at the two conspecific individuals in the images according to their roles in the interaction (i.e. giver or receiver of affiliation/aggression). Their gaze distribution to non-conspecific individuals was systematically varied according to the viewed species and the nature of interactions, suggesting a contribution of both prior experience and innate bias in guiding social attention. Furthermore, the monkeys’ gaze behavior was qualitatively similar to that of humans, especially when viewing negative interactions. Detailed analysis revealed that both species directed more gaze at the face than the body region when inspecting individuals, and attended more to the body region in negative than in positive social interactions. Our study suggests that monkeys and humans share a similar pattern of role-sensitive, species- and context-dependent social attention, implying a homologous cognitive mechanism of social attention between rhesus macaques and humans.     

Improving anti‐predator responses of hatchery reared salmonids by social learning

Predation shortly after release is the main source of mortality among hatchery‐reared fish used to restore or enhance endangered salmonid populations. We found, that hatchery‐reared salmonid young originating from endangered stocks have weak innate responses to their natural fish predators. The ability to avoid predation in fish can be improved through social learning from experienced to naïve individuals. Huge benefits would be achieved, if social learning processes could be successfully applied on a large scale to enhance viability of hatchery fish prior to release into the wild. By using model predators together with chemical cues from real predators we tested if social learning could be used to train hatchery‐reared salmonid young to avoid fish predators. As there are clear differences in social behaviour among the salmonid species, we first examined whether these differences affect the probability and efficiency of learning anti‐predator skills from trained demonstrators. We compared anti‐predator responses of observers (fish trained by using experienced fish as demonstrators) with those of control fish, which had been ‘trained’ by untrained naïve conspecifics. We also examined how the efficiency of social learning depends on the ratio of experienced to naïve fish involved in social transmission trials. The results of these experiments will give guidelines how social learning could be utilized in developing hatchery scale training protocols.     

The costs of hemispheric specialization in a fish

Laboratory and field studies have documented better cognitive performance associated with marked hemispheric specialization in organisms as diverse as chimpanzees, domestic chicks and topminnows. While providing an evolutionary explanation for the emergence of cerebral lateralization, this evidence represents a paradox because a large proportion of non-lateralized (NL) individuals is commonly observed in animal populations. Hemispheric specialization often determines large left–right differences in perceiving and responding to stimuli. Using topminnows selected for a high or low degree of lateralization, we tested the hypothesis that individuals with greater functional asymmetry pay a higher performance cost in situations requiring matching information from the two eyes. When trained to use the middle door in a row of a nine, NL fish correctly chose the central door in most cases, while lateralized fish showed systematic leftward or rightward biases. When choosing between two shoals, each seen with a different eye, NL fish chose the high-quality shoal significantly more often than the lateralized fish, whose performance was affected by eye preference for analysing social stimuli. These findings suggest the existence of a trade-off between computational advantages of hemispheric specialization and the ecological cost of making suboptimal decisions whenever relevant information is located on both sides of the body.     

The impact of individual perceptual and cognitive factors on collective states in a data-driven fish school model

In moving animal groups, social interactions play a key role in the ability of individuals to achieve coordinated motion. However, a large number of environmental and cognitive factors are able to modulate the expression of these interactions and the characteristics of the collective movements that result from these interactions. Here, we use a data-driven fish school model to quantitatively investigate the impact of perceptual and cognitive factors on coordination and collective swimming patterns. The model describes the interactions involved in the coordination of burst-and-coast swimming in groups of Hemigrammus rhodostomus. We perform a comprehensive investigation of the respective impacts of two interactions strategies between fish based on the selection of the most or the two most influential neighbors, of the range and intensity of social interactions, of the intensity of individual random behavioral fluctuations, and of the group size, on the ability of groups of fish to coordinate their movements. We find that fish are able to coordinate their movements when they interact with their most or two most influential neighbors, provided that a minimal level of attraction between fish exist to maintain group cohesion. A minimal level of alignment is also required to allow the formation of schooling and milling. However, increasing the strength of social interactions does not necessarily enhance group cohesion and coordination. When attraction and alignment strengths are too high, or when the heading random fluctuations are too large, schooling and milling can no longer be maintained and the school switches to a swarming phase. Increasing the interaction range between fish has a similar impact on collective dynamics as increasing the strengths of attraction and alignment. Finally, we find that coordination and schooling occurs for a wider range of attraction and alignment strength in small group sizes.     

