Indirect genetic effects should make group size more evolvable than expected.

Group size is an important trait for many ecological and evolutionary processes. However, it is not a trait possessed by individuals but by social groups, and as many genomes contribute to group size understanding its genetic underpinnings and so predicting its evolution is a conceptual challenge. Here I suggest how group size can be modelled as a joint phenotype of multiple individuals, and so how models for evolution accounting for indirect genetic effects are essential for understanding the genetic variance of group size. This approach makes it clear that (a) group size should have a larger genetic variance than initially expected as indirect genetic effects always contribute exactly as much as direct genetic effects and (b) the response to selection of group size should be faster than expected based on direct genetic variance alone as the correlation between direct and indirect effects is always at the maximum positive limit of 1. Group size should therefore show relatively rapid evolved increases and decreases, the consequences of which and evidence for I discuss.

Dolphin social phenotypes vary in response to food availability but not the North Atlantic Oscillation index.

Social behaviours can allow individuals to flexibly respond to environmental change, potentially buffering adverse effects. However, individuals may respond differently to the same environmental stimulus, complicating predictions for population-level response to environmental change. Here, we show that bottlenose dolphins (Tursiops truncatus) alter their social behaviour at yearly and monthly scales in response to a proxy for food availability (salmon abundance) but do not respond to variation in a proxy for climate (the North Atlantic Oscillation index). There was also individual variation in plasticity for gregariousness and connectedness to distant parts of the social network, although these traits showed limited repeatability. By contrast, individuals showed consistent differences in clustering with their immediate social environment at the yearly scale but no individual variation in plasticity for this trait at either timescale. These results indicate that social behaviour in free-ranging cetaceans can be highly resource dependent with individuals increasing their connectedness over short timescales but possibly reducing their wider range of connection at longer timescales. Some social traits showed more individual variation in plasticity or mean behaviour than others, highlighting how predictions for the responses of populations to environmental variation must consider the type of individual variation present in the population.

Direct and indirect phenotypic effects on sociability indicate potential to evolve.

The decision to leave or join a group is important as group size influences many aspects of organisms' lives and their fitness. This tendency to socialise with others, sociability, should be influenced by genes carried by focal individuals (direct genetic effects) and by genes in partner individuals (indirect genetic effects), indicating the trait's evolution could be slower or faster than expected. However, estimating these genetic parameters is difficult. Here, in a laboratory population of the cockroach Blaptica dubia, I estimate phenotypic parameters for sociability: repeatability (R) and repeatable influence (RI), that indicate whether direct and indirect genetic effects respectively are likely. I also estimate the interaction coefficient (Ψ), which quantifies how strongly a partner's trait influences the phenotype of the focal individual and is key in models for the evolution of interacting phenotypes. Focal individuals were somewhat repeatable for sociability across a 3-week period (R = 0.080), and partners also had marginally consistent effects on focal sociability (RI = 0.053). The interaction coefficient was non-zero, although in opposite sign for the sexes; males preferred to associate with larger individuals (Ψmale  = -0.129), while females preferred to associate with smaller individuals (Ψfemale  = 0.071). Individual sociability was consistent between dyadic trials and in social networks of groups. These results provide phenotypic evidence that direct and indirect genetic effects have limited influence on sociability, with perhaps most evolutionary potential stemming from heritable effects of the body mass of partners. Sex-specific interaction coefficients may produce sexual conflict and the evolution of sexual dimorphism in social behaviour.

Social Selection and the Evolution of Maladaptation.

Evolution by natural selection is often viewed as a process that inevitably leads to adaptation or an increase in population fitness over time. However, maladaptation, an evolved decrease in fitness, may also occur in response to natural selection under some conditions. Social selection, which arises from the effects of social partners on fitness, has been identified as a potential cause of maladaptation, but we lack a general rule identifying when social selection should lead to a decrease in population mean fitness. Here we use a quantitative genetic model to develop such a rule. We show that maladaptation is most likely to occur when social selection is strong relative to nonsocial selection and acts in an opposing direction. In this scenario, the evolution of traits that impose fitness costs on others may outweigh evolved gains in fitness for the individual, leading to a net decrease in population mean fitness. Furthermore, we find that maladaptation may also sometimes occur when phenotypes of interacting individuals negatively covary. We outline the biological situations where maladaptation in response to social selection can be expected, provide both quantitative genetic and phenotypic versions of our derived result, and suggest what empirical work would be needed to test it. We also consider the effect of social selection on inclusive fitness and support previous work showing that inclusive fitness cannot suffer an evolutionary decrease. Taken together, our results show that social selection may decrease population mean fitness when it opposes individual-level selection, even as inclusive fitness increases.

