Proceedings of the Royal Society B: Biological Sciences

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.

Helminths are widespread parasites that can modulate host immunity, potentially increasing susceptibility to viral infections. However, evidence for these effects varies across systems and environments, and links between laboratory and wild populations remain unclear. We developed a tractable system using wood mice, Heligmosomoides spp. nematodes, and wood mouse herpes virus (WMHV) to bridge this gap. Combining laboratory and field experiments with population modelling, we examined how helminth infection, anthelmintic treatment and diet affect viral dynamics. Across lab and field data, helminth infection consistently increased WMHV risk, with stronger effects at higher worm burdens. Field results showed that anthelmintic treatment reduced viral infection, and laboratory experiments showed that improved nutrition mitigates helminth-induced increases in viral susceptibility. Our population-level modelling suggested that helminth burden-dependent facilitation can generate nonlinear effects on viral spread, dependent on helminth virulence. Our findings highlight the potential importance of helminths as facilitators of viral infections, and suggest that anthelmintic treatment may provide indirect benefits for viral control. We also show the value of integrating lab and field approaches on the same (or closely related) species, in particular the potential offered by the wood mouse - Heligmosomoides - WMHV system, to understand the drivers and consequences of host-helminth-viral interactions.

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.

Eusocial insects fascinate researchers with their sophisticated communication systems and sensory specialisations. Ants and termites have coexisted in a long-standing predator-prey arms race, offering insight into the interplay between ecology and evolution. The subterranean termite Coptotermes acinaciformis can detect the predatory ant Iridomyrmex purpureus through footstep-induced vibrations, triggering defensive responses. Ants produce noisier walking signatures than termites, while the inquiline termite Macrognathotermes sunteri walks more quietly than its host, suggesting species-specific vibroacoustic strategies. Using statistical analysis of video-tracked motion and footstep vibrations in confined arenas across six ant and ten termite species, we show that C. acinaciformis, despite its body size, moves more smoothly than ants, which alternate between directed and erratic paths. Inquiline termites, by contrast, displayed erratic movements. Ants consistently produced stronger vibrations closely linked to body mass, while Highly Comparative Time Series Analysis revealed termite motions approaching chaotic dynamics. Notably, while C. acinaciformis and I. purpureus produced distinct vibrational signatures, M. sunteri s signals overlapped with its host, consistent with vibroacoustic mimicry. Although the ecological nature of this association remains unresolved, our findings underscore the central role of vibrational cues in shaping interspecific dynamics and highlight vibroacoustic communication as an underappreciated driver of social insect ecology and evolution.

Understanding the fitness advantages conferred by eusociality remains a central challenge in behavioral ecology. One promising approach is to identify collective strategies that shift efficiency within social groups. Here, we test the hypothesis that reserve workforces in eusocial insect colonies represent an adaptive mechanism that enhances flexibility and foraging efficiency under fluctuating environmental conditions. We examine how such reserve workers modulate the departure and return rates of foragers and how these time-dependent dynamics shape the colonys overall energetic balance. By integrating an energetic-balance framework with stochastic search simulations inspired by empirical results from Aphaenogaster senilis, we quantify the energetic requirements for colony viability, incorporating energy intake, search costs, and basal metabolic demands. Our results show that as colonies grow, maintaining a positive energy balance requires a disproportionately larger relative workforce. By modulating departure and return rates over time, colonies control the synchrony of their collective search and efficiently activate or suppress their reserve workforce to scale foraging effort as needed. These findings suggest that the "lazy" or weakly engaged workers commonly observed in large colonies function as an essential reserve that stabilizes colony energetics and enhances responsiveness. Together, our results provide a functional explanation for sublinear metabolic scaling in eusocial groups and highlight workforce modulation as a key factor underlying their energetic stability and evolutionary success.

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.

Phenotypic diversity is often thought to arise from the evolutionary modification of developmental processes. However, developmental processes are tightly coupled in space and time, with each process beginning from conditions set by the one before it. While we know from dynamical systems theory that initial conditions can significantly affect a systems out-come, their importance as a source of phenotypic evolvability has been largely overlooked. Here we show for the first time, that phenotypic evolution can proceed through changes in developmental initial conditions while the underlying developmental process remains conserved. Somitogenesis is the process by which vertebral precursors, known as somites, are periodically patterned in the pre-somitic mesoderm (PSM). Somitic count (total number of somites) is thought to diversify through the evolution of components of somitogenesis such as the tempo of the segmentation clock or the mechanisms driving axial morphogenesis. Using two closely related species of Lake Malawi cichlid fishes that differ in vertebral counts, we show that somite count evolution has happened without changes to somitogenesis itself, but instead, by altering the size of the PSM at the onset of this process. This work will expand what we consider developmental drivers of phenotypic evolution and highlight the importance of comparative studies to understand the diversification of phenotypes.

