Proceedings of the Royal Society B

Ecology is a key driver of morphological evolution during adaptive radiations, but alternative factors like phylogeny and allometry can have a strong influence on morphology. Lepidosaurs, the most diverse clade of tetrapods, including lizards and snakes, have evolved a remarkable variety of forms and adapted to disparate ecological niches, representing an ideal case study to understand drivers of morphological evolution. Here, we quantify morphological variation in the lower jaw using three-dimensional geometric morphometrics on a broad sample of 153 lepidosaur species. Our results suggest that phylogeny has significantly influenced mandibular shape evolution, and snakes have diverged from a lizard-like jaw morphology during their evolution. Allometry and ecological factors like diet, foraging mode and substrate also appear to drive the diversification of mandibular forms. Ecological groups differ in patterns of disparity, convergence and rates of evolution, indicating that divergent evolutionary mechanisms are responsible for the acquisition of different diets and habitats. Our analyses support that lepidosaurs ancestrally use their jaws to capture prey, contrary to the traditional view favouring lingual prehension as ancestral. Specialized or ecologically diverse lineages show high rates of jaw shape evolution, suggesting that morphological innovation in the mandible has contributed to the spectacular ecomorphological diversification of lepidosaurs.

The evolution of diverse and novel morphological traits is poorly understood, especially how symbiotic interactions can drive these adaptations. The extreme diversity of external traits in insect-induced galls is currently explained by the Enemy Hypothesis, in which these traits have selective advantage in deterring parasitism. While previous tests of this hypothesis used only taxonomic identity, we argue that ecologically functional traits of enemies (i.e. mode of parasitism, larval development strategy) are a crucial addition. Here, we characterize parasitoid guild composition across four disparate gall systems and find consistent patterns of association between enemy guild and gall morphology. Specifically, galls with a longer average larva-to-surface distance host a significantly higher proportion of enemies with a distinct combination of functional traits (i.e. ectoparasitic, idiobiont, elongate ovipositor). Our results support the Enemy Hypothesis and highlight the importance of species ecology in examining insect communities and the evolution of novel defensive characters.

Understanding the roles of habitat filtering, dispersal limitations and biotic interactions in shaping the organization of animal communities is a central research goal in ecology. Attempts to extend these approaches into deep time have the potential to illuminate the role of these processes over key intervals in evolutionary history. The Ediacaran marks one such interval, recording the first macroscopic benthic communities and a stepwise intensification in animal ecosystem engineering. Here, we use taxonomic co-occurrence analysis to evaluate how community structure shifted through the late Ediacaran and the role of different community assembly processes in driving these changes. We find that community structure shifted significantly throughout the Ediacaran, with the most dramatic shift occurring at the White Sea–Nama boundary (approx. 550 Ma) characterized by a split between older, more enigmatic taxonomic groups (the ‘Ediacara-type’ fauna) and more recognizable (‘Cambrian-type’) metazoans. While ecosystem engineering via bioturbation is implicated in this shift, dispersal limitations also played apart in separating biota types. We hypothesize that bioturbation acted as a local habitat filter in the late Ediacaran, selecting against genera adapted to microbial mat ecosystems. Ecosystem engineering regime shifts in the Ediacaran may thus have had a large impact on the development of subsequent metazoan communities.

People use the mechanical interplay between stability and manoeuvrability to successfully walk. During single-limb support, body states (position and velocity) that increase in lateral stability will inherently resist lateral manoeuvres, decrease medial stability and facilitate medial manoeuvres. Although not well understood, people can make behavioural decisions exploiting this relationship in anticipation of perturbations or direction changes. To characterize the behavioural component of the stability–manoeuvrability relationship, 24 participants performed many repetitions of a discrete stepping task involving mid-trial reactive manoeuvres (medial or lateral direction) in a Baseline (no external perturbations) and Perturbed (random mediolateral perturbations applied to their pelvis) environment. We hypothesized people would make systematic changes in lateral stability dependent on both environment (increasing lateral stability in the Perturbed environment) and anticipated manoeuvre direction (reducing lateral stability to facilitate lateral manoeuvres). Participants increased lateral stability in the Perturbed environment, coinciding with an increase in manoeuvre reaction time for laterally but not medially directed manoeuvres. Moreover, we observed lower lateral stability in both environments when people anticipated making a lateral manoeuvre when compared to medial manoeuvres. These results support the hypothesis that people behaviourally exploit the mechanical relationship between lateral stability and manoeuvrability depending on walk task goals and external environment.