Der Micos-Fisch,Höhlenfisch in statu nascendi oder Bastard ?

The Micos Population–cave fish in statu nascendi or hybrid? Observations on the evolution of cavernicoles The Micos-Cave in the Sierra de la Colmena in the State of San Luis Potosi, Mexico, contains a cavernicolous population of Astyanax mexicanus, whose members are for the most part blind, but, in contrast to other cave dwelling populations of the same species, appear almost normal in their pigmentation. Besides these, there are also large eyed and pigmented specimens to be found in this cave. Any transitional stages between the blind and the normal visioned fish are lacking. Offspring of the blind cavernicoles that are raised under light conditions develop a superficially lying eye which is markedly smaller than normal, attaining its size proportional to the light-intensity of the experimental conditions. The size and structure of the eye-remnants of the blind fish as well as the eyes of their offspring are considerably more variable than in the river specimens. Crossings of the blind Micos fish with the river fish Astyanax and also with a blind and unpigmented troglobiont of the same species - Sabinos fish - result in both cases in a more or less intermediate F¹-hybrid. A strict inbreeding within the Micos fish, selecting specimens with especially large eyes, produced animals whose eyes are comparable to those of the river fish after only three offspring generations. Electrophoresis studies on the allozyme variability at various loci prove that the Micos fish is genetically only slightly different compared to the river fish. On the other hand in some allele frequencies there is an alternative variation between the two. The Micos fish also differs from the typical troglobionts which are monomorphic at almost all loci examined and also possess alleles that are not found in the river form. Based on the genetic constitution, the Micos fish and the river fish found in the cave do not form a panmictic population. It is also doubtful that the Micos fish is the progeny of a hybrid swarm which previously resulted from a cross between a real troglobiont and the newly arrived river fish, because the Micos fish is in every characteristic genetically very similar to the river fish, whereas no clear traces of troglobiont relationship are found. Thus the Micos fish actually appears to be a cave form in statu nascendi against which the river fish that find their way in from time to time cannot compete.     

On the social nature of eyes: The effect of social cues in interaction and individual choice tasks

In an experimental setting, we applied a dual strategy to better understand the effect of pictures of eyes on human behavior. First, we investigated whether the effect of eyes was limited to interaction tasks in which the subjects' decisions influenced the outcomes of other subjects. We expanded the range of tasks to include individual choice tasks in which the subjects' decisions only influenced their own outcomes. Second, we investigated whether pictures of eyes were one of many social cues or were unique in their effect. We compared the effect of pictures of eyes with the effect of a different condition in which we presented the subjects with pictures of other students (peers). Our results suggest that the effect of pictures of eyes is limited to interaction tasks and that eyes should be considered distinct from other social cues, such as reminders of peers. While pictures of eyes uniformly enhanced pro-social behavior in interaction tasks, this was not the case for reminders of peers. Furthermore, the reminders of peers led to more rational behavior in individual choice tasks, whereas the effect of pictures of eyes was limited to situations involving interaction. Combined, these findings are in line with the claim that the effect of pictures of eyes on behavior is caused by a social exchange heuristic that works to enhance mutual cooperative behavior.     

The circular RNA circBCL2L1 regulates innate immune responses via microRNA-mediated downregulation of TRAF6 in teleost fish

Growing numbers of studies have shown that circular RNAs (circRNAs) can function as regulatory factors to regulate the innate immune response, cell proliferation, cell migration, and other important processes in mammals. However, the function and regulatory mechanism of circRNAs in lower vertebrates are still unclear. Here, we discovered a novel circRNA derived from the gene encoding Bcl-2-like protein 1 (BCL2L1) gene, named circBCL2L1, which was related to the innate immune responses in teleost fish. Results indicated that circBCL2L1 played essential roles in host antiviral immunity and antibacterial immunity. Our study also identified a microRNA, miR-30c-3-3p, which could inhibit the innate immune response by targeting inflammatory mediator TRAF6. And TRAF6 is a key signal transduction factor in innate immune response mediated by TLRs. Moreover, we also found that the antiviral and antibacterial effects inhibited by miR-30c-3-3p could be reversed with the expression of circBCL2L1. Our data revealed that circBCL2L1 functioned as a competing endogenous RNA (ceRNA) of TRAF6 by competing for binding with miR-30c-3-3p, leading to activation of the NF-κB/IRF3 inflammatory pathway and then enhancing the innate immune responses. Our results suggest that circRNAs can play an important role in the innate immune response of teleost fish.     

