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.

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.

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.

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.

Active sperm attraction is a widespread function of female reproductive fluids (FRF), identified in both internal and external fertilisers. However, it remains unknown whether FRF retains this function in species where gamete encounters are mediated by physical processes. Such systems, where fertilisation occurs within confined or flow-driven microhabitats, may relax selection on chemotactic sperm guidance. Hence, we hypothesised that the sperm attractant properties of FRF may be lost in species with unconventional fertilisation modes. We tested this hypothesis using the bitterling, a small fish that parasitise freshwater mussels. Bitterling deposit sperm and eggs inside the mussel gills and gamete interactions are facilitated by the water current generated by mussel respiration. Using a recently developed sperm selection chamber and the European bitterling, we find that more sperm accumulate in the FRF channel compared to the water control. Moreover, European bitterling sperm showed no preference for conspecific over a distantly related heterospecific FRF. Our results suggest that bitterling FRF resembles that of species with conventional fertilisation modes, implying that it could mediate sperm selection and cryptic female choice. We discuss alternative evolutionary scenarios underlying the persistence of sperm attractant properties of bitterling FRF despite the shift to a physically mediated fertilisation environment.

1.Many group-living mammals and birds groom the fur (or preen the feathers) of their close associates, and this social grooming (or social preening) seems to build and maintain affiliative relationships. Female common vampire bats (Desmodus rotundus) lick each other in ways that appear to be responsive to cues of need, which suggests that this social grooming could be a low-cost form of helping in addition to being a social signal. If social grooming is a form of helping, then vampire bats should preferentially groom others in locations that are difficult to self-groom. We show that social grooming (n = 1586 events) did indeed occur most often on parts of the recipients body where self-grooming (n = 1515 events) was least likely, often in locations where the recipient could not lick itself, like the back of the head. The finding that vampire bats preferentially groom each other in hard-to-reach locations provides further support for the hypothesis that social grooming is a low-cost form of help in vampire bats.

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.

Social living is widely considered a key driver of cognitive evolution, yet individuals within a species and even within the same group can differ substantially in their sociability (i.e., an individuals propensity to form and maintain social bonds), which can ultimately shape the social environment they experience by influencing how they interact with, respond to, and engage in it. How such individual variation in this personality trait affects social cognition, however, remains poorly understood. To address this question, we used two selectively bred lines of Japanese quail (Coturnix japonica) that consistently differ in social motivation, a key component of sociability, which we used as a proxy for this broader trait. In these lines, S+ individuals show high social motivation, whereas S- individuals show low social motivation. We compared their sociocognitive performance across three tasks: a gaze following task, a social buffering task, and a social discrimination learning task. Our findings revealed that Japanese quail reliably followed the gaze of conspecifics, providing the first evidence of this ability in this species. However, there was no difference between lines, suggesting that basic gaze following into the distance is independent of social motivation. In contrast, line differences emerged in the other tasks. S+ quail were more sensitive and less adaptable in response to environmental changes, particularly under social isolation, although the presence of a conspecific strongly buffered these effects. S- quail, on the other hand, outperformed S+ individuals in the social discrimination learning task, rapidly exploiting available social cues to guide foraging decisions. Overall, this study demonstrates that social motivation modulates sociocognitive performance in a context-dependent manner. Rather than conferring a general cognitive advantage, divergent selection on social motivation leads to different strategies of social information use across tasks and contexts, highlighting the complex interplay between personality, social environment, and cognition.

