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Showing papers in "Proceedings of The Royal Society B: Biological Sciences in 2015"


Journal ArticleDOI
TL;DR: A picture emerges of a child born with an immature, innate and adaptive immune system, which matures and acquires memory as he or she grows then goes into decline in old age.
Abstract: This article reviews the development of the immune response through neonatal, infant and adult life, including pregnancy, ending with the decline in old age. A picture emerges of a child born with an immature, innate and adaptive immune system, which matures and acquires memory as he or she grows. It then goes into decline in old age. These changes are considered alongside the risks of different types of infection, autoimmune disease and malignancy.

1,163 citations


Journal ArticleDOI
TL;DR: The structure, core assumptions and novel predictions of the extended evolutionary synthesis (EES) are spelled out, and it is shown how it can be deployed to stimulate and advance research in those fields that study or use evolutionary biology.
Abstract: Scientific activities take place within the structured sets of ideas and assumptions that define a field and its practices. The conceptual framework of evolutionary biology emerged with the Modern Synthesis in the early twentieth century and has since expanded into a highly successful research program to explore the processes of diversification and adaptation. Nonetheless, the ability of that framework satisfactorily to accommodate the rapid advances in developmental biology, genomics and ecology has been questioned. We review some of these arguments, focusing on literatures (evo-devo, developmental plasticity, inclusive inheritance and niche construction) whose implications for evolution can be interpreted in two ways—one that preserves the internal structure of contemporary evolutionary theory and one that points towards an alternative conceptual framework. The latter, which we label the 'extended evolutionary synthesis' (EES), retains the fundaments of evolutionary theory, but differs in its emphasis on the role of constructive processes in development and evolution, and reciprocal portrayals of causation. In the EES, developmental processes, operating through developmental bias, inclusive inheritance and niche construction, share responsibility for the direction and rate of evolution, the origin of character variation and organism-environment complementarity. We spell out the structure, core assumptions and novel predictions of the EES, and show how it can be deployed to stimulate and advance research in those fields that study or use evolutionary biology.

790 citations


Journal ArticleDOI
TL;DR: Promising results, based on robust analysis of a larger meta-dataset, suggest that appropriate investment in agroecological research to improve organic management systems could greatly reduce or eliminate the yield gap for some crops or regions.
Abstract: Agriculture today places great strains on biodiversity, soils, water and the atmosphere, and these strains will be exacerbated if current trends in population growth, meat and energy consumption, and food waste continue. Thus, farming systems that are both highly productive and minimize environmental harms are critically needed. How organic agriculture may contribute to world food production has been subject to vigorous debate over the past decade. Here, we revisit this topic comparing organic and conventional yields with a new meta-dataset three times larger than previously used (115 studies containing more than 1000 observations) and a new hierarchical analytical framework that can better account for the heterogeneity and structure in the data. We find organic yields are only 19.2% (±3.7%) lower than conventional yields, a smaller yield gap than previous estimates. More importantly, we find entirely different effects of crop types and management practices on the yield gap compared with previous studies. For example, we found no significant differences in yields for leguminous versus non-leguminous crops, perennials versus annuals or developed versus developing countries. Instead, we found the novel result that two agricultural diversification practices, multi-cropping and crop rotations, substantially reduce the yield gap (to 9 ± 4% and 8 ± 5%, respectively) when the methods were applied in only organic systems. These promising results, based on robust analysis of a larger meta-dataset, suggest that appropriate investment in agroecological research to improve organic management systems could greatly reduce or eliminate the yield gap for some crops or regions.