Induction of toll-like receptor (TLR) 2, and MyD88-dependent TLR- signaling in response to ligand stimulation and bacterial infections in the Indian major carp,mrigal (<Emphasis Type="Italic">Cirrhinus mrigala)</Emphasis>

Toll-like receptor 2 (TLR2) is a member of TLR family. It recognizes a wide range of bacteria and their products, and is involved in inducing innate immune responses. In this article, we reported inductive expression of TLR2 and myeloid differentiation primary response gene 88 (MyD88)-dependent signaling in the Indian major carp, mrigal (Cirrhinus mrigala) which is highly commercially important fish species in the Indian subcontinent. Ontogeny analysis of TLR2, MyD88 and TRAF6 (TNF receptor associated factor 6) genes by quantitative real-time PCR (qRT-PCR) revealed constitutive expression of these genes in all embryonic developmental stages, indicating their involvement in embryonic innate immune defense system in fish. Tissue specific expression analysis of these genes by qRT-PCR showed their wide distribution in various organs and tissues. Highest expression of TLR2 was in gill, MyD88 in liver and TRAF6 was in kidney. Inductive expression of TLR2, MyD88 and TRAF6 genes were observed following peptidoglycan (PGN)-treatment, and Streptococcus uberis and Aeromonas hydrophila infections. Expression of interleukin (IL)-8 and TNF-α in various organs were significantly enhanced by PGN-treatment and bacterial infections, and were closely associated with TLR2 induction. These findings together highlighted the contribution of TLR2 in augmenting innate immunity in fish, and indicated it’s important role in immune surveillance of various organs during pathogenic invasion. This study will enrich the information in understanding the innate immune mechanism in fish, and will be helpful in developing preventive measures against infectious diseases in fish.     

Effects of social isolation on growth,stress response,and immunity of zebrafish

Stressful housing conditions like social isolation have been shown to profoundly affect the physiology and health of various organisms which is rarely addressed in fish species. In the present study, we used a shoaling species, zebrafish, to investigate the stress reactivity of grouped and individually housed fish. We also hypothesized if isolation is a stressful condition may disrupt growth performance and innate immune response of individuals. To this end, fish were housed individually (social isolated treatment) or in groups of five fish (control treatment) for 60 days. Growth indices of fish were not affected by social isolation. Sixty-day social isolation did insignificant effect on baseline cortisol levels of specimens; however, individually housed zebrafish showed lower plasma cortisol to chasing stress than the control grouped fish. On the contrary, exposure to predator caused higher cortisol levels in social isolated fish. Serum lysozyme activity of isolated individuals was significantly lower than control fish, but activity of serum complement remained unchanged. Our results represent evidences that zebrafish experienced social isolation showed broad changes in physiological and immunological functions which may affect the quality of life.     

The influence of sex, line, and fight experience on aggressiveness of the Siamese fighting fish in intrasexual competition

We examined the influence of sex, line, i.e., broods from different parents, and previous fight experience on the aggressiveness of the Siamese fighting fish Betta splendens in intrasexual competition. The innate aggressiveness of the fish against their mirror images was measured on the day prior to the direct fight with other individuals, and it was found to be influenced by the line type but not by the sex. In the direct fight with other individuals, the males invested more effort in the fight than the females. In addition, the individuals of a particular line that exhibited a lower innate aggressiveness spent less time in the direct fight and were often losers when compared with those of other lines. After the direct fight with other individuals, the aggressiveness of the fish against their mirror images was remarkably influenced by the outcome of the direct fight, i.e., the winners exhibited more aggressive behavior, whereas the losers exhibited a lesser degree of aggressive behavior. This influence of the previous fight experience on subsequent aggressiveness was the greatest in the individuals of the line that have exhibited the lowest innate aggressiveness. However, the positive effect of the winning experience or the negative effect of the losing experience on subsequent aggressiveness decreased following several days after the previous fight increased.     

