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Data from: Rearing group size determines social competence and brain structure in a cooperatively breeding cichlid
Social animals can greatly benefit from well-developed social skills. Because the frequency and diversity of social interactions often increase with the size of social groups, the benefits of advanced social skills can be expected to increase with group size. Variation in social skills often arises during ontogeny, depending on early social experience. Whether variation of social-group sizes affects development of social skills and related changes in brain structures remains unexplored. We investigated whether, in a cooperatively breeding cichlid, early group size (1) shapes social behavior and social skills and (2) induces lasting plastic changes in gross brain structures and (3) whether the development of social skills is confined to a sensitive ontogenetic period. Rearing-group size and the time juveniles spent in these groups interactively influenced the development of social skills and the relative sizes of four main brain regions. We did not detect a sensitive developmental period for the shaping of social behavior within the 2-month experience phase. Instead, our results suggest continuous plastic behavioral changes over time. We discuss how developmental effects on social behavior and brain architecture may adaptively tune phenotypes to their current or future environments.
Data from: 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 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 or not to socially associate. In particular, we found that individuals altered when they socially associated according to 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 intra-sexual conflict or sexual harassment is high. Using a behavioural 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.
Data from: Using social parasitism to test reproductive skew models in a primitively eusocial wasp
Remarkable variation exists in the distribution of reproduction (skew) among members of cooperatively breeding groups, both within and between species. Reproductive skew theory has provided an important framework for understanding this variation. In the primitively eusocial Hymenoptera, two models have been routinely tested: concessions models, which assume complete control of reproduction by a dominant individual, and tug-of-war models, which assume on-going competition among group members over reproduction. Current data provide little support for either model, but uncertainty about the ability of individuals to detect genetic relatedness and difficulties in identifying traits conferring competitive ability mean that the relative importance of concessions versus tug-of-war remains unresolved. Here, we suggest that the use of social parasitism to generate meaningful variation in key social variables represents a valuable opportunity to explore the mechanisms underpinning reproductive skew within the social Hymenoptera. We present a direct test of concessions and tug-of-war models in the paper wasp Polistes dominulus by exploiting pronounced changes in relatedness and power structures that occur following replacement of the dominant by a congeneric social parasite. Comparisons of skew in parasitized and unparasitized colonies are consistent with a tug-of-war over reproduction within P. dominulus groups, but provide no evidence for reproductive concessions.
Data from: Reduced cellular immune response in social insect lineages
Social living poses challenges for individual fitness because of the increased risk of disease transmission among conspecifics. Despite this challenge, sociality is an evolutionarily successful lifestyle, occurring in the most abundant and diverse group of organisms on earth—the social insects. Two contrasting hypotheses predict the evolutionary consequences of sociality on immune systems. The social group hypothesis posits that sociality leads to stronger individual immune systems because of the higher risk of disease transmission in social species. By contrast, the relaxed selection hypothesis proposes that social species have evolved behavioural immune defences that lower disease risk within the group, resulting in lower immunity at the individual level. We tested these hypotheses by measuring the encapsulation response in 11 eusocial and non-eusocial insect lineages. We built phylogenetic mixed linear models to investigate the effect of behaviour, colony size and body size on cellular immune response. We found a significantly negative effect of colony size on encapsulation response (Markov chain Monte Carlo generalized linear mixed model (mcmcGLMM) p < 0.05; phylogenetic generalized least squares (PGLS) p < 0.05). Our findings suggest that insects living in large societies may rely more on behavioural mechanisms, such as hygienic behaviours, than on immune function to reduce the risk of disease transmission among nest-mates.
Data from: Social feedback and the emergence of rank in animal society
Dominance hierarchies are group-level properties that emerge from the aggression of individuals. Although individuals can gain critical benefits from their position in a hierarchy, we do not understand how real-world hierarchies form. Nor do we understand what signals and decision-rules individuals use to construct and maintain hierarchies in the absence of simple cues such as size or spatial location. A study of conflict in two groups of captive monk parakeets (Myiopsitta monachus) found that a transition to large-scale order in aggression occurred in newly-formed groups after one week, with individuals thereafter preferring to direct aggression more frequently against those nearby in rank. We consider two cognitive mechanisms underlying the emergence of this order: inference based on overall levels of aggression, or on subsets of the aggression network. Both mechanisms were predictive of individual decisions to aggress, but observed patterns were better explained by rank inference through subsets of the aggression network. Based on these results, we present a new theory, of a feedback loop between knowledge of rank and consequent behavior. This loop explains the transition to strategic aggression and the formation and persistence of dominance hierarchies in groups capable of both social memory and inference.
