Biology Letters

Kin discrimination allows organisms to preferentially cooperate with kin, reduce kin competition, and avoid inbreeding. In vertebrates, kin discrimination often occurs through prior association. There is less evidence for recognition of unfamiliar kin. Here, we present the first evidence of unfamiliar kin recognition in bats. We captured female vampire bats (Desmodus rotundus) from a single roost, allowed them to breed in captivity for 22 months, then released 17 wild-caught females and six captive-born daughters back into the same wild roost. We then used custom-built proximity sensors to track the free-ranging social encounters among the previously captive bats and 27 tagged control bats from the same roost. Using microsatellite-based relatedness estimates, we found that previously captive bats preferentially associated with related control bats, and that captive-born bats preferentially associated with unfamiliar kin among control bats. Closer analyses showed that these unfamiliar-kin-biased associations were not caused by mothers or other familiar close kin, because the kinship bias was evident even when those bats were not nearby. This striking evidence for unfamiliar kin recognition in vampire bats warrants further investigation and provides new hypotheses for how cooperative relationships might be driven synergistically by both social experience and phenotypic similarity.

The Earths magnetic field is used as a navigational cue by many animals. For mammals, however, there is little data to show that navigation ability relies on sensing the natural magnetic field. In migratory bats, however, the calibration of a magnetic compass became plausible following experiments demonstrating a role for the solar azimuth at sunset in their orientation system. Here, we investigated how an altered magnetic field at sunset changes the nocturnal orientation of the bat Pipistrellus pygmaeus. We exposed bats to either the natural magnetic field, a horizontally shifted field (120{degrees}), or the same shifted field combined with a reversal of the natural value of inclination (70{degrees} to -70{degrees}). We later released the bats and found that the take-off orientation differed between all treatments. Bats that were exposed to the 120{degrees} shift were unimodally oriented northwards, in contrast to controls which exhibited a North-South distribution. Surprisingly, the orientation of bats exposed to both a 120{degrees}-shift and reverse inclination was indistinguishable from a uniform distribution. These results provide the missing link that these migratory bats calibrate a magnetic compass at sunset, and for the first time, they show that bats are sensitive to the angle of magnetic inclination.

The early Paleozoic saw a dramatic diversification of shelly epibenthic metazoans adapted to suspension and filter-feeding, but the extent to which these radiations affected the evolution of non-biomineralized suspension-feeding taxa is uncertain because these organisms are not typically well represented in the fossil record. Luolishaniids are a highly derived and disparate clade of (typically) armoured lobopodians widely interpreted as having a suspension-feeding ecology based on the presence of five or six anterior pairs of setulose appendages. Luolishaniids are globally widespread and represent the only Cambrian non-biomineralized free living epibenthic bilaterians regarded as having a suspension feeding mode of life, but their proposed ecology only relies on a qualitative interpretation of their functional morphology. Here we test the hypothesis that the setulose appendages of luolishaniids were adapted for a suspension feeding function. Quantitative morphological comparisons reveal a positive and statistically significant relationship between body length and the mesh spacing of the setulose anterior limbs of luolishaniids. This pattern correlates with suspension-feeding scaling in extant aquatic organisms, and suggests that luolishaniids primarily fed on mesoplanktonic seston. We provide quantitative evidence for suspension-feeding in luolishaniids, which represents the first statistically supported example of modern-like predator-prey scaling patterns observed in Cambrian soft-bodied metazoans.

The Middle Jurassic was a critical time in pterosaur evolution, witnessing the inception of major morphological innovations that underpinned successive radiations by rhamphorhynchids, basal monofenestratans and pterodactyloids. Frustratingly, this interval is particularly sparsely sampled, with a record consisting almost exclusively of isolated fragmentary remains. Here, we describe new material from the Bathonian-aged Kilmaluag Formation of Skye, Scotland, which helps to close this gap. REDACTED (gen. et sp. nov.) is based on a three-dimensionally preserved partial skeleton, which represents the first associated Middle Jurassic pterosaur. REDACTED is one of the first pterosaurs to be fully digitally prepared and CT scanning reveals multiple elements of the skeleton that remain fully embedded within the matrix, which are otherwise inaccessible. Novel anatomical features of this new Middle Jurassic pterosaur help to confirm the existence of the controversial clade Darwinoptera, greatly clarifying our understanding of Jurassic pterosaur evolution.

