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.

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.

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.

True crabs (Brachyura) are among the most iconic marine arthropods, representing noteworthy examples of morphological and ecological disparity. A striking feature of brachyurans are their anterior pincer-like appendages: chelipeds. These structures showcase a large diversity of morphologies that reflect ecology and overall multifunctionality. Yet, a comprehensive assessment of appendage functional morphology within phylogenetic and ecological trait contexts has never been attempted. By combining 3D geometric morphometrics, finite element analyses, multilocus molecular phylogeny, and ecological trait data for 80 crab species, including three fossil forms, we unveil a complex evolutionary history for crab chelipeds. Despite extreme shape diversity amongst chelipeds, stress distributions are very similar across taxa and hint a many-to-one pattern. High concentrations of chelipeds within constrained morphospace regions associated with peak pinch forces illustrates that brachyuran morphologies optimised for shell crushing may have arisen in the Cretaceous. Deviations from this morphospace highlight the diversification of non-shell-crushing life modes and the influence of sexual selection on appendages. Neither cheliped shape nor pinch force show phylogenetic signal. Together these results indicate that the evolution of cheliped shape is closely associated with, and inferred to have been strongly influenced by, crab ecology, biomechanical needs and sexual selection. SIGNIFICANCE STATEMENTChelipeds, the pincer-like claws of crabs, are among the most morphologically diverse appendages within Arthropoda, yet the evolutionary forces driving this diversity remain poorly understood. By integrating 3D geometric morphometrics, biomechanical modelling, molecular phylogeny, and ecological data across 80 crab species including fossil forms, we demonstrate that cheliped morphology is driven by ecology, biomechanical demands, and sexual selection rather than phylogenetic relatedness. The multifunctionality of these structures produces strong evidence for many-to-one mapping of form to function. Morphologies optimised for durophagy appear to have originated in the Cretaceous, with subsequent diversification into manipulative and sexually selected forms from a morphologically flexible foundation. These findings demonstrate that cheliped diversity reflects a complex interplay between ecological specialisation, biomechanical optimisation, and sexual selection across Brachyura.

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.

The energetic demands of courtship are central to sexual selection, but their magnitude and temporal variation remain poorly quantified in many signalling systems. We used closed-chamber respirometry and low-light video analysis to estimate courtship-associated metabolic rates in males of the bioluminescent ostracod Photeros sp. EGD. Low-activity metabolic rate varied strongly across the diel cycle: in small vessels that constrained movement, individually measured males consumed significantly more oxygen at night than during the day. We then compared oxygen consumption across vessels that differed in opportunities for movement and courtship. Metabolic rates were highest in large vessels that permitted bioluminescent courtship displays, intermediate in medium vessels that allowed swimming but not full displays, and lowest in small vessels that constrained movement. Oxygen consumption in large vessels at night was approximately 500% of small-vessel daytime rates, 280% of small-vessel nighttime rates, and 160% of medium-vessel nighttime rates. Because measurements integrated oxygen use over multi-hour intervals, these values represent time-averaged metabolic demand rather than instantaneous costs of individual light pulses or display trains. Video analyses suggested a positive association between signalling rate and oxygen consumption, although this relationship was not statistically supported in our large-vessel dataset, which had low statistical power. Together, these results show that male Photeros undergo strong diel shifts in metabolic state and that the whole-animal performance required to construct bioluminescent courtship displays may often impose substantial energetic demands.

The shift to terrestrial environments in ancestrally aquatic animals is often associated with key physiological and physical changes, including shifts in respiratory physiology and in some cases, even the evolution of completely novel respiratory structures. Examining how respiration operates across a gradient of submersion states in ancestrally aquatic terrestrial animals may shed light on how complex biological traits shift under different selective regimes. In this work, we begin exploring respiration in terrestrially-adapted land crabs that still use their gills to respire while underwater. We tested the relationship between aquatic respiratory rates, body size, and sex in red devil vampire crabs (Geosesarma hagen) at two ecologically-relevant temperatures. We found small females respire more than small males at 28{degrees}C, while large females respire more than large males at 21{degrees}C. Additionally, body size is a significant factor affecting respiratory rates of both sexes at 21{degrees}C and warmer temperatures significantly increase respiration in small crabs of both sexes. Interactions between these factors also led to emerging trends that can be explained by both physiological rules, such as reproductive investment and surface-to-volume ratios and heat transfer. We also report a temperature coefficient (Q10) of 1.52 for this species, showing an expected 52% change in respiratory and metabolic rate for every 10{degrees}C increase. This work also demonstrates the importance of understanding how and to what extent biological variables like sex and body size interact with abiotic environmental factors when measuring physiological traits in ectothermic invertebrate animals.

