Effects of the maternal social environment on the mating signals and mate preferences of adult offspring in Enchenopa treehoppers.

Much is known about how the maternal environment can shape offspring traits via intergenerational effects. It is less clear, however, whether such effects may reach adult offspring sexual traits, with potential consequences for sexual selection and speciation. Here, we report effects of adult female aggregation density on the mating signals and mate preferences of their offspring in an insect that communicates via plant-borne vibrational signals. We experimentally manipulated the density of aggregations experienced by egg-laying mothers, reared the offspring in standard densities, and tested for corresponding differences in their signals and preferences. We detected a strong effect in male signals, with sons of mothers that experienced low aggregation density signalling more. We also detected a weak effect on female mate preferences, with daughters of mothers that experienced low aggregation density being less selective. These adjustments may help males and females find mates and secure matings in low densities, if the conditions they encounter correspond to those their mothers experienced. Our results thus extend theory regarding adjustments to the social environment to the scale of intergenerational effects, with maternal social environments influencing the expression of the sexual traits of adult offspring.

A tale of two males: Behavioral and neural mechanisms of alternative reproductive tactics in midshipman fish.

An amalgam of investigations at the interface of neuroethology and behavioral neuroendocrinology first established the most basic behavioral, neuroanatomical, and neurophysiological characters of vocal-acoustic communication morphs in the plainfin midshipman fish, Porichthys notatus Girard. This foundation has led, in turn, to the repeated demonstration that neuro-behavioral mechanisms driving reproductive-related, vocal-acoustic behaviors can be uncoupled from gonadal state for two adult male phenotypes that follow alternative reproductive tactics (ARTs).

Roles of the 5-HT2C receptor on zebrafish sociality.

Serotonin (5-HT) receptors have been implicated in social behavior in vertebrates. Zebrafish (Danio rerio) have been increasingly being used behavioral neuroscience to study the neurobiological correlates of behavior, including sociality. Nonetheless, the role of 5-HT2C receptors in different social functions were not yet studied in this species. Zebrafish were treated with the agonist MK-212 (2 mg/kg) or the antagonist RS-102221 (2 mg/kg) and tested in the social interaction and social novelty tests, conditional approach test, or mirror-induced aggressive displays. MK-212 increased preference for an unknown conspecific in the social investigation test, but also increased preference for the known conspecific in the social novelty test; RS-102221, on the other hand, decreased preference in the social investigation test but increased preference for the novel conspecific in the social novelty test. MK-212 also decreased predator inspection in the conditional approach test. While RS-102221 decreased time in the display zone in the mirror-induced aggressive display test, it increased display duration. Overall, these results demonstrate the complex role of 5-HT2C receptors in different social contexts in zebrafish, revealing a participation in social plasticity in vertebrates.

Repeatability and heritability of social reaction norms in a wild agamid lizard.

In the evolutionary transition from solitary to group living, it should be adaptive for animals to respond to the environment and choose when to socialize to reduce conflict and maximize access to resources. Due to the associated proximate mechanisms (e.g. neural network, endocrine system), it is likely that this behavior varies between individuals according to genetic and non-genetic factors. We used long-term behavioral and genetic data from a population of eastern water dragons (Intellagama lesueurii) to explore variation in plasticity of social behavior, in response to sex ratio and density. To do so, we modeled individual variation in social reaction norms, which describe individuals' mean behavior and behavioral responses to changes in their environment, and partitioned variance into genetic and non-genetic components. We found that reaction norms were repeatable over multiple years, suggesting that individuals consistently differed in their behavioral responses to changes in the social environment. Despite high repeatability of reaction norm components, trait heritability was below our limit of detection based on power analyses (h2 < 0.12), leading to very little power to detect heritability of plasticity. This was in contrast to a relatively greater amount of variance associated with environmental effects. This could suggest that mechanisms such as social learning and frequency-dependence may shape variance in reaction norms, which will be testable as the dataset grows.

Social Stress Increases Anxiety-Like Behavior Equally in Male and Female Zebrafish.

