Proceedings of the Royal Society B: Biological Sciences

Humans and other animals live in interconnected social communities that are essential for survival and well-being. In principle, social communities can persist despite changes in constituent members. However, gradually accumulating changes to membership could push systems past critical thresholds into alternate states. We investigated social network dynamics for 443 wild female Asian elephants over 12 years by tracking community membership and structure. Following accumulated demographic turnover, networks fractured into smaller and more isolated social communities. Connections were changed not only due to turnover of members but also rewired among remaining individuals. This provides the first empirical evidence of a social network state change in a long-lived mammal.

Multifunctional anatomical structures must accommodate potentially competing performance demands, leading to functional tradeoffs. The mammal rostrum (snout) is involved in multiple functions, including feeding, respiratory conditioning, olfaction, and, in most bats, echolocation. Therefore, it serves as an ideal system to investigate whether and how functional tradeoffs promote or constrain morphological diversification. While the external morphology of the rostrum has been linked with mechanical demands of feeding in bats, the factors and processes influencing its internal morphology, including the turbinals in the nasal cavity, remain comparatively unexplored. Here we investigate how internal rostral morphology reflects specialization and tradeoffs among respiratory air conditioning, echolocation, and olfaction by quantifying turbinal morphological diversity in a phylogenetically and ecologically diverse sample of bat species. We find that echolocation mode predominantly influences both the ethmoturbinal complex (ETc) and maxilloturbinal (MT) systems, with nasal-emitting bats having reduced and less complex turbinals compared to oral and non-laryngeally echolocating bat species. MT complexity and surface area are not associated with bioclimatic variables representing thermal variability and aridity. However, the ETc exhibits higher complexity in plantivorous bats than faunivorous bats, suggesting higher olfactory reliance. While MT morphological disparity was predominantly explained by echolocation mode, ETc morphological disparity was associated with both echolocation mode and diet, suggesting potentially opposing demands favoring turbinal reduction for sound transmission and elaboration for olfaction. Among nasal emitters, which must accommodate both demands within the nasal cavity, ETc complexity exhibited higher relative disparity compared to MT complexity. These patterns suggest that competing functional demands may promote or maintain morphological diversity, possibly through ecological specialization and/or many-to-one mapping between morphology and performance.

The most studied symbiosis between land vertebrates and algae, is the one between Ambystoma maculatum and Oophila amblystomatis, where the latter colonizes the amphibian''s eggs. Although clear benefit given by algal growth for the salamander embryo has been observed, mutualism is not widely accepted. Mutualistic hypotheses posit benefits from the host to the algae which include protection, N- and C-sources, but no experimental evidence has been obtained. In fact, recent studies suggest that the algae are stressed during this relationship and propose fermentation rather than photosynthesis as main driver for algal growth. In this work, we analyzed embryonic host developmental rate, algal and embryo growth and photosynthetic function of eggs housed at different light intensities. We provide evidence that photosynthetic growth is the main driver for Oophila and that higher algal growth yields faster developmental rate and embryo size. Also, we provide strong evidence that rates of photosynthetic electron transport (and the concomitant O2 evolution) must be higher than those of consumption by the embryo for this symbiosis to be mutualistic. Since photosynthetic rate is dependent on light, this work illustrates the importance of light intensity in this symbiotic relationship.

Ecosystem engineers are ecological niche constructors: by modifying local environments, they alter the conditions under which organisms establish, persist and interact. Although niche construction is often framed as a population-level evolutionary feedback, it could also operate at the assemblage level when communities collectively shape their environments and filter future recruitment. Reef-building corals provide a perfect system to test this idea because adult colonies form three-dimensional carbonate structures that can persist after colony death, creating an inherited habitat for subsequent coral generations. Here, we tested whether coral recruitment to the juvenile stage was associated with local adult coral abundance, reef structure, and larval settlement supply. Combining spatially explicit coral censuses, photogrammetric reef digital elevation models and data from settlement tiles across 15 reef sites at two time points at Jiigurru, Great Barrier Reef, we found that juvenile abundance increased additively on the log scale with adult abundance and with fractal dimension, a metric of fine-scale structural complexity. Surface rugosity had weaker effects, and interactions between adult abundance and habitat structure were limited, indicating largely additive, rather than synergistic or antagonistic, effects. Our results show that both adult assemblages and the concurrent structural complexity, consistent with assemblage-level niche construction and ecological inheritance theory, shape coral recruitment.

