The benefit of being a social butterfly: communal roosting deters predation

Aposematic passion-vine butterflies from the genus Heliconius form communal roosts on a nightly basis. This behaviour has been hypothesized to be beneficial in terms of information sharing and/or anti-predator defence. To better understand the adaptive value of communal roosting, we tested these two hypotheses in field studies. The information-sharing hypothesis was addressed by examining following behaviour of butterflies departing from natural roosts. We found no evidence of roost mates following one another to resources, thus providing no support for this hypothesis. The anti-predator defence hypothesis was tested using avian-indiscriminable Heliconius erato models placed singly and in aggregations at field sites. A significantly higher number of predation attempts were observed on solitary models versus aggregations of models. This relationship between aggregation size and attack rate suggests that communally roosting butterflies enjoy the benefits of both overall decreased attack frequency as well as a prey dilution effect. Communal roosts probably deter predators through collective aposematism in which aggregations of conspicuous, unpalatable prey communicate a more effective repel signal to predators. On the basis of our results, we propose that predation by birds is a key selective pressure maintaining Heliconius communal roosting behaviour.     

Evolving the neuroendocrine physiology of human and primate cooperation and collective action

While many hormones play vital roles in facilitating or reinforcing cooperative behaviour, the neurohormones underlying competitive and cooperative behaviours are largely conserved across all mammals. This raises the question of how endocrine mechanisms have been shaped by selection to produce different levels of cooperation in different species. Multiple components of endocrine physiology—from baseline hormone concentrations, to binding proteins, to the receptor sensitivity and specificity—can evolve independently and be impacted by current socio-ecological conditions or individual status, thus potentially generating a wide range of variation within and between species. Here, we highlight several neurohormones and variation in hormone receptor genes associated with cooperation, focusing on the role of oxytocin and testosterone in contexts ranging from parenting and pair-bonding to reciprocity and territorial defence. While the studies reviewed herein describe the current state of the literature with regard to hormonal modulators of cooperation and collective action, there is still a paucity of research on hormonal mechanisms that help facilitate large-scale collective action. We end by discussing several potential areas for future research.     

Balancing costs and benefits in primates: ecological and palaeoanthropological views

Maintaining the balance between costs and benefits is challenging for species living in complex and dynamic socio-ecological environments, such as primates, but also crucial for shaping life history, reproductive and feeding strategies. Indeed, individuals must decide to invest time and energy to obtain food, services and partners, with little direct feedback on the success of their investments. Whereas decision-making relies heavily upon cognition in humans, the extent to which it also involves cognition in other species, based on their environmental constraints, has remained a challenging question. Building mental representations relating behaviours and their long-term outcome could be critical for other primates, but there are actually very little data relating cognition to real socio-ecological challenges in extant and extinct primates. Here, we review available data illustrating how specific cognitive processes enable(d) modern primates and extinct hominins to manage multiple resources (e.g. food, partners) and to organize their behaviour in space and time, both at the individual and at the group level. We particularly focus on how they overcome fluctuating and competing demands, and select courses of action corresponding to the best possible packages of potential costs and benefits in reproductive and foraging contexts.This article is part of the theme issue ‘Existence and prevalence of economic behaviours among non-human primates’.     

Coordination of Group Movements in Wild Red-fronted Lemurs (<Emphasis Type="Italic">Eulemur rufifrons</Emphasis>): Processes and Influence of Ecological and Reproductive Seasonality

Group-living species have to coordinate collective actions to maintain cohesion. In primates, spatial movements represent a meaningful model to study group coordination processes across different socio-ecological contexts. We studied 4 groups of red-fronted lemurs (Eulemur rufifrons) in Kirindy Forest, Madagascar, between 2008 and 2010 across different ecological and reproductive seasons. We collected data on ranging patterns using GPS collars and observational data on different predefined parameters of group movements, including initiation, leadership, followership, overtaking events, termination, and travel distances. Cohesion of these relatively small, egalitarian lemur groups was high year-round, but daily path length and home range size varied considerably between ecological seasons, presumably due to long-distance migrations of some groups at the beginning of the rainy season. Individuals of different age and sex classes successfully initiated group movements. However, stable female leadership prevailed year-round, irrespective of ecological and reproductive season, which might be due to higher or more specific energetic requirements of reproduction. In contrast to lemur species with a more despotic social structure, female red-fronted lemurs did not recruit more followers than males. Adult leaders recruited more followers than subadult ones. Further, recruitment success was higher during the peak of the dry season, when predation risk appeared to be higher. Distances of single group movements did not depend on the initiator’s sex and age or on ecological seasons. Our results provide new insights into seasonal variability of coordination processes and the role of social dominance in lemur group movements, thereby contributing to a comparative perspective from a primate radiation that evolved group living independently of anthropoids.     