Brain size and structure are hypothesized to be adaptively designed to satisfy the behavioral requirements of securing food and living socially. The importance of these socioecological and sociobiological selective forces in brain evolution is constantly debated. Socioecological divergence is striking in the Neotropical ant genus Neoponera: N. apicalis is a generalist solitary predator forming small colonies of ~100 whereas N. commutata colonies are approximately 10 times as large and workers pheromonally organize cooperatively raids only on Syntermes termite colonies. We interspecifically compared the size and structure of the compound eyes, size and number of antennal glomeruli, mosaic brain scaling and synaptic processing (microglomeruli-MG). Our results indicate that N. apicalis workers have a larger number of ommatidia, antennal lobe glomeruli, and allometrically larger antennal and optic lobes than N. commutata. These sensory traits were associated with differences in higher-order processing architectures in the mushroom body (MB) microglomeruli (MG). N. commutata workers had an allometrically larger MB, perhaps due to their socially complex chemical foraging communication, although MG density in N. apicalis was higher in both the MB lip and collar, regions associated with processing olfactory and visual information, respectively. The increase in MG density in N. apicalis may be associated with higher demands for navigation, learning, and memory, as well as a higher density of antennal lobe glomeruli to support prey odor discrimination. In contrast, N. commutata workers had larger ommatidia and antennal lobe glomeruli. Larger ommatidia correlate with their diurnal/nocturnal habits and a larger MB Our findings indicate that differences in behavioral performance demands associated with socioecological differentiation are reflected in variation in visual and olfactory system structure, brain size, mosaicism, and synaptic organization. Our results support both social and ecological brain hypothesis as drivers of mosaic brain evolution.

Long-distance movement in insects has crucial impacts on agriculture, human health, and biodiversity. Although it was long assumed that only large, specialist insects had the navigation capacity to support long-distance dispersal, recent studies have demonstrated that smaller insects, such as the tiny fruit fly Drosophila melanogaster, can maintain extended, straight paths while flying or walking. This raises the question of whether other Drosophila species possess the navigation capacity to support extended dispersal. Resolving this question is particularly important for Drosophila suzukii(spotted-wing drosophila), a potent pest species that causes enormous damage worldwide to ripe fruit and berries. Spotted-wing drosophila has been thought to lack a capacity for long-distance dispersal, as prior studies have estimated maximal daily dispersal distances of less than 90 m. We developed a system to continuously track the flight trajectories of magnetically tethered D. suzukii relative to a discrete, overhead LED that mimicked the sun. We found that flies maintained remarkably straight flight headings that varied unpredictably across individuals. Male and female D. suzukii exhibited a similar navigation capacity; both sexes responded to rotation of a discrete sun stimulus with compensatory turns to maintain a stable relative heading. Our results suggest that D. suzukiihas an underappreciated capacity for rapid, radial dispersal, which could exceed 250 m in 15 min. This capacity may contribute to the pest species' invasiveness and its reliable, annual re-establishment in seasonally intolerable climates. Our findings highlight the importance of developing area-wide, regional strategies to manage the impacts of D. suzukii.

Sharks exhibit extraordinary morphological diversity across a wide range of ecological niches, yet large-scale, high-resolution digital datasets of their internal anatomy remain limited. Here we present an open-access 3D shark anatomical repository derived from published X-ray computed tomography (CT) data, featuring manually segmented and systematically annotated models of the chondrocranium, visceral arches, axial skeleton, musculature, and viscera in standard STL format. The dataset comprises 117 individuals, representing 72 species across 25 families and all nine extant shark orders, with 115 full-body reconstructions and two head-only models. This open-access dataset offers a comprehensive resource for comparative anatomy, biomechanical simulations, evolutionary developmental biology and biomimetics research of extant sharks.

