Proceedings of the Royal Society B: Biological Sciences

Complex environments combining multiple stressors are the new norm worldwide. Adaptive evolution will be critical to population persistence under these combined challenges, but how environmental complexity affects the pace of evolution remains poorly understood. Using a meta-experimental evolution approach, we exposed 14 species, from bacteria to unicellular eukaryotes and plants, to single stressors and their pairwise combinations for multiple generations, while keeping the overall stress level comparable. Populations evolving under combined stressors had lower fitness increase in the selective environments, higher fitness reductions in the control environment, and shallower relation between initial maladaptation and fitness gain, than under single stressors. However, these responses varied with species and stressor type. Accounting for such constraints on evolutionary dynamics should prove crucial for the management of biodiversity.

Cooperatively breeding species are disproportionately found in extreme and unpredictable climates globally, suggesting that cooperation is beneficial to persistence in climatically challenging conditions. Notably, other dimensions of sociality, like group living and tendency to engage in affiliative social behaviors, offer fitness-related benefits that could make them similarly advantageous in such climates. Here, I present a phylogenetic analysis of Primates aimed at testing whether these two dimensions of sociality--average group size and average percent time spent social grooming--are predicted by climatic challenges in species environments. Results show that time spent grooming is highest in extreme and unpredictable climates, with how dry conditions are explaining the greatest amount of variation. Thus, climate may influence the evolution and/or persistence of social grooming. While multiple mechanisms could mediate this association, subsequent analyses point to the benefits of social affiliation in environments where groupmates have highly competitive dynamics as one potential explanation.

The evolution of eye coloration in mammals and its potential ecological significance remain understudied. Evidence from anthropoid primates suggests that photoprotective demands are crucial determinants of pigmentation in the peri-iridal tissues, which encompass the conjunctiva and portions of the sclera peripheral to the iris. However, it is unclear to what extent these findings can be generalized. Here, we quantify peri-iridal brightness in a photographic sample of 62 terrestrial non-primate mammal species (n = 930). Phylogenetically-controlled analyses revealed significant effects of eye size as well as ecology on ocular pigmentation. Peri-iridal brightness exhibits a notable phylogenetic signal, correlates negatively with eye size and hence exposure to UV light, and is more pronounced in nocturnal species. Significant interspecific effects of latitude on peri-iridal brightness were not recovered, but tentative evidence for non-negligible impacts of this variable at the intraspecific level were found. Overall, these results align with and help to contextualize findings on primates and suggest that photoprotective demands importantly shape ocular appearance across the mammalian radiation. Furthermore, they have implications for hypotheses tying eye pigmentation chiefly to gaze signaling and provide a broad evolutionary framework for the emergence of human eye appearance.

Allopatric isolation under contrasting environments can drive rapid phenotypic divergence, even over contemporary timescales. Rapid changes in morphology or physiology can allow organisms to adapt to biotic and abiotic characteristics of their habitats. While studying metabolism, growth and resources needs may allow to understand adaptation to several selective pressures, these traits are rarely jointly considered. We investigated morphological, growth, and metabolic divergence in two allopatric populations of Arctic charr (Salvelinus alpinus) sharing a common evolutionary origin but inhabiting contrasting environments. We combined field observations, common garden and quantitative genetic approaches to disentangle contributions of genetic divergence and plasticity to phenotypic variability. Wild adults differed in body shape and growth trajectories, potentially reflecting plasticity related to resource availability and temperature variations. Under common garden conditions, juveniles displayed inter-population differences in routine metabolic rate, its allometric scaling with body mass. These patterns suggest divergent selection on physiological traits. Despite low neutral genetic differentiation, phenotypic divergence unfolded in fewer than 100 years, suggesting that plasticity and selection can promote rapid multi-trait changes. These findings highlight that considering changes in physiological, growth and morphological traits can reveal the adaptive potential of small, isolated populations facing rapid environmental change.

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.