Within species, individuals of the same age can differ in size. Previously, parental genetics, nutrition, space, and social interactions have been suggested to explain different growth rates. However, direct effects of larger individuals on the physiology and growth of smaller individuals are poorly understood. In this study, we investigated how larger individuals of the marine worm Platynereis dumerilii can impact the growth of smaller conspecifics. Comparing growth distributions in communally and individually reared worms, we show that larger worms suppress the growth of smaller ones. Furthermore, we were able to demonstrate that this suppression is chemically mediated. The chemical cue does not originate from faeces but is water soluble, stable for several days and smaller than 3 kDa. Our findings highlight the importance of non-reproduction related chemical signalling, showing evidence that dominant individuals can chemically suppress the growth of their conspecifics. This study provides new insights into how hierarchy can be established and maintained in a population and is particularly relevant for the growing community studying this model species.

Usutu virus (USUV) is a mosquito-borne flavivirus that has recently expanded northwards in Europe and become endemic in the UK [1-3]. USUV emergence often precedes the closely related West Nile virus (WNV), potentially reflecting differences in epidemiological parameters [4, 5]. One key parameter is the extrinsic incubation period (EIP), the time required for a mosquito to become infectious following an infected blood meal. Here we present the first ever estimate of the temperature-dependent EIP for USUV in the vector Culex pipiens molestus. We were able to quantify the shortening of the EIP with temperature by re-analysing published laboratory data with bespoke Bayesian model that accounted for key features of the experimental design. Under typical UK summer temperatures, the median EIP (EIP50) of USUV is shorter than that of WNV, and the potential transmission season of USUV is both longer and geographically more extensive. Under RCP8.5 climate projections, WNV transmission suitability is expected to match or exceed current USUV levels between 2055 and 2065, highlighting the future threat to the UK from emerging mosquito-borne pathogens. Our findings support USUV as a precursor for WNV in northern Europe and provide a robust characterisation of a key epidemiological parameter of USUV, enabling accurate modelling of its transmission dynamics.

Plastic pollution represents a major contemporary threat to aquatic ecosystems, with well-documented consequences for organismal performance and fitness across numerous taxa, including fishes. Importantly, plastic-derived stress does not occur in isolation, but interacts with other anthropogenic pressures such as size-selective harvesting, which can impose strong directional selection on life-history and behavioural traits. In this study, we exposed three experimentally evolved selection lines: large-harvested, small-harvested, and randomly harvested to microplastic contamination and quantified effects on growth and behaviour over a 14-day period. Microplastic exposure reduced boldness and exploratory activity while simultaneously increasing feeding probability and feeding frequency. Prior size-selective harvesting influenced only exploratory behaviour, suggesting that most behavioural responses to microplastics are robust to previous evolutionary history. We detected no effect of microplastics on growth, potentially due to compensatory increases in feeding behaviour. Collectively, these findings demonstrate that microplastic exposure alters key behavioural traits across genetically divergent fish lines and contribute to a broader understanding of how multiple anthropogenic stressors may interact to shape population dynamics in rapidly changing environments.

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.

Global warming is known to increase arboviral disease risk by enabling the expansion of tropical vectors such as Aedes aegypti and Aedes albopictus. However, whether climate-driven shifts in seasonal dynamics within temperate regions, such as warmer springs and shorter winters, create thermal settings favourable for additional vectors, which can reshape disease risk maps, is poorly understood. To answer this question, we used the invasive temperate mosquito species Aedes koreicus and tested its thermal developmental resilience, along with its vector competence for dengue and chikungunya viruses. We observed significant phenotypic variation in thermal tolerance across life stages, which translates into distinct thermal performance curves for life-history traits, ultimately shaping overall mosquito fitness. We further found that temperature effects are virus-specific, with differential impacts on infection and transmission between dengue and chikungunya viruses. These stage- and pathogen-specific responses generate carry-over effects across life stages, indicating that thermal responses may be constrained by life-history trade-offs rather than be defined by a single thermal optimum. Our results highlight the need to move beyond static, species-based risk assessments toward mechanistic frameworks that integrate thermal biology across life stages and vector-pathogen systems. As climate change increasingly reshapes seasonal structure rather than simply elevating mean temperatures, cold-adapted and temperate vectors such as Ae. koreicus, provide critical model systems to understand how transmission risk emerges outside mosquito classical thermal optima, calling for a broader paradigm shift in how global change and vector-borne disease risk are conceptualised.

