Proceedings of the Royal Society B: Biological Sciences

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.

Bright red coloration is a signal of male competitive ability in animal species across a range of taxa, including non-human primates. Does the effect of red on competition extend to humans? A landmark study in evolutionary psychology established such an effect through analysis of data for four combat sports at the 2004 Athens Olympics [1]. Here we show that the results do not replicate in an equivalent, independent dataset for the 2008 Beijing Olympics, and that there is substantial variation in the fraction of wins by red across sports in both years. We uncover a number of shortcomings with the research design, analysis, and interpretation underlying the original results. For example, the variation observed in the data may reflect bias towards wins by one color over the other, linked to specific features of the tournament structure for the sports analysed. Reanalysis of the data to address these shortcomings indicates that there is no evidence for an effect of red on the outcomes of Olympic combat sports. Our results refute past claims based on analysis of this system, challenging the related notion that any effect of red in human competition is an evolved response shaped by sexual selection.

Understanding ectotherm responses to environmental change is central to coping with many of humanitys current and future challenges in public health, biodiversity conservation, and food security. Complex relationships between abiotic and biotic factors can influence ectotherm abundance and distribution patterns by introducing stage-specific variation in fitness trait responses. Variation in temperature, rainfall, competition, and habitat have all been considered in previous attempts to understand how environmental factors can interact and vary in their relative influence on species maximal population growth rates, rm. However, the combined effects of temperature and humidity on this fundamental metric are poorly understood. We show that variation in relative humidity can influence juvenile trait responses and rms temperature dependence in Anopheles stephensi, an important malaria vector. Our climate suitability maps show that the interactive effects of temperature x humidity on juvenile traits have important implications for predicting how environmental change will influence arthropod-mediated systems.

While humans cooperate with unrelated individuals to an extent that far outstrips any other species, we also display extreme variation in decisions about whether to cooperate or not. A diversity of cognitive, affective, social, and physiological mechanisms interact to shape these decisions. For example, group membership, shared intentionality talk (i.e. talk about shared goals), and natural initial oxytocin levels affect cooperation in adults in an optimal foraging paradigm that is loosely modelled on the iterated prisoners dilemma. In this egg hunt, shared intentionality talk was key to achieve cooperation, and it occurred more between participants who shared the same group membership and had higher initial oxytocin levels. Such complex interactions raise the question of the age at which humans develop the necessary mechanisms to cooperate effectively in the egg hunt game. Here, we tested children in secondary school aged between 10 and 14 years. We found that, as for adults, shared intentionality talk was crucial for successful cooperation. Furthermore, initial oxytocin levels affected cooperation through shared intentionality talk. In contrast, group membership did not affect behaviour. Finally, pre- and post-experiment oxytocin levels showed various interactions with group membership and gender. Thus, childrens performance was relatively similar to adults while showing some differences with respect to underlying mechanisms. Our study is a rare contribution to further our understanding of the role of oxytocin in early adolescent social behaviour.

In most arthropods, adult females are larger than males, and male competition is a race to quickly locate and mate with scattered females (scramble competition polygyny). In this context, smaller males may be favored due to more efficient locomotion leading to higher mobility during mate searching while larger males may benefit from increased speed and higher survivorship. Understanding how body size affects different aspects of the locomotor performance of males is therefore essential to shed light on the evolution of this widespread mating system. Using a combination of empirical measures of flight performance and substrate adhesion, and modelling of body aerodynamics, we show that large body size impairs both flight and landing (attachment) performance in male leaf insects (Phyllium philippinicum), a species where relatively small and skinny males fly through the canopy in search of large sedentary females. Smaller males were more agile in the air, ascended more rapidly during flight, and had a lower risk of detaching from the substrates on which they walk and land. Our models revealed variation in body shape affected body lift and drag, but tradeoffs with weight meant that effects were negligible, suggesting that flight costs do not explain the evolution of strong sexual dimorphism in body shape in this species. Graphical abstract O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=177 SRC="FIGDIR/small/451325v1_ufig1.gif" ALT="Figure 1"> View larger version (54K): org.highwire.dtl.DTLVardef@193d0adorg.highwire.dtl.DTLVardef@1693bccorg.highwire.dtl.DTLVardef@1d50b53org.highwire.dtl.DTLVardef@1da8572_HPS_FORMAT_FIGEXP M_FIG C_FIG

Socially-controlled sex changing fishes provide powerful model systems for investigating sexual development and phenotypic plasticity in both behavior and physiology. The remarkable sexual transformation these fishes undertake is strongly influenced by their position in dominance hierarchies. However, the behavioral mechanisms underlying hierarchical formation remain understudied, particularly among female groups. Here, we investigated the role of winner-loser effects among females in establishing social dominance in a female-to-male sex changing fish. Individuals with prior losing experiences were more likely to lose subsequent size-matched fights, demonstrating clear loser effects, while there was no evidence for winner effects. Initial mirror aggression and some prior fighting behaviors, particularly submission, significantly and positively correlated with aggression in size-matched fights and subsequent mirror aggression; however, contest outcomes were not altered by these factors. Additionally, mirror aggression increased significantly only in subjects that drew size-matched fights. These findings demonstrate complex fighting dynamics in female-female competition and confirm the presence of loser effects in a sequential hermaphroditic species. These effects may represent evolutionarily advantageous mechanisms underlying sex change, thereby offering further context for examining how social rank advantages drive sexual transition.