The ability to understand relational concepts, such as ‘same’ and ‘different’, is a critical feature of human cognition. To what extent non-human animals can acquire such concepts and which factors influence their learning are still unclear. We examined the acquisition and the breadth of understanding the ‘same–different’ concept in budgerigars (Melopsittacus undulatus). Budgerigars trained to discriminate stimulus pairs in which two identical figures were either the same or different size (Experiment 1) successfully generalized the discrimination to novel stimuli belonging to various categories (size, colour, shape, geometric type and number of dots). The results of Experiment 1 thus demonstrate that budgerigars can perceive and generalize the same–different concept across dimensions after training with a limited set of stimuli differing along a single dimension. In contrast, while most budgerigars trained to discriminate two pairs of discs that were either the same or different in colour (Experiment 2) could generalize the discrimination to novel stimuli within the training category (colour), only few generalized the discrimination to another category suggesting a generalization based on perceptual similarity. The results thus show that whether budgerigars generalize a relationship by conceptual or perceptual similarity depends on the nature of the training stimuli.

Bending the curve of biodiversity loss requires the business and financial sectors to disclose and reduce their biodiversity impacts and help fund nature recovery. This has sparked interest in developing generalizable, standardized measurements of biodiversity—essentially a ‘unit of nature’. We examine how such units are defined in the rapidly growing voluntary biodiversity credits market and present a framework exploring how biodiversity is quantified, how delivery of positive outcomes is detected and attributed to the investment and how the number of credits issued is adjusted to account for uncertainties. We demonstrate that there are deep uncertainties throughout the process and question if the benefits of biodiversity credits, and other efforts to abstract nature to a single unit, outweigh the harms. Credits can only be positive for biodiversity if they are used with unprecedentedly strict regulation that ensures businesses mostly avoid negative impacts and if they are purchased to quantify positive contributions rather than as direct offsets. While there may be a role for markets in attracting conservation funding, they will only ever be part of the solution, especially for the many aspects of nature that cannot be reduced to a unit.

The migratory movements undertaken by birds are among the most energetically demanding behaviours observed in nature. Mitochondria are the source of aerobic energy production on which migration depends, but a key component of mitochondrial function, mitochondrial remodelling, has not been investigated in the context of bird migration. We measured markers of mitochondrial remodelling in the skeletal muscles of the Gambel’s (migratory) and Nuttall’s (non-migratory) white-crowned sparrows within and outside migratory periods. Gambel’s were collected in (i) a non-migration period (baseline), (ii) preparation to depart for spring migration (pre-migration) and (iii) active autumn migration (mid-migration). Nuttall’s were collected at timepoints corresponding to baseline and mid-migration in Gambel’s. Across all sampling periods, we found that migratory birds had greater mitochondrial remodelling compared with non-migratory birds. Furthermore, birds from the migratory population also displayed flexibility, increasing several markers of mitochondrial remodelling (e.g. NRF1, OPA1 and Drp1) pre- and during migration. Further, the greater levels of mitochondrial remodelling and its upregulation during migration were specific to the pectoralis muscle used in flapping flight. Our study is the first to show that mitochondrial remodelling supports migration in Gambel’s white-crowned sparrows, indicating a highly specific and efficient phenotype supporting the increased energetic demands of migration.

Microbial populations are often exposed to long-term abiotic disturbances, which can reduce population viability and cause local extinction. Eco-evolutionary theory suggests that spatial refuges can facilitate persistence and evolutionary rescue. However, one drawback of spatial refuges is reduced exposure to nutrients such as carbon and oxygen, suggesting the protective effect of refuges depends on the interplay between environmental conditions and the degree of stress. Here, we test this general idea using mathematical modelling, and experimental evolution of the model bacterium Pseudomonas fluorescens SBW25 under salinity stress. As our model predicted, we find that the ability of spatial refuges to rescue evolving populations from extinction crucially depends on nutrient availability. Populations evolving under salinity stress where nutrient-rich spatial refuges were available, harboured clones that displayed enhanced salt resistance, indicating that nutrient-rich spatial refuges can facilitate evolutionary rescue. Furthermore, while control-salinity-evolved populations adapted to spatial structure by evolving enhanced motility (likely through parallel mutations in PFLU_4551, a predicted aerotaxis response regulator), this phenotype was constrained under high salinity, because increased motility negates the benefits of a spatial refuge. Our results reveal a general interplay between spatial refuges and nutrient availability that could be leveraged to reduce extinction risk in natural populations.