This study addresses the functional diversity of wild Limnospira platensis strains from two continents. Wild strains retain regulatory and metabolic flexibility often lost during domestication, making them essential for exploring natural adaptation within the species evolutionary history. We investigated the comparative growth performance of five Limnospira strains under controlled temperature and light regimes to identify phenotypic differences attributable to single environmental variables. We then evaluated their biochemical and biophysical responses under naturally fluctuating light conditions, linking energy use strategies to phylogenetic relationships. Our analyses reveal that while certain traits, such as fine-tuning of photosynthetic reactions, are shared among closely related strains, overall growth performance is highly variable even within phylogenetically similar groups. For example, photosensitive strains (e.g., UTEX 3086) differ markedly from high light tolerant strains (e.g., UTEX LB 2342) in their mechanisms of coping with light stress. Together, these comparative analyses highlight how environmental sensitivity and energy-use strategies vary across strains of the same species, reflecting broader patterns of diversification within Limnospira.

Global warming will impact natural selection on plant traits and their plasticity by influencing phenotypes, biotic interactions, and fitness. Because warming affects biotic interactions, community composition may influence how warming affects selection on plants, but this is little studied. We grew full-sibling pairs of Brassica rapa plants in an ambient and hot temperature environment and exposed them to visitation by a pollinator (Bombus terrestris), a pollinating herbivore (Pieris rapae), or their combination. We recorded plant phenotypes, insect visitation, herbivory, and plant fitness. We used these to calculated phenotypic selection on plant traits and their plasticity, including additive and nonadditive effects. Elevated temperature changed selection on traits related to pollinator attraction, such as flower number, nectar production, and floral scent emission. We found both positive and negative selection on temperature-mediated trait plasticity depending on the biotic treatment. Elevated temperature changed patterns of additive and non-additive selection on a variety of traits including flower morphology and scent. This study shows that elevated temperatures can reshape patterns of phenotypic selection, including nonadditive effects, and plastic trait expression. Effects of elevated temperature on phenotypic selection depended on the biotic interactors, highlighting the importance of community context for the effects of warming on natural selection.

The toxicity of chemical defences is well studied, but the potential contribution of compound structure to predator deterrence remains largely unexplored. Whether predation acts more strongly on toxicity or unpalatability remains largely untested, partly because few systems allow toxin structure to vary independently of quantity. Heliconius sara larvae provide such a system: those reared on Passiflora auriculata sequester cyclopentenyl cyanogenic glucosides (CGs), while those reared on P. biflora biosynthesise comparable quantities of aliphatic CGs. Using two invertebrate predators, Camponotus floridanus ants and Hierodula membranacea mantids, we tested whether this structural difference affects palatability independent of toxicity. Mantids rejected larvae with cyclopentenyl CGs more often than larvae with aliphatic CGs, despite no detectable difference in total CG content. This pattern was mirrored in extract-based assays with ants, independently of cyanide release: extracts with cyclopentenyl CGs remained deterrent, while extracts with aliphatic CGs did not differ in deterrence from water. Live larvae, by contrast, elicited similar responses from ants regardless of CG structure. These results show that variation in toxin structure can strongly affect palatability, with some compounds conferring greater protection than others. This demonstrates the importance of chemical structural diversity in the evolution of chemical defences.

