Philosophical Transactions of the Royal Society B: Biological Sciences

Cooperation is foundational to complex sociality, yet presents profound evolutionary dilemmas - costs and benefits are rarely distributed evenly and the decision to collaborate or defect can involve a complex contextual calculus. These challenges are compounded when cooperation scales from pairs to groups. Group-level cooperation is fundamental to many species success, but how is it sustained and regulated in nature? One promising route to addressing this question is to examine how individuals reorganise their affiliative interactions in anticipation of group-level cooperation. We examine such pre-cooperative reorganisation using long-term data (2013-2018) from three neighbouring groups of wild chimpanzees at the Tai National Park, Cote dIvoire, who routinely cooperate as a collective to defend their territory against other groups. We found that chimpanzees adjusted the distribution of their social contacts in anticipation of risky and proactive territorial defence by forming more broadly connected, yet more diffuse, affiliative networks. Specifically, adult chimpanzees groomed and played with more group members on days of proactive territorial defence, and this pattern was temporally-sensitive, with increased affiliation occurring before, rather than after, the cooperative act. Chimpanzees accessed a broader range of partners through increased interaction efficiency by switching between more partners with shorter interactions per partner. This pattern suggests a shared evolutionary basis of dynamic social readjustment in preparation for group-level social dilemmas in hominids, potentially providing the foundation for the formalized systems of affiliation found in human societies.

We compare the trajectory of deaths (both in hospitals and care homes) on a daily basis in Sweden and England and Wales (which constitute 90 per cent of the UK population) from 11 March to 7 August 2020, the latest date at which the relevant data is available for England and Wales. Deaths in both Sweden and England and Wales peaked on 8 April. The build up to the peak was very similar in both. Given the time lag between infection and death, the lockdown would have had little effect on the peak number of deaths. By the first week of August, the deaths are very similar in both. However, from early May the decline in England and Wales has been much sharper. We estimate that to 7 August, lockdown saved 17,700 lives in England and Wales, or just under 20,000 extrapolating to a UK level.

A populations social structure, often represented as a social network, shapes fundamental biological processes including the spread of disease, information, and behaviour. The Friendship Paradox is a network phenomenon whereby the average individual has fewer friends than their friends do. This effect can be quantified as relationship disparity (the difference between an individuals connectedness and those they are connected to) which captures the local social environment. Previous work has shown that such relationship disparity can be exploited in effective outbreak monitoring, targeted health interventions and optimized contact tracing. Yet, how its magnitude varies across real-world social networks remains poorly understood. Here, we analyse relationship disparity across 391 empirical animal social networks to test how intrinsic network properties and biological attributes predict its extent. We find that smaller and sparser networks exhibit stronger relationship disparity, and that mammalian and avian social systems generally showed stronger relationship disparity than reptilian systems. After controlling for variation in individual sociability, mammalian and reptilian social networks displayed weaker relationship disparity than expected based on network structure alone. Together, these findings demonstrate that both network structure and biological attributes shape relationship disparity in natural social systems, providing a foundation for predicting how higher-order network architecture influences social processes such as contagion. Significance StatementIn natural populations, social connections are unevenly distributed, often resulting in a small subset of individuals that are highly connected while many are relatively peripheral. The Friendship Paradox is a measure of relationship disparity between individuals and their local social environment. Understanding how features of the social network and biological system are associated with relationship disparity can contribute to understanding what shapes social behaviour. Relationship disparity may not just be an emergent network property but could reflect a higher level of social structuring, and therefore shape processes that depend on social contacts. Our findings demonstrate the value of comparative network analysis for generating insights into fundamental principles structuring real-world societies.