Permanent workers in social insects, who forgo reproduction to help others, are a defining feature of superorganisms and a major evolutionary transition. Most theories assume that helping in the natal nests is inherently mutually exclusive from dispersal to found a new colony. This assumption holds for many adult societies whose workers cannot molt and change castes (e.g., Hymenoptera), but not for juvenile societies whose workers may differentiate and disperse after a period of helping (e.g., termites). The evolutionary advantage of permanent workers remains unknown in such juvenile societies with developmental flexibility. Here we develop a demographic model in which individuals can disperse either before or after a period of helping, capturing reversible helpers and permanent workers in termites. We found that permanent workers are favored when colony growth is divided into distinct ergonomic and reproductive phases, even if their performance is the same as that of reversible helpers. Without this phase separation, there is no selective advantage for workers to lose dispersal for colony foundation. After the phase separation, on the other hand, permanent workers increase continuous demographic growth and evolve through kin selection. By mapping diverse termite social systems onto a continuous landscape of ontogeny, the model traces a pathway linking different social forms. These results generalize social evolution theory beyond adult-worker systems by providing a demographic mechanism that favors the loss of the reproductive option.

Batesian mimicry is a defensive adaptation where predators learn to avoid aposematic prey and generalize their warning signals to phenotypically similar mimics. The phenotypic accuracy needed for mimics to benefit from this adaptation depends on the relative densities of models and mimics and the models unpalatability. As aposematic models become more unpalatable or more common relative to their mimics, warning signals become stronger, allowing even poor mimics to benefit. However, few studies have disentangled the importance of relative frequencies of models and mimics from absolute density of the prey community (both models and mimics) in driving relaxed selection on imperfect mimics. Here, we test the hypothesis that increasing model unpalatability and absolute prey community density accelerates predator avoidance learning and enhances protection for imperfect mimics. Using replicas of the model Adelpha iphiclus (Linnaeus), its imperfect mimic Adelpha serpa (Boisduval), and the palatable control Junonia evarete (Cramer), we conducted field experiments that enhanced model unpalatability and doubled absolute prey density while maintaining a constant ratio of model, mimic, and control phenotypes. We found that enhanced model unpalatability and increased absolute density significantly reduced predation on all species, highlighting absolute community density as an underappreciated mechanism shaping selection on imperfect Batesian mimics.

How morphology forms during development and changes during evolution remain major questions in biology. In vertebrates, teeth have long served as model systems to address these questions. In threespine stickleback fish (Gasterosteus aculeatus), repeated and convergent increases in pharyngeal tooth number in derived freshwater sticklebacks occur, suggesting increased tooth number is adaptive in freshwater environments, likely due to a diet of larger prey in freshwater. Whether changes in oral tooth patterning also occur in freshwater sticklebacks was unknown. Here we describe oral tooth number and patterning in a dense developmental time course of lab-reared ancestral marine and derived freshwater fish. We address three major questions. First, is the spatial sequence of early oral tooth formation invariant as we previously described for the pharyngeal dentition? Second, is oral tooth patterning in the upper and lower jaw sexually dimorphic, and if so, when during development does this dimorphism arise? Third, have freshwater fish evolved increases in oral tooth number? We find that (1) unlike the pharyngeal dentition, the oral jaw early spatial sequence is variable, especially in the lower jaw (2) sexual dimorphism in both oral jaws arises at the late juvenile stage with males having more teeth and (3) freshwater fish have evolved more oral teeth similar to the evolved tooth gain in the pharyngeal jaw. Together our morphological descriptions advance the stickleback oral jaw as a model system to study how morphology forms during development and evolves in nature.