Social selection is density dependent but makes little contribution to total selection in New Zealand giraffe weevils.

Social selection occurs when traits of interaction partners influence an individual's fitness and can alter total selection strength. However, we have little idea of what factors influence social selection's strength. Further, social selection only contributes to overall selection when there is phenotypic assortment, but simultaneous estimates of social selection and phenotypic assortment are rare. Here, we estimated social selection on body size in a wild population of New Zealand giraffe weevils (Lasiorhynchus barbicornis). We measured phenotypic assortment by body size and tested whether social selection varied with sex ratio, density and interacted with the body size of the focal individual. Social selection was limited and unaffected by sex ratio or the size of the focal individual. However, at high densities social selection was negative for both sexes, consistent with size-based competitive interactions for access to mates. Phenotypic assortment was always close to zero, indicating negative social selection at high densities will not impede the evolution of larger body sizes. Despite its predicted importance, social selection may only influence evolutionary change in specific contexts, leaving direct selection to drive evolutionary change.

Assessing the repeatability, robustness to disturbance, and parent-offspring colony resemblance of collective behavior.

Groups of animals possess phenotypes such as collective behaviour, which may determine the fitness of group members. However, the stability and robustness to perturbations of collective phenotypes in natural conditions is not established. Furthermore, whether group phenotypes are transmitted from parent to offspring groups with fidelity is required for understanding how selection on group phenotypes contributes to evolution, but parent-offspring resemblance at the group level is rarely estimated. We evaluated the repeatability, robustness to perturbation and parent-offspring resemblance of collective foraging aggressiveness in colonies of the social spider Anelosimus eximius. Among-colony differences in foraging aggressiveness were consistent over time but changed if the colony was perturbed through the removal of individuals or via individuals' removal and subsequent return. Offspring and parent colony behaviour were correlated at the phenotypic level, but only once the offspring colony had settled after being translocated, and the correlation overlapped with zero at the among-colony level. The parent-offspring resemblance was not driven by a shared elevation but could be due to other environmental factors. The behaviour of offspring colonies in a common garden laboratory setting was not correlated with the behaviour of the parent colony nor with the same colony's behaviour once it was returned to the field. The phenotypes of groups represent a potentially important tier of biological organization, and assessing the stability and heritability of such phenotypes helps us better understand their role in evolution.

Behavioral and physiological evidence that increasing group size ameliorates the impacts of social disturbance.

Intra-group social stability is important for the long-term productivity and health of social organisms. We evaluated the effect of group size on group stability in the face of repeated social perturbations using a cooperatively breeding fish, Neolamprologus pulcher In a laboratory study, we compared both the social and physiological responses of individuals from small versus large groups to the repeated removal and replacement of the most dominant group member (the breeder male), either with a new male (treatment condition) or with the same male (control condition). Individuals living in large groups were overall more resistant to instability but were seemingly slower to recover from perturbation. Members of small groups were more vulnerable to instability but recovered faster. Breeder females in smaller groups also showed greater physiological preparedness for instability following social perturbations. In sum, we discover both behavioral and physiological evidence that living in larger groups helps to dampen the impacts of social instability in this system.

Territory acquisition mediates the influence of predators and climate on juvenile red squirrel survival.

Juvenile survival to first breeding is a key life-history stage for all taxa. Survival through this period can be particularly challenging when it coincides with harsh environmental conditions such as a winter climate or food scarcity, leading to highly variable cohort survival. However, the small size and dispersive nature of juveniles generally make studying their survival more difficult. In territorial species, a key life-history event is the acquisition of a territory. A territory is expected to enhance survival, but how it does so is not often identified. We tested how the timing of territory acquisition influenced the winter survival of juvenile North American red squirrels Tamiasciurus hudsonicus, hereafter red squirrels, and how the timing of this event mediated the sources of mortality. We hypothesized that securing a territory prior to when food resources become available would reduce juvenile susceptibility to predation and climatic factors overwinter. Using 27 years of data on the survival of individually marked juvenile red squirrels, we tested how the timing of territory acquisition influenced survival, whether the population density of red squirrel predators and mean temperature overwinter were related to individual survival probability, and if territory ownership mediated these effects. Juvenile red squirrel survival was lower in the years of high predator abundance and in colder winters. Autumn territory owners were less susceptible to lynx Lynx canadensis and possibly mustelid Mustela and Martes spp., predation. Autumn territory owners had lower survival in colder winters, but surprisingly non-owners had higher survival in cold winters. Our results show how the timing of a life-history event like territory acquisition can directly affect survival and also mediate the effects of biotic and abiotic factors later in life. This engenders a better understanding of the fitness consequences of the timing of key life-history events.