Data from: Pair bonds, reproductive success and rise of alternate mating strategies in a social carnivore.
Monogamy is commonly observed across a wide variety of species and taxa and arises when young are altricial, parental investment in young is high, and mate monopolization is generally not possible. In such species, pairs may bond for multiple breeding seasons while successfully rearing young. Individuals, however, may attempt to bypass the dominant mating strategy particularly when breeding opportunities are limited. Currently, we do not know how pair bond duration affects the efficacy of alternative mating strategies in populations with a monogamous mating system. Additionally, inferences about pair bond effects on reproductive success (i.e., both clutch size and recruitment) are largely limited to long-lived birds and little is known about effects on mammalian cooperative breeders. I used genetic sampling and pedigrees to examine the effects of pair bond duration on reproductive success (i.e., litter size, recruitment) and mating strategies in a population of gray wolves (Canis lupus) in Idaho USA. There was a positive, marginally significant relationship between pair bond duration and apparent survival of offspring. Increased pair bond duration was also associated with a dampening in the prevalence of other alternative mating strategies such as sneaker males and polygamy. The selective advantage of alternative mating strategies are a combination of population, group (for applicable species), individual, and social influences such as pair bonds. The distribution of pair bonds in a monogamous population affects the selective advantage, and hence frequency, of various mating strategies observed.
Data from: Patterns of reproductive isolation in a haplodiploid – strong post‐mating, prezygotic barriers among three forms of a social spider mite
In speciation research, much attention is paid to the evolution of reproductive barriers, preventing diverging groups from hybridizing back into one gene pool. The prevalent view is that reproductive barriers evolve gradually as a byproduct of genetic changes accumulated by natural selection and genetic drift in groups that are segregated spatially and/or temporally. Reproductive barriers, however, can also be reinforced by natural selection against maladaptive hybridization. These mutually compatible theories are both empirically supported by studies, analyzing relationships between intensity of reproductive isolation and genetic distance in sympatric taxa and allopatric taxa. Here, we present the – to our knowledge – first comparative study in a haplodiploid organism, the social spider mite Stigmaeopsis miscanthi, by measuring premating and postmating pre- and postzygotic components of reproductive isolation, using three recently diverged forms of the mite that partly overlap in home range. We carried out cross experiments and measured genetic distances (mtDNA and nDNA) among parapatric and allopatric populations of the three forms. Our results show that the three forms are reproductively isolated, despite the absence of premating barriers, and that the postmating, prezygotic component contributes most to reproductive isolation. As expected, the strength of postmating reproductive barriers positively correlated with genetic distance. We did not find a clear pattern of prezygotic barriers evolving faster in parapatry than in allopatry, although one form did show a trend in line with the ecological and behavioral relationships between the forms. Our study advocates the versatility of haplodiploid animals for investigating the evolution of reproductive barriers.
Data from: Social context alters host behavior and infection risk
Variation in infection risk and transmission potential are widespread in human and wildlife diseases and play a central role in host-pathogen dynamics. To explain this variation, most studies focus on linking host traits to differences in pathogen exposure, infection, and transmission, but typically do not to account for hosts' social context. Yet, an individual's risk of acquiring infection is likely influenced jointly by their own traits and their social environment. Here, we use three natural genotypes of the fruit fly Drosophila melanogaster to test how variation in pathogen transmission is linked to differences in host behavior and social context. We constructed groups of 12 flies from one of three different genotypes and five different sex ratios (0%, 33%, 50%, 67%, or 100% female) in a fully factorial design. To each group we added a male or female "primary case" fly that had been exposed to the generalist fungal entomopathogen Metarhizium robertsii. We then recorded groups' aggregation behavior, mating frequency, and infection prevalence. Aggregation and mating behavior were influences either jointly or additively by fly genotype and sex ratio. However, a combination of individual-level (mating history; the sex of the primary case) and group-level factors (sex ratio) jointly influenced individuals' infection risk. There were more infections in female-biased groups, though the sex of the primary case also influenced sex-biased mortality and the relationship between individuals' mating history and infection risk. Thus, an individual's social environment can be an important predictor of social dynamics and their survival outcomes.
