Showing papers in "Proceedings of The Royal Society B: Biological Sciences in 2017"

Mitochondrial phylogenomics of Hemiptera reveals adaptive innovations driving the diversification of true bugs.

Abstract: Hemiptera, the largest non-holometabolous order of insects, represents approximately 7% of metazoan diversity. With extraordinary life histories and highly specialized morphological adaptations, hemipterans have exploited diverse habitats and food sources through approximately 300 Myr of evolution. To elucidate the phylogeny and evolutionary history of Hemiptera, we carried out the most comprehensive mitogenomics analysis on the richest taxon sampling to date covering all the suborders and infraorders, including 34 newly sequenced and 94 published mitogenomes. With optimized branch length and sequence heterogeneity, Bayesian analyses using a site-heterogeneous mixture model resolved the higher-level hemipteran phylogeny as (Sternorrhyncha, (Auchenorrhyncha, (Coleorrhyncha, Heteroptera))). Ancestral character state reconstruction and divergence time estimation suggest that the success of true bugs (Heteroptera) is probably due to angiosperm coevolution, but key adaptive innovations (e.g. prognathous mouthpart, predatory behaviour, and haemelytron) facilitated multiple independent shifts among diverse feeding habits and multiple independent colonizations of aquatic habitats.

The sources of adaptive variation

Abstract: The role of natural selection in the evolution of adaptive phenotypes has undergone constant probing by evolutionary biologists, employing both theoretical and empirical approaches. As Darwin noted...

Fear of the human 'super predator' reduces feeding time in large carnivores.

Abstract: Large carnivores' fear of the human 'super predator' has the potential to alter their feeding behaviour and result in human-induced trophic cascades. However, it has yet to be experimentally tested if large carnivores perceive humans as predators and react strongly enough to have cascading effects on their prey. We conducted a predator playback experiment exposing pumas to predator (human) and non-predator control (frog) sounds at puma feeding sites to measure immediate fear responses to humans and the subsequent impacts on feeding. We found that pumas fled more frequently, took longer to return, and reduced their overall feeding time by more than half in response to hearing the human 'super predator'. Combined with our previous work showing higher kill rates of deer in more urbanized landscapes, this study reveals that fear is the mechanism driving an ecological cascade from humans to increased puma predation on deer. By demonstrating that the fear of humans can cause a strong reduction in feeding by pumas, our results support that non-consumptive forms of human disturbance may alter the ecological role of large carnivores.

Spatio-temporal interactions facilitate large carnivore sympatry across a resource gradient

Abstract: Species within a guild vary their use of time, space and resources, thereby enabling sympatry. As intra-guild competition intensifies, such behavioural adaptations may become prominent. We assessed...

Odours from marine plastic debris induce food search behaviours in a forage fish

Abstract: Plastic pollution is an anthropogenic stressor in marine ecosystems globally. Many species of marine fish (more than 50) ingest plastic debris. Ingested plastic has a variety of lethal and sublethal impacts and can be a route for bioaccumulation of toxic compounds throughout the food web. Despite its pervasiveness and severity, our mechanistic understanding of this maladaptive foraging behaviour is incomplete. Recent evidence suggests that the chemical signature of plastic debris may explain why certain species are predisposed to mistaking plastic for food. Anchovy (Engraulis sp.) are abundant forage fish in coastal upwelling systems and a critical prey resource for top predators. Anchovy ingest plastic in natural conditions, though the mechanism they use to misidentify plastic as prey is unknown. Here, we presented wild-caught schools of northern anchovy (Engraulis mordax) with odour solutions made of plastic debris and clean plastic to compare school-wide aggregation and rheotactic responses relative to food and food odour presentations. Anchovy schools responded to plastic debris odour with increased aggregation and reduced rheotaxis. These results were similar to the effects food and food odour presentations had on schools. Conversely, these behavioural responses were absent in clean plastic and control treatments. To our knowledge, this is the first experimental evidence that adult anchovy use odours to forage. We conclude that the chemical signature plastic debris acquires in the photic zone can induce foraging behaviours in anchovy schools. These findings provide further support for a chemosensory mechanism underlying plastic consumption by marine wildlife. Given the trophic position of forage fish, these findings have considerable implications for aquatic food webs and possibly human health.