One eye but no vision: cave fish with induced eyes do not respond to light

One of the most intriguing questions in evolutionary biology is the degree to which behavior is a necessary consequence of morphology. We explore this issue by examining phototactic behavior in epigean (eyed surface-dwelling) and troglomorphic (blind cave) forms of the teleost Astyanax fasciatus whose eyes were modified during embryogenesis by removing one or both lens vesicles from the epigean form or by transplanting the lens vesicle from an epigean fish into the optic cup of a blind cave form. Lens removal results in eye degeneration and blindness in adult epigean fish, whereas lens transplantation stimulates growth of the eye, inducing the development of optic tissues in the normally eyeless adult cave fish. Photoresponsiveness was examined by placing fish in an aquarium with one half illuminated and the other half dark and scoring their presence in the illuminated or dark half. Both the eyeless epigean fish and cave fish with induced eyes are indifferent to the illumination whereas the surface forms are scotophilic, suggesting that optic development and phototactic behavior are decoupled.     

Asymmetry of the behavioral response in roach Rutilus rutilus (L.) (Teleostei: Cyprinidae) to a new object

The young roach Rutilus rutilus (L.) (Cyprinidae) displays lateralized behavior when facing a barrier through which a simulated bigger fish was visible. The asymmetry consists in a significant tendency to detour a barrier rightwards in the presence of a dummy fish. However, asymmetry is insignificant without the model. A comparison with the available literature shows that the roach has the same direction of this lateral bias as some other shoaling cyprinid fishes, which also preferentially turn to the right in the presence of a dummy fish. This seems to be a characteristic of cyprinids, as opposed to species of some other families displaying a leftward bias or a lack of asymmetry. The results of the study testify to the hypothesis that behavioral lateralization is associated with the taxonomic status of fishes. Currently, it is unclear whether the asymmetry found in roach in a detour test is due to the preferential use of the lateral fields of the right and left eyes as in some other fishes, or if it is a result of motor lateralization, which becomes evident in the presence of an unfamiliar and potentially dangerous object.     

From fish to fashion: experimental and theoretical insights into the evolution of culture

Recent years have witnessed a re-evaluation of the cognitive capabilities of fishes, including with respect to social learning. Indeed, some of the best experimental evidence for animal traditions can be found in fishes. Laboratory experimental studies reveal that many fishes acquire dietary, food site and mating preferences, predator recognition and avoidance behaviour, and learn pathways, through copying other fishes. Concentrating on foraging behaviour, we will present the findings of laboratory experiments that reveal social learning, behavioural innovation, the diffusion of novel behaviour through populations and traditional use of food sites. Further studies reveal surprisingly complex social learning strategies deployed by sticklebacks. We will go on to place these observations of fish in a phylogenetic context, describing in which respects the learning and traditionality of fish are similar to, and differ from, that observed in other animals. We end by drawing on theoretical insights to suggest processes that may have played important roles in the evolution of the human cultural capability.     

The norm-dependent effect of watching eyes on donation

Although many previous studies have shown that eye-like images promote generosity, the mechanism of this “watching eyes effect” remains unclear. One possible cause is the concern for a good reputation as a generous person, while the other is the concerns for a bad reputation as a norm violator. To elucidate which of these two concerns is the main influencer, the present study conducted a laboratory experiment that investigated whether the watching eyes effect changed depending on social norms. If the concern for a good reputation leads to the effect, prosocial behavior would be more likely in the presence of watching eyes, regardless of the social norms involved. However, if the concern for avoiding a bad reputation as a norm violator leads to the effect, watching eyes promote prosocial behavior only in the existence of prosocial norms. In the original study, participants were asked to make a charitable donation under conditions in which eye-like images either were or were not present. In addition to the eye-like images, we manipulated prosocial norms by informing each participant of either high or low mean donation amounts given by previous participants. We found that watching eyes promoted donations only when a prosocial norm existed. This supports the idea that the watching eyes effect is caused by a concern for avoiding a bad reputation from violating norms. However, in a replication study, we were unable to replicate the original results; watching eyes did not promote generosity regardless of the norm. Taken together, we discussed the moderation effect of norms and the possibility of other moderators.     