Indirect effects on fitness between individuals that have never met via an extended phenotype.

Interactions between organisms are ubiquitous and have important consequences for phenotypes and fitness. Individuals can even influence those they never meet, if they have extended phenotypes that alter the environments others experience. North American red squirrels (Tamiasciurus hudsonicus) guard food hoards, an extended phenotype that typically outlives the individual and is usually subsequently acquired by non-relatives. Hoarding by previous owners can, therefore, influence subsequent owners. We found that red squirrels breed earlier and had higher lifetime fitness if the previous hoard owner was a male. This was driven by hoarding behaviour, as males and mid-aged squirrels had the largest hoards, and these effects persisted across owners, such that if the previous owner was male or died in mid-age, subsequent occupants had larger hoards. Individuals can, therefore, influence each other's resource-dependent traits and fitness without ever meeting, such that the past can influence contemporary population dynamics through extended phenotypes.

Opposite responses to selection and where to find them.

We generally expect traits to evolve in the same direction as selection. However, many organisms possess traits that appear to be costly for individuals, while plant and animal breeding experiments reveal that selection may lead to no response or even negative responses to selection. We formalize both of these instances as cases of "opposite responses to selection." Using quantitative genetic models for the response to selection, we outline when opposite responses to selection should be expected. These typically occur when social selection opposes direct selection, when individuals interact with others less related to them than a random member of the population, and if the genetic covariance between direct and indirect effects is negative. We discuss the likelihood of each of these occurring in nature and therefore summarize how frequent opposite responses to selection are likely to be. This links several evolutionary phenomena within a single framework.

Collective aggressiveness limits colony persistence in high- but not low-elevation sites at Amazonian social spiders.

Identifying the traits that foster group survival in contrasting environments is important for understanding local adaptation in social systems. Here, we evaluate the relationship between the aggressiveness of social spider colonies and their persistence along an elevation gradient using the Amazonian spider, Anelosimus eximius. We found that colonies of A. eximius exhibit repeatable differences in their collective aggressiveness (latency to attack prey stimuli) and that colony aggressiveness is linked with persistence in a site-specific manner. Less aggressive colonies are better able to persist at high-elevation sites, which lack colony-sustaining large-bodied prey, whereas colony aggression was not related to chance of persistence at low-elevation sites. This suggests that low aggressiveness promotes colony survival in high-elevation, prey-poor habitats, perhaps via increased tolerance to resource limitation. These data reveal that the collective phenotypes that relate to colony persistence vary by site, and thus, the path of social evolution in these environments is likely to be affected.

Social effects of territorial neighbours on the timing of spring breeding in North American red squirrels.

Organisms can affect one another's phenotypes when they socially interact. Indirect genetic effects occur when an individual's phenotype is affected by genes expressed in another individual. These heritable effects can enhance or reduce adaptive potential, thereby accelerating or reversing evolutionary change. Quantifying these social effects is therefore crucial for our understanding of evolution, yet estimates of indirect genetic effects in wild animals are limited to dyadic interactions. We estimated indirect phenotypic and genetic effects, and their covariance with direct effects, for the date of spring breeding in North American red squirrels (Tamiasciurus hudsonicus) living in an array of territories of varying spatial proximity. Additionally, we estimated indirect effects and the strength of selection at low and high population densities. Social effects of neighbours on the date of spring breeding were different from zero at high population densities but not at low population densities. Indirect phenotypic effects accounted for a larger amount of variation in the date of breeding than differences attributable to the among-individual variance, suggesting social interactions are important for determining breeding dates. The genetic component to these indirect effects was however not statistically significant. We therefore showcase a powerful and flexible method that will allow researchers working in organisms with a range of social systems to estimate indirect phenotypic and genetic effects, and demonstrate the degree to which social interactions can influence phenotypes, even in a solitary species.

Analysing animal social network dynamics: the potential of stochastic actor-oriented models.

