Biology Letters

Body size, through its links to various physiological traits, has often been hypothesized to influence evolutionary rates. Negative body size-rate correlations have been reported in the morphological or molecular evolution of several extant vertebrate groups, including mammals, birds, reptiles, and teleost fishes. In this study, we estimated body masses for 89 species of plesiosaurs, a clade of Mesozoic aquatic reptiles, and found that their body size evolution conforms to a three-regime Ornstein-Uhlenbeck process, indicative of constrained evolution. Rates of morphological evolution, inferred using the skyline fossilized birth-death process and the variable-rates model, show minimal support for a correlation with body size in this clade. Our results thus serve as a counterexample, suggesting that the negative body size-rate relationship is not a universal vertebrate pattern, but rather a trend restricted to certain lineages.

The population of Madagascar exhibits a globally unique combination of African and Asian genetic ancestries. Previous studies have described the admixture history of Madagascar at island-wide scales [1,2], but less focus has been paid to fine-scale population structure across the island. We present new genome-wide genetic data from 192 individuals sampled across five regions of Madagascar. We identify population structure at extremely fine spatial scales ([~]10 km) among the Merina of the central highlands. By analysing subpopulations separately, we found one Merina group exhibited similarity to coastal populations in f4 ratios, estimated admixture dates, and pairwise FST distances, while another group was similar to other highland individuals in the same measures. This fine-scale substructure is likely associated with historical coastal-to-highland migration during the 18th and 19th centuries. In contrast, we also observe macro-scale structure in estimated timing of admixture across the island, with southeastern coastal groups exhibiting the earliest estimated admixture timings, and northern groups exhibiting the latest. This pattern corroborates previous results [1,2], and may suggest differing histories of admixture timing among Malagasy populations. Our results emphasise the importance of deep micro-geographic sampling to complement macro-scale analysis when characterising demographic history.

Locating, tracking, and intercepting objects is a fundamental behavior for many organisms. For instance, predators must track and capture erratically moving prey for their survival. Using the echolocating bat as a model species, we investigate how short-term changes in target motion predictability affect longer-term motor plans when tracking a prey item. We used a paradigm where prey motion is under experimental control, and then applied computational methods to characterize how target motion predictability influences short- and long-term behavioral control. We find that target motion predictability during the tracking phase of insect capture influences both short-term changes in sonar call control, as well as longer-term behavioral control for transitioning between hunting phases. For changes in immediate behavioral control, bats produce more bursts of calls at a higher rate when tracking unpredictable moving prey, an indication that the bat is collecting more information about the targets motion for unpredictable than predictable trials. In terms of longer-term behavioral control, target motion unpredictability delays the transition from tracking to capture phase behaviors. We suggest that the bat does this to collect more information about target motion to time the transition from tracking to capture behaviors for hunting success. Additionally, we find the effects of target motion unpredictability are first seen as changes in the vocal motor plan and then the auditory motor plan (ear motion), hinting at a sequencing of motor changes that warrant further investigation. SummaryWhen presented with a more challenging hunting task, bats will increase their production of bursts of calls at a higher rate and delay their transition into capture behaviors.