Moral elevation: Indications of functional integration with welfare trade-off calibration and estimation mechanisms

Moral elevation is a positive social emotion, which is triggered by observing third parties behaving benevolently, and which in turn triggers a motivation to behave benevolently towards others in general. It has been suggested that this relatively obscure emotion may be the output of a naturally selected cognitive adaptation which functions to help us retain our position in the competition for access to beneficial social relationships. This suggestion is here interpreted within the framework of ‘recalibrational emotions’. This framework offers the computational vocabulary necessary to understand how mental adaptations governing affect and motivation perform their functions at the cognitive level. Parallels are drawn between the suggested function and known phenomenological attributes of moral elevation, and the recently explicated functional operation of other social emotions (such as anger, guilt, and gratitude). Specifically, these other social emotions are thought to share a common computational pathway; recalibration of our welfare trade-off ratios (WTRs). WTRs are the computational element which dictate our willingness to benefit others at some cost to ourselves.A series of studies was conducted to explore whether a reliable relationship exists between moral elevation and WTRs. The results suggest that elevation does have a positive recalibrational effect on our WTRs, and that it may also be functionally integrated with a mental mechanism designed by natural selection to estimate the WTRs of other social actors.     

Distance and shape: perception of the 3-dimensional world by weakly electric fish.

Weakly electric fish orient at night in complete darkness by employing their active electrolocation system. They emit short electric signals and perceive the consequences of these emissions with epidermal electroreceptors. Objects are detected by analyzing the electric images which they project onto the animal's electroreceptive skin surface. This process corresponds to similar processes during vision, where visual images are cast onto the retinas of eyes. Behavioral experiments have shown that electric fish can measure the distance of objects during active electrolocation, thus possessing three-dimensional depth perception of their surroundings. The fundamental mechanism for distance determination differs from stereopsis used during vision by two-eyed animals, but resembles some supplementary mechanisms for distance deduction in humans. Weakly electric fish can also perceive the three-dimensional shape of objects. The fish can learn to identify certain objects and discriminate them from all other objects. In addition, they spontaneously categorize objects according to their shapes and not according to object size or material properties. There is good evidence that some fundamental types of perceptional invariances during visual object recognition in humans are also found in electric fish during active electrolocation. These include size invariance (maybe including size constancy), rotational invariance, and translational invariance. The mechanisms of shape detection during electrolocation are still unknown, and their discoveries require additional experiments.     

Evolutionary implications of the adaptation to different immune systems in a parasite with a complex life cycle

Many diseases are caused by parasites with complex life cycles that involve several hosts. If parasites cope better with only one of the different types of immune systems of their host species, we might expect a trade-off in parasite performance in the different hosts, that likely influences the evolution of virulence. We tested this hypothesis in a naturally co-evolving host-parasite system consisting of the tapeworm Schistocephalus solidus and its intermediate hosts, a copepod, Macrocyclops albidus, and the three-spined stickleback Gasterosteus aculeatus. We did not find a trade-off between infection success in the two hosts. Rather, tapeworms seem to trade-off adaptation towards different parts of their hosts' immune systems. Worm sibships that performed better in the invertebrate host also seem to be able to evade detection by the fish innate defence systems, i.e. induce lower levels of activation of innate immune components. These worm variants were less harmful for the fish host likely due to reduced costs of an activated innate immune system. These findings substantiate the impact of both hosts' immune systems on parasite performance and virulence.     

Diverse sensory cues for individual recognition

To be social, the ability to recognize and discriminate conspecific individuals is indispensable in social animals, including primates, rodents, birds, fish, and social insects which live in societies or groups. Recent studies using molecular biology, genetics, in vivo and in vitro physiology, and behavioral neuroscientific approaches have provided detailed insights into how animals process and recognize the information of individuals. Here, we review the most distinct sensory modalities for individual recognition in animals, namely, olfaction and vision. In the case of rodents, two polymorphic gene complexes have been identified in their urine as the key and essential pheromonal components for individual recognition: the major histocompatibility complex (MHC) and the major urinary protein (MUP). Animals flexibly utilize MHC and/or MUP, which are detected by the main olfactory epithelium (MOE) and/or the vomeronasal organ (VNO) for various types of social recognition, such as strain recognition, kin recognition, and individual recognition. In contrast, primates, including humans, primarily use facial appearance to identify others. Face recognition in humans and other animals is naturally unique from genetic, cognitive, developmental, and functional points of view. Importantly note that nurture effects during growth phase such as social experience and environment can also shape and tune this special cognitive ability, in order to distinguish subtle differences between individuals. In this review, we address such unique nature and nurture mechanisms for individual recognition.