Zebrafish anxiety-like behavior was assessed in the novel tank test after the formation of dominant-subordinate hierarchies. Ten pairs of animals were subjected to dyadic interactions for 5 days, and compared with control animals. After this period, a clear dominance hierarchy was established across all dyads, irrespective of sex. Social status affected parameters of anxiety-like behavior in the novel tank test, with subordinate males and females displaying more bottom-dwelling, absolute turn angle, and freezing than dominant animals and controls. The results suggest that subordinate male and female zebrafish show higher anxiety-like behavior, which together with previous literature suggests that subordination stress is conserved across vertebrates.

Non-genetic inheritance: Evolution above the organismal level.

The article proposes to further develop the ideas of the Extended Evolutionary Synthesis by including into evolutionary research an analysis of phenomena that occur above the organismal level. We demonstrate that the current Extended Synthesis is focused more on individual traits (genetically or non-genetically inherited) and less on community system traits (synergetic/organizational traits) that characterize transgenerational biological, ecological, social, and cultural systems. In this regard, we will consider various communities that are made up of interacting populations, and for which the individual members can belong to the same or to different species. Examples of communities include biofilms, ant colonies, symbiotic associations resulting in holobiont formation, and human societies. The proposed model of evolution at the level of communities revises classic theorizing on the major transitions in evolution by analyzing the interplay between community/social traits and individual traits, and how this brings forth ideas of top-down regulations of bottom-up evolutionary processes (collaboration of downward and upward causation). The work demonstrates that such interplay also includes reticulate interactions and reticulate causation. In this regard, we exemplify how community systems provide various non-genetic 'scaffoldings', 'constraints', and 'affordances' for individual and sociocultural evolutionary development. Such research complements prevailing models that focus on the vertical transmission of heritable information, from parent to offspring, with research that instead focusses on horizontal, oblique and even reverse information transmission, going from offspring to parent. We call this reversed information transfer the 'offspring effect' to contrast it from the 'parental effect'. We argue that the proposed approach to inheritance is effective for modelling cumulative and distributed developmental process and for explaining the biological origins and evolution of language.

Genotype-by-genotype epistasis for exploratory behaviour in D. simulans.

Social interactions can influence the expression and underlying genetic basis of many traits. Yet, empirical investigations of indirect genetic effects (IGEs) and genotype-by-genotype epistasis-quantitative genetics parameters representing the role of genetic variation in a focal individual and its interacting partners in producing the observed trait values-are still scarce. While it is commonly observed that an individual's traits are influenced by the traits of interacting conspecifics, representing social plasticity, studying this social plasticity and its quantitative-genetic basis is notoriously challenging. These challenges are compounded when individuals interact in groups, rather than (simpler) dyads. Here, we investigate the genetic architecture of social plasticity for exploratory behaviour, one of the most intensively studied behaviours in recent decades. Using genotypes of Drosophila simulans, we measured genotypes both alone, and in social groups representing a mix of two genotypes. We found that females adjusted their exploratory behaviour based on the behaviour of others in the group, representing social plasticity. However, the direction of this plasticity depended on the identity of group members: focal individuals were more likely to emerge from a refuge if group members who were the same genotype as the focal remained inside for longer. By contrast, focal individuals were less likely to emerge from a refuge if partner-genotype group members remained inside for longer. Exploratory behaviour also depended on the identities of both genotypes that composed the group. Together, these findings demonstrate genotype-by-genotype epistasis for exploratory behaviour both within and among groups.

Individual Variation in the Social Plasticity of Water Dragons.

Individuals should alter when they socially associate with conspecifics to avoid potentially costly interactions. Moreover, individuals may vary in their propensity to use information about conspecifics when making such social decisions. However, surprisingly little is known about either the determinants of or the individual variation in such "social plasticity." We show here that eastern water dragons (Intellegama lesueurii lesueurii) may simultaneously use information from different components of their social environment when deciding whether to socially associate. In particular, we found that individuals altered when they socially associated with conspecifics according to the levels of potential conflict and competition in their social environment; both sexes socially associated more at higher local density than would be expected under increased random encounters. Further, females were more likely to socially associate during the breeding season and when there were more males and/or conspecifics whom they typically avoided in their social environment. This suggests that females may seek safety in numbers when the potential for intrasexual conflict or sexual harassment is high. Using a behavioral reaction norm framework, we also provide novel evidence to show that individuals vary in the extent and direction of their social plasticity and that males varied more than females. Our study thus implies that individuals use multiple cues in their environment when deciding to socially associate and that the resulting social plasticity varies between the sexes and between individuals.

