Behavioural specialization and learning in social networks.

Interactions in social groups can promote behavioural specialization. One way this can happen is when individuals engage in activities with two behavioural options and learn which option to choose. We analyse interactions in groups where individuals learn from playing games with two actions and negatively frequency-dependent payoffs, such as producer-scrounger, caller-satellite, or hawk-dove games. Group members are placed in social networks, characterized by the group size and the number of neighbours to interact with, ranging from just a few neighbours to interactions between all group members. The networks we analyse include ring lattices and the much-studied small-world networks. By implementing two basic reinforcement-learning approaches, action-value learning and actor-critic learning, in different games, we find that individuals often show behavioural specialization. Specialization develops more rapidly when there are few neighbours in a network and when learning rates are high. There can be learned specialization also with many neighbours, but we show that, for action-value learning, behavioural consistency over time is higher with a smaller number of neighbours. We conclude that frequency-dependent competition for resources is a main driver of specialization. We discuss our theoretical results in relation to experimental and field observations of behavioural specialization in social situations.

The evolution of social learning as phenotypic cue integration.

Most analyses of the origins of cultural evolution focus on when and where social learning prevails over individual learning, overlooking the fact that there are other developmental inputs that influence phenotypic fit to the selective environment. This raises the question of how the presence of other cue 'channels' affects the scope for social learning. Here, we present a model that considers the simultaneous evolution of (i) multiple forms of social learning (involving vertical or horizontal learning based on either prestige or conformity biases) within the broader context of other evolving inputs on phenotype determination, including (ii) heritable epigenetic factors, (iii) individual learning, (iv) environmental and cascading maternal effects, (v) conservative bet-hedging, and (vi) genetic cues. In fluctuating environments that are autocorrelated (and hence predictable), we find that social learning from members of the same generation (horizontal social learning) explains the large majority of phenotypic variation, whereas other cues are much less important. Moreover, social learning based on prestige biases typically prevails in positively autocorrelated environments, whereas conformity biases prevail in negatively autocorrelated environments. Only when environments are unpredictable or horizontal social learning is characterized by an intrinsically low information content, other cues such as conservative bet-hedging or vertical prestige biases prevail. This article is part of the theme issue 'Foundations of cultural evolution'.

Underappreciated features of cultural evolution.

Cultural evolution theory has long been inspired by evolutionary biology. Conceptual analogies between biological and cultural evolution have led to the adoption of a range of formal theoretical approaches from population dynamics and genetics. However, this has resulted in a research programme with a strong focus on cultural transmission. Here, we contrast biological with cultural evolution, and highlight aspects of cultural evolution that have not received sufficient attention previously. We outline possible implications for evolutionary dynamics and argue that not taking them into account will limit our understanding of cultural systems. We propose 12 key questions for future research, among which are calls to improve our understanding of the combinatorial properties of cultural innovation, and the role of development and life history in cultural dynamics. Finally, we discuss how this vibrant research field can make progress by embracing its multidisciplinary nature. This article is part of the theme issue 'Foundations of cultural evolution'.

A deepening understanding of animal culture suggests lessons for conservation.

A key goal of conservation is to protect biodiversity by supporting the long-term persistence of viable, natural populations of wild species. Conservation practice has long been guided by genetic, ecological and demographic indicators of risk. Emerging evidence of animal culture across diverse taxa and its role as a driver of evolutionary diversification, population structure and demographic processes may be essential for augmenting these conventional conservation approaches and decision-making. Animal culture was the focus of a ground-breaking resolution under the Convention on the Conservation of Migratory Species of Wild Animals (CMS), an international treaty operating under the UN Environment Programme. Here, we synthesize existing evidence to demonstrate how social learning and animal culture interact with processes important to conservation management. Specifically, we explore how social learning might influence population viability and be an important resource in response to anthropogenic change, and provide examples of how it can result in phenotypically distinct units with different, socially learnt behavioural strategies. While identifying culture and social learning can be challenging, indirect identification and parsimonious inferences may be informative. Finally, we identify relevant methodologies and provide a framework for viewing behavioural data through a cultural lens which might provide new insights for conservation management.