579 citations


Journal ArticleDOI
TL;DR: This analysis indicates that behavioural and evolutionary mechanisms will be critical in allowing ectotherms to buffer themselves from extreme temperatures, and proposes that limited potential for behavioural plasticity favours the evolution of greater plasticity in physiological traits, consistent with the ‘Bogert effect’.
Abstract: Global warming is increasing the overheating risk for many organisms, though the potential for plasticity in thermal tolerance to mitigate this risk is largely unknown. In part, this shortcoming stems from a lack of knowledge about global and taxonomic patterns of variation in tolerance plasticity. To address this critical issue, we test leading hypotheses for broad-scale variation in ectotherm tolerance plasticity using a dataset that includes vertebrate and invertebrate taxa from terrestrial, freshwater and marine habitats. Contrary to expectation, plasticity in heat tolerance was unrelated to latitude or thermal seasonality. However, plasticity in cold tolerance is associated with thermal seasonality in some habitat types. In addition, aquatic taxa have approximately twice the plasticity of terrestrial taxa. Based on the observed patterns of variation in tolerance plasticity, we propose that limited potential for behavioural plasticity (i.e. behavioural thermoregulation) favours the evolution of greater plasticity in physiological traits, consistent with the ‘Bogert effect’. Finally, we find that all ectotherms have relatively low acclimation in thermal tolerance and demonstrate that overheating risk will be minimally reduced by acclimation in even the most plastic groups. Our analysis indicates that behavioural and evolutionary mechanisms will be critical in allowing ectotherms to buffer themselves from extreme temperatures.

538 citations


Journal ArticleDOI
TL;DR: This study provides new insights into the general mechanisms that link biodiversity to ecosystem functioning in natural animal communities and suggests that the observed responses were due to the identity and dominance patterns of the trait composition rather than the number or abundance of species per se.
Abstract: Drastic biodiversity declines have raised concerns about the deterioration of ecosystem functions and have motivated much recent research on the relationship between species diversity and ecosystem functioning. A functional trait framework has been proposed to improve the mechanistic understanding of this relationship, but this has rarely been tested for organisms other than plants. We analysed eight datasets, including five animal groups, to examine how well a trait-based approach, compared with a more traditional taxonomic approach, predicts seven ecosystem functions below- and above-ground. Trait-based indices consistently provided greater explanatory power than species richness or abundance. The frequency distributions of single or multiple traits in the community were the best predictors of ecosystem functioning. This implies that the ecosystem functions we investigated were underpinned by the combination of trait identities (i.e. single-trait indices) and trait complementarity (i.e. multi-trait indices) in the communities. Our study provides new insights into the general mechanisms that link biodiversity to ecosystem functioning in natural animal communities and suggests that the observed responses were due to the identity and dominance patterns of the trait composition rather than the number or abundance of species per se.

501 citations


Journal ArticleDOI
TL;DR: While urban pollinator assemblages were more homogeneous across space than those in farmland or nature reserves, there was no significant difference in the numbers of rarer species between the three landscapes.
Abstract: Insect pollinators provide a crucial ecosystem service, but are under threat. Urban areas could be important for pollinators, though their value relative to other habitats is poorly known. We compared pollinator communities using quantified flower-visitation networks in 36 sites (each 1 km2) in three landscapes: urban, farmland and nature reserves. Overall, flower-visitor abundance and species richness did not differ significantly between the three landscape types. Bee abundance did not differ between landscapes, but bee species richness was higher in urban areas than farmland. Hoverfly abundance was higher in farmland and nature reserves than urban sites, but species richness did not differ significantly. While urban pollinator assemblages were more homogeneous across space than those in farmland or nature reserves, there was no significant difference in the numbers of rarer species between the three landscapes. Network-level specialization was higher in farmland than urban sites. Relative to other habitats, urban visitors foraged from a greater number of plant species (higher generality) but also visited a lower proportion of available plant species (higher specialization), both possibly driven by higher urban plant richness. Urban areas are growing, and improving their value for pollinators should be part of any national strategy to conserve and restore pollinators.

