Dopamine receptor antagonism disrupts social preference in zebrafish: a strain comparison study

Zebrafish form shoals in nature and in the laboratory. The sight of conspecifics has been found reinforcing in zebrafish learning tasks. However, the mechanisms of shoaling, and those of its reinforcing properties, are not known. The dopaminergic system has been implicated in reward among other functions and it is also engaged by drugs of abuse as shown in a variety of vertebrates including zebrafish. The ontogenetic changes in dopamine levels and, to a lesser degree, in serotonin levels, have been found to accompany the maturation of shoaling in zebrafish. Thus, we hypothesized that the dopaminergic system may contribute to shoaling in zebrafish. To test this we employed a D1-receptor antagonist and quantified behavioral responses of our subjects using a social preference (shoaling) paradigm. We found significant reduction of social preference induced by the D1-R antagonist, SCH23390, in the AB strain of zebrafish, an alteration that was not accompanied by changes in motor function or vision. We also detected D1-R antagonist-induced changes in the level of dopamine, DOPAC, serotonin and 5HIAA, respectively, in the brain of AB zebrafish as quantified by HPLC with electrochemical detection. We found the antagonist-induced behavioral changes to be absent and the levels of these neurochemicals to be lower in another zebrafish population, SF, demonstrating naturally occurring genetic variability in these traits. We conclude that this variability may be utilized to unravel the mechanisms of social behavior in zebrafish, a line of research that may be extended to other vertebrates including our own species.     

Conditioned place preference behavior in zebrafish

This protocol describes conditioned place preference (CPP) in zebrafish following a single exposure to a substance. In the CPP paradigm, animals show a preference for an environment that has previously been associated with a substance (drug), thus indicating the positive-reinforcing qualities of that substance. The test tank consists of two visually distinct compartments separated by a central alley. The protocol involves three steps: the determination of initial preference, one conditioning session and the determination of final preference. This procedure is carried out in ～2 d; other reported CPP protocols take up to 2 weeks. An increase in preference for the drug-associated compartment is observed after a single exposure. Establishment of this high-throughput protocol in zebrafish makes it possible to investigate the molecular and cellular basis of choice behavior, reward and associative learning. The protocol is also a tool for testing psychoactive compounds in the context of a vertebrate brain.     

Boldness predicts social status in zebrafish (Danio rerio)

This study explored if boldness could be used to predict social status. First, boldness was assessed by monitoring individual zebrafish behaviour in (1) an unfamiliar barren environment with no shelter (open field), (2) the same environment when a roof was introduced as a shelter, and (3) when the roof was removed and an unfamiliar object (Lego® brick) was introduced. Next, after a resting period of minimum one week, social status of the fish was determined in a dyadic contest and dominant/subordinate individuals were determined as the winner/loser of two consecutive contests. Multivariate data analyses showed that males were bolder than females and that the behaviours expressed by the fish during the boldness tests could be used to predict which fish would later become dominant and subordinate in the ensuing dyadic contest. We conclude that bold behaviour is positively correlated to dominance in zebrafish and that boldness is not solely a consequence of social dominance.     

Mating preference of female zebrafish, Danio rerio, in relation to male dominance

Mating success tends to be skewed toward dominant males, thoughfemale mate preferences may not always correlate with male dominance.In this study, we investigated the mating preferences of femalezebrafish, Danio rerio, in the absence of male–male competition.We paired females sequentially with males of known dominancerank, using a nested, repeated measures design, with egg productionas a measure of female mate preference. We predicted that femaleswould spawn more frequently and produce larger clutches whenpaired with males of higher dominance rank. We found significantdifferences among females in the size of clutches produced andamong males in the size of clutches received, but these differenceswere independent of male dominance rank. Male body size wasnot related to either dominance rank or clutch size received.These results indicate that females vary clutch size in relationto the males with which they are paired but that they do notfavor dominant males. Thus, male competition may normally overridefemale mate preference in zebrafish.     

Species preference by infant macaques with controlled social experience

In Experiment 1, infant Japanese monkeys and rhesus monkeys were artificially reared in pairs with conspecific or heterospecific monkeys. Preferences of these monkeys for a variety of pictures of Japanese monkeys and rhesus monkeys were repeatedly tested during the first 1 or 2 years of life. The duration of lever-pressing responses to see those pictures was a measure of the preference. All monkeys, Japanese or rhesus, preferred pictures of rhesus monkeys to pictures of Japanese monkeys, without regard to their social experiences. Experiment 2, with an adult Japanese monkey as the subject, and Experiment 3, with different pictures as stimuli, suggested that this preference was not a consequence of any bias in the pictures used. In Experiment 4, a Japanese monkey reared by a rhesus foster mother and rhesus monkeys reared by Japanese monkey mothers received the same preference test. The Japanese monkey infant preferred to see pictures of rhesus monkeys. However, rhesus infants did not show clear species preferences. These results suggest that infants of both Japanese and rhesus monkeys have a native tendency to prefer to see physical characteristics of rhesus monkeys over Japanese monkeys.     