Some predators depend heavily on one or a few prey types, and others have exceptionally broad diets. It is unclear how this diet variation arises. Here, we demonstrate a strong link between diet species richness and Shannon entropy of prey frequencies (a diet diversity spectrum) for a globally distributed group of apex predators–raptors. For many raptors, diet entropy is consistent with random sampling expectations given a lognormal distribution of abundances among prey species. Yet most species-rich diets often approach the maximum possible diet entropy, indicating an unexpected level of diet evenness that is not predicted by theory. Positioning along this diet diversity spectrum is linked to evolutionary history, the types of prey that are acceptable and the role of raptors as food web integrators through cross-habitat sampling. These results suggest that raptors may have a highly stabilizing effect on terrestrial food webs and play an important role in maintaining biodiversity.

Genomes encode elaborate networks of genes whose products must seamlessly interact to support living organisms. Humans’ capacity to understand these biological systems is limited by their sheer size and complexity. In this article, we develop a proof of concept framework for training a machine learning (ML) algorithm to model bacterial genome composition. To achieve this, we create simplified representations of genomes in the form of binary vectors that indicate the encoded genes, henceforth referred to as genome vectors. A denoising variational autoencoder was trained to accept corrupted genome vectors, in which most genes had been masked, and reconstruct the original. The resulting model, DeepGenomeVector, effectively captures complex dependencies in genomic networks, as evaluated by both qualitative and quantitative metrics. An in-depth functional analysis of a generated genome vector shows that its encoded pathways are interconnected, near complete, and ecologically cohesive. On the test set, where the model’s ability to reconstruct uncorrupted genome vectors was evaluated, Area Under the Receiver Operating Curve (AUROC) and F1 scores of 0.98 and 0.83, respectively, support the model’s strong performance. This article showcases the power of ML approaches for synthetic biology and highlights the possibility that artifical intelligence agents may one day be able to design genomes that animate carbon-based cells.

Climate change is exacerbating a global decline in biodiversity. Numerous observational studies link rising temperatures to declining biological abundance, richness and diversity in terrestrial ecosystems, yet few studies have considered the highly diverse and functionally significant communities of tropical forest soil and leaf litter fauna. Here, we report major declines in the order-level richness and diversity of soil and leaf litter fauna following three years of experimental whole-profile soil warming in a tropical forest. These declines were greatest during the dry season, suggesting that warming effects could be exacerbated by drought. Contrary to findings from higher latitudes, total faunal abundance increased under warming, and these effects were paralleled by major shifts in community composition. These responses were driven by increased dominance of a relatively small number of thermophilic taxa, and of oribatid mites in particular. Our study provides direct experimental evidence that warming causes diversity declines and compositional shifts for tropical forest soil and leaf litter fauna, a result with potential consequences for soil functions and biogeochemical cycles, and that highlights the vulnerability of tropical biodiversity to climate change.

Many invertebrates exhibit parental care, posited as a precursor to sociality. For example, solitary foundresses of the facultative social orchid bee Euglossa viridissima guard their brood for 6+ weeks before offspring emerge, when the nest may become social. Guarding comes at the fitness cost of foregoing the production of additional offspring. Yet it is unclear whether guarding (extended maternal care) can enhance offspring survival such that it outweighs those fitness costs, or if it is a consequence of the selective benefits of sociality, including extended female longevity. Experimental removal of solitary foundresses from nests of E. viridissima revealed an immediate fitness loss: decreased offspring survival. A mathematical model exploring the trade-off between extended maternal care versus non-guarding revealed that extended maternal care is immediately advantageous to a solitary mother if nest establishment takes longer than a threshold 1.7–12.5 days. Below this threshold, our model suggests that social fitness gains (acquiring helper daughters) need to be invoked to explain the evolution of extended maternal care. Enhanced survival of offspring through guarding and nest inheritance may nevertheless ease conditions for the evolution of sociality by favouring extended adult longevity and brood care in incipient social species like E. viridissima.