413 citations


Journal ArticleDOI
TL;DR: The results argue against a major role for parasitic symbionts in driving arthropod diversification by developing a maximum-likelihood approach to estimating incidence, and testing hypotheses about its variation.
Abstract: Intracellular endosymbiotic bacteria are found in many terrestrial arthropods and have a profound influence on host biology. A basic question about these symbionts is why they infect the hosts that they do, but estimating symbiont incidence (the proportion of potential host species that are actually infected) is complicated by dynamic or low prevalence infections. We develop a maximum-likelihood approach to estimating incidence, and testing hypotheses about its variation. We apply our method to a database of screens for bacterial symbionts, containing more than 3600 distinct arthropod species and more than 150 000 individual arthropods. After accounting for sampling bias, we estimate that 52% (CIs: 48–57) of arthropod species are infected with Wolbachia , 24% (CIs: 20–42) with Rickettsia and 13% (CIs: 13–55) with Cardinium . We then show that these differences stem from the significantly reduced incidence of Rickettsia and Cardinium in most hexapod orders, which might be explained by evolutionary differences in the arthropod immune response. Finally, we test the prediction that symbiont incidence should be higher in speciose host clades. But while some groups do show a trend for more infection in species-rich families, the correlations are generally weak and inconsistent. These results argue against a major role for parasitic symbionts in driving arthropod diversification.

408 citations


Journal ArticleDOI
TL;DR: Focusing on Hendra virus, but also addressing Nipah virus, Ebola virus, Marburg virus and coronaviruses, this work delineates this cross-species spillover dynamic from the within-host processes that drive virus excretion to land-use changes that increase interaction among species.
Abstract: Viruses that originate in bats may be the most notorious emerging zoonoses that spill over from wildlife into domestic animals and humans. Understanding how these infections filter through ecological systems to cause disease in humans is of profound importance to public health. Transmission of viruses from bats to humans requires a hierarchy of enabling conditions that connect the distribution of reservoir hosts, viral infection within these hosts, and exposure and susceptibility of recipient hosts. For many emerging bat viruses, spillover also requires viral shedding from bats, and survival of the virus in the environment. Focusing on Hendra virus, but also addressing Nipah virus, Ebola virus, Marburg virus and coronaviruses, we delineate this cross-species spillover dynamic from the within-host processes that drive virus excretion to land-use changes that increase interaction among species. We describe how land-use changes may affect co-occurrence and contact between bats and recipient hosts. Two hypotheses may explain temporal and spatial pulses of virus shedding in bat populations: episodic shedding from persistently infected bats or transient epidemics that occur as virus is transmitted among bat populations. Management of livestock also may affect the probability of exposure and disease. Interventions to decrease the probability of virus spillover can be implemented at multiple levels from targeting the reservoir host to managing recipient host exposure and susceptibility.

407 citations


Journal ArticleDOI
TL;DR: A phylogeny based on 75 chloroplast genes for 39 species representing all orchid subfamilies and 16 of 17 tribes, time-calibrated against 17 angiosperm fossils shows that orchids appear to have undergone one significant acceleration of net species diversification in the orchidoids, and two accelerations and one deceleration in the upper epidendroids.
Abstract: Orchids are the most diverse family of angiosperms, with over 25 000 species, more than mammals, birds and reptiles combined. Tests of hypotheses to account for such diversity have been stymied by ...

343 citations


Journal ArticleDOI
TL;DR: It is demonstrated that genetic differences are likely to be a major contributor to variation in animal personality and support the phenotypic gambit: that evolutionary inferences drawn from repeatability estimates may often be justified.
Abstract: Individual animals frequently exhibit repeatable differences from other members of their population, differences now commonly referred to as ‘animal personality’. Personality differences can arise,...

303 citations


Journal ArticleDOI
TL;DR: Structural changes at the food web level induced by poleward shifts via topological network analysis of highly resolved boreal and arctic food webs of the Barents Sea are addressed, revealing that habitats form natural boundaries for food web modules, and that generalists play an important functional role in coupling pelagic and benthic modules.
Abstract: Climate-driven poleward shifts, leading to changes in species composition and relative abundances, have been recently documented in the Arctic. Among the fastest moving species are boreal generalist fish which are expected to affect arctic marine food web structure and ecosystem functioning substantially. Here, we address structural changes at the food web level induced by poleward shifts via topological network analysis of highly resolved boreal and arctic food webs of the Barents Sea. We detected considerable differences in structural properties and link configuration between the boreal and the arctic food webs, the latter being more modular and less connected. We found that a main characteristic of the boreal fish moving poleward into the arctic region of the Barents Sea is high generalism, a property that increases connectance and reduces modularity in the arctic marine food web. Our results reveal that habitats form natural boundaries for food web modules, and that generalists play an important functional role in coupling pelagic and benthic modules. We posit that these habitat couplers have the potential to promote the transfer of energy and matter between habitats, but also the spread of pertubations, thereby changing arctic marine food web structure considerably with implications for ecosystem dynamics and functioning.