Arboreal insects have developed various strategies to navigate their discontinuous habitats. Many insects, including leafhoppers, katydids, and praying mantises, exhibit the ability to actively leap across their leafy platforms and land on a distant substrate. This behavior is especially important for non-winged insects, including nymphal forms of winged insects, which cannot fly between these substrates. To make a targeted jump, an animal must first orient towards the target, estimate the target distance and angular location, and jump with the appropriate take-off speeds and angles to land on their intended substrate. In three-dimensional space, jumping from one point to another requires estimating distance, as well as azimuthal and elevational angles. Jumping insects such as mantises typically reorient their bodies on the substrate to align with the azimuthal direction of the target. This behavior effectively reduces the task to a two-dimensional problem, in which they must estimate only the distance to the target and its elevational angle. Many insects, including praying mantises, perform rhythmic lateral head movements called peering before performing a targeted jump. Although previous studies suggest that mechanisms such as motion parallax while peering are used for distance estimation, the full repertoire of behaviors that enable mantises to jump to arbitrarily located substrates remains unclear. We hypothesized that mantises have distinct behaviors for distance and elevation angle estimation, which enable them to independently modulate their take-off speeds and angles before jumping. To test this hypothesis, we developed behavioral assays in which mantises were placed on a launch platform and jumped to a target platform positioned at variable distances and angles. Using this apparatus, we filmed the jumps of Giant Asian mantis nymphs (Hierodula spp.) with high-speed videography and tracked body parts to quantify take-off speed and angle. Because mantis jumps are ballistic, their trajectories can be modeled as projectile motion. Our results indicate that mantises estimate target distance and elevation angle using two separate behavioral strategies: distance is assessed through peering maneuvers that generate motion parallax, whereas elevation angle is determined through visual fixation of the target accompanied by specific postural adjustments. By combining these behaviors, mantises modulate the magnitude and direction of propulsive force to achieve successful jumps.

Night-migratory songbirds use the Earths magnetic field to guide their migratory journeys. Most evidence suggests that the magnetic compass sensor is a flavin-tryptophan radical pair whose operation is disrupted by broadband radiofrequency (RF) fields at frequencies up to [~]116 MHz. Here, we test whether broadband 110-120 MHz RF fields affect the magnetic orientation behaviour of night-migratory Eurasian blackcaps (Sylvia atricapilla). We found that the birds oriented in their expected migratory direction in the natural geomagnetic field (NMF) control condition and that they turned their orientation [~]120{degrees} when the field was rotated 120{degrees} horizontally (changed magnetic field, CMF). When they were exposed to broadband 110-120 MHz RF fields, the birds continued to orient in the appropriate direction in the NMF. In the CMF, we found orientation behaviour that was not consistent with the expected direction. We conclude that the birds could still orient when exposed to 110-120 MHz fields, but speculate that their magnetic orientation capabilities might have been somewhat reduced compared to the control condition. We suggest that 110-120 MHz could represent a grey zone of reduced magnetic orientation capability centred at the cut-off frequency predicted for a flavin-based radical pair (probably in the flavoprotein cryptochrome).

Eye loss has long fascinated evolutionary biologists and occurs across the animal kingdom. Spiders have two parallel visual systems -- two primary and six secondary eyes -- but eye losses, leaving six, four, two, or no eyes, have occurred in multiple lineages. Despite their significance, reports of eye loss are scattered, limiting broader analysis. Here we present the first comprehensive analysis of eye loss across all known spider lineages. We show that eye loss occurs in [~]12% of extant species, mainly within the clade Synspermiata. Six-eyed spiders are most common (>5,300 species), while four-eyed, two-eyed, and eyeless forms are rarer and often linked to troglobitic lifestyles. Principal eye loss is widespread, occurring in 49 families across nearly all major lineages. Using a recent phylogeny of the order Araneae, we demonstrate a strong correlation between eye loss and occupancy of low-light environments, but this is complicated by differential effects across eye types and phylogenetic groups through geological time. These findings reveal striking lability in eye number and lay groundwork for future research into ecological, developmental, and neurological drivers of eye loss. [hidden Markov models, ancestral state reconstruction, Araneae, discrete character evolution, principal eyes, secondary eyes, low light environments].

