Proceedings of the Royal Society B: Biological Sciences

The origin of novel phenotypes can influence access to new ecological resources, which may have positive, neutral, or negative effects on subsequent phenotypic diversification. In this study, we tested the macroevolutionary consequences of a pair of putative functional innovations occurring in deep-sea fishes of the order Stomiiformes. Integrating phylogenetic comparative methods, micro-CT scans, and external body measurements, we recover a mosaic of diversification trends associated with these innovations. We found some evidence for elevated evolutionary rates in tooth morphology associated with the predatory dragonfishes, which possess a gap between their vertebral column and skull that exposes the notochord and enables neck-like flexibility. However, a second novelty building upon the first, a functional neck joint enabling extreme cranial kinesis, was linked to faster rates of skull evolution. Our results suggest that innovations that help shift ecological roles and overcome functional constraints related to those roles, like gape-limitation in prey depauperate habitats, may play an important role in promoting phenotypic diversification. This work builds on a growing body of evidence highlighting how the deep sea promotes phenotypic diversity, generating the extreme forms that are celebrated by scientists and the public alike.

The impacts of increasingly frequent and intense heatwaves on parasitism are an important frontier for understanding disease risk under climate change. These impacts are complex because parasitism arises from multiple interacting host and parasite traits that can vary in thermal sensitivity and among populations adapted to different temperature regimes. Here, we used a lab microcosm experiment to investigate the effects of heatwaves occurring during two different phases of a winter-adapted mosquito host - ciliate parasite interaction, for six pairs of sympatric host and parasite populations sourced from two geographic regions with differing histories of winter heat. We found that because heatwaves allowed mosquito larvae to evade infection, they reduced parasitism and increased survival. An early heatwave during initial parasite attack had stronger effects than a later heatwave occurring after infections had established. We did not find evidence of local adaptation to heatwaves: impacts were consistent regardless of population, and were mechanistically predictable from previously measured thermal performance curves that described lower infection and stronger host defenses at warm constant temperatures. The results suggest that increasingly frequent heatwaves may accelerate geographic shifts in parasitism, and demonstrate how fundamental host - parasite thermal biology links to the impacts of extreme temperature events.

Coordinated dynamics between individuals are a hallmark of social interaction, yet the temporal structure and physiological basis of such coupling beyond human species remain poorly understood. Here, we investigated cross-species biobehavioral synchrony by simultaneously quantifying motion dynamics and autonomic activity with hyperscanning of human-canine dyads. We observed both spontaneous and task-related synchrony across motion dynamics, heart rate, and heart rate variability at multiple timescales. Importantly, synchrony was modulated by individual and relational factors. Task-related autonomic synchrony was affected by the human temperament, whereas greater familiarity within the dyad altered the leader-follower dynamics, shifting directional influence from human-led toward canine-driven coordination. Motion synchrony emerged with minimal delay, whereas cardiac synchrony unfolded across longer timescales, suggesting coordinated processes underlying the shared activity, arousal, and autonomic regulation. Our findings extend current models of social synchrony beyond human interactions and reveal that regulatory dynamics underlying coordinated behavior operate across species boundaries.

In a wide variety of animals, developmental crowding results in adults with smaller bodies. The crowding effect on body size in Drosophila melanogaster is canonically attributed to heightened competition for nutrition. However, whether other consequences of crowding also contribute to its effect on size remains an open question. We tested the relative contributions of nutritional competition, oxygen availability, and larval-generated metabolites to the crowding effect on size. We found that while nutrition explains most of the variation in body size due to crowding, oxygen also contributes in a sex- and nutrition-dependent manner. We found no evidence that larval-generated chemicals affect body size. These data confirm a widely suspected but untested role of nutrition in producing the crowding effect on size in D. melanogaster, while revealing an unexpected role of oxygen, and raise the possibility that behavior may be a mediator of density-dependent plasticity. Research HighlightsWe found that both nutrition and oxygen mediate the crowding effect on size in Drosophila melanogaster.