Environmental enrichment as an experience-dependent modulator of social plasticity and cognition.

Social plasticity is the ability to adaptively change the expression of social behaviour according to experience, allowing animals to optimize their social relationships in the context of previous experience and the complexities of social environments. Environmental enrichment (EE) mimics a stimulating lifestyle at the laboratory level and has demonstrated beneficial effects on various aspects of brain structure, function, behaviour and cognition. EE has also been shown to induce neuroprotection and functional compensation that is therapeutic in a range of different brain disorders. The effects of EE on social plasticity have received little attention, despite the fact that many components of the mechanisms of social plasticity and EE-induced plasticity are overlapping. We review and discuss EE effects on social plasticity, with a focus on laboratory rodent studies. This review presents evidence that EE affects social plasticity, via both direct and indirect mechanisms, as well as under pathological conditions. In conclusion, EE is a valuable tool to study social cognition and behaviour, and could inform therapeutic approaches to the many brain disorders involving social dysfunction, including schizophrenia and autism spectrum disorders.

The role of indirect genetic effects in the evolution of interacting reproductive behaviors in the burying beetle, Nicrophorus vespilloides.

Social interactions can give rise to indirect genetic effects (IGEs), which occur when genes expressed in one individual affect the phenotype of another individual. The evolutionary dynamics of traits can be altered when there are IGEs. Sex often involves indirect effects arising from first-order (current) or second-order (prior) social interactions, yet IGEs are infrequently quantified for reproductive behaviors. Here, we use experimental populations of burying beetles that have experienced bidirectional selection on mating rate to test for social plasticity and IGEs associated with focal males mating with a female either without (first-order effect) or with (second-order effect) prior exposure to a competitor, and resource defense behavior (first-order effect). Additive IGEs were detected for mating rate arising from (first-order) interactions with females. For resource defense behavior, a standard variance partitioning analysis provided no evidence of additive genetic variance-either direct or indirect. However, behavior was predicted by focal size relative to that of the competitor, and size is also heritable. Assuming that behavior is causally dependent on relative size, this implies that both DGEs and IGEs do occur (and may potentially interact). The relative contribution of IGEs may differ among social behaviors related to mating which has consequences for the evolutionary trajectories of multivariate traits.

Social plasticity in the fish brain: Neuroscientific and ethological aspects.

Social plasticity, defined as the ability to adaptively change the expression of social behavior according to previous experience and to social context, is a key ecological performance trait that should be viewed as crucial for Darwinian fitness. The neural mechanisms for social plasticity are poorly understood, in part due to skewed reliance on rodent models. Fish model organisms are relevant in the field of social plasticity for at least two reasons: first, the diversity of social organization among fish species is staggering, increasing the breadth of evolutionary relevant questions that can be asked. Second, that diversity also suggests translational relevance, since it is more likely that "core" mechanisms of social plasticity are discovered by analyzing a wider variety of social arrangements than relying on a single species. We analyze examples of social plasticity across fish species with different social organizations, concluding that a "core" mechanism is the initiation of behavioral shifts through the modulation of a conserved "social decision-making network", along with other relevant brain regions, by monoamines, neuropeptides, and steroid hormones. The consolidation of these shifts may be mediated via neurogenomic adjustments and regulation of the expression of plasticity-related molecules (transcription factors, cell cycle regulators, and plasticity products).

Social structure modulates the evolutionary consequences of social plasticity: A social network perspective on interacting phenotypes.

Organisms express phenotypic plasticity during social interactions. Interacting phenotype theory has explored the consequences of social plasticity for evolution, but it is unclear how this theory applies to complex social structures. We adapt interacting phenotype models to general social structures to explore how the number of social connections between individuals and preference for phenotypically similar social partners affect phenotypic variation and evolution. We derive an analytical model that ignores phenotypic feedback and use simulations to test the predictions of this model. We find that adapting previous models to more general social structures does not alter their general conclusions but generates insights into the effect of social plasticity and social structure on the maintenance of phenotypic variation and evolution. Contribution of indirect genetic effects to phenotypic variance is highest when interactions occur at intermediate densities and decrease at higher densities, when individuals approach interacting with all group members, homogenizing the social environment across individuals. However, evolutionary response to selection tends to increase at greater network densities as the effects of an individual's genes are amplified through increasing effects on other group members. Preferential associations among similar individuals (homophily) increase both phenotypic variance within groups and evolutionary response to selection. Our results represent a first step in relating social network structure to the expression of social plasticity and evolutionary responses to selection.