Early studies of synaptic transmission by Bernard Katz and colleagues suggested that neurotransmitter release at graded-potential synapses occurs through statistically independent (i.e. Poissonian) quanta [1, 2]. Subsequent experimental work supported this framework [3]. However, these measurements were performed in vitro on relatively simple synapses and under non-physiological conditions, often converting spiking neurons into graded-potential neurons through the use of channel blockers. Relying on the conventional assumption that vesicle exocytosis follows a Poisson process, measurements of the contrast power transfer spectrum and noise power spectral density of large monopolar cells (LMCs) in the blowfly C. vicina imply a sustained vesicle release rate exceeding 105 vesicles per second per LMC. Given the physical dimensions of photoreceptors and synaptic vesicles, such a release rate appears physiologically implausible. If vesicle release is more temporally structured, low-frequency noise could be suppressed, substantially reducing the vesicle release rate required to account for experimental observations. The reduction of noise at low frequencies is especially advantageous given inputs such as photoreceptor signals which are already low-pass filtered. Visual activity generates substantial extracellular potentials within the lamina cartridge [4]. We propose that these extracellular potentials regulate vesicle release by modulating the voltage sensors that trigger exocytosis. We provide experimental evidence for the connection between currents driving the LMC and the extracellular potentials during visual activity, and demonstrate, using simple models, how effective "Poisson" rates are maximized due to vesicle regularization.

The haemagglutinin (HA) and neuraminidase (NA) genes of seasonal influenza A evolve under continual immune-driven positive selection. To test whether the tempo of selection has changed over time, we mapped branch- and site-specific episodic diversifying selection (MEME) onto Bayesian relaxed-clock time trees for HA and NA in H1N1 and H3N2, across multiple countries and four sequence-subsampling schemes. We dated each selection episode and tested whether episodes accumulated through time after accounting for the growing number of sampled lineages. Positive-selection episodes increased over time in every gene-subtype combination, at about 2-6% per lineage-year, and rose faster for NA than HA. Episodes were concentrated at a small number of codon sites, especially recurrent sites in H3N2 HA that fell within canonical antigenic regions of the HA1 head. This increase was robust to subsampling scheme and time-bin width, and was driven disproportionately by recent lineages. A detrended spatial analysis found no association with latitude or temperature anomalies. Overall, positive selection on influenza surface antigens appears to be intensifying through time, most likely because of immune escape and expanded surveillance rather than climate warming.

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.

Cuticular hydrocarbons (CHCs) are essential for insect waterproofing, yet how they change seasonally in social insects remains poorly understood. Due to its distinct seasonal worker phenotypes (summer and winter bees) and diverse subspecies, the western honey bee (Apis mellifera) is an ideal model to study seasonal CHC plasticity across populations with distinct local adaptations. We performed a common garden experiment to investigate the seasonal plasticity in CHC profiles across five European subspecies (A. m. carnica, A. m. iberiensis, A. m. ligustica, A. m. macedonica, A. m. ruttneri). We compared the CHC composition of workers performing tasks inside ("in-hive") or outside ("out-hive") the colony during summer and winter. Notably, out-hive workers consistently exhibited more waterproofing CHC profiles compared to in-hive workers, regardless of season or subspecies. The persistence of this stereotypical task-related differentiation in long-lived winter bees, which largely lack an age-based division of labor, indicates a robust, age-independent regulatory mechanism linked to the environment faced by the workers rather than a simple response to seasonal desiccation pressure. Moreover, we demonstrate CHC seasonal plasticity for the first time in honey bees. However, these seasonal shifts in hydrocarbon classes and chain length were not uniform; they varied across subspecies and critically depended on the task the workers performed.

Escape behaviour directly influences survival, yet individuals often vary substantially in escape performance. Laboratory studies have documented trade-offs between anti-predator responses and life-history traits, but it remains unclear whether such trade-offs occur under natural predation risk. We studied a natural population of the field cricket Gryllus campestris. Mortality risk and behavioural performance are known to change with age in this species. We aimed to determine whether individuals expressing a higher escape response pay a cost in terms of a faster increase in mortality risk with age or a shorter lifespan. We quantified escape speed in response to a vibrational predation cue. We found no clear evidence for a trade-off between escape performance and lifespan or age-specific mortality risk. The relationship between escape speed and the among-individual effect of age differed between sexes: older males showed faster escape speeds compared with younger males, whereas younger females were faster than older females. This pattern is consistent with sex-specific selective disappearance. Individual baseline mortality risk varied with sex and escape speed, but age-dependent mortality did not. It suggests that such trade-offs in the wild may be context- or condition-dependent rather than reflecting a universal life-history trade-off.