With over 15,000 extant species, Decapoda--or ten-legged crustaceans such as crabs, shrimp, lobsters, and relatives-- are among the most speciose and economically important group of crustaceans. Despite of their diversity, anatomical disparity, and remarkable fossil record extending back to the Late Paleozoic, the origins of Decapoda and their phylogenetic relationships with eumalacostracans remains elusive and inconclusive. Molecular dating suggests that decapods originated in the Late Ordovician (~450 Mya), but no reliable fossil crown groups are found until the Late Devonian. Moreover, there is no consensus on which lineages belong to stem groups, obscuring our understanding of the roots of the ten-legged decapod body plans as a whole, and how they relate to other non-decapod crustaceans. We present new, exceptional fossils from the Late Devonian of Czech Republic and Poland that belong to {dagger}Angustidontida, an odd shrimp-looking crustacean with a combination of anatomical features unlike those of any crown eumalacostracan known--extinct or extant. Our phylogenetic analyses, including representatives of all major lineages of crown eumalacostracans plus {dagger}Angustidontida, identify angustidontids as the only known stem-group decapod, and give hints about the transformation series, polarity of change, and evolutionary pathways leading to the modern decapod body plans seen today.

The temperature dependence of infection reflects changes in the performance of parasites and hosts. High temperatures (i.e., fever) often mitigate infection by favoring heat-tolerant hosts over heat-sensitive parasites. Honey bees exhibit an endothermic, colony-level temperature regulation that is exceptional among insects and favors resistance to several parasites. However, proliferation of viruses is heavily host-dependent, suggesting that viral infection could be linked to--not threatened by--optimum host function. To understand how temperature-driven changes in performance of viruses and hosts shape virus proliferation, we compared the temperature dependence of isolated viral enzyme activity, three honey bee traits, and infection of honey bee pupae. Viral enzyme activity varied by <2-fold over a >30 {degrees}C interval that spanned the temperatures typical of ectothermic insects and honey bees. In contrast, metrics of honey bee performance peaked at high ([&ge;] 35 {degrees}C) temperatures and were highly temperature-sensitive, with respiration varying 8-fold over a 20 {degrees}C interval and successful development requiring a narrow 8 {degrees}C temperature range. Although these results suggested that hosts would gain a relative advantage over viruses with increasing temperature, the temperature dependence of pupal infection matched that of pupal development, falling only near pupaes upper thermal limits. Our results reflect the host-dependent nature of virus proliferation, suggesting that infection is accelerated--not curtailed--by optimum host function, contradicting predictions of infection based on the relative performance of parasites and hosts, and suggesting tradeoffs between infection resistance and host survival. Despite a 98% reduction in infection at the upper end of the colony temperature range, the narrow thermal safety margin for honey bee development might preclude the effectiveness of fever for controlling viruses.

Sickness behaviours, like lethargy, can slow the spread of pathogens across a social network. We conducted a field experiment to investigate how sickness behaviour reduces individual connectedness in a high-resolution dynamic social network. We captured adult female vampire bats (Desmodus rotundus) from a wild roost. To create sick bats, we injected a random half of the bats (n=16) with the immune-challenging substance, lipopolysaccharide, and injected control bats with saline (n=15). Over the next three days, we used proximity sensors to continuously track their associations under natural conditions. The sick bats showed a clear decrease in social connectedness (degree, strength, and eigenvector centrality). Bats in the control group encountered fewer sick bats and also spent less time near them. These effects varied by time of day and declined over 48 hours. High-resolution proximity data allow researchers to define network connections based on how a pathogen spreads (e.g. the minimum contact time or distance for transmission). We therefore show how the estimate of the sickness effect changes as network ties are defined using varying distances and durations of association. Tracking the effects of sickness behaviour on high-resolution dynamic social networks can help create more sophisticated simulations of pathogen transmission through structured populations.

Path integration (PI) is an essential navigation strategy. Through PI, animals integrate their movements during foraging into a home vector" that allows direct return to the origin. In humans, feedback from body movement contributes to readout of the home vector: physical estimation by walking toward the origin improves peoples ability to identify the origin point. However, how such feedback affects home vector readout in other animals remains unclear. Here, we show that leg movement feedback contributes to a robust readout of the home vector despite social interference in fiddler crabs. We found that whereas the internal estimation of burrow location during the return path is subject to induced errors by social behavior, the physical estimation is not, and feedback from leg movement contributes to robust distance measurement. Our findings suggest that animals may have evolved complex navigational systems to handle the inevitable interplay between navigational cues and social behavior.