Economic behaviours among non-human primates

Do we have any valid reasons to affirm that non-human primates display economic behaviour in a sufficiently rich and precise sense of the phrase? To address this question, we have to develop a set of criteria to assess the vast array of experimental studies and field observations on individual cognitive and behavioural competences as well as the collective organization of non-human primates. We review a sample of these studies and assess how they answer to the following four main challenges. (i) Do we see any economic organization or institutions emerge among groups of non-human primates? (ii) Are the cognitive abilities, and often biases, that have been evidenced as underlying typical economic decision-making among humans, also present among non-human primates? (iii) Can we draw positive lessons from performance comparisons among primate species, humans and non-humans but also across non-human primate species, as elicited by canonical game-theoretical experimental paradigms, especially as far as economic cooperation and coordination are concerned? And (iv) in which way should we improve models and paradigms to obtain more ecological data and conclusions? Articles discussed in this paper most often bring about positive answers and promising perspectives to support the existence and prevalence of economic behaviours among non-human primates.This article is part of the theme issue ‘Existence and prevalence of economic behaviours among non-human primates’.     

Spatial and temporal extinction dynamics in a freshwater cetacean

Geographical range contraction is a fundamental ecological characteristic of species population decline, but relatively little investigation has been conducted into general trends in the dynamic properties of range collapse. The Yangtze River dolphin or baiji (Lipotes vexillifer), probably the first large mammal species to have become extinct in over 50 years, was believed to have experienced major range collapse during its decline through progressive large-scale range contraction and fragmentation. This range-collapse model is challenged by a new dataset of 406 baiji last-sighting records collected from across the baiji''s historical range during an interview survey of Yangtze fishing communities. Although baiji regional abundance may have varied across its range, analyses of the extensive new sighting series provide comprehensive evidence that baiji population decline was not associated with any major contraction in geographical range across the middle–lower Yangtze drainage, even in the decade immediately before probable global extinction of the species. Extinction risk in baiji was therefore seemingly not related to evidence of range collapse. Baiji apparently underwent large-scale periodic and seasonal movements across their range, and we propose that range contraction and fragmentation may not be general biogeographic characteristics for declining populations of mobile species in connected landscapes.     

Aspects of the Social Ethology of Some Kalahari Rodents

Studied the social structure of nine rodent species in a subdesert environment by means of direct observation and live- and snaptrapping. Six social groupings — asocial, solitary dispersed; social, solitary clustered; social, communal pair; social, communal but non-colonial; social, communal with little contact; social, communal with close contact (colonial) — are recognized. Diurnal species tend to live in colonies, probably with mutual warning systems against predators. For most species the social structure exhibited is an adaptation to predation, with the effect of food requirements playing a subsidiary role. Larder hoarding is common in solitary and asocial species.     

The ecology of cooperative breeding behaviour

Ecology is a fundamental driving force for the evolutionary transition from solitary living to breeding cooperatively in groups. However, the fact that both benign and harsh, as well as stable and fluctuating, environments can favour the evolution of cooperative breeding behaviour constitutes a paradox of environmental quality and sociality. Here, we propose a new model – the dual benefits framework – for resolving this paradox. Our framework distinguishes between two categories of grouping benefits – resource defence benefits that derive from group‐defended critical resources and collective action benefits that result from social cooperation among group members – and uses insider–outsider conflict theory to simultaneously consider the interests of current group members (insiders) and potential joiners (outsiders) in determining optimal group size. We argue that the different grouping benefits realised from resource defence and collective action profoundly affect insider–outsider conflict resolution, resulting in predictable differences in the per capita productivity, stable group size, kin structure and stability of the social group. We also suggest that different types of environmental variation (spatial vs. temporal) select for societies that form because of the different grouping benefits, thus helping to resolve the paradox of why cooperative breeding evolves in such different types of environments.     