Understanding the genetic basis of adaptation in natural populations to changing environmental conditions is challenging. The relatively simple genotype-to-phenotype relationship between opsin genes and visual pigments offers a particularly informative model to explore the molecular mechanisms underpinning adaptive phenotypic change in natural populations. Here we leveraged the natural experiment provided by the tectonic closure of the Central American seaway that created allopatric, sister taxa in multiple, independent lineages of marine organisms and exposed them to distinct underwater light environments: either the more turbid Tropical Eastern Pacific (TEP), or the spectrally broader Caribbean Sea. Using two species pairs of planktivorous teleosts, the Azurina multilineata/A. atrilobata damselfish and the Cephalopholis (Paranthias) furcifer/C. colonus groupers, we explore to what extent visual sensitivity converged to similar adaptations in response to similar foraging strategies and shared underwater light in each marine basin. We found that the compression of the underwater light field towards the central portion of the spectrum from Caribbean to TEP waters is reflected in similar shifts towards the centre of the light spectrum in overall single and double cone sensitivities in both families. Both TEP species have single (short-wavelength) cone sensitivities shifted to longer wavelengths and double (long-wavelength) cone sensitivities shifted to shorter wavelengths, compared to their Caribbean counterparts. These parallel shifts in visual sensitivities observed in response to shared underwater light environments are accomplished by different underlying opsin gene toolsets in the two lineages. Similarly, expression changes in pathways associated with the visual system revealed limited parallelism at the molecular level.

Eye loss has long fascinated evolutionary biologists and occurs across the animal kingdom. Spiders have two parallel visual systems -- two primary and six secondary eyes -- but eye losses, leaving six, four, two, or no eyes, have occurred in multiple lineages. Despite their significance, reports of eye loss are scattered, limiting broader analysis. Here we present the first comprehensive analysis of eye loss across all known spider lineages. We show that eye loss occurs in [~]12% of extant species, mainly within the clade Synspermiata. Six-eyed spiders are most common (>5,300 species), while four-eyed, two-eyed, and eyeless forms are rarer and often linked to troglobitic lifestyles. Principal eye loss is widespread, occurring in 49 families across nearly all major lineages. Using a recent phylogeny of the order Araneae, we demonstrate a strong correlation between eye loss and occupancy of low-light environments, but this is complicated by differential effects across eye types and phylogenetic groups through geological time. These findings reveal striking lability in eye number and lay groundwork for future research into ecological, developmental, and neurological drivers of eye loss. [hidden Markov models, ancestral state reconstruction, Araneae, discrete character evolution, principal eyes, secondary eyes, low light environments].

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.

Although social behavior has been predicted to correlate with increased complexity in vocal signals, its relationship with auditory sensitivity between the sexes remains poorly understood. Here, we used phylogenetic comparative analyses to examine sex-specific differences in auditory processing across rodent species representing different social lifestyle strategies. We detected significant sex differences in click and frequency evoked auditory brainstem response (ABR) thresholds across sociality, with social female rodents exhibiting lower thresholds than solitary males. Males generally exhibited higher ABR wave I and IV amplitude ratios than females, whereas interpeak latencies were similar between the sexes across social groups. Females exhibited significantly higher binaural interaction component (BIC) relative amplitudes and faster BIC normalized latencies than males across tested interaural time differences (ITDs). Together, these findings demonstrate that sociality plays an important role in shaping differences in auditory physiology between male and female rodents and highlights the potential influence of social behavior on the evolution of mammalian auditory systems.