Why male primates invest in costly behaviours producing public goods remains debated, with two leading explanations, paternal care and reputation-based partner choice (RBPC). Using long-term data from four groups of wild vervet monkeys, we tested: (1) whether males show a bias in four protective "male services" (predator alarm calling, participation in between-group conflicts, leading river crossings and sentinelling); (2) which males contribute most; and (3) whether service provision predicts mating success during the mating season. We confirmed a male bias in all services. Consistent with the paternal care hypothesis, contributions were positively associated with past mating success, independently of rank, although potential fathers did not contribute more than non-fathers. Among non-fathers, service provision varied with rank, suggesting that newly immigrated males adjust their behaviour according to competitive state. Crucially, variation in alarm calling and between-group conflicts predicted future mating success, with between-group conflict emerging as the strongest and most consistent predictor of mating success across years and within mating seasons, whereas rank, tenure and social integration added little explanatory power. In contrast, sentinelling and leading river crossings did not reliably translate into mating benefits. Our findings indicate that male services are shaped by multiple selective pressures operating across different male career stages and that some forms of public goods provision function as signals of quality and cooperativeness to females. By directly linking cooperative investment to mating outcomes in a wild primate, this study provides rare empirical support for reputation-based partner choice beyond humans and highlights female choice as a potentially important force in the evolution of cooperation.

Many proposed mechanisms for the evolution of cooperation among unrelated individuals rely on relatively demanding cognitive abilities that are not widespread across taxa. In contrast, individual heterogeneity is a pervasive feature of animal groups, encompassing differences in personality as well as physical and cognitive traits. Such heterogeneity can promote the evolution of cooperation, yet its role has received comparatively little attention, particularly as a source of variation giving rise to social organization such as leadership. A specific form of leadership can emerge under unstable environmental conditions, when some individuals become better suited than others to initiate action and influence the behavior of their peers. Unlike fixed dominance hierarchies, emergent leadership can rapidly adjust to changing environmental conditions, thereby reshaping group organization. Because it does not require the maintenance of stable hierarchies, this form of leadership can arise even in species that do not have the cognitive capabilities to sustain complex social structures. In this work, we investigate the combined effects of individual heterogeneity and emergent leadership on the evolution of cooperation using an evolutionary game-theoretic model in which individuals may assume the roles of leaders or followers according to their strength, representing individual differences in suitability to prevailing environmental conditions. We examine different levels of population heterogeneity together with increasingly complex strategy sets requiring progressively greater informational requirements, allowing individuals to condition cooperation on their own strength, leadership role, or both. Our results show that the interplay between leadership and heterogeneity promotes the evolution of cooperation, particularly when only a small fraction of individuals act as leaders. Under these circumstances, cooperation evolves even when individuals employ the simplest possible strategies. Under harsher ecological conditions, cooperation can be sustained by more sophisticated strategies, specifically by conditional strategies that prescribe cooperation when individuals are strong or leading and defect when acting independently. Author summaryIn this study, we propose that emergent leadership mediated by individual diversity can boost the evolution of cooperation in animal groups. Building on growing evidence on the heterogeneity of animal capabilities and personalities, we focus on the fleeting leadership that emerges in animal groups when facing rapidly changing environmental conditions. We suggest that this type of leadership that emerges from individual differences in strength--a generic quality encompassing those characteristics that make an individual more fit to lead in a given situation--does not require complex cognitive capabilities from the animals and represents a valid alternative to more demanding strategies proposed in the past to explain the evolution of cooperation. Using an evolutionary game theory model, we show that if a population includes a few strong players, these can become influential leaders and guide the actions of their peers to achieve cooperation. Although the naive strategy of always cooperating is sufficient for cooperation to evolve, the introduction of more complex strategies leads players to cooperate only when they are more likely to be recognized as influential leaders. These strategies are more effective in promoting cooperation under unfavorable ecological conditions and are also more robust against exploitation by defectors.

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.

True crabs (Brachyura) are among the most iconic marine arthropods, representing noteworthy examples of morphological and ecological disparity. A striking feature of brachyurans are their anterior pincer-like appendages: chelipeds. These structures showcase a large diversity of morphologies that reflect ecology and overall multifunctionality. Yet, a comprehensive assessment of appendage functional morphology within phylogenetic and ecological trait contexts has never been attempted. By combining 3D geometric morphometrics, finite element analyses, multilocus molecular phylogeny, and ecological trait data for 80 crab species, including three fossil forms, we unveil a complex evolutionary history for crab chelipeds. Despite extreme shape diversity amongst chelipeds, stress distributions are very similar across taxa and hint a many-to-one pattern. High concentrations of chelipeds within constrained morphospace regions associated with peak pinch forces illustrates that brachyuran morphologies optimised for shell crushing may have arisen in the Cretaceous. Deviations from this morphospace highlight the diversification of non-shell-crushing life modes and the influence of sexual selection on appendages. Neither cheliped shape nor pinch force show phylogenetic signal. Together these results indicate that the evolution of cheliped shape is closely associated with, and inferred to have been strongly influenced by, crab ecology, biomechanical needs and sexual selection. SIGNIFICANCE STATEMENTChelipeds, the pincer-like claws of crabs, are among the most morphologically diverse appendages within Arthropoda, yet the evolutionary forces driving this diversity remain poorly understood. By integrating 3D geometric morphometrics, biomechanical modelling, molecular phylogeny, and ecological data across 80 crab species including fossil forms, we demonstrate that cheliped morphology is driven by ecology, biomechanical demands, and sexual selection rather than phylogenetic relatedness. The multifunctionality of these structures produces strong evidence for many-to-one mapping of form to function. Morphologies optimised for durophagy appear to have originated in the Cretaceous, with subsequent diversification into manipulative and sexually selected forms from a morphologically flexible foundation. These findings demonstrate that cheliped diversity reflects a complex interplay between ecological specialisation, biomechanical optimisation, and sexual selection across Brachyura.