Convergent exaptation and adaptation in solitary island lizards

Independent evolutionary lineages often display similar characteristics in comparable environments. Three kinds of historical hypotheses could explain this convergence. The first is adaptive and evolutionary: nonrandom patterns may result from analogous evolutionary responses to shared conditions. The second explanation is exaptive and ecological: species may be filtered by their suitability for a particular type of environment. The third potential explanation is a null hypothesis of random colonization from a historically nonrandom source pool. Here we demonstrate that both exaptation and adaptation have produced convergent similarity in different size-related characters of solitary island lizards. Large sexual size dimorphism results from adaptive response to solitary existence; uniform, intermediate size results from ecological filtering of potential colonizers. These results demonstrate the existence of deterministic exaptive convergence and suggest that convergent phenomena may require historical explanations that are ecological as well as evolutionary.     

Life on the edge: carnivore body size variation is all over the place

Evolutionary biologists have long been fascinated by both the ways in which species respond to ecological conditions at the edges of their geographic ranges and the way that species'' body sizes evolve across their ranges. Surprisingly, though, the relationship between these two phenomena is rarely studied. Here, we examine whether carnivore body size changes from the interior of their geographic range towards the range edges. We find that within species, body size often varies strongly with distance from the range edge. However, there is no general tendency across species for size to be either larger or smaller towards the edge. There is some evidence that the smallest guild members increase in size towards their range edges, but results for the largest guild members are equivocal. Whether individuals vary in relation to the distance from the range edges often depends on the way edge and interior are defined. Neither geographic range size nor absolute body size influences the tendency of size to vary with distance from the range edge. Therefore, we suggest that the frequent significant association between body size and the position of individuals along the edge-core continuum reflects the prevalence of geographic size variation and that the distance to range edge per se does not influence size evolution in a consistent way.     

Natural cooperators: Food sharing in humans and other primates

The study of cooperation is rich with theoretical models and laboratory experiments that have greatly advanced our knowledge of human uniqueness, but have sometimes lacked ecological validity. We therefore emphasize the need to tie discussions of human cooperation to the natural history of our species and its closest relatives, focusing on behavioral contexts best suited to reveal underlying selection pressures and evolved decision rules. 1 - 3 Food sharing is a fundamental form of cooperation that is well‐studied across primates and is particularly noteworthy because of its central role in shaping evolved human life history, social organization, and cooperative psychology. 1 - 16 Here we synthesize available evidence on food sharing in humans and other primates, tracing the origins of offspring provisioning, mutualism, trade, and reciprocity throughout the primate order. While primates may gain some benefits from sharing, humans, faced with more collective action problems in a risky foraging niche, expanded on primate patterns to buffer risk and recruit mates and allies through reciprocity and signaling, and established co‐evolving social norms of production and sharing. Differences in the necessity for sharing are reflected in differences in sharing psychology across species, thus helping to explain unique aspects of our evolved cooperative psychology.     

Solving the puzzle of collective action through inter-individual differences

Models of collective action infrequently account for differences across individuals beyond a limited set of strategies, ignoring variation in endowment (e.g. physical condition, wealth, knowledge, personality, support), individual costs of effort, or expected gains from cooperation. However, behavioural research indicates these inter-individual differences can have significant effects on the dynamics of collective action. The papers contributed to this theme issue evaluate how individual differences affect the propensity to cooperate, and how they can catalyse others’ likelihood of cooperation (e.g. via leadership). Many of the papers emphasize the relationship between individual decisions and socio-ecological context, particularly the effect of group size. All together, the papers in this theme issue provide a more complete picture of collective action, by embracing the reality of inter-individual variation and its multiple roles in the success or failure of collective action.     

Application of in silico and in vitro methods in the development of adverse outcome pathway constructs in wildlife

There is a long history of using both in silico and in vitro methods to predict adverse effects in humans and environmental species where toxicity data are lacking. Currently, there is a great deal of interest in applying these methods to the development of so-called ‘adverse outcome pathway’ (AOP) constructs. The AOP approach provides a framework for organizing information at the chemical and biological level, allowing evidence from both in silico and in vitro studies to be rationally combined to fill gaps in knowledge concerning toxicological events. Fundamental to this new paradigm is a greater understanding of the mechanisms of toxicity and, in particular, where these mechanisms may be conserved across taxa, such as between model animals and related wild species. This presents an opportunity to make predictions across diverse species, where empirical data are unlikely to become available as is the case for most species of wildlife.     