It has previously been thought that the social brain hypothesis applies in its full quantitative form only to primates. Using more appropriate brain indices and less error-prone statistical methods, we here show that it does in fact apply to both Insectivorans and Carnivorans, as well as to elephants and orcas. While Insectivorans form a grade on their own, reflecting a simple transition from small-brained solitary social systems to slightly larger-brained pairbonded monogamy, the Carnivorans map directly onto the primate socio-cognitive grades, dividing between loose sociality and more bonded sociality paralleling the pattern observed in monkeys. In addition, the subgroupings of species with multilevel social systems (including hyaenids elephants and orcas) map across the grades in the same way as do primates with similar societies. This suggests that common principles and trajectories underlie social evolution in mammals.

Recent evidence of extensive call sequence use in non-human primates has led to the theory that syntax evolved to mitigate the constraints of their genetically fixed repertoires, before vocal production learning later emerged in humans. However, evidence of similarly extensive sequence repertoires in an open-ended vocal production learner--the Western Australian magpie (Gymnorhina tibicen dorsalis)--offers a unique opportunity to explore potential alternative pathways to syntactic communication. Our previous work revealed fledgling magpies learn group-specific repertoires of structured call sequences from their social contacts, with more sociable individuals acquiring larger repertoires earlier in development. Notably however, the individual vocal segments that combine to form their calls and call sequences were shared across groups and emerged as early as the first week post-fledging--suggesting the underlying vocal elements may not be learned. Here we utilised acoustic neighbourhood-based dimensionality reduction to compare clustering patterns of vocal segments across magpie fledgling developmental stages, and between fledglings and adults. We found no evidence of acoustic development over time, and no significant distinction between fledgling and adult productions of the same vocal segments. The same coarticulatory effects--where a vocal element is produced differently when combined with another--and geographic variation established previously in adults were supported in fledglings too. These findings support that the vocal building blocks underpinning magpie call sequences are innate, suggesting usage learning better explains how fledglings learn to combine calls. In a species capable of open-ended production learning, this suggests learning to combine existing signals may be more adaptive than productively learning new ones. Rather than evolving solely to compensate for genetically fixed repertoires, syntax may have evolved as a flexible, convergent solution to the various challenges of expanding communicative capacity--whether due to genetic constraints, cognitive limitations or the cost of establishing new meaning in novel signals.

Previous work has shown that environment affects SARS-CoV-2 transmission, but it is unclear whether emerging strains show similar responses. Here we show that, like other SARS-CoV-2 strains, lineage B.1.1.7 spread with greater transmission in colder and more densely populated parts of England. However, we also find evidence of B.1.1.7 having a transmission advantage at warmer temperatures compared to other strains. This implies that spring and summer conditions are unlikely to slow B.1.1.7s invasion in Europe and across the Northern hemisphere - an important consideration for public health interventions.

Tactical emotion communication has long been considered uniquely-human. As a species, we readily exaggerate, inhibit and modify emotional expressions according to social context and audience. Notably, emitting emotional displays, such as those pertaining to distress states, can evoke empathic responses in others such as the offering of consolation to victims after a fight. Animal emotion expressions, by contrast, are traditionally viewed as uncontrollable arousal responses. Our study challenges this view by assessing the level of control in the emotional signalling of sanctuary-living bonobo victims following aggressive attacks (N = 27 victims, N = 144 attacks) and its and its corresponding effect on receivers. Results show that the production of paedomorphic signals by adult bonobo victims increased chances of receiving consolation from bystanders and reduced risk of future aggression from former opponents, highlighting a strategic function. Victim signalling also increased with audience size, yet strategies differed by age: immature bonobos were more likely to cease signalling in proximity of close-social partners, whereas adults were more likely to cease signalling after having been consoled. These data suggest that bonobo emotion communication has a developmental trajectory and that tactical emotion signalling is a Pan-human capacity, preceding the split of Homo.