Eusocial Hymenoptera present the highest known recombination rates among metazoans, which evolved several times independently among bees, ants and wasps. Several hypotheses have been proposed to explain this observation, including stronger selection for recombination caused by coevolving parasites and pathogens, and strong sexual selection among haploid males due to male-biased sex ratios among reproductive individuals. In this article, we explore the effects of haplodiploidy and differential selection between sexes on the evolution of recombination, by analyzing a three-locus model in which selection for recombination stems from negative epistasis between selected loci. Our analytical predictions are compared with the results of individual-based simulations in which deleterious mutations occur along a linear chromosome. Our results show that, at mutation-selection balance for deleterious alleles, increasing the strength of selection against deleterious alleles (due to the effect of male haploidy and/or sexual selection) tends to reduce selection for recombination. However, an increase in the overall magnitude of negative epistasis (which may also be due to male haploidy and/or sexual selection) combined with the fact that recombination only occurs in females may increase selection for recombination substantially. Our model also shows that, in conditions favoring recombination, increasing recombination in meioses leading to parthenogenetic ovules (and male offspring) may yield stronger benefits than in meioses leading to fertilized ovules (and female offspring).

To make adaptive foraging decisions, naive individuals need to gather information about the local prey community. Besides sampling prey personally, the young could gather information about prey profitability by observing the foraging behaviour of other individuals, and parental provisioning provides the first opportunity to acquire this social information. Still, previous research on vertical transmission of prey preferences from parents has provided mixed results that are often confounded with other information sources, such as siblings and peers. It is also not known whether information from parents can change potential innate biases against certain prey types, such as avoidance of warningly coloured insects. Here, we tested whether social information acquired by offspring during parental provisioning influences the development of prey preferences in a generalist predator, the Great Tit (Parus major). We brought 15 great tit broods and their parents into captivity at late nestling stage (14 days old) and divided them into three social information treatments where parents were provided with either brown, red or yellow palatable maggots to feed to their dependent young for 8 days. Once foraging independently from parents, we conducted a preference test where juveniles were offered the full array of coloured maggots. Regardless of palatable exposure to typical warning-coloured maggots (i.e. red and yellow), juveniles consistently preferred yellow over red, and preferred brown maggots the most (i.e. lacking warning coloration). This supports the existence of innate biases against typical warning colours, and that social information from parents is unlikely to override these, at least when alternative prey is easily available.

Behaviour innovation plays a pivotal role in a species adaptability to dynamic environments. Investigating innovative behaviour and its underlying mechanism is therefore crucial for elucidating the development of cognitive flexibility across animals. Animal personality--which shapes how individuals perceive and engage with their surroundings--could offer insights into individual variation in this process. This study used a three-step foraging puzzle to evaluate the innovation capacity in 28 rosy-faced lovebirds (Agapornis roseicollis), specifically examining their capacity to recombine individually innovated component behaviours into integrated, more sophisticated techniques. We found that nearly half of the individuals spontaneously innovated multiple component behaviours to solve novel puzzles. Crucially, when challenged with a more sophisticated task, they recombined these behaviours into functionally dependent sequences without prior social demonstration. We further identified sex, persistence, and asocial learning capacity as key predictors of innovative problem-solving performance, with females, persistent individuals, and superior asocial learners excelled at problem-solving. Our findings demonstrate that behavioural innovation is not a static event, but a dynamic process--modulated by physical, cognitive, and personality variables--in which behaviours are flexibly transferred and recombined into increasingly complex forms to enable rapid individual adaptation.

