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Skip to Next Section Group-living animals must adjust the expression of their social behaviour to changes in their social environment and to transitions between life-history stages, and this social plasticity can be seen as an adaptive trait that can be under positive selection when changes in the environment outpace the rate of genetic evolutionary change. Here, we propose a conceptual framework for understanding the neuromolecular mechanisms of social plasticity. According to this framework, social plasticity is achieved by rewiring or by biochemically switching nodes of a neural network underlying social behaviour in response to perceived social information. Therefore, at the molecular level, it depends on the social regulation of gene expression, so that different genomic and epigenetic states of this brain network correspond to different behavioural states, and the switches between states are orchestrated by signalling pathways that interface the social environment and the genotype. Different types of social plasticity can be recognized based on the observed patterns of inter- versus intra-individual occurrence, time scale and reversibility. It is proposed that these different types of social plasticity rely on different proximate mechanisms at the physiological, neural and genomic level.

The physiological mechanisms underlying variation in aggression in fish remain poorly understood. One possibly confounding variable is the lack of standardization in the type of stimuli used to elicit aggression. The presentation of controlled stimuli in videos, a.k.a. video playback, can provide better control of the fight components. However, this technique has produced conflicting results in animal behaviour studies and needs to be carefully validated. For this, a similar response to the video and an equivalent live stimulus needs to be demonstrated. Further, different physiological responses may be triggered by live and video stimuli and it is important to demonstrate that video images elicit appropriate physiological reactions. Here, the behavioural and endocrine response of male Siamese fighting fish Betta splendens to a matched for size conspecific fighting behind a one-way mirror, presented live or through video playback, was compared. The video playback and live stimulus elicited a strong and similar aggressive response by the focal fish, with a fight structure that started with stereotypical threat displays and progressed to overt attacks. Post-fight plasma levels of the androgen 11-ketotestosterone were elevated as compared to controls, regardless of the type of stimuli. Cortisol also increased in response to the video images, as previously described for live fights in this species. These results show that the interactive component of a fight, and its resolution, are not needed to trigger an endocrine response to aggression in this species. The study also demonstrates for the first time in a fish a robust endocrine response to video stimuli and supports the use of this technique for researching aggressive behaviour in B. splendens.

The role of hormones as modulators of aggressive behavior in fish remains poorly understood. Androgens and corticosteroids, in particular, have been associated with aggressive behavior in fish but it is still not clear if animals adjust the secretion of these hormones to regulate behavior during ongoing fights, in response to fight outcomes in order to adjust aggressive behavior in subsequent fights, or both. With its stereotyped displays and high aggression levels, the Siamese fighting fish Betta splendens is an excellent model to investigate this question. Here, we compared the behavioral and endocrine response of male B. splendens to fights where there is no winner or loser by presenting them with a size-matched live interacting conspecific behind a transparent partition or with a mirror image. The aggressive response started with threat displays that were overall similar in frequency and duration towards both types of stimuli. Fights transitioned to overt attacks and interacting with a live conspecific elicited a higher frequency of attempted bites and head hits, as compared with the mirror image. There was a pronounced increase in plasma androgens (11-ketotestosterone and testosterone) and corticosteroids (cortisol) levels in response to the aggression challenge, independent of stimulus type. Post-fight intra-group levels of these hormones did not correlate with measures of physical activity or aggressive behavior. A linear discriminant analysis including all behavioral and endocrine data was a poor classifier of fish from the conspecific and mirror trials, showing that overall the behavioral and endocrine response to mirror images and conspecifics was similar. The results show that fight resolution is not necessary to induce an evident increase in peripheral levels of androgens and corticosteroids in B. splendens. However, the function of these hormones during present and future aggressive contests remains to be clarified.

Aggressive behavior is an adaptive trait present across all taxa. However, the neuroendocrine mechanisms regulating it, particularly in fish, are not well understood. Oxytocin (OXT) and arginine vasotocin (VT) are known modulators of aggression, but their actions remain controversial. This study tested the possible modulation of endocrine and behavioral responses to an aggression challenge by these nonapeptides in Siamese fighting fish, Betta splendens, a species known for its intrinsic aggressiveness. Male B. splendens were injected with different dosages of either Manning compound or L-368,899, VT and OXT receptor antagonists respectively, and were exposed to a mirror challenge for 30 min. While all fish displayed high levels of aggression toward their mirror image, no differences were observed between control-injected and treatment fish. However, blocking VT inhibited the post-fight increase in plasma levels of the androgen 11-ketotestosterone (KT). To further investigate this result, testis tissue from males was incubated with and without VT and Manning compound, and KT levels were measured after 180 min. Results showed a direct effect of VT on in vitro KT secretion, indicating the presence of VT receptors in the testes of this species. Overall, the study does not support a modulatory role of VT or OXT in aggressive behavior, although VT might be implicated in the regulation of peripheral androgen response to aggression in B. splendens.