Vector-borne pathogens cause 17% of all human infectious diseases, and rising global temperatures are shifting the distribution and abundance of mosquito vectors. Because mosquitoes are ectotherms, temperature strongly governs biological rates and physiology; however, mosquitoes also experience other environmental factors that may interact with temperature to shape the thermal performance of traits driving population dynamics. Here, we use a factorial life-table experiment spanning five relative humidities (30-90%) and seven temperatures (16-38{whitebullet}C) to show that humidity modifies the thermal performance of key fitness traits in adult Anopheles stephensi, an invasive urban malaria vector. When integrated into a demographic model, humidity markedly reshapes projections of population fitness relative to temperatureonly models, suppressing growth and contracting year-round suitability in hot, arid regions while enhancing fitness in more humid or high-elevation climates characteristic of South Asia and Africa. Together, these results highlight the need to integrate multiple environmental drivers into projections of climatic suitability, as temperature-only approaches may mischaracterize both the magnitude and spatial structure of mosquito population fitness. More broadly, our findings demonstrate how moisture availability reshapes thermal niches, population fitness, and climate-driven projections of vector distributions.

1. Ecological networks comprising of mutualistic interactions can suddenly transition to undesirable states, such as collapse, due to small changes in environmental conditions such as a rise in local environmental temperature. 2. However, little is known about the capacity of such interaction networks to adapt to changing temperatures and thereby impact the occurrence of critical transitions. 3. Here, combining quantitative genetics and mutualistic dynamics in an eco-evolutionary framework, we evaluate the resilience of mutualistic networks to critical transitions as environmental temperature increases. Specifically, we model the dynamics of a phenological optimum trait that determines the tolerance to local environmental temperature as well as temperature-dependent species interaction and evaluate the impact of trait variation and evolutionary dynamics in the occurrence of tipping points and community collapses. 4. We found that mutualistic network architecture, i.e., community size and the arrangement of species interactions, interacted with evolutionary dynamics to impact the onset of network collapses. In addition, some networks had more capacity to track the rise in temperatures than others and thereby delay the occurrence of threshold temperatures at which the networks collapsed. 5. However, such a result was modulated by the amount of heritable trait variation species exhibited, with high trait variation in the mean optimum trait value delaying the environmental temperature at which the network collapses. 6. Our study argues that mutualistic network architecture modulates the capacity of networks to adapt to changes in temperature and thereby impact the occurrence of community collapses.

Environmental stress drives biodiversity loss by altering competitive hierarchies and pushing taxa towards extinction. Parasites and their communities are particularly vulnerable to stress due to environmental sensitivity of infection steps, variation in species tolerance during co-infections, and dependence on host fitness. Parasite populations might avoid extinction through evolutionary rescue - whereby rapid adaptation to stress enables persistence - but whether this process can preserve community diversity remains unclear. Here, we study the impact of evolutionary rescue in a simple parasite community by propagating populations of two viral parasites (bacteriophages {phi}14-1 and {phi}LUZ19) of Pseudomonas aeruginosa in monoculture and co-culture under two thermal conditions, a control temperature (37{degrees}C) and a high temperature that restricts {phi}14-1 growth (42{degrees}C). We show that evolutionary rescue of {phi}14-1 prevented extinction in monoculture. Rescue of this phage in co-culture made it a superior competitor, and it replaced {phi}LUZ19 as the dominant phage at high temperature. We determine that evolutionary rescue occurred through mutations in genes linked to attachment to bacterial hosts and within-host replication. We also show that competitive suppression by {phi}14-1 constrained {phi}LUZ19 molecular evolution. Our findings suggest that evolutionary rescue can prevent the extinction of some parasites, but may inadvertently destabilise the community and facilitate further biodiversity loss. This work underscores the need to take an eco-evolutionary approach to predict the responses of communities to global climate change.