A central challenge in characterizing species niches is ensuring that foraging data accurately capture both the resources used and their relative importance, and the role of resource abundance in shaping foraging patterns. Most studies infer diet breadth and resource-use patterns from observational records, yet such data can mask resource-specific decisions when animals forage with different goals. Here, we test this experimentally using individually identifiable bees in controlled resource communities to quantify foraging decisions between nectar (for sustenance) and pollen (for offspring provisioning). Combining observations, pollen DNA metabarcoding, and pollen microscopy, we show that observed visitation patterns misrepresent the floral resources most important for offspring provisioning, which ultimately determines offspring survival and population persistence. We further show that interaction patterns are structured from processes beyond resource abundance. Our results demonstrate that commonly used observational approaches can mischaracterize diet breadth, potentially challenging conclusions about species generalization.

Extremely elongate necks have convergently evolved in several amniote lineages, including both aquatic and terrestrial forms (Fig. 1). The development of such a feature brings with it advantages in obtaining food items, but also biomechanical challenges, such as flexibility, stability, lift, and inertia. In Tanystropheus, a particularly long-necked Triassic archosauromorph, the neck is composed of only 13, mostly extraordinarily elongated and slender cervical vertebrae and accompanying rod-like, overlapping ribs, making it arguably the most extreme example of neck elongation in tetrapod evolution (Fig. 1;1-6). Understanding the function of this remarkable neck provides insights into the limits of neck elongation in amniotes and the evolution of morphological novelties in Triassic reptiles. Here we present the first quantitative biomechanical analysis of the Tanystropheus neck using a digital model based on three-dimensionally preserved bones. We assessed its range of motion (ROM) and performed finite element analysis (FEA) on the individual cervical ribs and the neck model in different configurations. Our results indicate that the neck of Tanystropheus was not extremely stiff, as previously postulated, and the ribs likely did not impair its movements. They transferred tensile forces towards the base of the neck, similar to what hypothesized for sauropods7. This study elucidates the bauplan of an extremely specialized animal and brings us closer to understanding the patterns of achieving neck elongation in vertebrates.

Gorgonopsian therapsids represent a transitional condition in the evolution of synapsid locomotion and postcranial structure. Most descriptions of gorgonopsians have focused on cranial material, however, limiting their usefulness for informing patterns of postcranial evolution on the mammal stem. While some recent work has begun to focus on postcrania, especially the pectoral girdle and forelimbs, comparatively little data are available on the pelvic girdle, hind limbs and tail. We report a new specimen of the late Permian gorgonopsian Aelurognathus tigriceps comprising a partial skull and well-preserved postcranial skeleton, including the near-complete series of dorsal vertebrae and ribs, complete pelvic girdle, hind limbs, feet, and a nearly complete tail. The tail is longer than any other published gorgonopsian. The new material presented here provides an opportunity to better establish broader patterns of morphology in the gorgonopsian postcranial skeleton.

Acoustic communication is fundamental to social interactions in many animal species, allowing individuals to transmit information about identity, reproductive status, and competitive ability. Because call production incurs inherent costs, individuals are expected to modify their vocalizations depending on the social context. However, while context-dependent call variation has been documented in several taxa, including anurans (frogs and toads), glass frogs (Centrolenidae) remain among those for which the acoustic repertoire across social contexts is poorly characterized. Here, we investigated context-dependent call modification in males of the Emerald glass frog, Espadarana prosoblepon, comparing calls produced across four social contexts: advertisement in isolation, advertisement in a group, courtship interactions with females, and agonistic interactions with other males. By integrating detailed behavioral field observations with a robust analytical framework, we present evidence that males modify multiple acoustic properties in response to the social context. Specifically, males produced longer, louder advertisement calls when calling in a group than when calling in isolation. Courtship calls contained more notes and were louder than other call types, whereas aggressive interactions were characterized by pulseless, low-frequency, soft calls. Our findings demonstrate that the distinct call types of E. prosoblepon are consistently associated with specific social contexts and can be reliably distinguished based on their acoustic structure, providing a framework for future studies investigating the functional significance of context-dependent acoustic signals in anurans.