Research on stochastic phenotypic variation (i.e., variation arising despite the apparent absence of genetic and environmental differences) has recently emerged as a rapidly growing area in biological research. But despite growing recognition of both its existence and fitness relevance, it remains unknown whether and to what extent such stochastically induced variation is transmitted across generations, potentially making it an unrecognized contributor to evolutionary processes and the adaptive potential of populations. In order to address this knowledge gap, we here performed a two-generation behavioral screening with a naturally clonal fish: 34 genetically identical mothers and their 232 offspring were separated directly after birth into near-identical environments and tracked continuously at high resolution, constituting a total of [~]19,000 observation hours. We find that consistent among-individual differences in behavioral profiles (i.e., activity and feeding patterns) of both mothers and offspring emerged despite the absence of apparent genetic and environmental differences. Mother feeding behavior - but not mother activity - was positively associated with offspring activity: mothers that spent more time feeding produced more active offspring, explaining [~] 33 % of the total variation in offspring activity. This link between mother and offspring behavior was not mediated by mother size or offspring size at parturition. Our study provides first evidence for the non-genetic transmission of among-individual phenotypic differences that arise despite the apparent lack of genetic or environmental variation, highlighting the potential importance of this variation for evolutionary processes and the adaptability of populations.

In the search for universals shaping acoustic communication across species, we increasingly look for patterns known from human languages and music in non-human animals. These parallels are often explored separately and with limited ecological context. Here, we take a deep dive into the temporal structure of a complex call used by the little auk (Alle alle), a pelagic seabird with elaborate vocal behaviour and socially complex colonial life. Based on syllable durations, intervals and silences, we examine its conformance to linguistic laws, rhythmic structure and information content. This reveals intricate problems of temporal organisation: while the calls conform not only to linguistic laws of brevity but also to the initial and final lengthening known from human prosody, these effects interact with the internal structure of the call and information carried within it. To our knowledge, this is the first time that conformance to multiple linguistic laws, exceeding simple vocal efficiency, has been described for a non-human, non-vocal learning animal. The calls rhythmic structure shows a progressive rallentando -- a systematic slowing driven by changes in syllable and silence durations and the intervals between syllable onsets. The exact patterns of this rallentando are indicative of the callers sex and individually specific. These results reveal how seabird communication is shaped not only by efficiency universals, but also the specific pressures of colonial life. Our work highlights the temporal structure as an important axis of communication evolution, but also serves as a reminder to consider the species ecological reality and the function, not only presence, of temporal organisation. O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=127 SRC="FIGDIR/small/713940v1_ufig1.gif" ALT="Figure 1"> View larger version (38K): org.highwire.dtl.DTLVardef@13de3a8org.highwire.dtl.DTLVardef@2d64adorg.highwire.dtl.DTLVardef@2ca53aorg.highwire.dtl.DTLVardef@113c38d_HPS_FORMAT_FIGEXP M_FIG C_FIG

Natural populations are often nonlinear and exhibit substantial variability. A central question is how stochasticity interacts with density-dependent regulation to shape population stability. We address this using four long-term time series of Trinidadian guppies and find that their dynamics are well described by a stochastic logistic model with multiplicative environmental noise. The model predicts that stochasticity does not merely add fluctuations around deterministic carrying capacity, but alters the equilibrium structure. Using stochastic bifurcation theory, we show that increasing noise shifts the most-probable population size below the deterministic equilibrium and can push populations closer to a noise-induced bifurcation, even when mean growth rates remain positive. The effects of stochasticity across populations align with known ecological differences among streams, particularly the effects of light level and seasonality. The analysis also identifies populations most sensitive to perturbations, which are not detected by standard early warning indicators. Temporal and spectral analyses further show that intrinsic growth rate governs local recovery, while seasonal variation interacts with density-dependence to shape longer-term population fluctuations. Together, our results show that stochasticity can alter resilience and vulnerability by reshaping ecological stability landscapes.

Biotic interactions can drive evolutionary diversification, but the underlying mechanisms differ depending on the type of interaction. For instance, Ehrlich and Ravens escape-and-radiate coevolution provides a pathway of diversification in antagonistic interactions, whereas in mutualistic networks, coevolution is hypothesized to result in trait convergence rather than diversification. The combined effect of mutualism and antagonism on diversification remains unclear, even though organisms naturally engage in multiple types of interactions simultaneously. Using an eco-evolutionary simulation model, we investigate diversification in tripartite ecological networks such as plant-pollinator-herbivore networks. We find that diversification patterns vary according to the way mutualism and antagonism are connected on the trait level. If the two interactions are governed by uncorrelated plant traits, we observe little diversification in the mutualistic and substantial diversification in the antagonistic subnetwork. By contrast, if the same plant trait mediates both mutualism and antagonism (an example of ecological pleiotropy), diversification rates in all guilds become interdependent. In this case, even the mutualistic guild diversifies considerably when antagonism is strong, while strong mutualism restricts diversification also in the antagonistic guild. Our study underlines that the inclusion of multiple interaction types is necessary to advance our understanding of evolutionary dynamics in ecological networks.