Social information use and collective foraging in a pursuit diving seabird.

Individuals of many species utilise social information whilst making decisions. While many studies have examined social information in making large scale decisions, there is increasing interest in the use of fine scale social cues in groups. By examining the use of these cues and how they alter behaviour, we can gain insights into the adaptive value of group behaviours. We investigated the role of social information in choosing when and where to dive in groups of socially foraging European shags. From this we aimed to determine the importance of social information in the formation of these groups. We extracted individuals' surface trajectories and dive locations from video footage of collective foraging and used computational Bayesian methods to infer how social interactions influence diving. Examination of group spatial structure shows birds form structured aggregations with higher densities of conspecifics directly in front of and behind focal individuals. Analysis of diving behaviour reveals two distinct rates of diving, with birds over twice as likely to dive if a conspecific dived within their visual field in the immediate past. These results suggest that shag group foraging behaviour allows individuals to sense and respond to their environment more effectively by making use of social cues.

Loser-effect duration evolves independently of fighting ability.

Winning or losing contests can impact subsequent competitive behaviour and the duration of these effects can be prolonged. While it is clear effects depend on social and developmental environments, the extent to which they are heritable, and hence evolvable, is less clear and remains untested. Furthermore, theory predicts that winner and loser effects should evolve independently of actual fighting ability, but again tests of this prediction are limited. Here we used artificial selection on replicated beetle populations to show that the duration of loser effects can evolve, with a realized heritability of about 17%. We also find that naive fighting ability does not co-evolve with reductions in the duration of the loser effect. We discuss the implications of these findings and how they corroborate theoretical predictions.

A case for environmental statistics of early-life effects.

There is enduring debate over the question of which early-life effects are adaptive and which ones are not. Mathematical modelling shows that early-life effects can be adaptive in environments that have particular statistical properties, such as reliable cues to current conditions and high autocorrelation of environmental states. However, few empirical studies have measured these properties, leading to an impasse. Progress, therefore, depends on research that quantifies cue reliability and autocorrelation of environmental parameters in real environments. These statistics may be different for social and non-social aspects of the environment. In this paper, we summarize evolutionary models of early-life effects. Then, we discuss empirical data on environmental statistics from a range of disciplines. We highlight cases where data on environmental statistics have been used to test competing explanations of early-life effects. We conclude by providing guidelines for new data collection and reflections on future directions. This article is part of the theme issue 'Developing differences: early-life effects and evolutionary medicine'.

Ecological Genetic Conflict: Genetic Architecture Can Shift the Balance between Local Adaptation and Plasticity.

Genetic polymorphism can contribute to local adaptation in heterogeneous habitats, for instance, as a single locus with alleles adapted to different habitats. Phenotypic plasticity can also contribute to trait variation across habitats, through developmental responses to habitat-specific cues. We show that the genetic architecture of genetically polymorphic and plasticity loci may influence the balance between local adaptation and phenotypic plasticity. These effects of genetic architecture are instances of ecological genetic conflict. A reduced effective migration rate for genes tightly linked to a genetic polymorphism provides an explanation for the effects, and they can occur both for a single trait and for a syndrome of coadapted traits. Using individual-based simulations and numerical analysis, we investigate how among-habitat genetic polymorphism and phenotypic plasticity depend on genetic architecture. We also study the evolution of genetic architecture itself, in the form of rates of recombination between genetically polymorphic loci and plasticity loci. Our main result is that for plasticity genes that are unlinked to loci with between-habitat genetic polymorphism, the slope of a reaction norm is steeper in comparison with the slope favored by plasticity genes that are tightly linked to genes for local adaptation.

Effects of ambient noise on zebra finch vigilance and foraging efficiency.