The sexual preference of female rats is influenced by males' adolescent social stress history and social status

Ongoing development of brain systems for social behaviour renders these systems susceptible to the influence of stressors in adolescence. We previously found that adult male rats that underwent social instability stress (SS) in mid-adolescence had decreased sexual performance compared with control males (CTL). Here, we test the hypotheses that SS in adolescence decreases the “attractiveness” of male rats as sexual partners compared with CTL rats and that dominance status is a protective factor against the effects of SS. The main prediction was that females would spend more time with CTL males than SS males, and that this bias would be greater for submissive than for dominant rats. Among dominant pairs (n = 16), females preferred SS males, spending more time with and visiting more often SS than CTL males (each pair tested 5 ×), and SS males had shorter latencies to ejaculation, shorter inter-ejaculation intervals, and made more ejaculations compared with CTL males. Among submissive pairs (n = 16), females spent more time with, visited more often, and displayed more paracopulatory behaviour with CTL than with SS males, and differences in sexual performance between SS and CTL males were modest and in the opposite direction from that in dominant pairs. The heightened motivation of SS males relative to CTL males for natural rewards may have attenuated differences in sexual performance in a paced mating context. In sum, the experience of stress in adolescence leads to long-lasting changes in males that are perceptible to females, are moderated by social status, and influence sexual behaviour.     

Social interactions elicit rapid shifts in functional connectivity in the social decision-making network of zebrafish

According to the social decision-making (SDM) network hypothesis, SDM is encoded in a network of forebrain and midbrain structures in a distributed and dynamic fashion, such that the expression of a given social behaviour is better reflected by the overall profile of activation across the different loci rather than by the activity of a single node. This proposal has the implicit assumption that SDM relies on integration across brain regions, rather than on regional specialization. Here we tested the occurrence of functional localization and of functional connectivity in the SDM network. For this purpose we used zebrafish to map different social behaviour states into patterns of neuronal activity, as indicated by the expression of the immediate early genes c-fos and egr-1, across the SDM network. The results did not support functional localization, as some loci had similar patterns of activity associated with different social behaviour states, and showed socially driven changes in functional connectivity. Thus, this study provides functional support to the SDM network hypothesis and suggests that the neural context in which a given node of the network is operating (i.e. the state of its interconnected areas) is central to its functional relevance.     

Sex steroids modulate changes in social and sexual preference during juvenile development in zebra finches

Zebra finches, like many other animals, have close social relationships mainly with the family at young ages but begin to express interest in opposite-sex extra-family animals as they enter the late juvenile period and sexual maturity. This experiment tested a set of hypotheses that sex steroids are involved in this developmental transition. At 25-30 days, subjects were implanted subcutaneously with Silastic tubes that were empty (controls), filled with testosterone propionate, filled with estradiol benzoate, or filled with a combination of ATD (an aromatization inhibitor) and flutamide (an anti-androgen). Once a week between ages 30 and 90 days, they were given three-choice tests where the three stimulus types were the family members, unpaired males, or unpaired females. The preferred category was defined as the one adjacent to the proximity zone in which the subject spent the most time. Control males were more likely to prefer females and less likely to prefer the family as they got older, and control females were increasingly likely to prefer males. Males treated with testosterone or estradiol showed a premature increase in preferences for females. Females treated with ATD plus flutamide failed to show the normal increase in preferences for males shown by controls. These results indicate an involvement of sex steroids in the maturation of sexual preferences in a socially monogamous species that relies on visual and auditory, rather than olfactory, cues for sexual or other social behavior.     

No speed dating please! Patterns of social preference in male and female house mice

Glass sponges (Class Hexactinellida) are important components of deep-sea ecosystems and are of interest from geological and materials science perspectives. The reconstruction of their phylogeny with molecular data has only recently begun and shows a better agreement with morphology-based systematics than is typical for other sponge groups, likely because of a greater number of informative morphological characters. However, inconsistencies remain that have far-reaching implications for hypotheses about the evolution of their major skeletal construction types (body plans). Furthermore, less than half of all described extant genera have been sampled for molecular systematics, and several taxa important for understanding skeletal evolution are still missing. Increased taxon sampling for molecular phylogenetics of this group is therefore urgently needed. However, due to their remote habitat and often poorly preserved museum material, sequencing all 126 currently recognized extant genera will be difficult to achieve. Utilizing morphological data to incorporate unsequenced taxa into an integrative systematics framework therefore holds great promise, but it is unclear which methodological approach best suits this task. Here, we increase the taxon sampling of four previously established molecular markers (18S, 28S, and 16S ribosomal DNA, as well as cytochrome oxidase subunit I) by 12 genera, for the first time including representatives of the order Aulocalycoida and the type genus of Dactylocalycidae, taxa that are key to understanding hexactinellid body plan evolution. Phylogenetic analyses suggest that Aulocalycoida is diphyletic and provide further support for the paraphyly of order Hexactinosida; hence these orders are abolished from the Linnean classification. We further assembled morphological character matrices to integrate so far unsequenced genera into phylogenetic analyses in maximum parsimony (MP), maximum likelihood (ML), Bayesian, and morphology-based binning frameworks. We find that of these four approaches, total-evidence analysis using MP gave the most plausible results concerning congruence with existing phylogenetic and taxonomic hypotheses, whereas the other methods, especially ML and binning, performed more poorly. We use our total-evidence phylogeny of all extant glass sponge genera for ancestral state reconstruction of morphological characters in MP and ML frameworks, gaining new insights into the evolution of major hexactinellid body plans and other characters such as different spicule types. Our study demonstrates how a comprehensive, albeit in some parts provisional, phylogeny of a larger taxon can be achieved with an integrative approach utilizing molecular and morphological data, and how this can be used as a basis for understanding phenotypic evolution. The datasets and associated trees presented here are intended as a resource and starting point for future work on glass sponge evolution.     