Journal ArticleDOI
TL;DR: It is argued that the Amazonian anthrome was no less socio-culturally diverse or populous than other tropical forested areas of the world prior to European conquest.
Abstract: During the twentieth century, Amazonia was widely regarded as relatively pristine nature, little impacted by human history. This view remains popular despite mounting evidence of substantial human influence over millennial scales across the region. Here, we review the evidence of an anthropogenic Amazonia in response to claims of sparse populations across broad portions of the region. Amazonia was a major centre of crop domestication, with at least 83 native species containing populations domesticated to some degree. Plant domestication occurs in domesticated landscapes, including highly modified Amazonian dark earths (ADEs) associated with large settled populations and that may cover greater than 0.1% of the region. Populations and food production expanded rapidly within land management systems in the mid-Holocene, and complex societies expanded in resource-rich areas creating domesticated landscapes with profound impacts on local and regional ecology. ADE food production projections support estimates of at least eight million people in 1492. By this time, highly diverse regional systems had developed across Amazonia where subsistence resources were created with plant and landscape domestication, including earthworks. This review argues that the Amazonian anthrome was no less socio-culturally diverse or populous than other tropical forested areas of the world prior to European conquest.

Journal ArticleDOI
TL;DR: A review of 26 studies of free-ranging vertebrate populations that explicitly tested for a trade-off between performance in early and late life brings overall support for the presence of early-late life trade-offs, suggesting that the limitation of available resources leads individuals to trade somatic maintenance later in life for high allocation to reproduction early in life.
Abstract: Empirical evidence for declines in fitness components (survival and reproductive performance) with age has recently accumulated in wild populations, highlighting that the process of senescence is nearly ubiquitous in the living world. Senescence patterns are highly variable among species and current evolutionary theories of ageing propose that such variation can be accounted for by differences in allocation to growth and reproduction during early life. Here, we compiled 26 studies of free-ranging vertebrate populations that explicitly tested for a trade-off between performance in early and late life. Our review brings overall support for the presence of early-late life trade-offs, suggesting that the limitation of available resources leads individuals to trade somatic maintenance later in life for high allocation to reproduction early in life. We discuss our results in the light of two closely related theories of ageing—the disposable soma and the antagonistic pleiotropy theories—and propose that the principle of energy allocation roots the ageing process in the evolution of life-history strategies. Finally, we outline research topics that should be investigated in future studies, including the importance of natal environmental conditions in the study of trade-offs between early- and late-life performance and the evolution of sex-differences in ageing patterns.

Journal ArticleDOI
TL;DR: This study provides a clear demonstration that wildlife-friendly management which supports ecosystem services is compatible with, and can even increase, crop yields.
Abstract: Ecological intensification has been promoted as a means to achieve environmentally sustainable increases in crop yields by enhancing ecosystem functions that regulate and support production. There is, however, little direct evidence of yield benefits from ecological intensification on commercial farms growing globally important foodstuffs (grains, oilseeds and pulses). We replicated two treatments removing 3 or 8% of land at the field edge from production to create wildlife habitat in 50–60 ha patches over a 900 ha commercial arable farm in central England, and compared these to a business as usual control (no land removed). In the control fields, crop yields were reduced by as much as 38% at the field edge. Habitat creation in these lower yielding areas led to increased yield in the cropped areas of the fields, and this positive effect became more pronounced over 6 years. As a consequence, yields at the field scale were maintained—and, indeed, enhanced for some crops—despite the loss of cropland for habitat creation. These results suggested that over a 5-year crop rotation, there would be no adverse impact on overall yield in terms of monetary value or nutritional energy. This study provides a clear demonstration that wildlife-friendly management which supports ecosystem services is compatible with, and can even increase, crop yields.