Age-dependent survival is central to understanding population dynamics and life-history evolution. We analysed carcass weight and age-at-harvest data from 6022 red foxes (Vulpes vulpes) collected across Sweden between 1967 and 1971 to evaluate latitudinal effects on body mass and age-dependent survival. Carcass weights decreased from south to north in both adults and sub-adults, contrary to Bergmann's rule, with southern foxes weighing approximately 1.27 times more than northern foxes. The latitudinal weight gradient exceeded the sex difference in both age classes, and no sex x region interaction was detected. The decrease in weight with latitude is consistent with reduced prey availability and harsher winter conditions in the north, which limit growth and body size during development. Using a Bayesian age-at-harvest model with region-specific population growth rates (lambda), we estimated age-dependent survival probabilities for four latitudinal regions and both sexes. Despite the strong latitudinal gradient in weight, survival did not show a corresponding pattern - regional differences were uncertain, with all credible intervals spanning zero. Regional population growth rates were consistent with slight decline in the north and near-stability in the south-central region, which suggests that body condition and population dynamics are coupled at the regional scale despite no survival gradient. The decoupling of body condition and survival across regions suggests that mortality patterns are similar across the latitudinal gradient. We discuss these patterns in terms of latitudinal productivity gradients, prey availability, and life-history trade-offs in a widely distributed carnivore.

Hearing in Lepidoptera mediates a range of ecologically important behaviours, including mate communication, predator avoidance, and acoustic signalling. In moths, the evolution of predator-prey interactions with bats has further shaped hearing through a sensory arms race, with repeated co-option of auditory organs to detect and evade echolocating predators. Despite significant prior characterization of the neurophysiology and behaviour of hearing in moths, the genetic basis of hearing is poorly understood in most insects. In this study, we identify a core set of putative auditory genes in Lepidoptera using a combination of homology-based searches from Drosophila and evolutionary rate analyses. We find 56 genes present across all species and investigate whether gene copy number varies among non-hearing and hearing lineages and among 3 different ear types. We discovered seven genes associated with ear type and one with ear presence, but did not find significant losses in gene copy number in non-hearing species. We identified three genes (btv, Dnai2, and nompB) with strong evidence of selection in hearing clades and five genes with weaker evidence of selection. We discuss the potential roles of btv, nompB, and Dnai2 in ciliary transport and the aging of hair cells, as well as the possibility of actively amplified hearing. Our study serves as a primer and resource for further gene mining and functional testing of auditory genes in moths and other insects.

Why male primates invest in costly behaviours producing public goods remains debated, with two leading explanations, paternal care and reputation-based partner choice (RBPC). Using long-term data from four groups of wild vervet monkeys, we tested: (1) whether males show a bias in four protective "male services" (predator alarm calling, participation in between-group conflicts, leading river crossings and sentinelling); (2) which males contribute most; and (3) whether service provision predicts mating success during the mating season. We confirmed a male bias in all services. Consistent with the paternal care hypothesis, contributions were positively associated with past mating success, independently of rank, although potential fathers did not contribute more than non-fathers. Among non-fathers, service provision varied with rank, suggesting that newly immigrated males adjust their behaviour according to competitive state. Crucially, variation in alarm calling and between-group conflicts predicted future mating success, with between-group conflict emerging as the strongest and most consistent predictor of mating success across years and within mating seasons, whereas rank, tenure and social integration added little explanatory power. In contrast, sentinelling and leading river crossings did not reliably translate into mating benefits. Our findings indicate that male services are shaped by multiple selective pressures operating across different male career stages and that some forms of public goods provision function as signals of quality and cooperativeness to females. By directly linking cooperative investment to mating outcomes in a wild primate, this study provides rare empirical support for reputation-based partner choice beyond humans and highlights female choice as a potentially important force in the evolution of cooperation.

Perception and action form a loop as an organism interacts with its environment. Here, we probe the interdependence between the two in the context of choice-history effects, the tendency of past choices and their outcomes to bias current choices. We investigated if the modulation by previous choices depended on the coupling between perceptual choices and the motor responses reporting these choices. We analyzed data from non-human primates (Macaca mulatta; three females and five males) performing two different perceptual decision-making tasks. Each task had a coupled variant with a fixed mapping between perceptual choices and motor plans used to report the choice, and an uncoupled variant, in which this mapping varied randomly across trials. We found that, in both tasks, the animals in the coupled variant had larger choice-history effects compared to the animals in the uncoupled variant. Decoupling choices from motor responses was further associated with an inability by the animals to learn experimentally induced stimulus sequence regularities. Together, these findings identify choice-response coupling as a factor shaping animals ability to use recent history to guide behavior and highlight the tight link between cognitive and motor processes.