The capacity to inhibit prepotent actions (inhibitory self-control) plays an important role in many aspects of the behaviour of birds and mammals. Although a number of studies have used it as an index of foraging skills, inhibition is also crucial for maintaining the temporal and spatial coherence of bonded social groups. Using three different sets of comparative data, we show that, across primate species, the capacity for self-control correlates better with the demands of social contexts than with the demands of foraging contexts, whereas a more generalised capacity for causal reasoning correlates better with foraging contexts. In addition, we confirm the Passingham-Wise Conjecture that the capacity for self-control is unique to anthropoid primates. These results suggest that the capacity for self-control most likely evolved because it was crucial for the evolution of bonded social groups. Significance StatementThe capacity for self-control has commonly been viewed as an index of foraging skills. In fact, it plays a much more important role in the social domain by enabling groups of animals to maintain social cohesion as they travel through time and space. In this respect, it is particularly important for species that live in stable bonded social groups (congregations). We show that, in this respect, it is uniquely characteristic of the anthropoid primates, in contrast to other kinds of reasoning tasks such as causal reasoning on which primates often perform no better than other birds and mammals.

Close contacts between individuals provide opportunities for the transmission of diseases, including COVID-19. Individuals take part in many different types of interactions, including those with classmates, co-workers, and household members; the conglomeration of all of these interactions produces a complex social contact network interconnecting individuals across the population. Thus, while an individual might decide their own risk tolerance in response to a threat of infection, the consequences of such decisions are rarely so confined, propagating far beyond any one person. We asses the effect of different population-level risk-tolerance regimes, population structure in the form of age and household-size distributions, and different types of interactions on epidemic spread in plausible human contact networks to gain insight into how contact network structure affects pathogen spread through a population. In particular, we find that changes in behaviour of vulnerable individuals in isolation is insufficient to reduce those individuals infection risk, that population structure can have varied and counter-acting effects on epidemic outcomes, and that, in general, interactions among co-workers have a greater contribution to disease spread than do interactions among children at school. Taken together, these results promote a nuanced understanding of disease spread on contact networks, with implications for public health strategies.

Although population-wide lockdowns have been successful in slowing the COVID-19 epidemic, there is a consensus among disease modellers that keeping the load on critical care services within manageable limits will require an adaptive social distancing strategy, alternating cycles of relaxation and reimposition until a vaccine is available. An alternative strategy that has been tentatively proposed is to shield the elderly and others at high risk of severe disease, while allowing immunity to build up in those at low risk until the entire population is protected. We examine the performance required from a classifier that uses information from medical records to assign risk status for a such a stratify-and-shield policy to be effective in limiting mortality when social distancing is relaxed. We show that under plausible assumptions about the level of immunity required for population-level immunity, the proportion shielded is constrained to be no more than 15% of the population. Under varying assumptions about the infection fatality ratio (from 0.1% to 0.4%) and the performance of the classifier (3 to 4.5 bits of information for discrimination), we calculate the expected number of deaths in the unshielded group. We show that with likely values of the performance of a classifier that uses information from age, sex and medical records, at least 80% of those who would die if unshielded would be allocated to the high-risk shielded group comprising 15% of the population. Although the proportion of deaths that would be prevented by effective shielding does not vary much with the infection fatality ratio, the absolute number of deaths in the unshielded varies from less than 10,000 if the infection fatality rate is 0.1% to more than 50,000 if the infection fatality rate is as high as 0.4%. For projecting the effect of an optimally applied stratify-and-shield policy, studies now under way should help to resolve key uncertainties: the extent to which infection confers immunity, the prevalence of immunity, the infection fatality ratio, and the performance of a classifier constructed using information from medical records. It is time to give serious consideration to a stratify-and-shield policy that could bring the COVID-19 epidemic to an end in a matter of months while restoring economic activity, avoiding overload of critical care services and limiting mortality.