Collective animal behavior occurs in high-stakes contexts where failing to coordinate effectively with group-mates can spell disaster for individuals. Yet, identifying instances of coordination failure is challenging, meaning their evolutionary effects remain mysterious. Synchronous calls in alternating frog choruses (i.e., inadvertent signal collisions) are unambiguous failure events that impose steep attractiveness costs. We modeled tungara frog chorusing dynamics to reveal the sensorimotor and social mechanisms underpinning synchrony. Ultimately, inter-male variation in two key sensorimotor attributes, the periods of male calling rhythms and call latencies, generated divergent synchrony engagement patterns. Modeling female preferences revealed that these varied behavioral outcomes then yielded disparate attractiveness consequences. By mechanistically linking the causes and consequences of coordination failure, we demonstrate that non-random failure patterns in collectives generate selection gradients that refine sensorimotor tuning.

If an individuals niche is determined by its genotype, then competition for limiting resources should be most intense among individuals of the same genotype. Theory predicts this will act to maintain genetic variation, but whether this mechanism operates under natural conditions is unclear. Using long-term observations of a population of free-living Trinidadian guppies, we asked (i) whether competition was strongest between kin, and (ii) whether this process maintained genetic variation. Competition between kin was 1.5-1.8 times stronger than that between non-kin. This contributed to balancing selection: after [~]10 generations, variation was 29% higher than expected under drift. Our results show that relatedness can play a major role in structuring ecological competition, with broader consequences for theories of inclusive fitness. One-sentence summaryHeritable variation is maintained due to resource competition being more intense among kin.

Conjugative plasmids drive the dissemination of antimicrobial resistance genes and other conditionally beneficial accessory genes, but otherwise inflict fitness costs on their hosts that limit their spread. These costs can be ameliorated by compensatory mutations on the chromosome, the plasmid, or both combined (combined compensation). Mutants with plasmid-borne or chromosomal compensation differ in how they spread and compete, making the location of compensation an important determinant of plasmid and antimicrobial resistance (AMR) dynamics. We collate experimental data on plasmid-host co-evolution which, albeit limited, suggest compensatory benefits differ by location and are highest for combined compensation. We develop and analyse a mathematical model of compensatory evolution, finding that the long-term location of compensation is mainly determined by the highest cost reduction. Short term, however, succession dynamics arise from differences between locations: for instance, plasmid-borne compensation spreads horizontally, initially dominates, and can even facilitate the establishment of chromosomal or combined compensation. Strong trade-offs between compensation and either resistance or conjugation render compensation non-viable, but only conjugation trade-offs are location-dependent, disadvantaging plasmid-borne compensation and generating oscillatory dynamics. Our findings suggest plasmid-borne compensation may initially accelerate AMR-plasmid spread, whereas long-term chromosomal or combined compensation may enable hosts to accumulate multiple AMR-plasmids, promoting multidrug resistance.

The number of chromosome sets per nucleus is a fundamental trait, but why this number is nearly always two for multicellular eukaryotes remains unclear. Chromosomes are made of nucleic acids, which possess abundant phosphorus (P). Therefore, producing new chromosomes, as well as generating new cells and organismal growth, demands substantial phosphorus. Yet, because P is often limiting in nature, P availability could influence the prevalence of diploidy versus polyploidy. Here, we compare growth rates of diploid and triploid Potamopyrgus antipodarum, a freshwater snail, relative to P availability. Because diploid P. antipodarum are obligately sexual while obligately asexual individuals are polyploid, costs associated with sensitivity to P limitation in polyploids could also help explain the maintenance of sexual P. antipodarum. We raised juvenile diploid and triploid snails on either P-adequate or P-deficient diets and found that independent of P availability, juvenile triploid asexual snails grew faster and harbored higher P content as adults than sexual diploid conspecifics. Together, these results suggest life-history advantages of polyploidy or asexual reproduction that exacerbate rather than ameliorate the cost of sex. These outcomes suggest that P availability is unlikely to be a main driver of ploidy polymorphism or the maintenance of sex in P. antipodarum.