Urbanization is a major driver of global environmental change, yet the evolutionary consequences for natural populations remain poorly understood. The cabbage white butterfly, Pieris rapae, is one of few butterfly species that thrives in cities, offering a unique opportunity to investigate whether urbanization drives parallel phenotypic evolution. In this study, we quantified phenotypic divergence between urban and non-urban populations across three independent metropolitan regions (Cleveland, Philadelphia, and Pittsburgh, U.S.), measuring body size, flight morphology, and wing pigmentation and reflectance in >500 field-caught individuals from 19 sites. Across regions, we found repeated reductions in overall body size and relative thorax mass in urban butterflies of both sexes, along with reduced relative forewing area in urban males, suggesting sex-specific impacts on mobility. Wing pigmentation showed limited urban-associated variation, but we detected novel sexual dimorphism in near-infrared reflectance within urban populations. Together, these results demonstrate repeatable divergence between urban and non-urban butterfly populations across multiple trait axes and suggest that plastic responses to urban stressors previously documented in experimental work manifest as consistent phenotypic shifts in natural populations.

AO_SCPLOWBSTRACTC_SCPLOWAdaptation to extreme environments is commonly assumed to occur through microevolutionary change. However, studies of high-altitude human populations show that organisms can also respond to nutritional stress through developmental plasticity, producing thrifty phenotypes that prioritize essential function over costly structures. Whether this adaptive strategy extends beyond humans, and how it operates in natural systems, remains largely unexplored. Here, we test the thrifty phenotype hypothesis (TPH) in a widely distributed superorganism, the carpenter ant Camponotus herculeanus, which inhabits some of the most environmentally challenging regions of the Northern Hemisphere. Colonies comprise inexpensive minor workers and energetically costly major workers, providing a powerful system for examining plastic investment under resource limitation. We quantified relationships between caste structure and climate and conducted a common-garden experiment to test the TPH. We show that the proportion of major workers declines with increasing latitude, independently of body size and colony size, and is best predicted by the number of days, annually, during which workers can nurse brood. Experimental results further demonstrate that colonies rapidly and plastically adjust caste structure in response to environmental conditions. Our findings reveal that thrifty phenotypes can emerge in superorganisms and could represent a conserved developmental response to environmental stress. By extending a central hypothesis from human biology to social insects, this work provides a unifying framework for understanding how developmental plasticity shapes adaptation across levels of biological organization.

Human life expectancy has jumped by several decades in the last century, but the healthspan has not followed suit. The ageing population has come with an increased prevalence of neurodegenerative disease, and insects have proven to be valuable models of these conditions and their associated cognitive decline. The Heliconius butterfly genus is an emerging system in insect cognition, having recently evolved a significant expansion in neural centres of learning and memory, alongside enhanced stability of visual long-term memory in comparison with their close relatives in the Heliconiini tribe. This is linked to the cognitive demands imposed by Heliconius spatially-faithful foraging behaviour for a protein-rich diet of pollen, and co-occurs with a dramatic lifespan extension in this genus over the other Heliconiini outgroups. Here, we investigate whether the Heliconius cognitive healthspan is similarly discrepant, or if any cognitive decline is instead delayed in accordance with their lifespan extension. We first report evidence that investment in learning and memory circuits co-evolves with Heliconiini lifespan. We then conduct learning and memory assays across the lifespans of a representative longer-lived Heliconius, H. hecale, and the shorter-lived Heliconiini outgroup, Dryas iulia. Across both species, and particularly in H. hecale, we find evidence for cognitive robustness in late life, in contrast to evidence for widespread cognitive declines in insects. Our results add a new taxonomic order to the study of age-related memory impairment, and suggest Heliconius as a valuable model system for mechanistic studies of the maintenance of neurological health in the context of extended life.

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

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.