Floral diversity is the hallmark of Angiosperms and is often shaped by pollinator-mediated selection, which drives floral divergence as plants evolve traits that attract specific pollinator groups. Mediterranean red, bowl-shaped flowers are specialized on pollination by glaphyrid beetles in areas with beetles and bees but evolved different colours and specialize on bees as pollinators when beetles are absent. What explains this geographic variation in specialization and concomitant flower colour differences? We assessed pollination effectiveness of honeybees and glaphyrids for the colour-polymorphic Anemone pavonina in its natural habitat. We recorded the duration and number of flower visits and quantified single-visit seed set. Per-visit effectiveness (relative seed set) was threefold higher for Pygopleurus (36.3%) than for honeybees (9.5%). Flower visitation lasted substantially longer for beetles (56.3 sec. on average) than for honeybees (2.3 sec.). For beetles, pollinator importance (single-visit seed set x visitation frequency) was highest at low elevations but declined with increasing elevation, whereas for bees pollinator importance remained low yet constant across the elevational gradient. The high pollinator effectiveness of beetles indicates that floral specialization for this pollinator group is advantageous, even to the point that excluding low-quality bee pollinators - by producing inconspicuous flower colours - is beneficial. Non-red flowers may only be beneficial at higher elevations, where bee pollinator importance exceeds that of beetles.

The diet of an individual is a result of the availability of dietary items and the individuals foraging skills and preferences. Behavioral differences may thus influence diet variation, but the evolvability of diet choice through behavioral evolution has not been studied. We used experimental evolution combined with a field enclosure experiment to test whether behavioral selection leads to dietary divergence. We analysed the individual dietary niche via stable isotope ratios of nitrogen ({delta}15N) and carbon ({delta}13C) in the hair of an omnivorous mammal, bank vole, from 4 lines selected for predatory behavior and 4 unselected control lines. Predatory voles had higher hair {delta}15N values than control voles, supporting our hypothesis that predatory voles would consume a higher trophic level diet (more animal vs. plant foods). This difference was significant in the early but not the late summer season. The {delta}13C values also indicated a seasonal change in the consumed plant matter and a difference in food sources among selection lines in the early summer. These results imply that environmental factors interact with evolved behavioral tendencies to determine dietary niche heterogeneity. Behavioral selection thus has potential to contribute to the evolution of diet choice and ultimately the species ecological niche breadth.

Vocalisations play a crucial role in the social systems of many animals, and may inadvertently reveal behavioural characteristics of the sender. Bats, the second largest mammalian order, rely extensively on vocalisations due to their nocturnal lifestyle and complex social systems, making them ideal for studying links between vocalisations and consistent behavioural traits. In this study, we developed a new testing regime to investigate if consistent individual vocalisation differences in nectarivorous bats are associated with specific behavioural types. We exposed 60 wild, male Glossophaga soricina handleyi bats to novel and risky stressors, and assessed their behavioural and vocal responses. Proactive, exploratory, and bold bats were more likely to produce social calls, and among the vocalising bats, more agitated bats produced higher numbers of social calls. We thus show that bat vocalisation behaviour can be indicative of a certain behavioural type, potentially allowing conspecifics to assess personalities from a distance, which in turn could impact subsequent social interactions, group dynamics, and reproductive success. Our results, in combination with previous findings in birds, suggest that advertent or inadvertent long-distance broadcasting of personality may be widespread, thus opening up new exciting questions about the links between vocalisations and sociality.