Introgression following hybridization is increasingly recognized as a major driver of evolution. However, its importance depends on its frequency in nature, which remains to be quantified. To address this, we provide a snapshot of ongoing introgression in a whole species assemblage (4126 ant colonies). 23% of all 82 local species show signs of introgression, which is more than twice previous estimates. Introgression is typically subtle, yet we find that it contributes measurably to genetic diversity. Species divergence, rather than classical prezygotic reproductive barriers (mating phenology, ecological niche, fine-scale habitat use) constrains introgression, suggesting that the main reproductive barriers are postzygotic at this stage of divergence. Our results indicate that introgression may be a common but often overlooked feature of natural communities.

Understanding how social complexity responds to environmental variation remains a longstanding challenge in evolutionary biology. Here, we investigated the drivers of social complexity using intraspecific social variation across seven locations of the obligatory shell-brooding cichlid Neolamprologus meeli in Lake Tanganyika. We quantified the number of subordinate individuals per female territory and examined the effects of predation risk, shell availability, and their interaction. Social complexity increased with shell availability under high predation risk but showed little association under low predation risk. A field manipulative-experiment further demonstrated that increasing shell availability led to higher juvenile retention, indicating a causal effect of territory quality. In addition, removal of subordinates reduced shell availability, suggesting the feedback between group size and territory maintenance. We also assessed genetic population structure based on nuclear SNPs obtained by MIG-seq and found only weak genetic differentiation among localities, suggesting that the observed social variation is unlikely to simply reflect strong genetic subdivision. Together, these results show that predation risk promotes group living, whereas nesting resource availability constrains its extent. Our study highlights that social complexity emerges from the interaction between macro- and micro-ecological factors, providing a mechanistic understanding of the evolution of social complexity and philopatry.

Many sea anemones reproduce asexually by pedal laceration, shedding fragments of the pedal disk that regenerate into polyps. How feeding affects the amount of this reproduction differs among species, but whether feeding also sets its timing has rarely been examined. We fed the sea anemone Cylista elegans (formerly Sagartia elegans) daily, every second day, every fourth day, or not at all, measured growth, laceration, and survival over 35 days, then reassigned anemones to new schedules to test whether laceration follows the current or previous schedule. Growth rose with feeding but saturated, animals fed daily and every second day growing at similar rates. Total laceration depended on whether an anemone was fed rather than how often. Every fed schedule produced more lacerates than starvation. The timing, by contrast, tracked the schedule closely. Laceration was suppressed for about a day after each meal and recovered before the next, so anemones fed every second or every fourth day lacerated on matching two- and four-day rhythms, while daily-fed animals were arrhythmic. When moved to a new schedule, the period shifted to match it, not the old one. Only starvation caused death. Asexual reproduction in C. elegans is therefore bound closely to feeding, which fuels laceration yet suppresses it during digestion, confining it between meals. This coupling distinguishes C. elegans from anemones with symbiotic microalgae, where starvation rather than feeding drives reproduction, and links it to the feeding-driven clonal proliferation of the invasive sea anemone Diadumene lineata.

Light is a fundamental regulator of human physiology and behaviour. Whether prior light exposure shapes subsequent higher-order cognition and mood beyond the period of exposure remains unknown. We tested this in a within-subject, randomised crossover experiment in which 24 healthy young adult males completed a multimodal cognitive battery following 2 x15 min of full-spectrum light (FL; median 1,029 melanopic equivalent daylight illuminance [mEDI]) or standard indoor light (SL; median 234 mEDI), with all testing conducted under identical dim illumination. FL improved Digit-Symbol Substitution Test accuracy and promoted digit-directed gaze reallocation, consistent with more efficient associative encoding. On the Balloon Analogue Risk Task, FL reduced reward-seeking behaviour and suppressed backward-referencing gaze transitions linking current and prior-trial reward information. Mood declined following SL but remained stable after FL. Sustained attention, vigilance, and subjective sleepiness were unaffected. Our findings identify pre-task FL exposure as a selective primer of higher-order cognition and mood, independent of alertness.