Social exploitation of intermittently available foods and the social reinstatement of food preference

To determine whether Norway rats, Rattus norvegicus, could use socially acquired information to track recurrences of an intermittently available food (experiment 1), we allowed observer rats to interact every 2-3 days with demonstrator rats fed one of two diets, then determined the amount of each diet eaten by observers. We found that observer rats showed repeated significant increases in their preferences for foods their respective demonstrators had eaten. Because social interactions repeatedly enhanced preference for a food, we reasoned that after the socially induced food preference of an animal (A1) had waned, that preference might be reinstated in A1 by interaction with a conspecific (A2) in whom A1 had previously induced a preference for the food. In experiment 2, we demonstrated such social reinstatement of a food preference. Copyright 2000 The Association for the Study of Animal Behaviour.     

Human social stratification and hypergyny: toward an understanding of male homosexual preference

Male homosexual preference (MHP) challenges evolutionary thinking because the preference for male–male relationships is heritable, implies a fertility cost (lower offspring number), and is relatively frequent in some societies (2%–6% in Western countries) for a costly trait. Proximate explanations include the hypothesis of a “sexually antagonistic factor” in which a trait that increases fertility in females also promotes the emergence of MHP. Because no animal species is known to display consistent MHP in the wild (only transient and contextual homosexual behavior has been described), additional human-specific features must contribute to the maintenance of MHP in human populations. We built a theoretical model that revealed that, in a stratified society, a relatively high frequency of MHP could be maintained as a result of the social ascension of females signaling high fertility (hypergyny). Additional computer simulations confirmed that this result applies to populations with various numbers of classes, conditions of demographic regulation, and mating systems. The prediction that MHP is more prevalent in stratified societies was significantly supported in a sample of 48 societies for which the presence or absence of MHP has been anthropologically documented. More generally, any traits associated with up-migration are likely to be selected for in a stratified society and will be maintained by frequency dependence even if they induce a pleiotropic cost, such as MHP. These results offer a new perspective for understanding seemingly paradoxical traits in human populations.     

Interspecific social learning: novel preference can be acquired from a competing species

Nongenetic transmission of behavioral traits via social learning allows local traditions in humans, and, controversially, in other animals [1-4]. Social learning is usually studied as an intraspecific phenomenon (but see [5-7]). However, other species with some overlap in ecology can be more than merely potential competitors: prior settlement and longer residence can render them preferable sources of information [8]. Socially induced acquisition of choices or preferences capitalizes upon the knowledge of presumably better-informed individuals [9] and should be adaptive under many natural circumstances [10, 11]. Here we show with a field experiment that females of two migrant flycatcher species can acquire a novel, arbitrary preference of competing resident tits for a symbol attached to the nest sites. The experiment demonstrates that such blind acquisition of heterospecific traits can occur in the wild. Even though genetic variation for habitat preferences exists in many taxa [12] and overlap between bird species likely induces costs [13], this result shows that interspecific social learning can cause increased overlap in nest-site preferences. Conventional, negative species interactions push ecological niches of species apart, but the use of competing species as a source of information counters that force and may lead to convergence.     

Measures of anxiety in zebrafish (Danio rerio): dissociation of black/white preference and novel tank test

The effects of wall color stimuli on diving, and the effects of depth stimuli on scototaxis, were assessed in zebrafish. Three groups of fish were confined to a black, a white, or a transparent tank, and tested for depth preference. Two groups of fish were confined to a deep or a shallow tank, and tested for black-white preference. As predicted, fish preferred the deep half of a split-tank over the shallow half, and preferred the black half of a black/white tank over the white half. Results indicated that the tank wall color significantly affected depth preference, with the transparent tank producing the strongest depth preference and the black tank producing the weakest preference. Tank depth, however, did not significantly affect color preference. Additionally, wall color significantly affected shuttling and immobility, while depth significantly affected shuttling and thigmotaxis. These results are consistent with previous indications that the diving response and scototaxis may reflect dissociable mechanisms of behavior. We conclude that the two tests are complementary rather than interchangeable, and that further research on the motivational systems underlying behavior in each of the two tests is needed.     

Targeted knockout of duox causes defects in zebrafish growth,thyroid development,and social interaction

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