Data from: Age and early social environment influence guppy social learning propensities
Social learning, learning from others, allows animals to quickly and adaptively adjust to changing environments, but only if social learning provides reliable, useful information in that environment. Early life conditions provide a potential cue to the reliability of social information later in life. Here, we addressed whether direct early life experience of the utility of social learning influences later social learning propensities. We reared guppy, Poecilia reticulata, fry for 45 days in three different social conditions which involved the presence of adult demonstrators providing cues about feeding locations in the tanks ('follow adults' and 'avoid adults' treatments), or their absence ('no adults' treatment). In the 'follow adults' treatment, juveniles that swam in the same direction as the adult demonstrators found food, whereas in the 'avoid adults' treatment, subjects that swam in the opposite direction to the demonstrators found food. We then tested the fish with a social learning task, to examine whether prior experience had influenced the social learning tendencies of the juveniles. After another 45 days of rearing under common-garden conditions with no adult fish present in the tanks, subjects were retested with the same social learning task, to investigate whether early experiences had effects persisting into adulthood. After 45 days of rearing we found no evidence for social learning in any of the experimental groups. However, after 90 days of rearing, we found evidence of social learning, but only in the 'follow adults' treatment. These results suggest that social learning propensities may develop over life, and that prior exposure to conspecifics providing useful foraging information during early life can shape the degree of reliance on social learning in adulthood.
Data from: Social buffering of stress in a group-living fish
Living in groups affords individuals many benefits including the opportunity to reduce stress. In mammals, such 'social buffering' of stress is mediated by affiliative relationships and production of the neuropeptide oxytocin, but whether these mechanisms facilitate social buffering across vertebrates remains an open question. Therefore, we evaluated whether the social environment influenced the behavioural and physiological recovery from an acute stressor in a group-living cichlid, Neolamprologus pulcher. Individual fish that recovered with their social group displayed lower cortisol levels than individuals that recovered alone. This social buffering of the stress response was associated with a tendency towards lower transcript abundance of arginine vasotocin and isotocin in the preoptic area of the brain, suggesting reduced neural activation of the stress axis. Individuals that recovered with their social group quickly resumed normal behaviour but received fewer affiliative acts following the stressor. Further experiments revealed similar cortisol levels between individuals that recovered in visual contact with their own social group and those in visual contact with a novel but non-aggressive social group. Collectively, our results suggest that affiliation and familiarity per se do not mediate social buffering in this group-living cichlid, and the behavioural and physiological mechanisms responsible for social buffering may vary across vertebrates.
Data from: Iterative evolution of increased behavioral variation characterizes the transition to sociality in spiders and proves advantageous
The evolution of group living is regarded as a major evolutionary transition and is commonly met with correlated shifts in ancillary characters. We tested for associations between social tendency and a myriad of abiotic variables and behavioral traits (e.g., boldness, activity level) in a clade of spiders that exhibit highly variable social structures.We found that social species tended to exhibit reduced aggressiveness towards prey, increased fearfulness towards predators, reduced activity levels, and occurred in warm, wet habitats with low wind velocities. Within-species variation in aggressiveness and boldness were greater in social species. We then assessed the functional consequences of within-species trait variation on reconstituted colonies of four species (A. eximius, A. rupununi, A. guacamayos, A. oritoyacu). We used colonies consisting of known ratios of docile versus aggressive individuals and group foraging success as a measure of colony performance.We found that groups composed of a mixture of docile and aggressive individuals outperformed monotypic groups: (1) mixed groups were more effective at subduing medium and large sized prey, and (2) mixed groups collectively gained more mass during shared feeding events. Our results suggest that the iterative evolution of depressed aggressiveness and increased within-species behavioral variation in social spiders is advantageous, and could be an adaptation to group living that is analogous to the formation of morphological castes within the social insects
Data from: Conflict between background matching and social signalling in a colour-changing freshwater fish
The ability to change coloration allows animals to modify their patterning to suit a specific function. Many freshwater fishes, for example, can appear cryptic by altering the dispersion of melanin pigment in the skin to match the visual background. However, melanin-based pigments are also used to signal dominance among competing males; thus colour change for background matching may conflict with colour change for social status signalling. We used a colour-changing freshwater fish to investigate whether colour change for background matching influenced aggressive interactions between rival males. Subordinate males that had recently darkened their skin for background matching received heightened aggression from dominant males, relative to males whose coloration had not changed. We then determined whether the social status of a rival male, the focal male's previous social status, and his previous skin coloration, affected a male's ability to change colour for background matching. Social status influenced skin darkening in the first social encounter, with dominant males darkening more than subordinate males, but there was no effect of social status on colour change in the second social encounter. We also found that the extent of skin colour change (by both dominant and subordinate males) was dependent on previous skin coloration, with dark males displaying a smaller change in coloration than pale males. Our findings suggest that skin darkening for background matching imposes a significant social cost on subordinate males in terms of increased aggression. We also suggest that the use of melanin-based signals during social encounters can impede subsequent changes in skin coloration for other functions, such as skin darkening for background matching.