Emotional contagion occurs in many animals, including rodents. To determine the social signals of emotional state-matching between individuals in mice, we conducted an empirical laboratory experiment using visual, olfactory and auditory stimuli. The Japanese wild-derived mouse strain MSM/Ms (MSM) was tested as observers, since our initial experiments indicated that MSM mice showed higher sensitivity to others’ pain compared with the laboratory strain C57BL/6J (B6). MSM observers were shown footage of an unfamiliar B6 mouse receiving painful foot shocks via a screen. For olfactory stimuli, one of the following was presented during observation: (i) urine collected from a shocked B6 mouse, (ii) urine collected from an unshocked B6 mouse, or (iii) reverse osmosis water. Consequently, MSM mice observing the footage with urine from shocked mice demonstrated significantly higher fear-induced freezing behaviour than in the other two conditions. Regarding visual and auditory stimuli, observing the pixelated video clip was significantly associated with reduced freeze responses, whereas blocking auditory cues did not affect the duration of freezing. These results provide clear-cut evidence that multiple cues, including olfactory and visual information, are sufficient social signals for emotional contagion in mice.

Pharmaceutical pollution poses an increasing threat to global wildlife populations. Psychoactive pharmaceutical pollutants (e.g. antidepressants, anxiolytics) are a distinctive concern owing to their ability to act on neural pathways that mediate fitness-related behavioural traits. However, despite increasing research efforts, very little is known about how these drugs might influence the behaviour and survival of species in the wild. Here, we capitalize on the development of novel slow-release pharmaceutical implants and acoustic telemetry tracking tools to reveal that exposure to environmentally relevant concentrations of the benzodiazepine pollutant temazepam alters movement dynamics and decreases the migration success of brown trout (Salmo trutta) smolts in a natural lake system. This effect was potentially owing to temazepam-exposed fish suffering increased predation compared with unexposed conspecifics, particularly at the river–lake confluence. These findings underscore the ability of pharmaceutical pollution to alter key fitness-related behavioural traits under natural conditions, with likely negative impacts on the health and persistence of wildlife populations.

As a social species, humans live in complexly bounded social groups. In order to navigate these networks, humans rely on a set of social–cognitive processes, including social working memory. Here, we designed a novel network memory task to study working memory for social versus non-social network information across 241 participants (18–65 years) in a tightly controlled, preregistered study. We show that humans demonstrate a working memory advantage for social, relative to non-social, network information. We also observed a self-relevant positivity bias, but an ‘other’ negativity bias. These findings are interpreted in the context of an evolutionary need to belong to one’s social group, to identify risks to one’s social safety and to appropriately track one’s social status within a complex network of social relationships.

The potential for aquatic gastropods to display phenotypic plasticity in response to predator cues is well documented. However, long-term phenotypic responses to predator exposure are difficult to evaluate at large scales in the field. Thus, the extent to which comparatively dilute predator cues experienced by natural snail populations influence morphometric development and whether energetic costs associated with defensive morphology have allometric impacts on other life-history characteristics is unclear. The 2013 sea star wasting disease outbreak in central California, USA provided a unique framework for a large-scale natural predator removal experiment, comparing the shell morphometrics and gonadosomatic index of subtidal Tegula turban snail populations at kelp forest sites where local predatory sea stars were completely absent or nearly so (SS−), with paired sites maintaining low predator densities (SS+). All three snail species displayed higher proportional allocation to shell mass at SS+ locations and concomitantly higher reproductive allocation with predators absent (SS−). Dietary stable isotope analysis suggests this may be partially an energetic consequence of behavioural grazing shifts displayed by snails following predator release. Interestingly, morphometric shifts in shell structure differed among the three Tegula species and appeared closely related to species-specific predator avoidance strategies.