Disturbances alter ecosystem resilience by killing organisms and leaving behind material legacies. We tested how material legacies from marine heat waves and cyclones govern transitions between coral- and seaweed-rich states on tropical reefs. Heat waves kill coral tissue but leave their skeletons to erode gradually, whereas cyclones scour away emergent biota. Field experiments revealed that dead skeletons protect seaweeds from herbivory, catalyzing a transition to a seaweed-rich state that becomes self-sustaining after skeletons disappear. After four years, 73% of skeleton-added (heat wave) plots transitioned to seaweeds compared to 0% of scoured (cyclone) plots that lacked skeletons, while 87% of seaweed-rich plots scoured to simulate a cyclone stayed seaweed-free. Reef trajectories after natural disturbances were similar: four years after heat wave-induced coral mortality, 63% of time-series plots had transitioned to seaweeds with none recovering to coral; four years after a cyclone removed skeletons from a prior disturbance, none had transitioned to seaweeds and 60% had returned to coral. A disturbance not only can displace an ecosystem state, it can rapidly reshape the resilience landscape through the material legacies it creates or removes. Our findings also show that successive disturbances need not have cumulative negative effects: after a reef is driven into a seaweed-rich state, a cyclone can act as a rescue disturbance by removing established seaweeds and, when structural refugia are also removed, shrinking the seaweed stability domain. By reshaping resilience through contrasting material legacies, disturbance type and sequence can be as important as frequency and severity in determining ecosystem trajectories.

Understanding the evolution of cognition is fundamental to understanding the origins and nature of our own cognitive abilities, with cross-species comparisons providing a cornerstone of this endeavor. Yet, comparative cognition so far has largely focused on endothermic vertebrates, particularly mammals and birds, while ectotherms--representing a substantial proportion of vertebrate diversity--remain relatively understudied. Moreover, variation in experimental methods makes existing data difficult to compare across species. Big-team science offers a way to overcome these limitations by enabling standardized cognitive testing across broad taxonomic scales. Here, we apply this approach to fishes, using inhibitory control as a proof of concept for standardized comparative testing in 444 individuals across 22 teleost species spanning 19 genera. We demonstrate that standardized cognitive testing across such diversity is feasible, while also revealing substantial heterogeneity in the sample. Performance varied markedly among species, but, strikingly, showed only a weak phylogenetic signal, contrasting with patterns previously reported in mammals and birds. In addition, we detected great within-species variation, including differences across research groups, suggesting that performance may reflect not only species-level evolutionary history but also ontogenetic experience and the capacity to adjust decision rules to local conditions. Together, our findings highlight the importance of both evolutionary and environmental sources of cognitive variation and demonstrate that extending standardized comparative approaches beyond traditionally studied endotherms can reveal a more dynamic and complex picture of cognitive evolution across the vertebrate lineage.

The consequences of maternal effects for offspring fitness can depend on the environmental conditions offspring encounter and the fitness traits considered. We used a transgenerational experiment in Daphnia magna to test how maternal exposure to warming and elevated salinity influenced offspring survival, reproduction and body size across matching, mismatching and multiple-stressor environments. Maternal exposure to salinity enhanced offspring survival under matching salinity, and benefits extended to mismatching environments. In contrast, maternal exposure to warming provided no survival benefit under matching warming and reduced survival in mismatching environments, while accelerating reproduction across contexts. Multiple-stressor conditions revealed pronounced maternal effects, while contrasting responses across survival, reproduction and body size showed that benefits to one fitness trait did not extend to others. Our findings demonstrate that environmental matching alone is insufficient to predict maternal effects, whose consequences depend on offspring environmental complexity and the fitness trait considered.

Rising temperatures linked to global climate change can disrupt the chemical communication that animals rely on for reproduction. Arthropods are particularly vulnerable due to their limited ability for thermoregulation and their reliance on cuticular hydrocarbons (CHCs), which have a dual role in social communication and heat protection. Heat-induced changes in cuticular composition may therefore lead to mate recognition errors. We tested this in the burying beetle Nicrophorus vespilloides, by exposing males to either benign temperatures (20{degrees}C) or a simulated 3-day heatwave (26{degrees}C). We recorded the frequency of same-sex sexual behaviour under these contrasting thermal conditions and examined associated changes in the males' cuticular profiles. Our results show a higher rate of same-sex mounting under heat stress, with the CHCs of heat-stressed males shifting toward more saturated, longer-chained compounds and more female-like compounds. We also found a positive association between chain length and the frequency of same-sex mounting, suggesting a trade-off between the social communication and waterproofing functions of CHCs. Overall, our findings provide evidence for a causal effect of heat on same-sex sexual behaviour, which may be partly explained by changes in cuticular lipids. Such disruption of chemical communication could have major consequences for animal reproduction in a warming world.