Animals are embedded in dynamically changing networks of relationships with conspecifics. These dynamic networks are fundamental aspects of their environment, creating selection on behaviours and other traits. However, most social network-based approaches in ecology are constrained to considering networks as static, despite several calls for such analyses to become more dynamic. There are a number of statistical analyses developed in the social sciences that are increasingly being applied to animal networks, of which stochastic actor-oriented models (SAOMs) are a principal example. SAOMs are a class of individual-based models designed to model transitions in networks between discrete time points, as influenced by network structure and covariates. It is not clear, however, how useful such techniques are to ecologists, and whether they are suited to animal social networks. We review the recent applications of SAOMs to animal networks, outlining findings and assessing the strengths and weaknesses of SAOMs when applied to animal rather than human networks. We go on to highlight the types of ecological and evolutionary processes that SAOMs can be used to study. SAOMs can include effects and covariates for individuals, dyads and populations, which can be constant or variable. This allows for the examination of a wide range of questions of interest to ecologists. However, high-resolution data are required, meaning SAOMs will not be useable in all study systems. It remains unclear how robust SAOMs are to missing data and uncertainty around social relationships. Ultimately, we encourage the careful application of SAOMs in appropriate systems, with dynamic network analyses likely to prove highly informative. Researchers can then extend the basic method to tackle a range of existing questions in ecology and explore novel lines of questioning.

A description of the gross pathology of drowning and other causes of mortality in seabirds.

BACKGROUND: Mortality of seabirds due to anthropogenic causes, especially entrapment in fishing gear, is a matter of increasing international concern. This study aimed at characterising the gross pathology of seabirds that drowned in fishing nets and comparing it with that in other common causes of mortality. RESULTS: Post-mortem examinations were performed on 103 common guillemots, 32 razorbills, 37 shags and 5 great northern divers found stranded in Cornwall during 1981-2016. Pathology in birds that died in confirmed incidents of drowning in fishing nets (n = 95) was compared with that in cases of suspected drowning (n = 6), oil (n = 53) and polyisobutylene (PIB) (n = 3) pollution, adverse weather (n = 6) and stranding of unknown cause (14). The majority of drowned birds were in good nutritional state, freshly dead and approximately 50% had freshly ingested fish in their proximal gut. Principle lesions were: gross distention of the heart and major veins with dark blood, intensely congested, swollen and oedematous lungs which released white frothy fluid when excised, watery fluid in the air sacs that ranged from clear to deep red depending on state of carcase preservation. PIB-affected birds were in good nutritional state; their pathology was largely consistent with that in confirmed drowning cases; it is likely that drowning was the ultimate cause of death. Birds affected by oil, adverse weather or that stranded due to unknown cause were all in poor or emaciated condition, the mean body mass of the guillemots and razorbills being, respectively, 53 and 57% of those that drowned. They had little or no food in their alimentary tracts and many showed evidence of enteric inflammation, haemorrhage and ulceration. None had fluid in their air sacs and none showed significant cardio-respiratory system lesions. CONCLUSIONS: Drowned birds consistently showed a distinctive set of gross pathological lesions. When combined with contemporaneous observations, the pathology may be sufficient to permit a diagnosis of drowning, especially where a batch of freshly dead birds are examined. The observations in this study are likely to be of value when investigating stranding incidents, particularly where it is suspected that legislation aimed at protecting seabirds is not being complied with.

Wild cricket social networks show stability across generations.

BACKGROUND: A central part of an animal's environment is its interactions with conspecifics. There has been growing interest in the potential to capture these interactions in the form of a social network. Such networks can then be used to examine how relationships among individuals affect ecological and evolutionary processes. However, in the context of selection and evolution, the utility of this approach relies on social network structures persisting across generations. This is an assumption that has been difficult to test because networks spanning multiple generations have not been available. We constructed social networks for six annual generations over a period of eight years for a wild population of the cricket Gryllus campestris. RESULTS: Through the use of exponential random graph models (ERGMs), we found that the networks in any given year were able to predict the structure of networks in other years for some network characteristics. The capacity of a network model of any given year to predict the networks of other years did not depend on how far apart those other years were in time. Instead, the capacity of a network model to predict the structure of a network in another year depended on the similarity in population size between those years. CONCLUSIONS: Our results indicate that cricket social network structure resists the turnover of individuals and is stable across generations. This would allow evolutionary processes that rely on network structure to take place. The influence of network size may indicate that scaling up findings on social behaviour from small populations to larger ones will be difficult. Our study also illustrates the utility of ERGMs for comparing networks, a task for which an effective approach has been elusive.

Behaviour in captivity predicts some aspects of natural behaviour, but not others, in a wild cricket population.