Maternally inherited, intracellular Bacteria of the genus Wolbachia are extremely widespread among arthropods. Their evolutionary success is owed to frequent host shifts and rapid subsequent spread within host populations, often facilitated by Wolbachia-induced reproductive manipulations. Theory suggests that carrying Wolbachia must also be beneficial for a successful spread, however the nature of such benefits remains unclear. Here, we demonstrate that Wolbachias success in many solitary bee species is strongly associated with the presence of a gene cassette enabling Wolbachia to synthesize Biotin (vitamin B7). This ability is absent from almost all other Wolbachia strains but common among bee associated strains. We show that Wolbachia occurs in up to 70% of all bee species and that strains carrying this rare genomic element have independently spread into numerous bee hosts recently. We further demonstrate that the presence of the biotin operon is associated with specialised diets in several bee species, suggesting a previously overlooked nutritional role of Wolbachia in this group of important pollinators. Overall, our results suggest that nutritional benefits provided by symbionts may represent a more widespread and important mechanism by which reproductive manipulators spread into new host species than previously appreciated.

Many arthropods (insects and crustaceans) rely on their antennular chemosensory system to detect key environmental resources like food. While odor mediated food search is well studied in insects, characterization of crustacean chemosensory behavior has been limited by the long lifespans and large size of traditional crustacean model species. Here, we report the first characterizations of the food search behaviors of the genetically tractable amphipod crustacean, Parhyale hawaiensis. We find that Parhyale can locate an odorous food pellet, and predominantly approach food using direct, targeted swims from the arena walls. Removal of both first and second antennae dramatically reduced foraging success and impaired Parhyales ability to control take-off angle and maintain a stable heading during swims. Removal of the first or second antenna alone did not significantly disrupt foraging, and resulted in mild disruption of orientation phenotypes. Intact animals performed sharp turns near the location of the food pellet, which were observed when either first or second antenna were present, but not when all antennae were removed. Turns were longer and had higher average angular velocities following removal of either set of antennae, with full antenna removals representing the most extreme phenotype. In contrast with the long-held theory that the crustacean second antennae exclusively mediate contact chemosensation, we report that first- and second- antennae both contribute similarly to food localization and stabilization of locomotion in Parhyale in our behavioral paradigm. This work establishes Parhyale as an accessible model for studying olfactory behaviors in an aquatic arthropod.

Animals rely on a wide range of environmental signals, including celestial and terrestrial cues for navigation. While celestial cues, such as the sun, play a major role in maintaining a constant heading during long-distance migration and dispersal, terrestrial cues provide an animal with a short-range navigation system, ideal to pinpoint highly specific locations. In Monarch butterflies, the simulation of a terrestrial landmark, i.e. a vertical stripe, induces an attraction behavior (all animals head toward the stimulus) while a small green light spot, simulating the sun, elicits menotactic orientation (animals adopt individual-specific headings relative to the stimulus). However, the mechanisms underlying how the animal distinguishes between a stimulus as a terrestrial landmark versus a celestial cue remains unclear. To explore this, we tested non-migratory Monarch butterflies (Danaus plexippus) in a flight simulator. The inner surface of simulator was equipped with an area of LEDs, allowing to present different visual stimuli to the butterflies during tethered flight. By systematically manipulating the stimulus width, height, brightness, and elevation we found that Monarch butterflies exhibited attraction behavior to high contrast areas, like stripe edges. Menotactic behavior was not achieved by solely decreasing the stimulus to a small light spot but also required for the stimulus to be presented at higher elevation to be interpreted as a sun stimulus. These findings suggest that multiple parameters, inherently set by the butterflys navigation system, are critical to interpret a visual stimulus as celestial cue or terrestrial landmark, producing dynamic switches between different orientation strategies during navigation.