The armoured lobopodian Hallucigenia sparsa embodies the seemingly uncanny nature of the animals that evolved during the Cambrian Explosion over 500 million years ago. Initially regarded as an evolutionary oddball, the exceptional preserved anatomy of H. sparsa has been substantially revised, leading to a better understanding of its relationships with other lobopodians and phylogenetic affinities with extant panarthropod phyla. However, the ecology and behaviour of H. sparsa remain largely enigmatic owing to the difficulties of interpreting its functional morphology and the perceived lack of modern analogues. Restudy of a composite fossil assemblage from the middle Cambrian Burgess Shale demonstrates swarm-like behaviour of several small H. sparsa individuals scavenging on a dead ctenophore. The lack of grasping, masticatory, or piercing mouthparts in H. sparsa points to suction feeding as a viable strategy to consume the gelatinous carcass. Reassessment of the morphology of H. sparsa reveals functional analogues shared with extant pycnogonids, including an elongate anterior end with a terminal mouth opening and enlarged foregut chambers lined up with sclerotized denticles. These observations suggest that suction feeding is ancestral for stem-group Onychophora and highlights the critical trophic role of small-bodied armoured lobopodians as degraders of soft-bodied carcasses in Cambrian benthic ecosystems.

A dietary shift from carnivory to insectivore has been proposed to explain the dramatic morphological evolution of alvarezsaurians, particularly the adaptation related to the manual digital reduction and body size miniaturization. However, based solely on morphological shifts, this hypothesis lacked direct dietary evidence to support either carnivory or insectivore. Here, we present the first convincing dietary evidence for alvarezsaurians, derived from the intestinal contents of the Early Cretaceous Bannykus wulatensis. Our analysis revealed significantly higher levels of calcium and phosphorus in the intestinal contents compared to the surrounding sandstone. Scanning electron microscopy identified hard tissue debris and possible soft tissues surrounding by phosphatized bacteria and tightly packed hollow microspheres, suggesting that the intestinal contents were strongly pseudomorphed by phosphatized microbes during fossilization. Raman spectroscopy showed characteristic peaks indicative of bone-derived material, consistent with the hard tissue debris appeared in the intestinal contents. Our results suggest that Bannykus had a carnivorous diet with strong chemical digestion, which likely compensated for its delicate cranial structures and small teeth. These results imply that if a dietary shift to insectivore occurred, it likely took place later in alvarezsaurian evolution, probably coinciding with a reduction in body size.

Pollinators, such as bees, develop flexible memories of colours, patterns and shapes, for efficient flower recognition. Here we tested whether other insects facing the same foraging problem have evolved similar cognitive abilities for flexible learning. We trained wild hornets from two species commonly found in Europe (Vespa velutina nigrithorax and Vespa crabro) to associate sucrose solution rewards to colour stimuli in a Y maze. Hornets of both species succeeded in differential and reversal learning, and developed short and long-term memories of the learnt associations. Thus, just like bees, hornet foragers can learn various visual cue-reward associations and remember them over several hours or days for selecting flowers. Our study in non-model species illustrates how standard conditioning approaches can be used to explore and compare the cognitive abilities of animals with similar foraging ecology.

The late Pleistocene was a time of global megafaunal extinctions that were particularly severe in North America. The continent lost many mammal taxa, but the validity of several remain ambiguous, including a high proportion of Cervidae taxa. Torontoceros hypogaeus is represented by a single specimen (ROMM75974) discovered in 1976 during excavation work for the Toronto subway in Canada. The species was described based on its unique antler morphology, but the variable nature of that trait and the species near absence in the fossil record leads to uncertainty concerning its systematic relationships. We used ancient DNA to clarify the taxonomic relationship and evolutionary history of T. hypogaeus. We performed mitochondrial and whole genome analyses with related cervids and showed that ROMM75974 has a close affinity, but relatively high divergence from the Odocoileus sister species. While some ambiguity remains, ROMM75974 could represent a distinct Odocoileus species to be included in the list of extinct North American taxa. This unique population was likely adapted to open landscape which was rapidly replaced with dense woodland in this region at the end of the Pleistocene, highlighting the role of climate change in the extinction of megafauna biodiversity at the end of the ice age.

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.

Navigating dense clutter requires honeybees to execute rapid visuomotor comparisons to identify the best route. How they resolve perceptual inputs to make a passage choice from multiple options is an open question. We studied this in a free flying paradigm where bees were challenged to choose between a taller and shorter aperture with varying height difference. We monitored choice across four height difference ratios at three spatial scales. Bees chose the taller aperture in all tests, but the precision of these choices depended heavily on the absolute size of the gap. For each size scale of aperture pairs, psychometric modelling revealed that when making a choice bees generally evaluate the relative height difference, conforming to Webers law. However, bees choices were non-uniformly sensitive across aperture size scales. Bees had greater sensitivity at the smallest spatial scale, where the likelihood of collision danger is larger. This deviation in behaviour due to absolute aperture size suggests a dynamic risk-cost trade-off. Bees appear to prioritise costly, high-acuity inspections only when imposed by critical physical constraints of the environment, relaxing this vigilance at safer, larger scales to conserve energy.