Data from: Causes of and contributors to infant mortality in a rural community of North India: evidence from verbal and social autopsy
Objective: Retrospective analysis of routinely collected data using verbal and social autopsy tools to identify the medical causes of death and contribution of non-biological factors towards infant mortality Setting: The study site was Health and Demographic Surveillance System (HDSS), Ballabgarh, North India Participants: All infant deaths during year 2008 to 2012 were included for verbal autopsy whereas infant deaths from July 2012 to December 2012 were included for social autopsy. Outcome measures: Cause of death ascertained by validated verbal autopsy tool and level of delay based on three delay model using INDEPTH social autopsy tool were the main outcome measures. Results: Infant mortality rate during study period was 46.5/100 live births. Neonatal deaths contributed to 54.3% of infant deaths and 39% occurred on first day of life. Birth asphyxia (31.5%) followed by Low Birth Weight (LBW)/prematurity (26.5%) were the most common causes of neonatal death. While infective cause (57.8) was the most common cause of post-neonatal death. Care-seeking was delayed among 50% of neonatal deaths and 41.2% of post-neonatal deaths. Delay at level 1 was most common, observed in 32.4% of neonatal deaths and 29.4% of post-neonatal deaths. Deaths due to LBW/prematurity were mostly followed by delay at level 1. Conclusion: High proportion of preventable infant mortality still exists in an area which is under continuous health and demographic surveillance. There is need to enhance home based preventive care to enable the mother to identify and respond to danger signs. Verbal autopsy and social autopsy could be routinely done to guide policy interventions aimed at reduction of infant mortality.
Data from: Gliding lizards use the position of the sun to enhance social display
Effective communication requires animal signals to be readily detected by receivers in the environments in which they are typically given. Certain light conditions enhance the visibility of colour signals and these conditions can vary depending on the orientation of the sun and the position of the signaller. We tested whether Draco sumatranus gliding lizards modified their position relative to the sun to enhance the conspicuousness of their throat-fan (dewlap) during social display to conspecifics. The dewlap was translucent, and we found that lizards were significantly more likely to orient themselves perpendicular to the sun when displaying. This increases the dewlap's radiance, and likely, its conspicuousness, by increasing the amount of light transmitted through the ornament. This is a rare example of a behavioural adaptation for enhancing the visibility of an ornament to distant receivers.
Data from: Phylogenetic tests reject Emery's rule in the evolution of social parasitism in yellowjackets and hornets (Hymenoptera: Vespidae, Vespinae)
Social parasites exploit the brood-care behaviour and social structure of one or more host species. Within the social Hymenoptera there are different types of social parasitism. In its extreme form, species of obligate social parasites, or inquilines, do not have the worker caste and depend entirely on the workers of a host species to raise their reproductive offspring. The strict form of Emery's rule states that social parasites share immediate common ancestry with their hosts. Moreover, this rule has been linked with a sympatric origin of inquilines from their hosts. Here, we conduct phylogenetic analyses of yellowjackets and hornets based on 12 gene fragments and evaluate competing evolutionary scenarios to test Emery's rule. We find that inquilines, as well as facultative social parasites, are not the closest relatives of their hosts. Therefore, Emery's rule in its strict sense is rejected, suggesting that social parasites have not evolved sympatrically from their hosts in yellowjackets and hornets. However, the relaxed version of the rule is supported, as inquilines and their hosts belong to the same Dolichovespula clade. Furthermore, inquilinism has evolved only once in Dolichovespula.
Data from: Personal information about danger trumps social information from avian alarm calls
Information about predators can mean the difference between life and death, but prey face the challenge of integrating personal information about predators with social information from the alarm calls of others. This challenge might even affect the structure of interspecific information networks: species vary in response to alarm calls, potentially because different foraging ecologies constrain the acquisition of personal information. However, the hypothesis that constrained personal information explains a greater response to alarm calls has not been experimentally tested. We used a within-species test to compare the antipredator responses of New Holland honeyeaters, Phylidonyris novaehollandiae, during contrasting foraging behaviour. Compared to perched birds, which hawk for insects and have a broad view, those foraging on flowers were slower to spot gliding model predators, showing that foraging behaviour can affect predator detection. Furthermore, nectar-foraging birds were more likely to flee to alarm call playbacks. Birds also assessed social information relevance: more distant calls, and those from another species, prompted fewer flights and slower reaction times. Overall, birds made flexible decisions about danger by integrating personal and social information, while weighing information relevance. These findings support the idea that a strategic balance of personal and social information could affect community function.