Independent evolution of baleen whale gigantism linked to Plio-Pleistocene ocean dynamics.

Abstract: Vertebrates have evolved to gigantic sizes repeatedly over the past 250 Myr, reaching their extreme in today's baleen whales (Mysticeti). Hypotheses for the evolution of exceptionally large size in mysticetes range from niche partitioning to predator avoidance, but there has been no quantitative examination of body size evolutionary dynamics in this clade and it remains unclear when, why or how gigantism evolved. By fitting phylogenetic macroevolutionary models to a dataset consisting of living and extinct species, we show that mysticetes underwent a clade-wide shift in their mode of body size evolution during the Plio-Pleistocene. This transition, from Brownian motion-like dynamics to a trended random walk towards larger size, is temporally linked to the onset of seasonally intensified upwelling along coastal ecosystems. High prey densities resulting from wind-driven upwelling, rather than abundant resources alone, are the primary determinant of efficient foraging in extant mysticetes and Late Pliocene changes in ocean dynamics may have provided an ecological pathway to gigantism in multiple independent lineages.

Sex chromosome evolution: historical insights and future perspectives

Abstract: Many separate-sexed organisms have sex chromosomes controlling sex determination. Sex chromosomes often have reduced recombination, specialized (frequently sex-specific) gene content, dosage compensation and heteromorphic size. Research on sex determination and sex chromosome evolution has increased over the past decade and is today a very active field. However, some areas within the field have not received as much attention as others. We therefore believe that a historic overview of key findings and empirical discoveries will put current thinking into context and help us better understand where to go next. Here, we present a timeline of important conceptual and analytical models, as well as empirical studies that have advanced the field and changed our understanding of the evolution of sex chromosomes. Finally, we highlight gaps in our knowledge so far and propose some specific areas within the field that we recommend a greater focus on in the future, including the role of ecology in sex chromosome evolution and new multilocus models of sex chromosome divergence.

Neonicotinoid pesticides and nutritional stress synergistically reduce survival in honey bees.

Abstract: The honey bee is a major pollinator whose health is of global concern. Declines in bee health are related to multiple factors, including resource quality and pesticide contamination. Intensive agricultural areas with crop monocultures potentially reduce the quality and quantity of available nutrients and expose bee foragers to pesticides. However, there is, to date, no evidence for synergistic effects between pesticides and nutritional stress in animals. The neonicotinoids clothianidin (CLO) and thiamethoxam (TMX) are common systemic pesticides that are used worldwide and found in nectar and pollen. We therefore tested if nutritional stress (limited access to nectar and access to nectar with low-sugar concentrations) and sublethal, field-realistic acute exposures to two neonicotinoids (CLO and TMX at 1/5 and 1/25 of LD50) could alter bee survival, food consumption and haemolymph sugar levels. Bee survival was synergistically reduced by the combination of poor nutrition and pesticide exposure (-50%). Nutritional and pesticide stressors reduced also food consumption (-48%) and haemolymph levels of glucose (-60%) and trehalose (-27%). Our results provide the first demonstration that field-realistic nutritional stress and pesticide exposure can synergistically interact and cause significant harm to animal survival. These findings have implications for current pesticide risk assessment and pollinator protection.

Open data and digital morphology

Abstract: Over the past two decades, the development of methods for visualizing and analysing specimens digitally, in three and even four dimensions, has transformed the study of living and fossil organisms. However, the initial promise that the widespread application of such methods would facilitate access to the underlying digital data has not been fully achieved. The underlying datasets for many published studies are not readily or freely available, introducing a barrier to verification and reproducibility, and the reuse of data. There is no current agreement or policy on the amount and type of data that should be made available alongside studies that use, and in some cases are wholly reliant on, digital morphology. Here, we propose a set of recommendations for minimum standards and additional best practice for three-dimensional digital data publication, and review the issues around data storage, management and accessibility.

Population viability at extreme sex-ratio skews produced by temperature-dependent sex determination.

