Biology Letters

Bees and wasps are ecologically vital, but many species are declining due to anthropogenic stressors. Social bees harbour host-specific and dense gut microbiomes that affect their resilience to stress. However, there are tens of thousands of other bee and wasp species that vary in sociality and diet (including pollen-feeding and predatory guilds), traits known to influence host-microbe symbioses. The role of gut microbes in the biology of these species is largely unknown. Here, we measured the composition and absolute abundance of bacterial communities in adult abdomens across 61 genera and 14 families of field-collected bees, predatory wasps, and pollen wasps. We found that solitary bees and both wasp guilds harbor distinct bacterial taxa and lower bacterial abundances as compared with social bees. Bacterial abundances also varied extensively among and within genera of solitary bees, with little variation explained by body size, diet breadth, or nesting ecology. Further, microbiome composition was only weakly differentiated among solitary bees and the two wasp groups, even comparing herbivorous (pollen-feeding) and carnivorous taxa. We suggest that the sparse and somewhat stochastic microbiomes of solitary bees and wasps reflect weak host dependence on microbially mediated functions, a trait that may influence their responses to environmental change.

Retro-orbital blood sampling, a method where the retro-orbital (post-orbital) sinus is punctured to draw blood, is often used in herpetological research given its ease, speed, and presumed minimal negative effect on the subject. Although literature establishing the method claims little to no impact on subjects, there exists little data explicitly testing the behavioral or welfare-related effects of this technique. We conducted a field experiment with western fence lizards (Sceloporus occidentalis) to address the potential impacts of retro-orbital blood sampling. Whereas handling the lizards had no demonstrable impact on lizard prey capture and feeding, there were significant short-term increases in time to initiate prey attack (attack latency) and time to successfully capture prey (feeding latency) in S. occidentalis immediately following blood draws. These increases diminished within 24 hours. Our experiments provide new evidence that this common blood sampling method reduces lizard feeding efficiency in the short-term. Researchers and welfare advocates may consider incorporating these findings into their research designs to optimize animal welfare and the generation of reliable ecological and behavioral data.

How social animals encode vocalizations, assign them value, and formulate behavioral responses remains largely unknown. We asked whether physiological signatures of social-call perception predict behavioral responses across contexts, using the Egyptian Fruit Bat (Rousettus aegyptiacus), an auditory specialist with a rich repertoire of social calls. Using heart rate monitoring during playback of conspecific vocalizations, we found that females showed larger heart rate responses than males to social calls (aggression and distress), whereas non-social echolocation calls evoked no sex difference. In vivo recordings from primary auditory cortex (A1) revealed call-selective units whose selectivity was independent of frequency tuning, with the largest selective fraction for distress calls. In a behavioral assay, female bats approached a distress-call playback only when a live conspecific was coupled with it. However, in isolation, the same calls elicited interest (grooming, pointing) but no approach. Together, the neural and autonomic signatures of social-call perception are present across contexts, whereas the behavioral response is not. Social context, therefore, does not modulate the behavioral readout of social calls; rather, it gates it. Significance StatementHow a social animal converts the perception of a vocalization into behavior remains poorly understood. Using the Egyptian Fruit Bat (Rousettus aegyptiacus), we show that physiological and neural responses to social calls are present in isolation, whereas approach behavior is not. We conclude that social context acts as a necessary gate between sensory representation and action, not a modulator that adjusts an existing response.

While asexual species can often outcompete their sexual counterparts over ecological timescales, their long-term evolutionary success is hindered by a diminished ability to purge deleterious mutations and to adapt to changing environments. However, some asexual species persist for millions of years, and a major question in evolutionary biology is how they do so. One solution is to occasionally reproduce sexually, as has been shown in a handful of primarily asexual species. Here, we investigate the possibility of rare sex in the clonal raider ant, Ooceraea biroi. We report the whole-genome sequence of a previously uncharacterized clonal line and, using population genetic and phylogenetic analyses, show that it originated through sexual reproduction between two extensively studied clonal lines. The mitochondrial genome of this clonal line differs from that of the maternal clonal line at only a single nucleotide, suggesting that the sexual reproduction event occurred within the past few hundred years. These results demonstrate that sex occurs sporadically in the clonal raider ant, allowing it to generate new genetic combinations and potentially to overcome some of the costs of asexuality.