Improving evolutionary forecasting requires progressing from studying repeated evolution of a single genotype under identical conditions to formulating broad principles. These principles should enable predictions of how similar species will adapt to similar selective pressures. Evolve-and-resequence experiments with multiple species allow testing forecasts on different biological levels and elucidating the causes for failed predictions. Here, we show that forecasts for adaptation to static culture conditions can be extended to multiple species by testing previous predictions for Pseudomonas syringae and Pseudomonas savastanoi. In addition to sequence divergence, these species differ in their repertoire of biofilm regulatory genes and structural components. Consistent with predictions, both species repeatedly produced biofilm mutants with a wrinkly spreader phenotype. Predominantly, mutations occurred in the wsp operon, with less frequent promoter mutations near uncharacterized diguanylate cyclases. However, mutational patterns differed on the gene level, which was explained by a lack of conservation in relative fitness of mutants between more divergent species. The same mutation was the most frequent for both species suggesting that conserved mutation hotspots can increase parallel evolution. This study shows that evolutionary forecasts can be extended across species, but that differences in the genotype–phenotype–fitness map and mutational biases limit predictability on a detailed molecular level.

In malaria-endemic regions, Plasmodium vivax and Plasmodium falciparum coexist and may interact. For instance, fevers induced by P. falciparum might activate dormant P. vivax parasites and concurrent radical cure of both species has been proposed to prevent relapses. Heterogeneous mosquito exposure may contribute to the dependence of both parasites. We conducted a literature review on their respective prevalence and that of co-infections. The data revealed a positive correlation between P. vivax and P. falciparum prevalence, and co-infection prevalences exceeding expectations assuming infections occur independently. We used the review data to fit a compartmental model of co-infections that features heterogenous mosquito exposure. The fit suggests that heterogeneous exposure sufficiently explains the observed departure from independence. Finally, we performed simulations under the model assessing the impact on P. vivax prevalence of the activation-by-fever hypothesis and the radical cure proposition. We demonstrated a moderate impact of allowing P. falciparum fevers to reactivate P. vivax and a substantial impact of treating P. falciparum cases with radical cure. Our model highlights dependence between P. falciparum and P. vivax and emphasizes the influence of heterogeneous mosquito exposure. This simple framework can inform the design of more complex models assessing integrated malaria control strategies in coendemic regions.

Phenological responses to climate change vary across trophic levels. However, how trophic phenological synchrony determines species’ distributions through its effects on population dynamics has rarely been addressed. Here, we show that phenological variation underlies population and geographical range dynamics in a range-shifting herbivore, and demonstrate its interplay with changing trophic interactions. Using a novel modelling approach, we identify drivers of variation in phenology and population growth (productivity) for populations of the brown argus butterfly (Aricia agestis) feeding on ancestral and novel host plants in the UK. We demonstrate host plant-specific links between phenology and productivity, highlighting their role in the consumer’s range expansion. Critically, later butterfly phenology is associated with higher productivity in the annual second brood, especially on novel annual hosts where later activity improves synchrony with germinating plants. In turn, later phenology and higher second brood productivity are associated with more rapid range expansion, particularly in regions where only the novel hosts occur. Therefore, phenological asynchrony imposes limits on local population growth, influencing consumer resource selection, evolutionary responses and emergent range dynamics. How existing and future trophic phenological synchrony determine population dynamics will be critical for the ecological and evolutionary outcomes of climate change.

Rhythm is an important component of human language and music production. Rhythms such as isochrony (intervals spaced equally in time) are also present in vocalizations of certain non-human species, including several birds and mammals. This study aimed to identify rhythmic patterns with music-based methods within the display behaviour of chimpanzees (Pan troglodytes), humans’ closest living relatives. Behavioural observations were conducted on individuals from two zoo-housed colonies. We found isochronous rhythms in vocal (e.g. pants, grunts and hoots) as well as in motoric (e.g. swaying and stomping) behavioural sequences. Among individuals, variation was found in the duration between onsets of behavioural elements, resulting in individual-specific tempi. Despite this variation in individual tempi, display sequences were consistently structured with stable, isochronous rhythms. Overall, directed displays targeted at specific individuals were less isochronous than undirected displays. The presence of rhythmic patterns across two independent colonies of chimpanzees suggests that underlying mechanisms for rhythm production may be shared between humans and non-human primates. This shared mechanism indicates that the cognitive requirements for rhythm production potentially preceded human music and language evolution.