If you think that high-pitched sounds match bright colours more than dark ones, you are not alone. Spontaneous associations between different sensory modalities --crossmodal associations-- are widely observed in humans. More recently, crossmodal associations have been reported in chimpanzees, monkeys, dogs, chickens, and tortoises, indicating a general cognitive strategy that reflects natural correlations in the environment or similarities in the architecture of the nervous system. Alternatively, or complementarily, crossmodal associations may arise from learning of species-specific occurrences. Recent research on primates has tentatively linked human pitch-luminance associations to the evolution of language. While humans and chimpanzees spontaneously match a high-pitched sound with a white shape and a low-pitched sound with a black shape, baboons and chickens do not exhibit any preferential association. Identifying spontaneous pitch-luminance associations in species that do not rely on vocal communication, such as the solitary Hermanns tortoises, would support the idea of a language-independent phenomenon. To test this idea, we studied tortoises for pitch-luminance associations in a spontaneous food-searching task. After hearing a high-pitched (700 Hz) vs low-pitched (450 Hz) sound, animals could choose to search for food behind either a light- or dark-coloured wall. When hearing the high-pitched sound, tortoises chose the white stimulus, whereas when hearing the low-pitched sound, they chose the black stimulus, similarly to what humans and chimpanzees do. These results demonstrate crossmodal pitch-luminance associations in tortoises. While showing this commonality in the perceptual organization of phylogenetically distant species, we shift the question on whether pitch-luminance associations reflect homology or convergent evolution.

Honeybees famously use waggle dances to communicate foraging locations to nestmates in the hive, thereby recruiting them to those sites. The decision to dance is governed by rules that, when operating collectively, are assumed to direct foragers to the most profitable locations with little input from potential recruits, who are presumed to respond similarly to any dance regardless of its information content. Yet variation in receiver responses can qualitatively alter collective outcomes. Here, we use network-based diffusion analysis to compare the collective influence of dance information during recruitment to feeders at different distances. We further assess how any such effects might be achieved at the individual level by dance-followers either persisting with known sites when novel targets are distant and/or seeking more accurate spatial information to guide long-distance searches. Contrary to predictions, we found no evidence that dance-followers responses depended on target distance. While dance information was always key to feeder discovery, its importance did not vary with feeder distance, and bees were in fact quicker to abandon previously rewarding sites for distant alternatives. These findings provide empirical support for the longstanding assumption that self-organized foraging by honeybee colonies relies heavily on signal performance rules with limited input from recipients.

Group foraging can enhance prey detection, but depending on resource availability, it may also generate conflicts among conspecifics. To understand how animals balance these benefits and costs, foraging performance must be evaluated together with inter-individual interactions. However, under fully natural conditions, it remains challenging to quantify both simultaneously. Here, we investigated how individual foraging efficiency and pairwise interactions are shaped when more than one individuals simultaneously exploit the same foraging patch, using the Japanese large-footed bat (Myotis macrodactylus) as a model system. We monitored an entire pond functioning as a natural foraging patch using two thermal cameras and an eight-channel microphone array, and reconstructed the arrival, prey-attack, and exit times of individual bats. Using a Poisson generalized linear mixed model (GLMM), we found that prey-attack rates were approximately 25% lower during paired flights than during solitary flights. We then constructed a null model in which arrival, attack, and departure events followed independent Poisson processes parameterized from the empirical data. Compared with null-model predictions, both the total duration and the duration of individual paired flights in the empirical data were significantly shorter, indicating that bats limited the time spent co-using the same patch relative to solitary foraging. In addition, the probability that the first exiting individual was the one that arrived earlier or later did not deviate from chance levels, providing no evidence for a prior residence advantage. Together, these results demonstrate that simultaneous patch use avoidance occurs independently of arrival order and coincides with reduced prey-attack rate, suggesting that bats leave shared patches and move to alternative foraging sites to mitigate losses in prey-attack efficiency. Our findings highlight bats as an excellent model system for non-invasively linking individual behavior and foraging performance via echolocation, and for elucidating the dynamics of foraging behavior and sensory interference in the wild.