Journal ArticleDOI
TL;DR: The results suggest that flowers are likely to be hotspots for the transmission of pollinator parasites and that considering potential vector, as well as host, species will be of general importance for understanding the distribution and transmission of parasites in the environment and between pollinators.
Abstract: The dispersal of parasites is critical for epidemiology, and the interspecific vectoring of parasites when species share resources may play an underappreciated role in parasite dispersal. One of the best examples of such a situation is the shared use of flowers by pollinators, but the importance of flowers and interspecific vectoring in the dispersal of pollinator parasites is poorly understood and frequently overlooked. Here, we use an experimental approach to show that during even short foraging periods of 3 h, three bumblebee parasites and two honeybee parasites were dispersed effectively onto flowers by their hosts, and then vectored readily between flowers by non-host pollinator species. The results suggest that flowers are likely to be hotspots for the transmission of pollinator parasites and that considering potential vector, as well as host, species will be of general importance for understanding the distribution and transmission of parasites in the environment and between pollinators.

Journal ArticleDOI
TL;DR: Evidence that broad supernatural punishment drives political complexity, whereas MHGs follow political complexity is found, suggesting that the concept of MHGs diffused as part of a suite of traits arising from cultural exchange between complex societies.
Abstract: Supernatural belief presents an explanatory challenge to evolutionary theorists—it is both costly and prevalent. One influential functional explanation claims that the imagined threat of supernatural punishment can suppress selfishness and enhance cooperation. Specifically, morally concerned supreme deities or ‘moralizing high gods9 have been argued to reduce free-riding in large social groups, enabling believers to build the kind of complex societies that define modern humanity. Previous cross-cultural studies claiming to support the MHG hypothesis rely on correlational analyses only and do not correct for the statistical non-independence of sampled cultures. Here we use a Bayesian phylogenetic approach with a sample of 96 Austronesian cultures to test the MHG hypothesis as well as an alternative supernatural punishment hypothesis that allows punishment by a broad range of moralizing agents. We find evidence that broad supernatural punishment drives political complexity, whereas MHGs follow political complexity. We suggest that the concept of MHGs diffused as part of a suite of traits arising from cultural exchange between complex societies. Our results show the power of phylogenetic methods to address long-standing debates about the origins and functions of religion in human society.

Journal ArticleDOI
TL;DR: In this paper, the authors use a simulation study to demonstrate potential pitfalls of the standard practice of fitting deterministic models to cumulative incidence data and demonstrate an alternative based on stochastic models fit to raw data from an early phase of 2014 West Africa Ebola virus disease outbreak.
Abstract: As an emergent infectious disease outbreak unfolds, public health response is reliant on information on key epidemiological quantities, such as transmission potential and serial interval. Increasingly, transmission models fit to incidence data are used to estimate these parameters and guide policy. Some widely used modelling practices lead to potentially large errors in parameter estimates and, consequently, errors in model-based forecasts. Even more worryingly, in such situations, confidence in parameter estimates and forecasts can itself be far overestimated, leading to the potential for large errors that mask their own presence. Fortunately, straightforward and computationally inexpensive alternatives exist that avoid these problems. Here, we first use a simulation study to demonstrate potential pitfalls of the standard practice of fitting deterministic models to cumulative incidence data. Next, we demonstrate an alternative based on stochastic models fit to raw data from an early phase of 2014 West Africa Ebola virus disease outbreak. We show not only that bias is thereby reduced, but that uncertainty in estimates and forecasts is better quantified and that, critically, lack of model fit is more readily diagnosed. We conclude with a short list of principles to guide the modelling response to future infectious disease outbreaks.