BackgroundMaximum running speed is a central performance trait, linking morphology, physiology and behaviour to fitness. It is shaped by physical capacity and ecological selection but may also be constrained by ancestry. To examine how these forces interact across macroevolutionary timescales, we conducted an allometric study in a hyper-diverse arthropod taxon--spiders (Araneae). ResultsDrawing on running performance data for 258 species from 64 of the 139 extant spider families, we integrated phylogenetic comparative methods and biomechanical modelling to disentangle the effects of body size, ancestry, leg morphology, ecological guild and preferred locomotor orientation. Maximum running speed varied substantially, both across body mass and among species of similar body mass. By accounting for body mass with a recent biomechanical model, we show that size-specific performance carries a strong phylogenetic signal, and that high-performing runners first evolved within the derived infraorder Araneomorphae.Strong running performance, after accounting for both body size and shared ancestry, was associated with relatively longer legs and, to a lesser extent, ecological guild, but not with leg slenderness or a preference for inverted versus upright locomotion. ConclusionsMacroevolutionary patterns of running performance thus reflect not only variation in body size, but also size-specific leg morphology, ecological differentiation and phylogenetic history. We hope this study contributes to the development of formal evolutionary biomechanics--one that seeks to explain patterns of diversity through the explicit integration of large-scale comparative data, natural history and quantitative models derived from first principles.

Colour and contrast are commonly deployed in anti-predator signals like aposematism or deimatism. In oceans, colour information diminishes with depth, leaving blue bioluminescence the most common visual signal, regardless of function. Bioluminescence can deter predators, but without contrasting colours, how so is largely uncharacterized. Here, we test this by observing fish predators responding to prey that use defensive bioluminescence (Ostracods, Cypridinidae). By manipulating potential chemical defences of prey, and by comparing feeding responses to both luminescent and nonluminescent prey, we show that luminescent prey are unpalatable and use facultative bioluminescence as an aposematic signal. We observed active, luminescent prey secrete bioluminescence only after being attacked. Predatory fishes rarely consumed luminescent prey, especially compared to nonluminescent alternatives. Food treatments revealed that luminescent species may possess some unidentified defence over nonluminescent relatives because fishes also readily ate luminescent prey that had been treated (frozen or boiled), which removed such defences. Over the course of four experimental trials, predators were less likely to consume luminescent prey as their cumulative exposure to anti-predator light displays increased, indicative of learning. Despite their intermittency, temporally dynamic signals like aposematic bioluminescence may be as common and effective as better-studied static coloration, especially in marine ecosystems.

Animals often attempt to resolve the trade-off between foraging and predation by regulating their activity timings and patterns. Driven by individual energetic requirements and the local environment, onset of activity in a species varies across space and time. These differences are particularly enhanced on a latitudinal gradient, influenced by varying lengths of daylight, temperature and seasonality. For a nocturnal mammal like the bat, such patterns translate to shorter activity windows at higher latitudes, both on a nightly and a seasonal basis. This constructs the timing of activity onset as a crucial variable for a successful night of foraging. While roost exit timings and influence of local conditions on bat activity have been extensively studied across species inhabiting a variety of locations around the world, our understanding of bat emergence behaviour on a global scale remains limited. To investigate emergence patterns in bats across a latitudinal gradient, we conducted a meta-analysis spanning 91 species from across 13 Chiropteran families. We evaluated how timing and luminosity (i.e., sun altitude) at exit varied across latitudes and species. Results revealed that bats across the globe tended to emerge under conserved thresholds of brightness, a pattern that was facilitated by a temporal delay in roost exits at higher latitudes. By maintaining emergence within the confines of nautical twilight (sun altitude between 0{degrees} to -12{degrees}), bats across the phylogeny thus seemed to balance the dilemma of predation versus foraging. This pattern was mirrored across the two broad dietary types (frugivores and insectivores) as well as different social structures (maternal v. non-maternal colonies). Furthermore, our models indicated that while local conditions dictate final exit decisions, shared ancestry was potentially influencing the extent of plasticity seen in emergence patterns. Taken together, these results highlight how broad-scale latitudinal gradients of light can influence the foraging strategies in a globally distributed nocturnal mammal.