Ambient noise can affect the availability of acoustic information to animals, altering both foraging and vigilance behaviour. Using captive zebra finches Taeniopygia guttata, we examined the effect of ambient broadband noise on foraging decisions. Birds were given a choice between foraging in a quiet area where conspecific calls could be heard or a noisy area where these calls would be masked. Birds foraging in noisy areas spent a significantly more time vigilant than those in quiet areas, resulting in less efficient foraging. Despite this there was no significant difference in the amount of time spent in the two noise regimes. However there did appear a preference for initially choosing quiet patches during individuals' second trial. These results emphasise how masking noise can influence the foraging and anti-predation behaviour of animals, which is particularly relevant as anthropogenic noise becomes increasingly prevalent in the natural world.

Towards a behavioural ecology of obesity.

Addressing the obesity epidemic depends on a holistic understanding of the reasons that people become and maintain excessive fat. Theories about the causes of obesity usually focus proximately or evoke evolutionary mismatches, with minimal clinical value. There is potential for substantial progress by adapting strategic body mass regulation models from evolutionary ecology to human obesity by assessing the role of information.

Individuals that are consistent in risk-taking benefit during collective foraging.

It is well established that living in groups helps animals avoid predation and locate resources, but maintaining a group requires collective coordination, which can be difficult when individuals differ from one another. Personality variation (consistent behavioural differences within a population) is already known to be important in group interactions. Growing evidence suggests that individuals also differ in their consistency, i.e. differing in how variable they are over time, and theoretical models predict that this consistency can be beneficial in social contexts. We used three-spined sticklebacks (Gasterosteus aculeatus) to test whether the consistency in, as well as average levels of, risk taking behaviour (i.e. boldness) when individuals were tested alone affects social interactions when fish were retested in groups of 2 and 4. Behavioural consistency, independently of average levels of risk-taking, can be advantageous: more consistent individuals showed higher rates of initiating group movements as leaders, more behavioural coordination by joining others as followers, and greater food consumption. Our results have implications for both group decision making, as groups composed of consistent individuals are more cohesive, and personality traits, as social interactions can have functional consequences for consistency in behaviour and hence the evolution of personality variation.

Detection vs. selection: integration of genetic, epigenetic and environmental cues in fluctuating environments.

There are many inputs during development that influence an organism's fit to current or upcoming environments. These include genetic effects, transgenerational epigenetic influences, environmental cues and developmental noise, which are rarely investigated in the same formal framework. We study an analytically tractable evolutionary model, in which cues are integrated to determine mature phenotypes in fluctuating environments. Environmental cues received during development and by the mother as an adult act as detection-based (individually observed) cues. The mother's phenotype and a quantitative genetic effect act as selection-based cues (they correlate with environmental states after selection). We specify when such cues are complementary and tend to be used together, and when using the most informative cue will predominate. Thus, we extend recent analyses of the evolutionary implications of subsets of these effects by providing a general diagnosis of the conditions under which detection and selection-based influences on development are likely to evolve and coexist.

Genes as Cues of Relatedness and Social Evolution in Heterogeneous Environments.

There are many situations where relatives interact while at the same time there is genetic polymorphism in traits influencing survival and reproduction. Examples include cheater-cooperator polymorphism and polymorphic microbial pathogens. Environmental heterogeneity, favoring different traits in nearby habitats, with dispersal between them, is one general reason to expect polymorphism. Currently, there is no formal framework of social evolution that encompasses genetic polymorphism. We develop such a framework, thus integrating theories of social evolution into the evolutionary ecology of heterogeneous environments. We allow for adaptively maintained genetic polymorphism by applying the concept of genetic cues. We analyze a model of social evolution in a two-habitat situation with limited dispersal between habitats, in which the average relatedness at the time of helping and other benefits of helping can differ between habitats. An important result from the analysis is that alleles at a polymorphic locus play the role of genetic cues, in the sense that the presence of a cue allele contains statistical information for an organism about its current environment, including information about relatedness. We show that epistatic modifiers of the cue polymorphism can evolve to make optimal use of the information in the genetic cue, in analogy with a Bayesian decision maker. Another important result is that the genetic linkage between a cue locus and modifier loci influences the evolutionary interest of modifiers, with tighter linkage leading to greater divergence between social traits induced by different cue alleles, and this can be understood in terms of genetic conflict.