Anseriformes (waterfowl) and Galliformes (landfowl) are among the worlds most recognisable groups of birds, together comprising the clade Galloanserae. Despite their close evolutionary relationship, the skulls of adult anseriforms and galliforms exhibit strikingly distinct morphologies, the developmental basis and evolutionary history of which is poorly understood. To illuminate the developmental and evolutionary underpinnings of cranial disparity between and within these major extant bird clades, we quantitatively investigated ontogenetic changes in cranial morphology across galloanseran phylogenetic diversity, focusing on the previously unexplored post-hatching interval during which adult morphology takes shape. Our results reveal the combined effects of multiple heterochronic shifts early in galloanseran evolutionary history including anseriform hypermorphosis, along with influential non-heterochronic changes leading to substantially more disparate ontogenetic trajectories--and greater cranial variability--in anseriforms than galliforms. Key galloanseran fossils help clarify the polarity of evolutionary shifts in cranial development through galloanseran phylogenetic history and demonstrate that extant galliform cranial morphology is more constrained and retains a more plesiomorphic morphology than that of anseriforms. Our work helps illuminate the developmental basis of the iconic differences in cranial form between waterfowl and landfowl and illustrates the importance of broad phylogenetic and ontogenetic sampling for clarifying patterns of post-hatching developmental divergence among major vertebrate clades.

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.

Understanding how anatomical structures evolve requires disentangling the roles of integration and modularity in shaping morphological variation. The vertebral column, a serially repeated and regionally differentiated structure, provides a powerful system for investigating these processes. Here, we examine how vertebral morphology evolves in relation to whole-body elongation across the adaptive radiation of Lake Malawi cichlid fishes. We tested for evolutionary integration between the precaudal and caudal domains, as well as assessed the contributions of vertebral count, centrum shape, and intervertebral spacing on body elongation. We find strong evolutionary integration between precaudal and caudal vertebral shape, with both vertebral shapes varying along shared axes of multivariate shape change. Despite this, precaudal and caudal vertebral counts evolve independently, indicating a decoupling between the evolution of identity and morphology. Whole-body elongation is significantly associated with coordinated changes in vertebral and rib morphology, including proportional increases in centrum size, posterior displacement of neural and haemal spines, and increased rib curvature. In contrast, centrum elongation and intervertebral spacing do not independently explain body elongation beyond vertebral counts. These results demonstrate that body elongation in cichlids necessitates integrated, multivariate changes in axial morphology. Our findings highlight the importance of morphological integration in facilitating coordinated evolutionary responses in anatomical systems.

Understanding how ecological interactions among species influence adaptation and population persistence in the face of environmental change is one of the greatest challenges for modern ecology and evolution, with important implications for conservation and other applied fields. As a ubiquitous interaction with potentially strong demographic and selective effects, predation is likely to alter how prey respond to a changing environment. However, whether and how adaptation in prey depends on the way selection operates on predators remains little understood. We investigate this question by combining the theory of adaptive tracking of a moving optimum with trait-matching predator-prey coevolution. We first show that, when coevolutionary processes emerge explicitly from interactions at the individual level, prey maladaptation in any environment does not increase linearly with the difference between the optimum phenotypes for predators and for prey, contrary to the predictions from most earlier coevolutionary models. Furthermore in a fluctuating environment, whether and how the predator evolves crucially affects how well the prey are able to track the moving optimum. Adaptive tracking in prey is facilitated when predators track the same optimum, but hampered when predators are selected towards a fixed optimum. When eco-evolutionary dynamics can occur, phenotypically mismatched predators have a reduced population size that decreases the strength of predatory selection and the intensity of coevolution, but the qualitative influence of predators on prey adaptation remains otherwise similar. Our findings highlight the importance of the evolutionary context of predators for their impacts on prey, and challenge conservation strategies based on predatory attenuation to benefit the prey. Significance statementSpecies in the wild face the dual challenge of adapting to changes in their physical environment and coping with detrimental interactions with other species, such as predators. While evolution by natural selection may jointly overcome both these challenges, the outcome of this process depends on how predator-prey coevolution interacts with environmental adaptation. Here, we show that the influence of coevolving predators on prey adaptation to a changing environment strongly depends on the selective scenario for the predators. Adaptation in prey is facilitated if selective predators also track the changing environment, but hampered if predators are selected towards a constant optimum phenotype, or cannot evolve. Our results challenge the relevance of predator removal as a conservation strategy for prey species.