To be or not to be convergent in salicin-based defence in chrysomeline leaf beetle larvae: evidence from Phratora vitellinae salicyl alcohol oxidase

Glandular chemical defence relying on the action of salicylaldehyde is characteristic for Chrysomela leaf beetle larvae. The salicylaldehyde precursor salicin, sequestered from salicaceous host plants, is deglucosylated and the aglycon further oxidized by a salicyl alcohol oxidase (SAO) to the respective aldehyde. SAOs, key enzymes in salicin-based glandular chemical defence, were previously identified and shown to be of a single evolutionary origin in Chrysomela species. We here identified and characterized SAO of Phratora vitellinae, the only species outside the genus Chrysomela that produce salicylaldehyde as a defensive compound. Although Chrysomela and Phratora are not closest relatives, their SAOs share glucose-methanol-choline oxidoreductase (GMC) affiliation, a specific GMCi subfamily ancestor, glandular tissue-specific expression and almost identical gene architectures. Together, this strongly supports a single origin of SAOs of both Chrysomela and Phratora. Closely related species of Chrysomela and P. vitellinae use iridoids as defensive compounds, which are like salicylaldehyde synthesized by the consecutive action of glucosidase and oxidase. However, we elucidated SAO-like sequences but no SAO proteins in the glandular secretion of iridoid producers. These findings support a different evolutionary history of SAO, related genes and other oxidases involved in chemical defence in the glandular system of salicylaldehyde and iridoid-producing leaf beetle larvae.     

Environmental fluctuations restrict eco-evolutionary dynamics in predator–prey system

Environmental fluctuations, species interactions and rapid evolution are all predicted to affect community structure and their temporal dynamics. Although the effects of the abiotic environment and prey evolution on ecological community dynamics have been studied separately, these factors can also have interactive effects. Here we used bacteria–ciliate microcosm experiments to test for eco-evolutionary dynamics in fluctuating environments. Specifically, we followed population dynamics and a prey defence trait over time when populations were exposed to regular changes of bottom-up or top-down stressors, or combinations of these. We found that the rate of evolution of a defence trait was significantly lower in fluctuating compared with stable environments, and that the defence trait evolved to lower levels when two environmental stressors changed recurrently. The latter suggests that top-down and bottom-up changes can have additive effects constraining evolutionary response within populations. The differences in evolutionary trajectories are explained by fluctuations in population sizes of the prey and the predator, which continuously alter the supply of mutations in the prey and strength of selection through predation. Thus, it may be necessary to adopt an eco-evolutionary perspective on studies concerning the evolution of traits mediating species interactions.     

Behavioral Interactions of Two Solitary,Halictine Bees with Comparisons among Solitary,Communal and Eusocial Species

Laboratory behavioral experiments were conducted with two solitary, halictine bee species, in the genus Lasioglossum, to examine the nature of behavioral interactions between non-nestmate females. The experimental design of this study was identical to previous work on both a communal (Kukuk 1992) and a eusocial Lasioglossum species (Breed et al. 1978), thereby providing data for comparison of female-female interactions in species within a single, very large genus that exhibit different sociality. Both solitary species exhibited low levels of aggressive behavior yet nearly all females were reproductively active, as determined by subsequent dissections. Neither ovarian width nor size was associated with aggression in either species. Interspecific comparisons reveal large differences in cooperation and aggression among the four congeneric species. The communal species exhibits significantly more cooperative and less aggressive behavior than all other species suggesting that communal social behavior in Lasioglossum is not phenetically intermediate between the behavior of solitary and eusocial species.     