Successful communication depends not just on what we say but also on how we repair it when understanding breaks down. People routinely respond to misunderstanding by gesturing more or speaking louder. Yet whether these responses actually reflect measurable bodily effort, and whether it helps communication, has not yet been directly tested. Extending the hypo- and hyper-articulation accounts to whole-body multimodal communication we ask: does regaining understanding require increased physical effort, and does that effort improve communicative outcomes? In a pre-registered biomechanical study, 61 pairs of participants conveyed concepts without conventionalized language, using gestures, vocalizations, or both, and repaired failed attempts. We measured communicative effort by capturing arm torque change (upper-limb effort), vocal amplitude (vocal effort), and postural adjustments (postural effort). Using Bayesian hierarchical models, we show that repair increases physical effort across all three measurements, but that performers communicate more over time rather than more forcefully at any particular moment in time. Upper-limb effort scale with the degree of misunderstanding but effort overall does not predict whether communication succeeds. We suggest that communicative effort on the level we measured here functions as an index of continued commitment rather than a mechanism for repairing misunderstanding.

Perception and action form a loop as an organism interacts with its environment. Here, we probe the interdependence between the two in the context of choice-history effects, the tendency of past choices and their outcomes to bias current choices. We investigated if the modulation by previous choices depended on the coupling between perceptual choices and the motor responses reporting these choices. We analyzed data from non-human primates (Macaca mulatta; three females and five males) performing two different perceptual decision-making tasks. Each task had a coupled variant with a fixed mapping between perceptual choices and motor plans used to report the choice, and an uncoupled variant, in which this mapping varied randomly across trials. We found that, in both tasks, the animals in the coupled variant had larger choice-history effects compared to the animals in the uncoupled variant. Decoupling choices from motor responses was further associated with an inability by the animals to learn experimentally induced stimulus sequence regularities. Together, these findings identify choice-response coupling as a factor shaping animals ability to use recent history to guide behavior and highlight the tight link between cognitive and motor processes.

While mutualistic symbioses with nitrogen-fixing bacteria enable plants to access fixed nitrogen, they also require substantial carbon investment. Under carbon limitation, such as shading, shifts in biomass allocation can decouple symbiotic investment from leaf and root growth, potentially compromising plant nitrogen status. Because shading shifts biomass allocation toward light acquisition, it could influence nitrogen fixing symbiosis in two opposing ways. If nodulation remains coupled to leaves rather than roots, nitrogen status should be maintained despite reduced root growth. Alternatively, if root growth constrains nodulation, nitrogen status should decline. We tested these hypotheses by manipulating light availability (full sunlight vs. 50% shade) and quantifying biomass allocation and symbiotic nodulation. Under shading, plants allocated proportionally more biomass to shoots than to roots and invested less biomass in root nodules. Relationships between nodulation and leaf or root biomass differed between treatments but converged with increasing plant size, although shaded plants never attained the root biomass observed in full sunlight. Leaf nitrogen concentration was maintained under shading because nodulation remained coupled to leaf investment despite reduced root allocation. These findings highlight that, under carbon limitation, maintaining leaf and nodule coupling enables plants to reduce nodule investment without compromising the nitrogen benefits of symbiosis.

Animals often rely on social information when making movement decisions. In zebrafish, classic work showed that shoal size and shoal activity both bias shoal choice. Here we extend these effects in Goldfish (Carassius auratus) and extend them with a drift-diffusion model (DDM) account of individual evidence accumulation under dynamic social cues. Using a three-chamber linear arena, we quantified a focal fishs position for 10 minutes while manipulating (i) numerical differences between flanking shoals and (ii) their activity (swimming speed) via temperature manipulation. ANOVA on time-proportion choices confirmed robust attraction to larger shoals; when shoal sizes were equal, the more active shoal was preferred. In combined manipulations, activity effects dominated at small numbers but saturated as group size increased, indicating a threshold-like integration where activity dominates at small shoal sizes (<3 fish) but saturates at larger sizes. We formalize these processes with a bounded DDM in which a sigmoidal stimulus function maps shoal size and average speed to momentary evidence, subject to random perturbations. The model reproduces the observed psychometric relations between relative numerosity, velocity differences, and choice. Our results (i) generalize zebrafish findings to a carp species with distinct ecology and physiology, and (ii) provide a compact mechanistic link between social cues and individual decision trajectories in dynamic social contexts.