Journal ArticleDOI
TL;DR: Investigation of fungal and bacterial communities found in settled dust collected from inside and outside approximately 1200 homes located across the continental US, homes that represent a broad range of home designs and span many climatic zones found that who you live with determines what bacteria are found inside your home.
Abstract: We spend the majority of our lives indoors; yet, we currently lack a comprehensive understanding of how the microbial communities found in homes vary across broad geographical regions and what factors are most important in shaping the types of microorganisms found inside homes. Here, we investigated the fungal and bacterial communities found in settled dust collected from inside and outside approximately 1200 homes located across the continental US, homes that represent a broad range of home designs and span many climatic zones. Indoor and outdoor dust samples harboured distinct microbial communities, but these differences were larger for bacteria than for fungi with most indoor fungi originating outside the home. Indoor fungal communities and the distribution of potential allergens varied predictably across climate and geographical regions; where you live determines what fungi live with you inside your home. By contrast, bacterial communities in indoor dust were more strongly influenced by the number and types of occupants living in the homes. In particular, the female : male ratio and whether a house had pets had a significant influence on the types of bacteria found inside our homes highlighting that who you live with determines what bacteria are found inside your home.

Journal ArticleDOI
TL;DR: The necessary assumptions and predictions of hypotheses concerning adaptive developmental plasticity (ADP) are discussed and guidelines for how to test empirically whether a particular example is adaptive are developed.
Abstract: Developmental plasticity describes situations where a specific input during an individual's development produces a lasting alteration in phenotype. Some instances of developmental plasticity may be adaptive, meaning that the tendency to produce the phenotype conditional on having experienced the developmental input has been under positive selection. We discuss the necessary assumptions and predictions of hypotheses concerning adaptive developmental plasticity (ADP) and develop guidelines for how to test empirically whether a particular example is adaptive. Central to our analysis is the distinction between two kinds of ADP: informational, where the developmental input provides information about the future environment, and somatic state-based, where the developmental input enduringly alters some aspect of the individual's somatic state. Both types are likely to exist in nature, but evolve under different conditions. In all cases of ADP, the expected fitness of individuals who experience the input and develop the phenotype should be higher than that of those who experience the input and do not develop the phenotype, while the expected fitness of those who do not experience the input and do not develop the phenotype should be higher than those who do not experience the input and do develop the phenotype. We describe ancillary predictions that are specific to just one of the two types of ADP and thus distinguish between them.

Journal ArticleDOI
TL;DR: It is emphasized that the evolutionary implications of symbiont transmission routes (intracellular versus extracellular) do not necessarily correspond to those of the transmission mode (vertical versus horizontal), a distinction of vital significance when addressing the genomic and physiological consequences for both host and symbia.
Abstract: Across animals and plants, numerous metabolic and defensive adaptations are a direct consequence of symbiotic associations with beneficial microbes. Explaining how these partnerships are maintained through evolutionary time remains one of the central challenges within the field of symbiosis research. While genome erosion and co-cladogenesis with the host are well-established features of symbionts exhibiting intracellular localization and transmission, the ecological and evolutionary consequences of an extracellular lifestyle have received little attention, despite a demonstrated prevalence and functional importance across many host taxa. Using insect–bacteria symbioses as a model, we highlight the diverse routes of extracellular symbiont transfer. Extracellular transmission routes are unified by the common ability of the bacterial partners to survive outside their hosts, thereby imposing different genomic, metabolic and morphological constraints than would be expected from a strictly intracellular lifestyle. We emphasize that the evolutionary implications of symbiont transmission routes (intracellular versus extracellular) do not necessarily correspond to those of the transmission mode (vertical versus horizontal), a distinction of vital significance when addressing the genomic and physiological consequences for both host and symbiont.

Journal ArticleDOI
TL;DR: This study is the first, to the best of the knowledge, to describe the seasonality of transmission in this emerging wildlife disease, and suggests the dominant driver of seasonal transmission dynamics was a change in host physiology, specifically hibernation.
Abstract: Seasonal patterns in pathogen transmission can influence the impact of disease on populations and the speed of spatial spread Increases in host contact rates or births drive seasonal epidemics in some systems, but other factors may occasionally override these influences White-nose syndrome, caused by the emerging fungal pathogen Pseudogymnoascus destructans, is spreading across North America and threatens several bat species with extinction We examined patterns and drivers of seasonal transmission of P destructans by measuring infection prevalence and pathogen loads in six bat species at 30 sites across the eastern United States Bats became transiently infected in autumn, and transmission spiked in early winter when bats began hibernating Nearly all bats in six species became infected by late winter when infection intensity peaked In summer, despite high contact rates and a birth pulse, most bats cleared infections and prevalence dropped to zero These data suggest the dominant driver of seasonal transmission dynamics was a change in host physiology, specifically hibernation Our study is the first, to the best of our knowledge, to describe the seasonality of transmission in this emerging wildlife disease The timing of infection and fungal growth resulted in maximal population impacts, but only moderate rates of spatial spread