Our biosphere exhibits remarkable diversity yet is constrained by universal organizational principles, including molecular homochirality. Advances in synthetic biology have raised the possibility of engineering alternative life forms based on mirror-image biomolecules, prompting both technological interest and biosecurity concerns. While current discussions of mirror life largely emphasize molecular feasibility and cellular function, its potential establishment in natural environments remains poorly understood. Here, we develop a theoretical framework to assess the invasion potential of mirror organisms within existing ecosystems. Using population-level models that incorporate resource competition, metabolic constraints, and ecological network interactions, we show that mirror life faces severe limitations arising from both nutrient incompatibility and competitive exclusion by established biota. In particular, the reliance on rare or achiral substrates and the asymmetry of interactions with natural organisms constrain growth and persistence across a broad range of ecological conditions. These results indicate that, beyond engineering challenges, the structure and dynamics of the biosphere itself act as a strong barrier to the spread of mirror life. We conclude that the widespread establishment of mirror organisms in the extant biosphere is highly unlikely, highlighting the importance of ecological constraints in evaluating the risks and feasibility of synthetic life.

Aims: Antimicrobial peptide (AMP) combinations have been proposed to delay resistance evolution, but it remains unclear what properties of a peptide pair determine whether a combination reduces resistance evolution relative to its component AMPs used alone. One suggested factor is mode of action, yet this has rarely been tested experimentally. In the current study we have asked whether mode of action or physicochemical similarity between peptides better predicts which combinations delay resistance. Methods: We evolved Staphylococcus aureus with six AMPs with reported membrane-targeting and intracellular-targeting activity, individually and in all 15 pairwise combinations. We quantified resistance evolution, cross-resistance and fitness costs across the full AMP panel, and performed whole-genome sequencing on 126 evolved lineages. Results: Resistance varied across AMPs and correlated with peptide chain length, not mode of action. Cross-resistance was associated with physicochemical similarity, and similar peptides selected for overlapping mutations. Most combinations reduced resistance relative to single-AMP treatment, but those whose components shared cross-resistance were less effective, channeling evolution into convergent trajectories that resolve both selective pressures at once. Notably, mode of action did not predict combination outcome. Conclusions: Cross-resistance, not mode of action, is a key factor in determining AMP combination efficacy. Physicochemical distance between peptides may serve as a practical predictor for cross-resistance, enabling selection of AMP combinations that are more likely to constrain resistance evolution.

Group living and social interactions among animals provide key benefits, such as the exchange of beneficial social information and novel behaviours, but also pose the risk of spreading costly infectious diseases, presenting a social trade-off. While both information and infections spread across social networks, they typically have distinct mechanisms of transmission. Here, we model social information and behaviour spread as a complex contagion governed by a conformist learning rule, while pathogen transmission follows a simple contagion mechanism. Building on theoretical foundations, our study applies computational models to examine how subgroup structure (modularity) influences the spread of these contagions across diverse animal social structures sourced from the Animal Social Network Repository (ASNR). Our findings reveal that high modularity and subgroup structure slow simple contagion spread, whereas complex contagions are less impeded by this fragmentation. Consequently, our results suggest that social networks divided into small groups or subgroups can help balance the competing pressures of acquiring social information and avoiding infectious disease in real-world networks.

Multilevel social systems in birds and mammals have attracted considerable interest, not least because they share some similarities with the natural structural organisation of human societies. I use a fractal analysis of a taxonomically wide range of species reported to have multilevel social systems to show that these in fact involve two very different phenomena: those that are fractally modular and those that are casually modular. The first have a strictly fractal structure identical to that found in human societies; the second lack formal structural coherence and are closer in form to casual herds. The former are associated with larger neocortices than the latter, suggesting that they may be cognitively more demanding. Understanding the evolution of multilevel systems and the cognition that underpins them obliges us to adopt a more nuanced approach to social evolution.

Oscine songbirds have been an important study system for social learning, particularly because their learned songs provide an analog for human languages and music. Here we propose a different analogy; from an evolutionary perspective, could a birds song be more like an arrowhead than an aria? We modify a model of human tool evolution to accommodate cultural evolution of birdsong: each song learner chooses the most skilled available tutor to emulate, and each is more likely to produce an inferior copy than a superior one. Similarly to human tool evolution, we show that larger populations foster improvements in song over time, even when learners restrict their pool of tutors to a subset of individuals. We also demonstrate that songs could be simplified instead of lost after population bottlenecks if lower-quality traits are easier to imitate than higher-quality ones. We show that these processes could plausibly generate empirically observed patterns of song evolution, and we make predictions about the types of song elements most likely to be lost when populations shrink. More broadly, we aim to connect the modeling approaches used in human and non-human systems, moving toward a cohesive theoretical framework that accounts for both cognitive and demographic processes.