Despite their currently scarce taxonomic diversity, rhinocerotoids were among the most evolutionarily successful clades of large herbivorous mammals throughout the Caenozoic. Within an array of morphological adaptations, the cranial horn represents the clades most remarkable and name-giving feature, imposing significant morpho-functional demands on the skull. In this paper, patterns and drivers of the rhinos cranial evolution were investigated for the first time by compiling a three-dimensional geometric morphometric dataset of living and extinct species. Multiple aspects of morphological evolution were explored using phylogenetic comparative methods, including craniofacial evolutionary allometry (CREA - tendency of larger species to have longer faces), phylogenetic constraints, and tempo of evolution. Cranial shape variation linked to horn presence and size evolved under a phylogenetically constrained framework, with a notable transition from hornless to horned species. Rhinos significantly deviated from CREA, likely due to diversity of cranial forms and proportions that evolved independently across the clade in response to varying horn morphologies and dietary habits. Hornless and horned rhinos exhibited similar rates of cranial evolution, and shape variation was obtained through multiple episodes of accelerated evolution. This highlights the role of morphological innovations and Caenozoic global cooling events in the emergence of phenotypic diversity.

Predation is considered a key driver of the rapid diversification of animals during the Cambrian explosion. While the fossil record documents a plethora of evidence of successful and failed predation on biomineralized invertebrates at low trophic levels, no previous evidence of predation on larger, often soft-bodied, animals at higher trophic levels has been reported. This means that the modeled links between higher trophic levels in Cambrian food webs lack supporting fossil evidence, hindering understanding of the complexity of Cambrian trophic relationships. Here, we report a healed injury on the swimming flap of the radiodont apex predator Amplectobelua symbrachiata-- one of the largest animals in the Cambrian oceans. The diagnostic W-shape with a healed margin supports interpretation of this wound as predatory in origin, with likely attackers including larger contemporaneous radiodonts - possibly members of the same species -- or the giant lobopodian Omnidens. Evidence that apex predators were attacked provides critical empirical data informing the complexity of Cambrian food webs. This finding provides empirical support for the existence of high-level feeding loops, analogous to those in modern marine ecosystems, documenting the rapid increase in trophic complexity during the latter stages of the Ediacaran-Cambrian Transition.

Climate change can threaten population viability by disrupting sex ratios in species whose sex is influenced by temperature. While species with sex chromosomes were historically considered immune, in some species, temperatures can override genetic sex determination via sex reversal, leaving them vulnerable to climate-driven sex ratio shifts. The Tasmanian spotted snow skink (Carinacincus ocellatus), a viviparous reptile with an XX/XY system, provides a compelling case study. While laboratory studies demonstrated that extreme thermal conditions induce female-to-male sex reversal (XX males), its occurrence in the wild remains unexplored, limiting our understanding of actual climate impacts. Integrating 23 years of phenotypic and genetic sexing data across two climatically distinct populations, we provide the first evidence of sex reversal in a wild viviparous reptile. XX reversal occurred in both populations, affecting up to 23.5% of XX births in the warmer population, and was associated with colder minimum daily temperatures. Despite high birth rates in some years, sex-reversed adults were rare. We also identified putative XY females, suggesting bidirectional sex reversal and reinforcing the extreme plasticity of reptilian sex determination. Ultimately, sex reversal could act as an evolutionary trap, potentially compromising population viability as climate instability increases.