Collective defence portfolios of ant hosts shift with social parasite pressure

Host defences become increasingly costly as parasites breach successive lines of defence. Because selection favours hosts that successfully resist parasitism at the lowest possible cost, escalating coevolutionary arms races are likely to drive host defence portfolios towards ever more expensive strategies. We investigated the interplay between host defence portfolios and social parasite pressure by comparing 17 populations of two Temnothorax ant species. When successful, collective aggression not only prevents parasitation but also spares host colonies the cost of searching for and moving to a new nest site. However, once parasites breach the host''s nest defence, host colonies should resort to flight as the more beneficial resistance strategy. We show that under low parasite pressure, host colonies more likely responded to an intruding Protomognathus americanus slavemaker with collective aggression, which prevented the slavemaker from escaping and potentially recruiting nest-mates. However, as parasite pressure increased, ant colonies of both host species became more likely to flee rather than to fight. We conclude that host defence portfolios shift consistently with social parasite pressure, which is in accordance with the degeneration of frontline defences and the evolution of subsequent anti-parasite strategies often invoked in hosts of brood parasites.     

Nonconvergence in the evolution of primate life history and socio-ecology

The goal of this study was to investigate the extent of convergence in four basic life history and socio-ecological traits among the primates of Africa, Asia, South America and Madagascar. The convergence hypothesis predicts that similar abiotic conditions should result in similar adaptations in independent taxa. Because primates offer a unique opportunity among mammals to examine adaptations of independent groups to tropical environments, we collected information on body mass, activity pattern, diet and group size from all genera for quantitative tests of this hypothesis. We revealed a number of qualitative and quantitative differences among the four primate groups, indicating a lack of convergence in these basic aspects of life history and socio-ecology. Our analyses demonstrated that New World primates are on average significantly smaller than primates in other regions and characterized by a lack of species larger than about 10 kg. Madagascar harbours significantly more nocturnal species than the other regions and is home to all but one of the primates with irregular bursts of activity. Asia is the only region with strictly faunivorous primates, but lacks primarily gummivorous ones. The Neotropics are characterized by the absence of primarily folivorous primates. Solitary species are not represented in the New World, whereas solitary and pair-living species make up the majority of Malagasy primates. Lemurs live in significantly smaller groups than other primates, even after controlling for differences in body size. The lack of convergence among the major primate groups is neither primarily due to phylogenetic constraints as a result of founder effects, nor can it be sufficiently explained as a passive consequence of body size differences. However, because the role of adaptive forces, such as interspecific competition, predation or phenology in shaping the observed differences is largely unexplored, we conclude that it is premature to discard the convergence hypothesis without further tests.     

How fast is fast? Eco‐evolutionary dynamics and rates of change in populations and phenotypes

It is increasingly recognized that evolution may occur in ecological time. It is not clear, however, how fast evolution – or phenotypic change more generally – may be in comparison with the associated ecology, or whether systems with fast ecological dynamics generally have relatively fast rates of phenotypic change. We developed a new dataset on standardized rates of change in population size and phenotypic traits for a wide range of species and taxonomic groups. We show that rates of change in phenotypes are generally no more than 2/3, and on average about 1/4, the concurrent rates of change in population size. There was no relationship between rates of population change and rates of phenotypic change across systems. We also found that the variance of both phenotypic and ecological rates increased with the mean across studies following a power law with an exponent of two, while temporal variation in phenotypic rates was lower than in ecological rates. Our results are consistent with the view that ecology and evolution may occur at similar time scales, but clarify that only rarely do populations change as fast in traits as they do in abundance.     

Knower–guesser differentiation in ravens: others' viewpoints matter

Differentiating between individuals with different knowledge states is an important step in child development and has been considered as a hallmark in human evolution. Recently, primates and corvids have been reported to pass knower–guesser tasks, raising the possibility of mental attribution skills in non-human animals. Yet, it has been difficult to distinguish ‘mind-reading’ from behaviour-reading alternatives, specifically the use of behavioural cues and/or the application of associatively learned rules. Here, I show that ravens (Corvus corax) observing an experimenter hiding food are capable of predicting the behaviour of bystanders that had been visible at both, none or just one of two caching events. Manipulating the competitors'' visual field independently of the view of the test-subject resulted in an instant drop in performance, whereas controls for behavioural cues had no such effect. These findings indicate that ravens not only remember whom they have seen at caching but also take into account that the other''s view was blocked. Notably, it does not suffice for the birds to associate specific competitors with specific caches. These results support the idea that certain socio-ecological conditions may select for similar cognitive abilities in distantly related species and that some birds have evolved analogous precursors to a human theory-of-mind.