Humans coordinate their actions while their bodies and brains synchronize in social interactions, yet how behavioral, physiological, and neural dynamics interact during interpersonal coordination remains largely unknown. We investigated how respiration and individual differences influence behavioral and inter-brain synchrony in a musical synchronization task, which requires precise temporal alignment. Eighty-eight individuals first produced a familiar melody at their most comfortable rate to measure their spontaneous production rate (SPR). They then synchronized the melody with a randomly assigned unfamiliar partner under natural (unpaced), instructed in-phase, and instructed anti-phase breathing conditions, while hyperscanning 64-channel electroencephalography (EEG), respiration, auditory-motor timing, and perceived social connectedness were recorded. Relative to natural respiration, both in-phase and anti-phase breathing increased inter-brain phase-locking and perceived social closeness but reduced behavioral synchrony; the instructed respiratory phase relationship was mirrored in their inter-brain relative phase. Differences in phase of respiratory cycles (inhalation and exhalation) also influenced coordination: Inhalation was associated with stronger inter-brain synchronization but less precise and stable behavioral coordination than was exhalation. Moreover, Individual differences influenced coordination: Partners with the faster SPR consistently preceded the slower partners and exhibited an alpha-band inter-brain phase advance in synchronization, whereas dyads with similar SPR showed greater behavioral synchrony and smaller inter-brain phase difference. Our findings identify respiration as a previously overlooked factor that organizes behavioral and neural synchronization, while individual intrinsic rhythms constrain how interacting partners align in time. Together, these findings reveal a dynamic interplay between the rhythms of the body and brain during human social interactions.

In diverse natural communities, cells and phages interact with many potential partners, but the impacts of pairwise coevolution on the overall structure of phage-bacteria interaction networks (PBINs) is not fully understood. Here, we conducted multiple pairwise coevolution experiments and examined how coevolution with one partner could simultaneously influence interactions with other partners. We then analyzed the underlying genetic changes that alter interactions in a large cross-experiment PBIN. The results reveal that interactions at the cell surface as well as intracellular interactions can alter patterns across the PBIN. When phages utilized the same set of host cell-surface receptor genes, pairwise coevolution with one partner did alter interactions with other partners. In contrast, if different sets of host cell-surface receptor genes were used, modular patterns in the cross-experiment PBIN were generally observed. On the phage side, resistance-breaking mutations arose in many putative receptor-binding proteins, and these changes could alter interactions with other hosts. However, in both the hosts and phages, over half of the mutated genes were not associated with cell-surface interactions. Host mutations likely altering intracellular phage-host interactions, including translation, protein stability, and DNA replication often led to broad resistance across the PBIN. In phages, mutations occurring in genes encoding endolysins, DNA methylases, oxygenases, transcriptional regulators, and tRNAs were observed potentially also influencing intracellular interactions. Based on these results, we propose a model to illustrate how these two different types of genetic signatures (i.e. extracellular cell-surface interactions verses intracellular interactions) can impact the structure of PBINs.