Skylight polarisation patterns provide a critical navigational cue for many insects. Bees perceive these patterns through specialised ommatidia in the dorsal rim area of their compound eyes, enabling them to estimate the suns direction and navigate between food sources and the hive. Although polarisation-based navigation has been extensively studied behaviourally, computational models that link DRA anatomy with navigational performance are lacking. Here, we simulate polarisation vision in honeybees (Apis mellifera) and bumblebees (Bombus terrestris) using real sky polarisation images to capture biologically relevant skylight properties. Our biologically grounded simulation incorporates species-specific DRA anatomy, including ommatidial optical axis directions, photoreceptor receptive fields, and microvillar orientations. We evaluate navigational accuracy and consistency across sun elevations under two distinct, potentially complementary navigational models: the matched filter, which requires scanning across body orientations to identify the solar axis, and the vector-sum model, which generates instantaneous sun azimuth estimates from a single body orientation, making it independent of active scanning. Matched filter errors in estimating solar axis are below 5{degrees} across most sun elevations and in both species. Absolute errors in the vector-sum model are lower for honeybees than bumblebees (median [~]10{degrees} and [~]30{degrees}, respectively), reflecting differences in DRA anatomy, particularly viewing direction and microvillar arrangement. Both models allow stable course control across most sun elevations in both species, yet the matched filter, being limited to solar axis alignment, only enables positive or negative phototaxis. Overall, this work provides a mechanistic and comparative framework based on realistic DRA anatomy to study polarisation-based navigation, generating testable predictions for insect navigation under natural sky conditions. Author SummaryMany insects, including bees, navigate with the help of skylight polarisation patterns which hold information about the suns position even when it is not visible. Bees detect these patterns through the dorsal rim area (DRA) of their complex eyes. How differences in DRA anatomy between bee species translate into differences in navigational ability has remained unclear. Here, we built a biologically realistic simulation of polarisation vision in honeybees and bumblebees. We used real sky images to examine what polarisation information is available to each species. We then tested two models of sun position estimation based on the polarisation pattern: one that requires the bee to actively scan the sky, and one that generates an instantaneous estimate from a single body orientation. In both species, both models show that accurate sun position estimation and stable navigation are possible using just polarisation information under a wide range of sun elevations. Differences in navigational performance between honeybees and bumblebees arise because the two DRAs look at different parts of the sky. Our results provide a robust framework for understanding how DRA anatomy shapes polarisation-based navigation in bees.

In many insect species, mating is coordinated through multimodal signaling, yet less obvious channels are often overlooked. In the burying beetle Nicrophorus vespilloides, chemical communication is well-documented, but the role of substrate-borne vibrational signals (stridulations) during courtship remains unknown. We investigated whether stridulation is essential for mating success through two sets of experiments. First, we found a positive correlation between the frequency of stridulations and both the number and duration of copulation events. Second, we employed a silencing experiment to test the necessity of these signals by silencing males, females, or both partners. We found no significant differences between silenced and control groups regarding the frequency or duration of physical contact and mounting events, suggesting that stridulation is not required for mate recognition or the initiation of courtship. However, the proportion of successful copulations relative to mounting events was significantly lower when females were silenced. These results suggest that while N. vespilloides relies on a redundant multimodal system that likely utilizes chemical cues to initiate mating, vibrational signals, particularly from the female, may play a critical role in facilitating successful copulation. This study provides the first evidence for the role of stridulation in the mating behavior of N. vespilloides and highlights the potential for female-mediated vibrational signaling in burying beetle courtship.