Behavioural tactic predicts preoptic-hypothalamic gene expression more strongly than developmental morph in fish with alternative reproductive tactics.

Reproductive success relies on the coordination of social behaviours, such as territory defence, courtship and mating. Species with extreme variation in reproductive tactics are useful models for identifying the neural mechanisms underlying social behaviour plasticity. The plainfin midshipman (Porichthys notatus) is a teleost fish with two male reproductive morphs that follow widely divergent developmental trajectories and display alternative reproductive tactics (ARTs). Type I males defend territories, court females and provide paternal care, but will resort to cuckoldry if they cannot maintain a territory. Type II males reproduce only through cuckoldry. We sought to disentangle gene expression patterns underlying behavioural tactic, in this case ARTs, from those solely reflective of developmental morph. Using RNA-sequencing, we investigated differential transcript expression in the preoptic area-anterior hypothalamus (POA-AH) of courting type I males, cuckolding type I males and cuckolding type II males. Unexpectedly, POA-AH differential expression was more strongly coupled to behavioural tactic than morph. This included a suite of transcripts implicated in hormonal regulation of vertebrate social behaviour. Our results reveal that divergent expression patterns in a conserved neuroendocrine centre known to regulate social-reproductive behaviours across vertebrate lineages may be uncoupled from developmental history to enable plasticity in the performance of reproductive tactics.

Dynamic modulation of sociality and aggression: an examination of plasticity within endocrine and neuroendocrine systems.

Endocrine and neuroendocrine systems are key mediators of behavioural plasticity and allow for the ability to shift social behaviour across dynamic contexts. These systems operate across timescales, modulating both rapid responses to environmental changes and developmental plasticity in behavioural phenotypes. Thus, not only do endocrine systems mediate behavioural plasticity, but also the systems themselves exhibit plasticity in functional capabilities. This flexibility at both the mechanistic and behavioural levels can be crucial for reproduction and survival. Here, we discuss how plasticity in nonapeptide and steroid actions may influence the expression of, and allow rapid shifts between, sociality and aggression-behavioural shifts that can be particularly important for social interactions. Recent findings of overlap in the mechanisms that modulate social and aggressive behaviour suggest the potential for a mechanistic continuum between these behaviours. We briefly discuss the potential for a sociality-aggression continuum and novel techniques that will enable probing of the functional connectivity of social behaviours. From an evolutionary perspective, we suggest that plasticity in endocrine and neuroendocrine mechanisms of behaviour may be important targets of selection, and discuss the conditions under which we would predict selection to have resulted in differences in endocrine plasticity across species that differ in social organization.This article is part of the themed issue 'Physiological determinants of social behaviour in animals'.

Crowd control: sex ratio affects sexually selected cuticular hydrocarbons in male Drosophila serrata.

Although it is advantageous for males to express costly sexually selected signals when females are present, they may also benefit from suppressing these signals to avoid costly interactions with rival males. Cuticular chemical profiles frequently function as insect sexual signals; however, few studies have asked whether males alter these signals in response to their social environment. In Drosophila serrata, an Australian fly, there is sexual selection for a multivariate combination of male cuticular hydrocarbons (CHCs). Here, we show that the ratio of females to males that an adult male experiences has a strong effect on his CHC expression, with female-biased adult sex ratios eliciting greater expression of CHC profiles associated with higher male mating success. Classical models predict that male reproductive investment should be highest when there is a small but nonzero number of rivals, but we found that males expressed the most attractive combination of CHCs when there were no rivals. We found that male CHCs were highly sensitive to adult sex ratio, with males expressing higher values of CHC profiles associated with greater mating success as the ratio of females to males increased. Moreover, sex ratio has a stronger effect on male CHC expression than adult density. Finally, we explore whether sex ratio affects the variance among a group of males in their CHC expression, as might be expected if individuals respond differently to a given social environment, but find little effect. Our results reveal that subtle differences in social environment can induce plasticity in male chemical signal expression.

Local population density and group composition influence the signal-preference relationship in Enchenopa treehoppers (Hemiptera: Membracidae).