BackgroundDuring the early phase of the Covid-19 pandemic in England, people with pre-existing conditions that put them at severe clinical risk if infected were advised to drastically reduce face-to-face contacts in a policy known as "shielding". The impact of this policy in preventing COVID-19 hospitalisations and deaths has not been evaluated at the national level using transmission-dynamic modelling. MethodsWith the approval of NHS England, we present a retrospective cohort evaluation of the shielding policy, drawing data from electronic health records (EHRs) for 24 million patients in England accessed through the OpenSAFELY platform. The study is from 1 January to 1 December 2020, prior to vaccination and new SARS-CoV-2 variants. We used a dynamic transmission model of SARS-CoV-2 transmission, infection, and hospitalisation, stratified by age and shielding status for the general population (excluding care homes). We estimated transmission rates in the shielding and non-shielding groups using data from the CoMix social contact survey, and fitted the model to hospitalisations and deaths in and outside hospital. FindingsWe found that the risk of hospitalisation was higher for shielding people in all age groups and increased with age. The hospital fatality ratio was similar between shielding and non-shielding people from January to June 2020 and greater in shielding people from July 2020 onward. By comparing the observed epidemic to a counterfactual scenario without shielding, we projected that between 7800 and 10,600 hospitalisations and 2300 to 3500 deaths due to COVID-19 were directly averted by the policy, corresponding to reductions of 25% (24, 28%) and 23% (21, 25%), respectively, in the shielding population in England up to 1 December 2020. Including also the indirect effect in the non-shielding population, we projected between 14,700, and 21,800 hospitalisations and 3700 and 5500 deaths due to COVID-19 were averted by the policy in the total population, each corresponding to reductions of 13% (11, 16%). InterpretationBased on the data and assumptions in this study, the shielding policy reduced pressure on the NHS and severe illness and mortality in clinically-extremely vulnerable shielding patients in England up to 1 December 2020, and, through indirectly-reduced exposure, also in the non-shielding population. Similar policies for other infections could have a comparable public health impact in reducing both mortality and pressure on public health services. FundingMedical Research Foundation, Medical Research Council, National Institute for Health and Care Research, NHS England, The Wellcome Trust.

Although division of labor as a means to increase productivity is a common feature in animal social groups, most previous studies have focused almost exclusively on eusocial insects with extreme task partitioning. Empirical evidence of division of labor in vertebrates is scarce, largely because we lack a theoretical framework to explore the conditions under which division of labor is likely to evolve in cooperatively breeding systems where helpers remain capable of breeding throughout their lifetime. By explicitly considering alternative helping tasks with varying fitness costs, we model how individual decisions on task specialization may influence the emergence of division of labor under both direct and indirect fitness benefits. Surprisingly, we find that direct survival benefits of living in larger groups are the primary force driving the evolution of cooperation to enhance group productivity, and that indirect fitness benefits derived from related group members are only a non-essential facilitator of more stable forms of division of labor in cooperative breeders. In addition, we find that division of labor in vertebrates is favored by harsh environments. Ultimately, our model not only makes key predictions that are consistent with existing empirical data, but also proposes novel avenues for new empirical work in vertebrate and invertebrate systems alike.