Organisms have spent their life histories exposed to background levels of natural ionizing radiation. To document the role that radiation plays, the deprivation of these natural levels has been studied by incubating organisms in the shielded space of underground laboratories. We report here on two studies (Study I and Study II) using Aedes aegypti for the first time as a model organism incubated 655 meters underground at the Waste Isolation Pilot Plant (WIPP) outside of Carlsbad, New Mexico, U.S.A. Male mosquitos were incubated at the surface exposed to natural background radiation, and were compared to two underground treatments in which incubators were supplemented with radiation sources used to mimic background and these groups were compared to the underground, radiation-deprived treatment. In Study I, the mosquitos incubated underground in the absence of natural radiation had higher levels of mortality compared to those incubated at the surface and PCA plots of the two transcriptomes were clearly differentiated. Study II was conducted the following year and the experiment was narrowed to include only the surface control and underground, radiation-deprived treatment which allowed for four biological replicates. Again, there was a higher level of mortality in the mosquitos grown underground compared mosquitos grown at the surface. Transcriptomes were not as clearly differentiated by PCA analysis and fecundity data were similar between the two groups. Functional analysis of transcriptomic DEGs from two independent studies suggested there are stress responses in radiation deprived mosquitoes. The absence of a secondary stressor in Study II is discussed as an explanation for the transcriptome differences in the two experiments.

Fossil data is crucial to construct phylogenetic time trees, which serve as the basis to test a wide range of evolutionary hypotheses. While the fossil record is known to be incomplete, modern stratigraphy provides predictions of the structure of the fossil record as expressed by gap location and duration. Advances in phylogenetic model development allow us to propagate this information into Bayesian phylogenetic inference in the form of priors on time-variable fossil sampling. However, the impact and role of stratigraphic architectures on time tree inference has so far remained unexplored. We introduce a novel simulation framework that combines realistic stratigraphic forward models with phylogenetic simulations. Using this framework, we examine (1) how stratigraphically plausible model violations of fossil sampling due to gaps affect total-evidence inference under the fossilized birth-death model and (2) if stratigraphic knowledge on gap duration and timing improves inference when incorporated in priors on fossil sampling. We find that total-evidence analysis is robust to stratigraphically plausible distribution of gaps in disparate stratigraphic architectures, with results being instead dominated by the number of morphological characters. Surprisingly, incorporating information on prominent gaps in the stratigraphic record does not improve phylogenetic inference. Our results suggest that phylogenetic inference is robust to model violations introduced by stratigraphic gaps over short timescales, with results being dominated by a priori known data availability constraints such as morphological character matrix size. This research establishes the foundations for joint modeling of phylogenetic and stratigraphic processes and narrows the knowledge gap between paleontology, stratigraphy, and neontology.

Fat accumulation and use is critical for sustaining life. Most insects show a typical response to feeding where fat is accumulated when sufficient sugars and other carbohydrates are consumed. Parasitoid insects are an exception, because most species do not accumulate fat when feeding on a sugar-rich diet. Studies on fat metabolism generally measure fat content early in life without considering lipid metabolism as a dynamic process that is expected to change as life progresses. In this paper, we compared fat accumulation and use throughout the lives of adult female Drosophila melanogaster and females of 5 inbred lines of the parasitoid wasp Leptopilina heterotoma. We expected that fat accumulation would take place irrespective of teneral fat content in D. melanogaster. We found that fat D. melanogaster initially used fat reserves, while lean flies economized on fat stores. Both lean and fat flies started accumulating fat after 7 days of life, indeed showing a typical response for insects. Unlike other parasitoids, L. heterotoma populations differs in fat accumulation patterns that we expected to observe also between inbred lines. In none of the inbred lines, however, did fat accumulation take place. Our results did reveal that inbred lines differed in the rate at which fat was used mainly later during life. We further confirmed that D. melanogaster pupal size was highly correlated with adult female size for both D. melanogaster and L. heterotoma. Overall, our findings for L. heterotoma provide strong evidence that genetic background has a major impact on the rate at which fat is used over a lifetime.