O_LIPhenological shifts are a major ecological consequence of climate change, yet studies often focus on single life stages meaning that the potential for carryover effects between life stages remains poorly understood. Failing to account for these effects may lead to inaccurate estimates of phenological shifts, with consequences for predicted synchrony among interacting species. This is especially relevant for temperate systems where climate warming is occurring unevenly across the year. C_LIO_LIHere, we investigated how temperature experienced the previous autumn and winter (during the pupal and egg stage) influences spring phenology in the winter moth (Operophtera brumata), a herbivorous insect with distinct life stages. Using 50 years of local climate data to create five experimental temperature regimes, we first quantified phenotypic plasticity in the duration and temporal variability of pupal and egg development. We then examined how timing of adult moth emergence affects timing of offspring hatching. C_LIO_LIWe found divergent effects of temperature on different life stages; pupal development time was shortest at intermediate temperatures while egg development time decreased linearly with increasing temperature. Furthermore, phenological shifts due to the conditions experienced by the mother were carried over to influence the phenology of her offspring. While this carryover effect was partially compensated during subsequent stages, compensation decreased under warming conditions. C_LIO_LIThese results refine our understanding of the sensitivity of the annual cycle of winter moth phenology to variation in temperature with potential implications for population dynamics and interspecific interactions. Overall, our findings highlight the need to consider the impacts of warming across multiple life stages so that carryover effects can be properly accounted for. Doing so will improve predictions of phenological shifts under future climates. C_LI

Many vertebrates exhibit colourful ornaments generated by carotenoid pigments that presumably evolve as signals under sexual selection. To function as sexual signals, carotenoid-based coloured ornaments should accurately reveal an individuals quality, commonly defined as fitness potential, which includes the ability to survive. We performed a meta-analysis for testing the association between the expression level of carotenoid-based ornaments and longevity estimates (annual survival or lifespan) in birds, the taxon with the largest body of evidence. We detected a significant positive correlation in males but not in females. This result contrasts with recent meta-analytic work showing a positive association between carotenoid-based coloured traits and avian fecundity in both sexes. The link to survival was consistent among colourations produced by enzymatically transformed pigments (mostly red ketocarotenoids) and those based on dietary yellow carotenoids. The latter suggests that the association with survival holds across the physiological mechanisms involved in the production of these ornaments. In summary, our study reveals sex-specific selection in the evolution of carotenoid-based ornaments.

Just as sexually antagonistic genetic variants have different effects on male and female fitness, environmental conditions too can have sexually antagonistic fitness effects. Such Charnov-Bull effects have been invoked to explain the origin and persistence of environmental sex determination (ESD), which allows development of each sex in the environments in which it has a comparative advantage. Here, we study different forms of Charnov-Bull effects to characterize how they shape the evolution and stability of ESD. We show that the precise functional form of Charnov-Bull effects can generate large differences in the vulnerability of ESD systems to the invasion of sex-biasing alleles, as well as in the fate of those alleles if they invade. For some configurations of Charnov-Bull effects, strong sex-biasing alleles are likely to spread to intermediate frequencies, rather than to fixation, resulting in mixed ESD systems in which large genetic effects segregate. Overall, our results indicate that the precise nature of Charnov-Bull effects can play a crucial role in the evolutionary dynamics of ESD.

Males during mating never transfer just sperm; to the best of our knowledge, they always deliver a rich seminal fluid as well. The proteins in the seminal fluid have an important sperm supporting role, but they also cause changes in the female physiology and can impose a mating cost. The associated costs and delay in the time of remating, lead to the view that those proteins evolved primarily due to sexual conflict and delay female remating beyond the optimal rate. To examine the role of seminal fluid proteins in sexual conflict we use a mathematical model of reproductive physiology, informed by the accumulated knowledge on Drosophila melanogaster. In accordance with the theory, we find that males always benefit from inducing longer remating intervals in females. But, we also find that this conflict is reduced when female reproduction is regulated by the male proteins. Without seminal fluid proteins females have a single, well-defined, optimal remating rate. However, when seminal proteins are used to regulate females reproduction, females can reach the same offspring production for a range of mating intervals. This wider range of possible remating times could provide females with a buffer against uncertain mating opportunity. It could also allow females to be more selective on male quality, by reducing the cost associated with delaying remating. Our results suggest that, while there is a conflict over the remating rate, seminal fluid proteins reduce its intensity, highlighting their role in aligning the interests of both sexes.