The peacock blenny Salaria pavo is notorious for its extreme male sexual polymorphism, with large males defending nests and younger reproductive males mimicking the appearance and behavior of females to parasitically fertilize eggs. The lack of a reference genome has, to date, limited the understanding of the genetic basis of the species phenotypic plasticity. Here, we present the first reference genome assembly of the peacock blenny using PacBio HiFi long-reads and Hi-C sequencing data. The final assembly of the S. pavo genome spanned 735.90 Mbp, with a contig N50 of 3.69 Mbp and a scaffold N50 of 31.87 Mbp. A total of 98.77% of the assembly was anchored to 24 chromosomes. In total, 24,008 protein-coding genes were annotated, and 99.0% of BUSCO genes were fully represented. Comparative analyses with closely related species showed that 86.2% of these genes were assigned to orthogroups. This high-quality genome of S. pavo will be a valuable resource for future research on this species’ reproductive plasticity and evolutionary history.

Distinct patterns of gene expression often underlie intra- and intersexual differences, and the study of this set of coregulated genes is essential to understand the emergence of complex behavioural phenotypes. Here, we describe the development of a de novo transcriptome and brain gene expression profiles of wild-caught peacock blenny, Salaria pavo, an intertidal fish with sex-role reversal in courtship behaviour (i.e., females are the courting sex) and sequential alternative reproductive tactics in males (i.e., larger and older nest-holder males and smaller and younger sneaker males occur). Sneakers mimic both female's courtship behaviour and nuptial coloration to get access to nests and sneak fertilizations, and later in life transition into nest-holder males. Thus, this species offers the unique opportunity to study how the regulation of gene expression can contribute to intersex phenotypes and to the sequential expression of male and female behavioural phenotypes by the same individual. We found that at the whole brain level, expression of the sneaker tactic was paralleled by broader and divergent gene expression when compared to either females or nest-holder males, which were more similar between themselves. When looking at sex-biased transcripts, sneaker males are intersex rather than being either nest-holder or female-like, and their transcriptome is simultaneously demasculinized for nest-holder-biased transcripts and feminized for female-biased transcripts. These results indicate that evolutionary changes in reproductive plasticity can be achieved through regulation of gene expression, and in particular by varying the magnitude of expression of sex-biased genes, throughout the lifetime of the same individual.

Understanding consistent inter-individual variability in animal behaviour, known as personality traits, is essential for exploring the mechanisms and evolutionary consequences of behavioural diversity. Aggressive behaviour influences survival, resource acquisition, and reproduction, so clarifying individual differences can enhance our understanding of ecological dynamics and improve experimental design accuracy in behavioural studies. In this study, ornamental male Betta splendens, a model organism for aggression research, were analysed for intra- and inter-individual variability in aggressive responses to their mirror image-a standard method for assessing aggression in fish-once per week, and their consistency was evaluated over three consecutive weeks There were significant differences in aggressive behaviour across individuals, with coefficients of variation ranging from 29 to 60%. While most fish exhibited the full suite of aggressive displays, some showed no aggressive behaviour, while others only displayed threat behaviours but did not advance to the attacks. The consistency of individual threat and attack behaviours varied, but repeatability was high overall (intra-class correlation coefficients >= 0.5), indicating that individual fish have different levels of aggression. There was habituation to the mirror assay, with aggression decreasing significantly by the second week, though the degree of habituation, a form of learning, varied among individuals in some behaviours. Air-breathing frequency correlated positively with aggression behaviours and can be considered an indicator to infer aggression level in this species. These results indicate that inter-individual variation in aggressive behaviour and habituation to repeated testing using the mirror assay should be considered in aggression studies using B. splendens and potentially in other species.

Alternative reproductive tactics (ARTs) evolve when there is strong intra-sexual competition between conspecifics for access to mates. Typically, larger “bourgeois” males reproduce by securing the access to reproductive resources while smaller “parasitic” males reproduce by stealing fertilizations from larger males. A number of factors can influence the reproductive success of each tactic, including intrinsic (e.g. size) and extrinsic (e.g. tactic relative frequency) variables. An example where plastic ARTs occur is the peacock blenny Salaria pavo, with large males reproducing by defending nests and attracting females (bourgeois tactic) and small males reproducing by achieving sneaked fertilizations (parasitic tactic). In this study, we conducted field observations on individually tagged animals to determine their social network and collected eggs from 11 nests to determine the fertilization success of each male tactic. Paternity estimates for 550 offspring indicated an average fertilization success for nest-holder males of 95%. Nest-holder male morphological traits and social network parameters were tested as predictors of fertilization success, but only the number of sneakers present in the nest-holder’s social networks was found to be a predictor of paternity loss. Although male morphological traits had been previously found to be strongly correlated with reproductive success of nest-holder males, as measured by the number of eggs collected in the male’s nest, no correlation was found between any of the measured morphological traits and fertilization success for these males. The results suggest a stronger influence of the social environment than of morphological variables in the proportion of lost fertilizations by nest-holder males of this species.