Cephalo-pelvic disproportion in humans has traditionally been interpreted through the obstetrical dilemma framework, assuming a trade-off between bipedal locomotion and childbirth. However, cephalo-pelvic covariation and pelvic sexual dimorphism might be common adaptations to parturition among mammals. We use a controlled hybridization model in mice to test whether cephalo-pelvic covariation and pelvic sexual dimorphism are population-specific, genetically structured, and sensitive to hybridization. We analyzed skull-pelvis variation and covariation, as well as sexual dimorphism of pelvic morphology across four divergent wild-derived mouse strains and their hybrids. Hybridization induced consistent cranial and pelvic size enlargement. Females exhibited significant cephalo-pelvic shape covariation, characterized by an association between rounder, wider birth canals and larger neurocrania, consistent with functional integration under obstetric selection. Hybrids showed disrupted size covariation, increased pelvis shape variance, and reduced cephalo-pelvic integration. Pelvic sexual dimorphism was systematically reduced in hybrids. Cephalo-pelvic covariation and pelvic sexual dimorphism are not exclusive to bipedal or encephalized species. They likely reflect widespread selection on birth canal morphology in mammals and have a complex genetic basis sensitive to hybridization. These findings weaken a human-exclusive interpretation of the obstetrical dilemma and highlight genetic introgression as an understudied factor shaping cephalo-pelvic integration and disproportion risk in mammals, including humans.

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.

In modular organisms, where growth and fragmentation blur the boundaries between individuals, the interplay between asexual and sexual reproduction creates complex fitness trade-offs. Life-history theory predicts that resources allocated to one fitness component necessarily reduce investment in others, yet detecting these trade-offs in wild populations of clonal organisms remains challenging. Phenotypic plasticity can enhance survival, yet its influence on reproductive capacity and life history trade-offs remains poorly understood. Using a fully crossed reciprocal transplant design, we tracked 263 colonies of the branching coral Acropora cervicornis across nine reef sites over 42 months, investigating relationships between fragmentation, morphological plasticity, and the capacity for sexual reproduction. Breakage patterns reflected both environmental and genetic factors. Primary branch breaks created a "double negative" effect--simultaneously more than doubling mortality risk and delaying attainment of a validated reproductive size class by [~]40%. Conversely, higher morphological plasticity in surface area-to-volume ratio accelerated sexual maturation up to 6-fold, counteracting the negative effects of fragmentation. In parallel, a simple demographic model parameterized with published fecundity data estimated that primary breakage reduces expected cumulative reproductive output by [~]58%, a result robust across a wide range of parameter assumptions. These results demonstrate a fundamental reproductive trade-off in which asexual reproduction through fragmentation undermines sexual reproductive potential by reducing colony size. Moreover, our findings reveal that fragmentation susceptibility is broadly heritable and subject to selection, and identify a compensatory mechanism through which plasticity enhances fitness beyond immediate survival.

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.

Coastal marine ecosystems are increasingly threatened by multiple stressors such as ocean acidification and deoxygenation, but how these co-occurring stressors interact is often poorly understood. This is especially true for tropical coral reefs where deoxygenation is an emerging yet understudied threat. Using hypoxia response curves combined with rigorous pH control, we show that acidification alters hypoxia sensitivity and oxyregulation of reef-building corals in a species-specific manner: three species exhibited increased sensitivity to various degrees, while the fourth showed enhanced tolerance. Consequently, acidification pushes critical hypoxia thresholds into oxygen regimes already prevalent on reefs today, potentially driving shifts in community composition and accelerating risks to reef resilience as these stressors intensify in the future. Our findings challenge assumptions of uniform coral vulnerability under multi-faceted climate change, emphasizing the need for trait-based approaches and to account for stressor interactions in predictive models to better anticipate coral reef futures under rapid climate change.