With its bag-like appearance, spiny ornament and single opening, Saccorhytus coronarius is one of the most enigmatic animals of the early Cambrian Kuanchuanpu Formation (ca 535 Ma) and has been at the heart of debates concerning the origin of two major animal lineages: the deuterostomes and the ecdysozoans. Although Ecdysozoa is now the most plausible option, key aspects of its palaeobiology have remained elusive. I suggest here that Saccorhytus was the possible larval stage of one of the numerous scalidophoran worms that co-existed with it in the Kuanchuanpu biota, especially those with bilateral pairs of broad-based sclerites such as Eokinorhynchus. This new interpretation is mainly based on the development of extant priapulid worms (Scalidophora). It would imply that Saccorhytus is a non-feeding larva and that its enigmatic single aperture with a pleated structure is not a mouth but more likely the opening through which the juvenile exited. Thus, the strange anatomy of Saccorhytus could be explained in a simple way without involving complex evolutionary processes (e.g. simplification, miniaturization, loss of anus, etc.). Instead of being a relatively basal member of the total group Ecdysozoa, Saccorhytus would find a more likely position among the total group Scalidophora.

Predators exert a powerful selective force, however, predator avoidance can conflict with other important activities such as attracting mates. Decisions over whether to court mates versus avoiding predators are vital to fitness, yet the mechanistic underpinnings of how animals manage such tradeoffs are poorly understood. Here, we investigate the flexibility of behaviour and gene regulation in response to a tradeoff between avoiding predators (survival) and courting potential mates (reproduction) in three-spined stickleback (Gasterosteus aculeatus). We compared behavioural and transcriptomic responses of male sticklebacks faced with a courtship opportunity and cues of a predator simultaneously with the responses of males faced with a courtship opportunity or cues of a predator alone, and found that males behaviourally compromised courtship in favour of predator avoidance when faced with a tradeoff between them. The need to manage this tradeoff elicited dynamic changes in brain gene expression, and sets of functionally connected genes were organized into discrete modules based on co-expression. Additionally, we found that behavioural flexibility in response to tradeoffs corresponded to flexibility in gene regulatory network structure. Combined, these results uncover the coordinated response by the brain to a fundamental ecological tradeoff, providing insight into the structure and function of genetic networks underpinning how animals make fitness-influencing decisions.

Organisms capture energy to support growth, survival and reproduction in diverse ways. Larger metazoans require less energy per unit time and mass than smaller ones. Thus, structures animals build to capture energy need not scale isometrically with body size. Web-building spiders use silk structures of diverse geometries to capture energy, including two-dimensional orbs in some families or three-dimensional tangles or sheet-and-tangles, in others. Despite this diversity, we show that energy consumption rate per unit mass scaled identically with body size across all web geometries with a less than 1 : 1 relationship to body size, as expected for metazoans from metabolic theory. Spiders thus appear to adjust the size and shape of their webs in precise ways to attain this relationship, including, as we show here, creating a hollow space within certain three-dimensional web types to maintain a constant prey capture surface area per unit spider mass as they grow in size without requiring more silk. Our findings show how the allometric relationship between energetic traits and body size can be mediated by extended phenotypes and suggest an equivalence paradigm akin to the equal fitness paradigm whereby the diverse adaptive strategies of organisms allow them to perform equally well in supplying a unit of mass the energy needed across a lifetime.

Behavioural avoidance of parasites in the environment generates what is known as the ‘landscape of disgust’ (analogous to the predator-induced ‘landscape of fear’). Despite the potential for improving our inference of host–parasite dynamics, three limitations of the landscape of disgust restrict the insight that is gained from current research: (i) many host–parasite systems will not be appropriate for invoking the landscape of disgust framework; (ii) existing research has primarily focused on immediate choices made by hosts on small scales, limiting predictive power, generalizability, and the value of the insight obtained; and (iii) relevant ecological and evolutionary theory has yet to be integrated into the framework, challenging our ability to interpret the landscape of disgust within the context of most host–parasite systems. In this review, we explore the specific requirements for implementing a landscape of disgust framework in empirical systems. We also propose greater integration of habitat selection and evolutionary theories, aiming to generate novel insight, by exploring how the landscape of disgust varies within and across generations, presenting opportunities for future research. Despite interest in the impacts of parasitism on animal movement and behaviour, many unanswered questions remain.