Abstract: For species with temperature-dependent sex determination (TSD) there is the fear that rising temperatures may lead to single-sex populations and population extinction. We show that for sea turtles, a major group exhibiting TSD, these concerns are currently unfounded but may become important under extreme climate warming scenarios. We show how highly female-biased sex ratios in developing eggs translate into much more balanced operational sex ratios so that adult male numbers in populations around the world are unlikely to be limiting. Rather than reducing population viability, female-biased offspring sex ratios may, to some extent, help population growth by increasing the number of breeding females and hence egg production. For rookeries across the world (n = 75 sites for seven species), we show that extreme female-biased hatchling sex ratios do not compromise population size and are the norm, with a tendency for populations to maximize the number of female hatchlings. Only at extremely high incubation temperature does high mortality within developing clutches threaten sea turtles. Our work shows how TSD itself is a robust strategy up to a point, but eventually high mortality and female-only hatchling production will cause extinction if incubation conditions warm considerably in the future.

Drought and immunity determine the intensity of West Nile virus epidemics and climate change impacts

Abstract: The effect of global climate change on infectious disease remains hotly debated because multiple extrinsic and intrinsic drivers interact to influence transmission dynamics in nonlinear ways. The dominant drivers of widespread pathogens, like West Nile virus, can be challenging to identify due to regional variability in vector and host ecology, with past studies producing disparate findings. Here, we used analyses at national and state scales to examine a suite of climatic and intrinsic drivers of continental-scale West Nile virus epidemics, including an empirically derived mechanistic relationship between temperature and transmission potential that accounts for spatial variability in vectors. We found that drought was the primary climatic driver of increased West Nile virus epidemics, rather than within-season or winter temperatures, or precipitation independently. Local-scale data from one region suggested drought increased epidemics via changes in mosquito infection prevalence rather than mosquito abundance. In addition, human acquired immunity following regional epidemics limited subsequent transmission in many states. We show that over the next 30 years, increased drought severity from climate change could triple West Nile virus cases, but only in regions with low human immunity. These results illustrate how changes in drought severity can alter the transmission dynamics of vector-borne diseases.

Uncertain-tree: discriminating among competing approaches to the phylogenetic analysis of phenotype data.

Abstract: Morphological data provide the only means of classifying the majority of life's history, but the choice between competing phylogenetic methods for the analysis of morphology is unclear. Traditional...

Re-evaluating the link between brain size and behavioural ecology in primates.

Abstract: Comparative studies have identified a wide range of behavioural and ecological correlates of relative brain size, with results differing between taxonomic groups, and even within them. In primates for example, recent studies contradict one another over whether social or ecological factors are critical. A basic assumption of such studies is that with sufficiently large samples and appropriate analysis, robust correlations indicative of selection pressures on cognition will emerge. We carried out a comprehensive re-examination of correlates of primate brain size using two large comparative datasets and phylogenetic comparative methods. We found evidence in both datasets for associations between brain size and ecological variables (home range size, diet and activity period), but little evidence for an effect of social group size, a correlation which has previously formed the empirical basis of the Social Brain Hypothesis. However, reflecting divergent results in the literature, our results exhibited instability across datasets, even when they were matched for species composition and predictor variables. We identify several potential empirical and theoretical difficulties underlying this instability and suggest that these issues raise doubts about inferring cognitive selection pressures from behavioural correlates of brain size.

Bird and bat species' global vulnerability to collision mortality at wind farms revealed through a trait-based assessment

Abstract: Mitigation of anthropogenic climate change involves deployments of renewable energy worldwide, including wind farms, which can pose a significant collision risk to volant animals. Most studies into the collision risk between species and wind turbines, however, have taken place in industrialized countries. Potential effects for many locations and species therefore remain unclear. To redress this gap, we conducted a systematic literature review of recorded collisions between birds and bats and wind turbines within developed countries. We related collision rate to species-level traits and turbine characteristics to quantify the potential vulnerability of 9538 bird and 888 bat species globally. Avian collision rate was affected by migratory strategy, dispersal distance and habitat associations, and bat collision rates were influenced by dispersal distance. For birds and bats, larger turbine capacity (megawatts) increased collision rates; however, deploying a smaller number of large turbines with greater energy output reduced total collision risk per unit energy output, although bat mortality increased again with the largest turbines. Areas with high concentrations of vulnerable species were also identified, including migration corridors. Our results can therefore guide wind farm design and location to reduce the risk of large-scale animal mortality. This is the first quantitative global assessment of the relative collision vulnerability of species groups with wind turbines, providing valuable guidance for minimizing potentially serious negative impacts on biodiversity.