Binocular vision provides animals with several evolutionary advantages. In praying mantises, one of these advantages is stereopsis that has different effects while attending to prey and capturing prey. However, the importance of binocular, compared to monocular, visual input has not been tested in either stage of predation. We therefore used an insect 3D cinema to present mantises with binocular and monocular stimuli to either prime their attention or elicit prey capture. We used a previous paradigm where a wide-field figure motion cue attracts mantis attention, which leads to predatory responses to a small-field elementary motion target. We found that binocular visual input enhances attention to cues, but monocular cues are also effective. However, prey capture responses were fundamentally dependent on binocular input. Thus, binocularity appears to be fundamental to prey capture in mantises but not for attending to prey.

Vertically transmitted symbionts experience progressive genome degradation driven by transmission bottlenecks each host generation that reduce genetic diversity and promote fixation of deleterious mutations. Direct estimates remain rare because inference requires scarce parent-offspring samples and sequencing sensitive enough to detect rare variants. Here, we investigate symbiont transmission bottlenecks in a vesicomyid clam by deeply sampling within-host endosymbiont genetic diversity using two ultra-accurate sequencing methods. Demographic modeling revealed an effective bottleneck size of approximately eight symbionts (95% CI: 1-17 genomes) per host generation. This estimate is sharply reduced relative to prior cytological estimates of bottleneck census size, with important implications for understanding the rate and dynamics of endosymbiont genome degradation.

In vertebrates, top-down visual attention is a cognitive process where internal goals modulate the tuning of peripheral sensory systems. This leads to increased perceived contrast to both goal-relevant objects and areas of the visual field that are attended. Such a system would also be beneficial to bees, enabling them to detect and recognise the most profitable flowers in their environment. We tested whether bumblebees possess a top-down attentional system resembling that seen in vertebrates. We trained two groups of bees to collect rewards under high contrast targets. To potentially induce a difference in attention while searching for the targets, one group received a higher concentration of sucrose rewards compared to the other. During tests, the targets were presented with a series of lower contrasts to measure the contrast sensitivity curves of the bees induced by the different learnt reward levels. We predicted a stronger effect of any attention-like process on contrast sensitivity in the high reward group. We also repeated this experiment with the neonicotinoid pesticide imidacloprid dissolved in the sucrose rewards to test whether this affects bee attention. Across all test contrasts, higher rewards significantly increased bee accuracy when locating targets, lowered contrast thresholds and reduced the latency to make first choices. Imidacloprid reduced bee accuracy but did not influence first choice latency. These results suggest that learnt floral rewards can influence bee behavioural contrast sensitivity in a manner resembling vertebrate top-down attention and that imidacloprid may modulate this through effects on their nervous system.

Parental care can have pervasive effects on offsprings neurodevelopment. Parent-offspring interactions are often modulated by the neuropeptide oxytocin, which is responsible for the development of social bonds. The development of the oxytocinergic system is dependent on the quality of parental care during the post-natal phase. However, it is yet unknown how post-natal direct interactions can influence the development of the oxytocinergic pathway. Here we tested how an obligate parental care behaviour, tadpole transport in poison frogs, influences the development of the oxytocinergic pathway. To this end, we quantified whole brain expression of oxytocin receptor and oxytocin precursor throughout three developmental stages of A. femoralis tadpoles, before, during and after tadpole transport. Our results show an overall downregulation during tadpole transport, which indicates that during transport tadpoles enter a dormant state to slow down development until they are placed in water. Interestingly, the expression of oxytocin precursor did not vary between the three developmental stages. This might indicate that oxytocin is being recruited during transport, but does not lead to neurodevelopmental changes. In sum, here we present the first evidence of a dormant state during tadpole transport which might be an adaptive response to the terrestrial reproduction in poison frogs.