Data from: Social disappointment explains chimpanzees' behaviour in the inequity aversion task
Chimpanzees' refusal of less-preferred food when an experimenter has previously provided preferred food to a conspecific has been taken as evidence for a sense of fairness. Here, we present a novel hypothesis—the social disappointment hypothesis—according to which food refusals express chimpanzees' disappointment in the human experimenter for not rewarding them as well as they could have. We tested this hypothesis using a two-by-two design in which food was either distributed by an experimenter or a machine and with a partner present or absent. We found that chimpanzees were more likely to reject food when it was distributed by an experimenter rather than by a machine and that they were not more likely to do so when a partner was present. These results suggest that chimpanzees' refusal of less-preferred food stems from social disappointment in the experimenter and not from a sense of fairness.
Data from: Spatial discounting of food and social rewards in guppies (Poecilia reticulata).
In temporal discounting, animals trade off the time to obtain a reward against the quality of a reward, choosing between a smaller reward available sooner versus a larger reward available later. Similar discounting can apply over space, when animals choose between smaller and closer versus larger and more distant rewards. Most studies of temporal and spatial discounting in nonhuman animals use food as the reward, and it is not established whether animals trade off other preferred stimuli in similar ways. Here, we offered female guppies (Poecilia reticulata) a spatial discounting task in which we measured preferences for a larger reward as the distance to it increased relative to a closer but smaller reward. We tested whether the fish discounted reward types differently by offering subjects either food items or same-sex conspecifics as rewards. Before beginning the discounting tasks, we conducted validation tests to ensure that subjects equally valued the food and social stimuli in the quantities provided. In the discounting task, subjects switched their preferences from the larger to the smaller reward as the distance to the larger reward increased (spatial discounting), but the pattern and magnitude of discounting did not differ across the two reward types. These findings indicate that guppies show similar patterns of discounting food and social rewards in a spatial task. In an analysis of travel times, however, the fish swam faster to food rewards than to shoaling partners. This difference in travel times implies that fish temporally discounted social rewards less steeply than food rewards. Thus, reward type influences temporal discounting, suggesting a dissociation between temporal and spatial discounting. Our results illustrate how animals adjust choices and travel times depending on both the type of cost (time, distance) and benefits (food, social partners).
Data from: The rate and effects of spontaneous mutation on fitness traits in the social amoeba, Dictyostelium discoideum
We performed a mutation accumulation (MA) experiment using the social amoeba Dictyostelium discoideum to estimate the rate and distribution of effects of spontaneous mutations affecting eight putative fitness traits. We found that the per generation mutation rate for most fitness components is 0.0019 mutations per haploid genome per generation, or larger. This rate is an order of magnitude higher than estimates for fitness components in the unicellular eukaryote Saccharomyces cerevisiae, even though the base-pair substitution rate is two orders of magnitude lower. The high rate of fitness-altering mutations observed in this species may be partially explained by a large mutational target relative to Saccharomyces cerevisiae. Also, fitness-altering mutations may occur primarily at simple sequence repeats, which are common throughout the genome, including in coding regions, and may represent a target that is particularly likely to give fitness effects upon mutation. The majority of mutations had deleterious effects on fitness, but there was evidence for a substantial fraction, up to 40%, being beneficial for some of the putative fitness traits. Competitive ability within the multicellular slug appears to be under weak directional selection, perhaps reflecting the fact that slugs are sometimes, but not often, comprised of multiple clones in nature. Evidence for pleiotropy among fitness components across MA lines was absent, suggesting that mutations tend to act on single fitness components.
Data from: Honey bee (Apis mellifera) sociability and nestmate affiliation is dependent on the social environment experienced post-eclosion
Underpinning the formation of a social group is the motivation of individuals to aggregate and interact with conspecifics, termed sociability. Here we developed an assay, inspired by vertebrate approaches to evaluate social behaviours, to simultaneously examine the development of honey bee (Apis mellifera) sociability and nestmate affiliation. Focal bees were placed in a testing chamber, which was separated from groups of nestmates and conspecific non-nestmates by single-layer mesh screens. Assessing how much time bees spent contacting the two mesh screens allowed us to quantify simultaneously how much bees sought proximity and interaction with other bees, and their preference for nestmates over non-nestmates. Both sociability and nestmate affiliation could be detected soon after emergence as an adult. Isolation early in adult life impaired honey bee sociability but there was no evidence for a critical period for the development of the trait since isolated bees exposed to their hive for 24 hours when as old as 6 days still recovered high levels of sociability. Our data show that even for advanced social insects, sociability is a developmental phenomenon and experience-dependent.
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Allen Brain Atlas
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Annotated Behaviour and Observability Dataset (ABODe)
ABODe is a University of Edinburgh DataShare dataset for behavior classification in group-housed mice using home-cage video, identities, bounding boxes, ground-plate positions, and annotator labels.
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