Drumming--rhythmic, percussive sound production using body parts or external objects--is rare among non-human animals, with confirmed tool-assisted cases previously limited to primates and Palm Cockatoos. Here, we report the first documented instance of spontaneous, tool-assisted drumming in a Galah (Eolophus roseicapilla). A captive, male Galah produced rhythmic tapping by striking a coconut shell against a metal bowl. Across 14 recorded sessions, the bird displayed consistent temporal structure characterised by two stable tapping rates (approximately 0.8 s and 0.2 s inter-onset intervals) arranged into recurring phrases. This pattern indicates a simple hierarchical rhythmic organisation with a 4:1 ratio between metrical levels. The birds behaviour emerged without training, apparent reinforcement, or known exposure to conspecific or human drumming models, suggesting an intrinsic capacity for rhythmic tool use. Although the function of the behaviour remains unclear--play, nutrient extraction, or communicative signalling--these observations extend known rhythmic and tool-using abilities within cockatoos and raise new evolutionary questions. Our findings highlight the potential for rhythmically structured, instrumental behaviour to arise in a broader range of avian taxa than previously recognised, motivating further comparative and experimental work on the cognitive and biomechanical foundations of drumming in parrots.

Global populations are ageing at an unprecedented rate. For many diseases, age is a strong indicator of susceptibility, morbidity, or mortality. Principles of evolutionary biology can be leveraged to understand how pathogens may optimally exploit new populations, and the impact of this on the global burden of infectious-disease-induced mortality. We parameterised an age-specific R0 model with 2017 epidemiological data on Measles, Tuberculosis, Meningitis, and Ebola, and age-specific demographic estimates for 2017 and 2050, for the seven Global Burden of Disease super-regions. We explored the theoretical trade-offs between pathogen virulence & transmission, and virulence & host recovery, parameterising trade-off parameters using Latin Hypercube Sampling. Population ageing between 2017-2050 saw an increase in virulence induced mortality in four settings: 1) Ebola in sub-Saharan Africa, 2) Measles in central/eastern Europe & central Asia region, 3) Measles in North Africa & the Middle East and 4) Tuberculosis in the central/eastern Europe & central Asia region. The decrease in infection duration due to an increase of elderly people drives pathogen virulence down for diseases in the remaining settings. Understanding the mechanisms that shape pathogen dynamics and leveraging this to predict future challenges is key to endemic disease management in a rapidly changing world. Author SummaryKey aspects of disease transmission including susceptibility to infection, the severity of infection, and the probability of dying from that infection, are affected by host age. Global populations are rapidly ageing, so that the mean age of most populations is generally higher than it used to be and is set to continue on this trajectory. This suggests that the dynamics of infectious diseases are also likely to change, although infectious disease dynamics tend to be non-linear as these key parameters interact. We have developed a dynamic modelling framework to explore how changes in population age structure might impact the optimal level of pathogen virulence in a population. We have chosen four infectious diseases as case studies, that differentially impact certain age classes to illustrate these dynamics. We have parameterised this framework with open access data for each of the seven Global Burden of Disease super-regions and show that population ageing can increase virulence for several diseases in differing global regions, whilst increased background rates of mortality can drive virulence down in others.

Collective behavior in animal societies can buffer individual costs and confer resilience to environmental challenges. However, the mechanisms by which groups sustain function when members are compromised remain poorly understood. In the presented study, we investigate how social context shapes collective fanning, a thermoregulatory behavior critical for colony function, in Western honeybees (Apis mellifera). Using oxytetracycline (OTC), a known physiologically disruptive antibiotic to honeybees, to selectively impair certain group members, we tested our hypothesis that the presence of untreated bees would rescue the fanning response in mixed-composition groups. We show that groups containing untreated individuals fan at levels comparable to fully untreated groups, despite the presence of OTC-impaired bees. This preservation of collective thermoregulatory function was correlated with both treated and untreated individuals in mixed groups shifting their interaction dynamics and social network positions. These findings reveal a decentralized mechanism of collective resilience, whereby behavioral compensation by individuals sustains group-level thermoregulation under partial disruption. Our results provide a framework for understanding how social insect colonies maintain function in the face of individual-level perturbations, with broader implications for predicting the limits of collective resilience in animal societies experiencing increasing environmental pressures.