Light-induced body color changes and direct optical sensing in the skin of amphibians and fishes have been debated for more than half a century. Previously reported chromatophore-mediated photoresponses generally occur on timescales of tens of seconds to minutes and are commonly attributed to intracellular molecular mechanisms, including opsin-dependent signaling pathways. In several invertebrates and amphibians, dermal photoreception has been detected electrophysiologically as rapid neural outputs. Here, I report an ultrafast, nonvisual photoresponse mediated by dermal iridophores in the silverside fish Hypoatherina tsurugae (Atherinidae). Upon exposure of living skin to white LED illumination, the light reflection from iridophores was rapidly quenched within seconds. Spectral analysis revealed that this quenching response was most sensitive to blue light compared with green and red illumination. The reflected light recovered to its original twinkling state within approximately 10 s after cessation of illumination. The speed and reversibility of this response suggest that mechanisms beyond slow intracellular structural rearrangements are involved and raise the possibility of neural modulation in addition to intrinsic photoreceptive processes. These findings uncover an unrecognized mode of dermal light sensing and provide insight into bioinspired design principles for artificial optical sensing skins.

Humans are widely regarded as unusually slow to develop, exhibiting prolonged childhood and extended dependence on caregivers. However, this view is based primarily on comparisons with other primates, leaving unresolved whether humans remain distinctive within the broader diversity of mammals. We addressed this question by situating human development in a comparative framework using gestation length, weaning age, and age at sexual maturity for both sexes across 462 mammalian species representing 25 orders. Each trait was examined both as an absolute value and as a proportion of the longest verified captive lifespan. In absolute terms, human developmental traits fell within the upper range of mammalian variation. When expressed relative to lifespan, however, gestation shifted toward the lower end of the distribution, whereas weaning age and sexual maturity occupied intermediate positions, indicating that human developmental timing largely follows general mammalian scaling patterns rather than representing a pronounced outlier. These findings suggest that key features of human dependency are better understood as extensions of broader evolutionary trends than as uniquely human life-history characteristics.

Marine species inhabit a three-dimensional stratified environment where metabolism is simultaneously influenced by decreasing temperature and increasing hydrostatic pressure with ocean depth. While the Metabolic Theory of Ecology (MTE) incorporates the effects of body mass and temperature, for marine organisms it neglects one of the fundamental thermodynamic state variables governing biochemical reaction kinetics: hydrostatic pressure. We derive a generalized metabolic theory by extending MTE with transition-state theory by explicitly incorporating pressure sensitivity into the Arrhenius formulation. The resulting model predicts that hydrostatic pressure increases the effective activation energy of biochemical reactions, leading to progressively lower metabolic rates with increasing depth. We tested this prediction using a global database comprising 689 metabolic measurements across 11 marine phyla and 22 taxonomic classes. Incorporating hydrostatic pressure substantially improved model performance relative to the classical MTE. Across major marine taxa, activation energy and activation volume varied largely independently, suggesting that pressure adaptation does not require corresponding changes in thermal sensitivity. Our results suggest that hydrostatic pressure is a fundamental thermodynamic constraint that regulates the pace of life across the ocean and consequently the ecological dynamics across Earths largest biome.