Despite extensive interest in the dynamic interactions between individuals that drive collective motion in animal groups, the dynamics of collective motion over longer time frames are understudied. Using three-spined sticklebacks, Gasterosteus aculateus, randomly assigned to twelve shoals of eight fish, we tested how six key traits of collective motion changed over shorter (within trials) and longer (between days) timescales under controlled laboratory conditions. Over both timescales, groups became less social with reduced cohesion, polarisation, group speed and information transfer. There was consistent inter-group variation (i.e. collective personality variation) for all collective motion parameters, but groups also differed in how their collective motion changed over days in their cohesion, polarisation, group speed and information transfer. This magnified differences between groups, suggesting that over time the typical collective motion cannot be easily characterised. The minimal sample size of independent groups and their divergence over time need to be considered in future studies.

The social environment has diverse consequences for individuals welfare, health, reproductive success, and survival. This environment consists of different kinds of dyadic bonds that exist at different levels; in many social species, smaller social units come together in larger groups, creating multilevel societies. In great tits (Parus major), individuals have four major types of dyadic bonds: pair mates, breeding neighbours, flockmates, and spatial associates, all of which have been previously linked to fitness outcomes. Here, we show that these different types of dyadic bonds are differentially linked with subsequent reproductive success metrics in this wild population and that considering spatial effects provides further insights into these relationships. We provide evidence that more social individuals had a higher number of fledglings, and individuals with more spatial associates had smaller clutch sizes. We also show individuals with stronger bonds with their pair mate had earlier lay dates. Our study highlights the importance of considering different types of dyadic relationships when investigating the relationship between wellbeing and sociality, and the need for future work aimed at experimentally testing these relationships, particularly in spatially structured populations.

Male animals are not given equal mating opportunities under competitive circumstances. Small males often exhibit alternative mating behaviours and produce spermatozoa of higher quality to compensate for their lower chances of winning physical contests against larger competitors [1]. Because the reproductive benefits of these phenotypes depend on social status/agonistic ranks that can change during growth or aging [2], sperm traits should be developed/switched into fitness optima according to their prospects. However, reproductive success largely relies upon social contexts arising instantaneously from intra- and inter-sexual interactions, which deter males from developing extreme traits and instead favour behavioural plasticity. Nevertheless, the extent to which such plasticity influences developmentally regulated alternative sperm traits remains unexplored. Squids of the family Loliginidae are excellent models to investigate this, because they show sophisticated alternative reproductive tactics (ARTs) by which small males, known as "sneakers", produce longer spermatozoa and perform extra-pair copulation to attach their sperm packages near the female seminal receptacle (SR). In contrast, large "consort" males have shorter spermatozoa and copulate via pair-bonding to insert their sperm packages near the internal female oviduct [3]. In addition, plasticity in male mating behaviour is common in some species while it is either rare or absent in others. Thus, squid ARTs display a broad spectrum of adaptive traits with a complex repertoire in behaviour, morphology and physiology [3].

Temporal thermal heterogeneity is expected to favour intermediate, generalist phenotypes that can maintain growth across a broad thermal range but have sub-optimal growth at any single temperature. Yet, thermal variation typically occurs in the presence of additional selection pressures which may interact to constrain adaptation to temperature. We propagated competing lytic viral parasites (bacteriophages {phi}14-1 and {phi}LUZ19) of Pseudomonas aeruginosa under fluctuating temperatures (37-42{degrees}C) in monoculture and in co-culture. Without competition, fluctuating temperatures favoured intermediate thermal phenotypes in the phage {phi}14-1 and resulted in more variable evolutionary outcomes compared to static conditions. However, co-selection from fluctuating temperatures and competition led to restricted thermal adaptation, slower evolutionary rates, and fewer putative adaptive mutations in the {phi}LUZ19 competitor. Our study highlights the potential for reduced adaptive capacity in interacting communities amidst global climate change.

The evolutionary mechanisms of cooperation are well-studied, yet what motivates individuals to cooperate remains unclear. Although conventionally associated with enhanced social tolerance (self-domestication hypothesis) and prosociality (cooperative-breeding hypothesis), individuals belonging to species that are neither self-domesticated nor cooperatively-breeding also cooperate. An overarching interdependency hypothesis posits that inter-individual dependencies promote cooperation, but comparative evidence is lacking. We experimentally studied cooperation, prosociality, and tolerance in six macaque species along a despotic-egalitarian gradient. Within-group cooperation was higher in despotic than egalitarian societies yet restricted to few partners. Prosociality, kinship, and tolerance positively predicted cooperation success. Agent-based models consistently showed that despotic societies have fewer but more stable social bonds and, thus, higher interdependencies than egalitarian ones. Our results suggest that interdependencies facilitate the emergence and maintenance of cooperation.