Ecological drift and the distribution of species diversity

Abstract: Ecological drift causes species abundances to fluctuate randomly, lowering diversity within communities and increasing differences among otherwise equivalent communities. Despite broad interest in ecological drift, ecologists have little experimental evidence of its consequences in nature, where competitive forces modulate species abundances. We manipulated drift by imposing 40-fold variation in the size of experimentally assembled annual plant communities and holding their edge-to-interior ratios comparable. Drift over three generations was greater than predicted by neutral models, causing high extinction rates and fast divergence in composition among smaller communities. Competitive asymmetries drove populations of most species to small enough sizes that demographic stochasticity could markedly influence dynamics, increasing the importance of drift in communities. The strong effects of drift occurred despite stabilizing niche differences, which cause species to have greater population growth rates when at low local abundance. Overall, the importance of ecological drift appears greater in non-neutral communities than previously recognized, and varies with community size and the type and strength of density dependence.

Why does drug resistance readily evolve but vaccine resistance does not

Abstract: Why is drug resistance common and vaccine resistance rare? Drugs and vaccines both impose substantial pressure on pathogen populations to evolve resistance and indeed, drug resistance typically emerges soon after the introduction of a drug. But vaccine resistance has only rarely emerged. Using well-established principles of population genetics and evolutionary ecology, we argue that two key differences between vaccines and drugs explain why vaccines have so far proved more robust against evolution than drugs. First, vaccines tend to work prophylactically while drugs tend to work therapeutically. Second, vaccines tend to induce immune responses against multiple targets on a pathogen while drugs tend to target very few. Consequently, pathogen populations generate less variation for vaccine resistance than they do for drug resistance, and selection has fewer opportunities to act on that variation. When vaccine resistance has evolved, these generalities have been violated. With careful forethought, it may be possible to identify vaccines at risk of failure even before they are introduced.

How predation shapes the social interaction rules of shoaling fish.

Abstract: Predation is thought to shape the macroscopic properties of animal groups, making moving groups more cohesive and coordinated. Precisely how predation has shaped individuals' fine-scale social inte ...

Dry habitats were crucibles of domestication in the evolution of agriculture in ants.

Abstract: The evolution of ant agriculture, as practised by the fungus-farming 'attine' ants, is thought to have arisen in the wet rainforests of South America about 55-65 Ma. Most subsequent attine agricultural evolution, including the domestication event that produced the ancestor of higher attine cultivars, is likewise hypothesized to have occurred in South American rainforests. The 'out-of-the-rainforest' hypothesis, while generally accepted, has never been tested in a phylogenetic context. It also presents a problem for explaining how fungal domestication might have occurred, given that isolation from free-living populations is required. Here, we use phylogenomic data from ultra-conserved element (UCE) loci to reconstruct the evolutionary history of fungus-farming ants, reduce topological uncertainty, and identify the closest non-fungus-growing ant relative. Using the phylogeny we infer the history of attine agricultural systems, habitat preference and biogeography. Our results show that the out-of-the-rainforest hypothesis is correct with regard to the origin of attine ant agriculture; however, contrary to expectation, we find that the transition from lower to higher agriculture is very likely to have occurred in a seasonally dry habitat, inhospitable to the growth of free-living populations of attine fungal cultivars. We suggest that dry habitats favoured the isolation of attine cultivars over the evolutionary time spans necessary for domestication to occur.

A new giant titanosaur sheds light on body mass evolution among sauropod dinosaurs

Abstract: Titanosauria was the most diverse and successful lineage of sauropod dinosaurs. This clade had its major radiation during the middle Early Cretaceous and survived up to the end of that period. Amon...

Dodging silver bullets: good CRISPR gene-drive design is critical for eradicating exotic vertebrates

Abstract: Self-replicating gene drives that can spread deleterious alleles through animal populations have been promoted as a much needed but controversial ‘silver bullet’ for controlling invasive alien spec...