One way that animals can cope with the challenge of locating ephemeral food in time and space is by tracking elapsed time and planning revisits to these resources. These abilities likely evolved under constraints of memory capacity. We expect that during evolution a trade-off emerged between a large memory size (quantity) and high accuracy (quality) of information. We used computer simulations of a forager moving through space and time to investigate how timing accuracy, memory size, and forgetting affect foraging efficiency across environmental conditions, and how foragers should trade off the quantity against quality of memorised information. Memory in general paid off, as it improved foraging efficiency. However, surprisingly, the largest accuracy and size were not always most beneficial. In resource-poor, heterogeneous, and highly dynamic environments, extensive memory was even detrimental, as individuals likely became trapped in overexploited familiar areas. This suggests that under certain environmental conditions, a hidden, non-energetic cost of memory can arise. Furthermore, environmental structure shaped a quantity-quality trade-off such that a minimal memory size and higher timing accuracy were favoured in resource-poor, temporally stable and homogenous environments. Finally, forgetting was beneficial when memory was constrained, and environments were poor, heterogenous and dynamic. Forgetting limited the benefits of increased memory size, highlighting that memory costs can emerge from how it shapes movement patterns and foraging decisions. Overall, our results highlight that larger and more accurate memory is not necessarily better and that forgetting can be adaptive. This study takes a first step toward the theoretical consideration of memory trade-offs in order to research how they shape, and are shaped, by foraging pressures. Author summaryHow can we explain foraging memory abilities differences in animals? In this study, we make an attempt to elucidate the current patterns of temporal memory using a computational model that was inspired by realistic environmental and cognitive mechanisms. Building on our previous theoretical and empirical investigations of the causes and consequences of spatiotemporal memory, we provide new insights into the ecological drivers of temporal memory, how they shape an accuracy-size trade off, and its consequences for movement behaviour. We show that a larger memory is favoured, at the cost of accuracy, in resource-rich and dynamic environments. Our results highlight that while memory is generally beneficial, a larger and more accurate memory is not necessarily better. Moreover, our model suggests that such constraints of memory stem from a hidden cost of how memory restricts movement and instigates local overexploitation. Our findings contribute to a broader understanding of how cognition evolves in response to ecological conditions.

Heatwaves can affect species abundances by changing how species interact with one another in local communities. These effects can be complex and remain poorly understood, especially in cases where the outcome of species interactions is contingent on the history of species arrival. We studied how heatwaves affect interactions between the yeast Metschnikowia reukaufii and the bacterium Acinetobacter nectaris, both commonly found in the floral nectar of Diplacus aurantiacus, a hummingbird-pollinated shrub native to California. The microbes were introduced to artificial nectar in different orders of arrival in the presence or absence of simulated two-day heatwaves. We found that heatwaves made yeast-bacterium interactions more contingent on arrival history, thereby causing large variation in nectar acidity, a factor known to affect hummingbird preference and seed production. In the absence of heatwaves, Acinetobacter always became abundant regardless of arrival history, suppressing Metschnikowia and reducing nectar pH. In contrast, in the presence of heatwaves, Acinetobacter dominance depended on arrival history and heatwave timing. If Acinetobacter arrived after Metschnikowia during a heatwave, Metschnikowia suppressed Acinetobacter substantially enough to keep nectar pH at a high level. These results suggest that heatwaves shift species interactions from determinism to historical contingency, with both taxonomic and functional consequences.

In temperate regions around the world, bats travel long distances every winter to gather at hibernation sites. A longstanding hypothesis is that each new generation of bats learns about the locations of these sites (called hibernacula) from older individuals, yet clear and compelling evidence demonstrating social transmission of this knowledge has been lacking. Here, we compiled 30,882 observations from 1985 to 2023 of 13,852 Greater mouse-eared bats (Myotis myotis) that were banded and observed at summer roosts, winter hibernacula, or both. Our analyses revealed four lines of evidence that Greater mouse-eared bats find suitable hibernacula using social information acquired at summer roosts. First, naive yearlings were more likely to be seen sharing their first hibernacula with adults from their summer birth colony relative to a null model where bats moved independently. Second, adult bats were also more likely to co-switch together into the same hibernacula across winters than expected from independent movements. Third, bats that roosted together in the summer were more likely to share a different site as a hibernaculum during the winter: being observed together during a summer changed the probability of a pair being observed together during a winter from 5% to 12%. Finally, high-resolution tracking revealed an instance of tandem flights to hibernacula sites during the summer, demonstrating that yearlings can learn from experienced adult bats months before hibernation. Together, our findings show that maternity colonies serve as "information centers" where females acquire knowledge of suitable hibernation sites throughout their long lives.