The Evolution of Individual and Cultural Variation in Social Learning.

It is often assumed in experiments and models that social learning abilities - how often individuals copy others, plus who and how they copy - are species-typical. Yet there is accruing evidence for systematic individual variation in social learning within species. Here we review evidence for this individual variation, placing it within a continuum of increasing phenotypic plasticity, from genetically polymorphic personality traits, to developmental plasticity via cues such as maternal stress, to the individual learning of social learning, and finally the social learning of social learning. The latter, possibly restricted to humans, can generate stable between-group cultural variation in social learning. More research is needed to understand the extent, causes, and consequences of this individual and cultural variation.

Information use in colonial living.

Despite the fact that many animals live in groups, there is still no clear consensus about the ecological or evolutionary mechanisms underlying colonial living. Recently, research has suggested that colonies may be important as sources of social information. The ready availability of information from conspecifics allows animals to make better decisions about avoiding predators, reducing brood parasitism, migratory phenology, mate choice, habitat choice and foraging. These choices can play a large part in the development and maintenance of colonies. Here we review the types of information provided by colonial animals and examine the different ways in which decision-making in colonies can be enhanced by social information. We discuss what roles information might take in the evolution, formation and maintenance of colonies. In the process, we illustrate that information use permeates all aspects of colonial living.

Genes as cues: phenotypic integration of genetic and epigenetic information from a Darwinian perspective.

The development of multicellular organisms involves a delicate interplay between genetic and environmental influences. It is often useful to think of developmental systems as integrating available sources of information about current conditions to produce organisms. Genes and inherited physiology provide cues, as does the state of the environment during development. The integration systems themselves are under genetic control and subject to Darwinian selection, so we expect them to evolve to produce organisms that fit well with current ecological (including social) conditions. We argue for the scientific value of this explicitly informational perspective by providing detailed examples of how it can elucidate taxonomically diverse phenomena. We also present a general framework for linking genetic and phenotypic variation from an informational perspective. This application of Darwinian logic at the organismal level can elucidate genetic influences on phenotypic variation in novel and counterintuitive ways.

Life-history trade-offs mediate 'personality' variation in two colour morphs of the pea aphid, Acyrthosiphon pisum.

Life-history trade-offs are considered a major driving force in the emergence of consistent behavioural differences (personality variation); but empirical tests are scarce. We investigated links between a personality trait (escape response), life-history and state variables (growth rate, size and age at first reproduction, age-dependent reproductive rates, lifetime reproductive success, life span) in red and green colour morphs of clonal pea aphids, Acyrthosiphon pisum. Escape response (dropping/non-dropping off a plant upon a predatory attack) was measured repeatedly to classify individuals as consistent droppers, consistent nondroppers or inconsistents. Red morphs experienced stronger trade-offs between early reproduction and life span than green morphs; and red consistent (non)droppers had highest lifetime reproductive success. Red droppers followed a risk-averse life-history strategy (high late reproduction), red nondroppers a risk-prone strategy (high early reproduction), while reproductive rates were equivalent for all green behavioural types and red inconsistents. This suggests that red morphs suffer the highest costs of dropping (they are most conspicuous to predators), which 'equivalates' fitness payoffs to both risk-takers (red non-droppers) and risk-averse red droppers. The strong trade-off also means that committing to a particular lifestyle (being consistent) maximises fitness. Our study suggests that life-history trade-offs likely mediate personality variation but effects might depend on interactions with other organismal characteristics (here: colour morph).