Identifying climate drivers of infectious disease dynamics: recent advances and challenges ahead.

Abstract: Climate change is likely to profoundly modulate the burden of infectious diseases. However, attributing health impacts to a changing climate requires being able to associate changes in infectious disease incidence with the potentially complex influences of climate. This aim is further complicated by nonlinear feedbacks inherent in the dynamics of many infections, driven by the processes of immunity and transmission. Here, we detail the mechanisms by which climate drivers can shape infectious disease incidence, from direct effects on vector life history to indirect effects on human susceptibility, and detail the scope of variation available with which to probe these mechanisms. We review approaches used to evaluate and quantify associations between climate and infectious disease incidence, discuss the array of data available to tackle this question, and detail remaining challenges in understanding the implications of climate change for infectious disease incidence. We point to areas where synthesis between approaches used in climate science and infectious disease biology provide potential for progress.

A cross-scale trophic cascade from large predatory fish to algae in coastal ecosystems.

Abstract: Trophic cascades occur in many ecosystems, but the factors regulating them are still elusive. We suggest that an overlooked factor is that trophic interactions (TIs) are often scale-dependent and p ...

A genetic legacy of introgression confounds phylogeny and biogeography in oaks

Abstract: Oaks (Quercus L) have long been suspected to hybridize in nature, and widespread genetic exchange between morphologically defined species is well documented in two- to six-species systems, but the

Global decline of bumblebees is phylogenetically structured and inversely related to species range size and pathogen incidence.

Abstract: Conservation biology can profit greatly from incorporating a phylogenetic perspective into analyses of patterns and drivers of species extinction risk. We applied such an approach to analyse patterns of bumblebee (Bombus) decline. We assembled a database representing approximately 43% of the circa 260 globally known species, which included species extinction risk assessments following the International Union fo Conservation of Nature Red List categories and criteria, and information on species traits presumably associated with bumblebee decline. We quantified the strength of phylogenetic signal in decline, range size, tongue length and parasite presence. Overall, about one-third of the assessed bumblebees are declining and declining species are not randomly distributed across the Bombus phylogeny. Susceptible species were over-represented in the subgenus Thoracobombus (approx. 64%) and under-represented in the subgenus Pyrobombus (approx. 6%). Phylogenetic logistic regressions revealed that species with small geographical ranges and those in which none of three internal parasites were reported (i.e. Crithidia bombi, Nosema spp. or Locustacarus buchneri) were particularly vulnerable. Bumblebee evolutionary history will be deeply eroded if most species from threatened clades, particularly those stemming from basal nodes, become finally extinct. The habitat of species with restricted distribution should be protected and the importance of pathogen tolerance/resistance as mechanisms to deal with pathogens needs urgent research.

Humans recognize emotional arousal in vocalizations across all classes of terrestrial vertebrates: evidence for acoustic universals

Abstract: Writing over a century ago, Darwin hypothesized that vocal expression of emotion dates back to our earliest terrestrial ancestors. If this hypothesis is true, we should expect to find cross-species acoustic universals in emotional vocalizations. Studies suggest that acoustic attributes of aroused vocalizations are shared across many mammalian species, and that humans can use these attributes to infer emotional content. But do these acoustic attributes extend to non-mammalian vertebrates? In this study, we asked human participants to judge the emotional content of vocalizations of nine vertebrate species representing three different biological classes—Amphibia, Reptilia (non-aves and aves) and Mammalia. We found that humans are able to identify higher levels of arousal in vocalizations across all species. This result was consistent across different language groups (English, German and Mandarin native speakers), suggesting that this ability is biologically rooted in humans. Our findings indicate that humans use multiple acoustic parameters to infer relative arousal in vocalizations for each species, but mainly rely on fundamental frequency and spectral centre of gravity to identify higher arousal vocalizations across species. These results suggest that fundamental mechanisms of vocal emotional expression are shared among vertebrates and could represent a homologous signalling system.

How do cuticular hydrocarbons evolve? Physiological constraints and climatic and biotic selection pressures act on a complex functional trait.

Abstract: Cuticular hydrocarbons (CHCs) cover the cuticles of virtually all insects, serving as a waterproofing agent and as a communication signal. The causes for the high CHC variation between species, and...