Extreme climatic events (ECEs) could potentially induce episodes of rapid adaptive evolution, altering the evolutionary trajectories and viability of wild populations experiencing increasingly stochastic environments. Adaptive potential stems substantially from additive genetic variance (V) in survival. However, the degree to which ECEs impact this variance, and the resulting evolutionary implications, have not been fully conceptualised or quantified in nature. These aims are highly challenging because underlying genetic and environmental variances have fundamentally non-linear effects on the dichotomous phenotypic outcome of survival versus death, while substantial data are required for estimation. We present a conceptual and analytical framework that formalises biological hypotheses for how V depends on environmental severity, how such dependences are reshaped by non-linear genotype-environment-phenotype relationships and demographic structure, and the implications for evolutionary responses. We then use 25 years of survival and pedigree data from European shags (Gulosus aristotelis) to decompose variance in adult survival across diverse environmental conditions including ECEs. Using a capture-recapture animal model, we demonstrate non-negligible V underlying adult survival across all years combined, implying notable adaptive potential. Yet, partitioning by environmental severity revealed substantial V in good years with high survival but negligible V in bad years with ECE-induced low survival, implying a genotype-by-environment interaction that constrains adaptive potential under severe conditions. However, scale transformations showed how the non-linear genotype-environment-phenotype relationship can distort or even reverse such patterns, by reducing the extent to which V is phenotypically expressed in good conditions with high mean survival and amplifying it in more severe conditions with lower mean survival. Evolutionary responses to severe conditions could consequently be non-negligible even given small underlying V. We thereby demonstrate how ECEs can reshape adaptive potential, highlighting the need to integrate impacts of environmental severity on genetic variation in fitness components into predictions of population resilience under climate change.

Categorical rhythmic patterns are fundamental features found in language and music across cultures. In humans, these rhythmic patterns occur in both vocal production and perceptual preference, highlighting a link between rhythmic production and preference. Categorical rhythmic patterns have recently been identified in animal vocalisations too, but whether rhythm production is linked with rhythmic preferences in non-human animals remains unclear. Within this context, zebra finches (Taeniopygia castanotis) are of particular interest, as both sexes develop a song preference, and their song has been suggested to exhibit an isochronous temporal structure. Here, we tested for the first time whether zebra finches prefer songs containing discrete rhythmic patterns, using operant preference tests with either two or four rhythmic patterns. Our results show that no categorical rhythmic pattern was consistently preferred across the population, although responses varied among individuals. These findings indicate that categorical rhythmic patterns are unlikely to be a primary driver of song preference in zebra finches. Together with previous work in other vocal-learning birds, our results suggest that preferences for categorical rhythmic patterns may not be universal and could instead reflect species-specific features of vocal displays rather than the rhythmic categories characteristic of human music.

Species interactions shape ecological dynamics, but adaptation to one interaction can trade off with others. Experiments that measure such evolved fitness changes across multiple interactions remain rare. We used experimental evolution to test whether recent selection under one ecological interaction changes fitness under other interactions in a fly-parasitoid system. We evolved a genetically diverse Drosophila melanogaster population for 15-17 generations under three regimes: benign conditions (control), high intraspecific competition, and infection by the parasitoid wasp Leptopilina boulardi. We then measured fly fitness (egg-to-adult survival and subsequent reproduction) under benign conditions, high intraspecific competition, and infection by three other parasitoid species and an additional conspecific L. boulardi strain. Selection history strongly influenced fitness across interactions. Populations maintained under high larval density showed reduced survival under infection by L. boulardi and L. victoriae, indicating a trade-off between past selection for competition and defence against some parasitoids. Populations evolved under parasitoid infection by L. boulardi showed increased resistance to a conspecific strain but reduced fitness when infected by another species, L. heterotoma. Our results show that rapid evolution in response to a single interaction can reshape multiple ecological interactions through fitness trade-offs, highlighting how recent evolutionary history may influence community dynamics and invasion susceptibility.