Sex ratio variation is of fundamental importance for population ecology, and the evolution of sex roles and life-histories. Yet, the ecological mechanisms underlying such variation remain often unknown. Using a multiyear dataset from captive and wild precocial Ruffs Calidris pugnax, we show that poorer survival and later fledging of males relative to females result in a female biased sex ratio of the fledgling population. Both sex-specific survival and maturation time contributed equally to an increasing sex ratio bias from hatching to fledging in this sexually dimorphic bird. On average, juvenile females fledged three days earlier than males due to expedited wing development, despite the higher absolute rate of wing growth in males. We argue that sex differences in growth, maturation, and offspring survival are likely the result of strong pre-sexual selection on males to achieve dominance and may help to enforce the Darwinian sex roles observed in this species.

1. Birdsong offers a powerful model to study the evolution of complex communication systems. While most song syntax and sharing research focuses on temperate species with fixed repertoires, we know far less about tropical songbirds with large, open-ended vocal systems. 2. We examined song structure and cultural transmission in the White-bellied Sholakili Sholicola albiventris, a tropical passerine endemic to the Shola Sky Islands of southern India. We studied song complexity and spectro-temporal variation using over 6,000 songs from 17 color-banded males across five years. We analyzed the song syntax using sequence-based metrics, including Levenshtein Distances and N-gram models. 3. Our results reveal high syntactic variability across short and long timescales, with stable note-type cores and structured expansions of combinatorial sequences. Higher-order N-gram turnover was rapid and strongly individual-specific, while broadly sharing the population-level note pool. Song sharing was significantly higher among neighbors than non-neighbors. 4. Using Generalized Additive Models, we explain how social and ecological factors, including neighbor count, territory area, repertoire size, N-gram usage, and the spectro-temporal structure of N-grams, determine consistency across years and sharing across individuals. This study highlights parallels between human linguistics and syntactic organization in the complex songs of a tropical passerine.

The spotted hyaena lives in unusually large social groups for a carnivore. Since the infertility trap normally limits the size of social groups in mammals, it seems likely that this species has evolved some way of mitigating the stresses involved. In primates, this usually takes the form of female-female alliances, often embedded in multilevel social systems. I show (1) that the distribution of hyaena clan sizes is multimodal, with a fractal scaling close to 3 and a base unit of 12-15 individuals (3-5 reproductive females) and (2) that fertility is a trade off between the benefits of having more males in the group and the costs incurred by having more females, with 4-5 as the limit on the number of females that can live together without their reproductive rates falling below the demographic replacement rate. I present evidence that females buffer themselves against the infertility trap by forming matrilineal alliances that in turn create a multilevel structure. In this respect, hyaena resemble cercopithecine primates in using social strategies to enable animals to live in larger groups than they would otherwise be able to do.

Kin selection has been the main hypothesis explaining helping behaviour in cooperative breeders, with evidence being largely based on the observation that helpers tend to provide to related offspring. However, kin-biased help could conceal additional, mechanisms contributing to the maintenance of cooperation. Under pay-to-stay, group augmentation and partner choice hypotheses, a range of direct benefits can arise through helping. Here, we explored this potential mechanism by testing whether the social associations of breeding individuals were related with the help that they received from non-breeding individuals. We collected social associations from PIT-tagged sociable weavers, Philetairus socius, at RFID feeding stations, which allowed us to compare associations between breeders and either their helpers (mostly kin) or their other kin that did not help--before, during and after reproduction. Using correlative tests and data-driven simulations, we show that helpers have stronger foraging bonds with breeders than non-helping kin, and that these stronger bonds are present both prior and post breeding. Furthermore, helper-breeding female social affiliations were positively correlated with the amount of help provided. Our results suggest that direct benefits of social associations complement kin selection to determine helping decision, and that these in turn influence future social associations.

Transparency reduces prey detectability by predators. While transparent aquatic species hold higher transparency levels as the light availability of their habitat increases, less is known about such variation in terrestrial species. Lepidoptera species exhibiting transparent wings display various levels of transparency. Using two complementary approaches, we explore how the evolution of different transparency degrees relates to habitat openness, activity rhythm and mimicry syndrome (bee/wasp versus dead-leaf mimic). First, by exposing artificial moth-like prey to wild avian predators in a range of habitat openness, we show that survival is lower in more open habitats. We also found that less transparent morphs are more attacked than more transparent ones, regardless of habitat openness degree. Second, by analysing the evolution of wing features and ecological traits in 107 clearwing species, we found that diurnal species transmit more light than nocturnal species under certain conditions (when considering only forewings, at smaller clearwing surfaces and at larger wing lengths) and that species flying in open habitats and exhibiting large percentages of clearwing surface transmit slightly more light than those flying in closed habitats, although this is reversed at smaller percentages of clearwing surfaces. Additionally, bee/wasp mimics are more often diurnal and have higher and less variable light transmittances than dead-leaf mimics, which are more often nocturnal. Flying during the day, in open habitats and mimicking insects with transparent wings seem to promote high light transmittance under certain circumstances. Activity rhythm, habitat openness and species interactions play a crucial role in determining transparency design on land.

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.