Examining the relevance of 'animal personality' involves linking consistent among- and within-individual behavioural variation to fitness in the wild. Studies aiming to do this typically assay personality in captivity and rely on the assumption that measures of traits in the laboratory reflect their expression in nature. We examined this rarely tested assumption by comparing laboratory and field measurements of the behaviour of wild field crickets (Gryllus campestris) by continuously monitoring individual behaviour in nature, and repeatedly capturing the same individuals and measuring their behaviour in captivity. We focused on three traits that are frequently examined in personality studies: shyness, activity and exploration. All of them showed repeatability in the laboratory. Laboratory activity and exploration predicted the expression of their equivalent behaviours in the wild, but shyness did not. Traits in the wild were predictably influenced by environmental factors such as temperature and sunlight, but only activity showed appreciable within-individual repeatability. This suggests that some behaviours typically studied as personality traits can be accurately assayed in captivity, but the expression of others may be highly context-specific. Our results highlight the importance of validating the relevance of laboratory behavioural assays to analogous traits measured in the wild.

True polyandry and pseudopolyandry: why does a monandrous fly remate?

BACKGROUND: The rate of female remating can have important impacts on a species, from affecting conflict and cooperation within families, to population viability and gene flow. However, determining the level of polyandry in a species can be difficult, with information on the mating system of many species being based on a single experiment, or completely absent. Here we investigate the mating system of the fruit fly Drosophila subobscura. Reports from England, Spain and Canada suggest D. subobscura is entirely monandrous, with no females remating. However, work in Greece suggests that 23% of females remate. We examine the willingness of female D. subobscura to remate in the laboratory in a range of conditions, using flies from both Greece and England. We make a distinction between pseudopolyandry, where a female remates after an ineffective first mating that is incapable of fertilising her eggs, and true polyandry, where a female remates even though she has received suitable sperm from a previous mating. RESULTS: We find a low rate of true polyandry by females (4%), with no difference between populations. The rate of true polyandry is affected by temperature, but not starvation. Pseudopolyandry is three times as common as true polyandry, and most females showing pseudopolyandry mated at their first opportunity after their first failed mating. However, despite the lack of differences in polyandry between the populations, we do find differences in the way males respond to exposure to other males prior to mating. In line with previous work, English flies responded to one or more rivals by increasing their copulation duration, a response previously thought to be driven by sperm competition. Greek males only show increased copulation duration when exposed to four or more rival males. This suggests that the response to rivals in D. subobscura is not related to sperm competition, because sperm competition is rare, and there is no correlation of response to rivals and mating system across the populations. CONCLUSIONS: These results illustrate the difficulties in determining the mating system of a species, even one that is well known and an excellent laboratory species, with results being highly dependent on the conditions used to assay the behaviour, and the population used.

When Do We Start Caring About Insect Welfare?

The world is facing an incoming global protein shortage due to existing malnutrition and further rapid increases in population size. It will however be difficult to greatly expand traditional methods of protein production such as cattle, chicken and pig farming, due to space limitations and environmental costs such as deforestation. As a result, alternative sources of protein that require less space and fewer resources, such as insects and other invertebrates, are being sought. The Neotropics are a key area of focus given the widespread prevalence of entomophagy and developing animal welfare regulations. Unlike vertebrate livestock however, insect "minilivestock" are typically not protected by existing animal welfare regulations. This is despite the fact that the evidence is mounting that insects possess "personalities", may experience affective states analogous to emotions and feel something like pain. In this forum article, we highlight this discrepancy, outline some of the emerging research on the topic and identify areas for future research. There are various empirical and ethical questions that must be addressed urgently while insect farming is ramped up around the globe. Finally, we describe the benefits and also potential costs of regulation for insect welfare.

Using multilayer network analysis to explore the temporal dynamics of collective behavior.

Social organisms often show collective behaviors such as group foraging or movement. Collective behaviors can emerge from interactions between group members and may depend on the behavior of key individuals. When social interactions change over time, collective behaviors may change because these behaviors emerge from interactions among individuals. Despite the importance of, and growing interest in, the temporal dynamics of social interactions, it is not clear how to quantify changes in interactions over time or measure their stability. Furthermore, the temporal scale at which we should observe changes in social networks to detect biologically meaningful changes is not always apparent. Here we use multilayer network analysis to quantify temporal dynamics of social networks of the social spider Stegodyphus dumicola and determine how these dynamics relate to individual and group behaviors. We found that social interactions changed over time at a constant rate. Variation in both network structure and the identity of a keystone individual was not related to the mean or variance of the collective prey attack speed. Individuals that maintained a large and stable number of connections, despite changes in network structure, were the boldest individuals in the group. Therefore, social interactions and boldness are linked across time, but group collective behavior is not influenced by the stability of the social network. Our work demonstrates that dynamic social networks can be modeled in a multilayer framework. This approach may reveal biologically important temporal changes to social structure in other systems.