Many animals exhibit social plasticity - changes in phenotype or behaviour in response to experience with conspecifics that change how evolutionary processes like sexual selection play out. Here, we asked whether social plasticity arising from variation in local population density in male advertisement signals and female mate preferences influences the form of sexual selection. We manipulated local density and determined whether this changed how the distribution of male signals overlapped with female preferences - the signal preference relationship. We specifically look at the shape of female mate preference functions, which, when compared to signal distributions, provide hypotheses about the form of sexual selection. We used Enchenopa binotata treehoppers, a group of plant-feeding insects that exhibit natural variation in local densities across individual host plants, populations, species and years. We measured male signal frequency and female preference functions across the density treatments. We found that male signals varied across local social groups, but not according to local density. By contrast, female preferences varied with local density - favouring higher signal frequencies in denser environments. Thus, local density changes the signal-preference relationship and, consequently, the expected form of sexual selection. We found no influence of sex ratio on the signal-preference relationship. Our findings suggest that plasticity arising from variation in local group density and composition can alter the form of sexual selection with potentially important consequences both for the maintenance of variation and for speciation.

Consequences of a warming climate for social organisation in sweat bees.

ABSTRACT: The progression from solitary living to caste-based sociality is commonly regarded as a major evolutionary transition. However, it has recently been shown that in some taxa, sociality may be plastic and dependent on local conditions. If sociality can be environmentally driven, the question arises as to how projected climate change will influence features of social organisation that were previously thought to be of macroevolutionary proportions. Depending on the time available in spring during which a foundress can produce worker offspring, the sweat bee Halictus rubicundus is either social or solitary. We analysed detailed foraging data in relation to climate change predictions for Great Britain to assess when and where switches from a solitary to social lifestyle may be expected. We demonstrate that worker numbers should increase throughout Great Britain under predicted climate change scenarios, and importantly, that sociality should appear in northern areas where it has never before been observed. This dramatic shift in social organisation due to climate change should lead to a bigger workforce being available for summer pollination and may contribute towards mitigating the current pollinator crisis. SIGNIFICANCE STATEMENT: The sweat bee Halictus rubicundus is socially polymorphic, expressing both solitary and social forms, and is socially plastic, capable of transitioning from solitary to social forms, depending on local environmental conditions. Here, we analyse detailed foraging data in relation to climate change predictions for Great Britain to show that worker numbers and sociality both increase under predicted climate change scenarios. Especially dramatic will be the appearance of social H. rubicundus nests in the north of Britain, where previously only solitary forms are found. Particularly, if more taxa are found to be socially plastic, environmentally driven shifts in social organisation may help to mitigate future pollinator crises by providing more individuals for pollination.

Group structure predicts variation in proximity relationships between male-female and male-infant pairs of mountain gorillas (Gorilla beringei beringei).

Relationships between conspecifics are influenced by both ecological factors and the social organization they live in. Systematic variation of both--consistent with predictions derived from socioecology models--is well documented, but there is considerable variation within species and populations that is poorly understood. The mountain gorilla (Gorilla beringei) is unusual because, despite possessing morphology associated with male contest competition (e.g., extreme sexual dimorphism), they are regularly observed in both single-male and multimale groups. Both male-female and male-infant bonds are strong because males provide protection against infanticide and/or predation. Risk of these threats varies with social structure, which may influence the strength of social relationships among group members (including females and offspring, if females with lower infant mortality risk are less protective of infants). Here, we investigate the relationship between group structure and the strength of proximity relationships between males and females, males and infants, and females and offspring. Data come from 10 social groups containing 1-7 adult males, monitored by the Dian Fossey Gorilla Fund's Karisoke Research Center in Volcanoes National Park, Rwanda. After controlling for group size and infant age, association strength was similar for male-female pairs across group types with both dominant and nondominant males, but male-infant relationships were strongest in single-male groups where paternity certainty was high and animals had fewer social partners to choose from. The male:female and male:infant ratios better predicted both male-female and male-infant associations than the absolute number of males, females, or infants did. The fewer the number of males per female or infant, the more both pair types associated. Dominant males in groups containing fewer males had higher eigenvector centrality (a measure of importance in a social network) than dominant males in groups with more males. Results indicate that nondominant males are an important influence on relationships between dominant males and females/infants despite their peripheral social positions, and that relationships between males and infants must be considered an important foundation of gorilla social structure.