Covert deformed wing virus infections have long-term deleterious effects on honeybee foraging and survival

Abstract: Several studies have suggested that covert stressors can contribute to bee colony declines. Here we provide a novel case study and show using radiofrequency identification tracking technology that covert deformed wing virus (DWV) infections in adult honeybee workers seriously impact long-term foraging and survival under natural foraging conditions. In particular, our experiments show that adult workers injected with low doses of DWV experienced increased mortality rates, that DWV caused workers to start foraging at a premature age, and that the virus reduced the workers' total activity span as foragers. Altogether, these results demonstrate that covert DWV infections have strongly deleterious effects on honeybee foraging and survival. These results are consistent with previous studies that suggested DWV to be an important contributor to the ongoing bee declines in Europe and the USA. Overall, our study underlines the strong impact that covert pathogen infections can have on individual and group-level performance in bees.

Family network size and survival across the lifespan of female macaques.

Abstract: Two decades of research suggest social relationships have a common evolutionary basis in humans and other gregarious mammals. Critical to the support of this idea is growing evidence that mortality is influenced by social integration, but when these effects emerge and how long they last is mostly unknown. Here, we report in adult female macaques that the impact of number of close adult female relatives, a proxy for social integration, on survival is not experienced uniformly across the life course; prime-aged females with a greater number of relatives had better survival outcomes compared with prime-aged females with fewer relatives, whereas no such effect was found in older females. Group size and dominance rank did not influence this result. Older females were less frequent targets of aggression, suggesting enhanced experience navigating the social landscape may obviate the need for social relationships in old age. Only one study of humans has found age-based dependency in the association between social integration and survival. Using the largest dataset for any non-human animal to date, our study extends support for the idea that sociality promotes survival and suggests strategies employed across the life course change along with experience of the social world.

Response of bats to light with different spectra: light-shy and agile bat presence is affected by white and green, but not red light.

Abstract: Artificial light at night has shown a remarkable increase over the past decades. Effects are reported for many species groups, and include changes in presence, behaviour, physiology and life-history traits. Among these, bats are strongly affected, and how bat species react to light is likely to vary with light colour. Different spectra may therefore be applied to reduce negative impacts. We used a unique set-up of eight field sites to study the response of bats to three different experimental light spectra in an otherwise dark and undisturbed natural habitat. We measured activity of three bat species groups around transects with light posts emitting white, green and red light with an intensity commonly used to illuminate countryside roads. The results reveal a strong and spectrum-dependent response for the slow-flying Myotis and Plecotus and more agile Pipistrellus species, but not for Nyctalus and Eptesicus species. Plecotus and Myotis species avoided white and green light, but were equally abundant in red light and darkness. The agile, opportunistically feeding Pipistrellus species were significantly more abundant around white and green light, most likely because of accumulation of insects, but equally abundant in red illuminated transects compared to dark control. Forest-dwelling Myotis and Plecotus species and more synanthropic Pipistrellus species are thus least disturbed by red light. Hence, in order to limit the negative impact of light at night on bats, white and green light should be avoided in or close to natural habitat, but red lights may be used if illumination is needed.

Personality-matching habitat choice, rather than behavioural plasticity, is a likely driver of a phenotype-environment covariance.

Abstract: An emerging hypothesis of animal personality posits that animals choose the habitat that best fits their personality, and that the match between habitat and personality can facilitate population differentiation, and eventually speciation. However, behavioural plasticity and the adjustment of behaviours to new environments have been a classical explanation for such matching patterns. Using a population of dunnocks (Prunella modularis), we empirically tested whether personality or behavioural plasticity is responsible for the non-random distribution of shy and bold individuals in a heterogeneous environment. We found evidence for bold individuals settling in areas with high human disturbance, but also that birds became bolder with increasing age. Importantly, personality primarily determines the distribution of individuals, and behavioural adjustment over time contributes very little to the observed patterns. We cannot, however, exclude a possibility of very early behavioural plasticity (a type of developmental plasticity) shaping what we refer to as 'personality'. Nonetheless, our findings highlight the role personality plays in shaping population structure, lending support to the theory of personality-mediated speciation. Moreover, personality-matching habitat choice has important implications for population management and conservation.