Earth's biodiversity is distributed unevenly, typically peaking in warm, vegetated, and stable environments. This has frequently been linked to energy availability, which boosts productivity, bolsters populations, and facilitates coexistence. Here, we examine the relationship between energy and biodiversity across coastal oceans using particulate organic matter biogeochemistry and environmental DNA. We reveal that energy quantity (concentrations of carbon, nitrogen, and hydrolyzable amino acids) and salinity, two variables that co-vary with freshwater inflow, jointly predict species richness at regional and global scales. Biodiversity was lowest at sites and locations with high energy inflow and low salinity, suggesting that environmental filtering associated with the osmotic stress induced by freshwater inflow outweighs raw resource availability in governing species richness. Independent of this gradient, however, energy quality (defined via C:N ratios, {delta}C values, and amino acid profiles) was associated with higher biodiversity. Labile, protein-rich, marine-derived resources supported higher biodiversity across all taxa at the regional scale, and a larger number of planktonic consumer taxa at both regional and global scales. High energy quality sites were also enriched in key planktonic groups such as calanoid and cyclopoid copepods, suggesting that these sites act as hotspots of planktonic biodiversity across coastal seascapes. Our findings suggest that few species can directly harness the plentiful resources provided by terrestrial subsidies in coastal oceans because they arrive in low salinity waters. In turn, high-quality food attracts a diverse range of consumers, which may seed the patchy foraging hotspots that characterize open-water food webs. Altered coastal hydrodynamics and biogeochemistry may therefore affect nearshore biodiversity, food webs, and fisheries.

Marine heatwaves cause widespread coral bleaching and mortality, yet thermal responses often differ between adult and juvenile corals, with the latter frequently being more tolerant. Whether the observed enhanced tolerance of juveniles reflects intrinsic physiological differences across life stages or simply reduced environmental stress due to shaded microhabitats occupied by juveniles, or a combination of both factors, remains unclear. To test whether colony size determines thermal responses and if a threshold size exists for tolerance, we exposed 89 colonies of the reef-building coral Acropora aff. digitifera to a 6-week, 32.5 C simulated marine heatwave under controlled light conditions, with cumulative stress reaching 20 C-weeks. Contrary to expectations, ~2 C-weeks less heat stress was required to trigger bleaching and mortality in coral juveniles compared to adults. Mortality divergence across colony sizes was greatest at ~10 C-weeks, when the smallest corals exceeded 80% mortality, whereas the largest colonies showed <10% mortality. A breakpoint in survival odds was apparent at 13.4 cm diameter, corresponding to the size at onset of sexual maturity in the native wild population for this species. These results indicate an ontogenetic shift in physiological heat tolerance, with larger reproductively mature colonies showing enhanced tolerance. The apparent survival advantage of juveniles in the reef frequently reported during bleaching events could be more likely due to micro-environmental buffering than intrinsic physiological tolerance. Our findings suggest that juvenile corals may be more vulnerable to climate change than previously thought, particularly as declining habitat complexity could reduce microhabitat refugia on future reefs.

Social relationships are strongly linked to health and biological fitness in humans and other animals. For example, social support may buffer individuals against harsh ecological conditions. Reciprocally, better health may allow for greater investment in social relationships. We examined links between health and social behaviour in an endangered population of northern bottlenose whales (Hyperoodon ampullatus). Using photo-identifications spanning 37 years, we visually classified whether individuals had poor body condition on each day they were observed (N = 3,086 whale-days). We then used generalized linear mixed models to explore how body condition varied with sex, age, and within-individual deviations in group size or other social metrics derived from Bayesian social networks. Approximately 11% of individuals were classified as being in poor condition at any time, though the prevalence of poor condition varied across raters and years. Visually assessed condition was successfully validated with morphometric measures, though there was only weak evidence that poor condition predicted apparent survival. Contrary to expectations, whales in poor condition were found in larger groups and had more social partners than their average across the study period. These findings run counter to the expectation that health and social connectedness are positively correlated in social mammals.

Whether sexual selection facilitates or hinders adaptation to novel environments is a question of fundamental importance due to current rapid environmental change. Using phylogenetic comparative analysis in 42 Drosophila species, we found that sperm length - a sexually selected ornament - positively associates with the ability of males to survive high temperatures. However, the ability to remain fertile does not increase with sperm length to the same extent, meaning that longer sperm species experience a larger gap between temperatures that kill and temperatures that sterilize males. The findings are consistent with the idea that strong sexual selection on condition-dependent exaggerated traits may facilitate somatic resilience to environmental stressors, but that susceptibility to heat-induced infertility may be a cost of extreme sperm ornamentation. Overall, the data suggests multifaceted links between postcopulatory sexual selection and climate change.