Journal ArticleDOI
TL;DR: It is hypothesized that while a reduction in the P/O ratio is energetically costly, it may be associated with advantages in terms of somatic maintenance through reduced production of reactive oxygen species.
Abstract: It is often assumed that an animal's metabolic rate can be estimated through measuring the whole-organism oxygen consumption rate. However, oxygen consumption alone is unlikely to be a sufficient marker of energy metabolism in many situations. This is due to the inherent variability in the link between oxidation and phosphorylation; that is, the amount of adenosine triphosphate (ATP) generated per molecule of oxygen consumed by mitochondria (P/O ratio). In this article, we describe how the P/O ratio can vary within and among individuals, and in response to a number of environmental parameters, including diet and temperature. As the P/O ratio affects the efficiency of cellular energy production, its variability may have significant consequences for animal performance, such as growth rate and reproductive output. We explore the adaptive significance of such variability and hypothesize that while a reduction in the P/O ratio is energetically costly, it may be associated with advantages in terms of somatic maintenance through reduced production of reactive oxygen species. Finally, we discuss how considering variation in mitochondrial efficiency, together with whole-organism oxygen consumption, can permit a better understanding of the relationship between energy metabolism and life history for studies in evolutionary ecology.

Journal ArticleDOI
TL;DR: This work uses data from 30 pollen-transport networks and 71 pollinator-visitation networks to compare the importance of various flower-visiting taxa as pollen-vectors and specifically compare non-syrphid Diptera and Syrphidae to determine whether neglect of the former in the literature is justified.
Abstract: Bees, hoverflies and butterflies are taxa frequently studied as pollinators in agricultural and conservation contexts. Although there are many records of non-syrphid Diptera visiting flowers, they are generally not regarded as important pollinators. We use data from 30 pollen-transport networks and 71 pollinator-visitation networks to compare the importance of various flower-visiting taxa as pollen-vectors. We specifically compare non-syrphid Diptera and Syrphidae to determine whether neglect of the former in the literature is justified. We found no significant difference in pollen-loads between the syrphid and non-syrphid Diptera. Moreover, there was no significant difference in the level of specialization between the two groups in the pollen-transport networks, though the Syrphidae had significantly greater visitation evenness. Flower visitation data from 33 farms showed that non-syrphid Diptera made up the majority of the flower-visiting Diptera in the agricultural studies (on average 82% abundance and 73% species richness), and we estimate that non-syrphid Diptera carry 84% of total pollen carried by farmland Diptera. As important pollinators, such as bees, have suffered serious declines, it would be prudent to improve our understanding of the role of non-syrphid Diptera as pollinators.

Journal ArticleDOI
TL;DR: The novel results highlight that although secondary metabolites may not rescue survival in infected bees, they may play a vital role in mediating Crithidia transmission within and between colonies by reducingCrithidia infection intensities.
Abstract: The synthesis of secondary metabolites is a hallmark of plant defence against herbivores. These compounds may be detrimental to consumers, but can also protect herbivores against parasites. Floral nectar commonly contains secondary metabolites, but little is known about the impacts of nectar chemistry on pollinators, including bees. We hypothesized that nectar secondary metabolites could reduce bee parasite infection. We inoculated individual bumblebees with Crithidia bombi, an intestinal parasite, and tested effects of eight naturally occurring nectar chemicals on parasite population growth. Secondary metabolites strongly reduced parasite load, with significant effects of alkaloids, terpenoids and iridoid glycosides ranging from 61 to 81%. Using microcolonies, we also investigated costs and benefits of consuming anabasine, the compound with the strongest effect on parasites, in infected and uninfected bees. Anabasine increased time to egg laying, and Crithidia reduced bee survival. However, anabasine consumption did not mitigate the negative effects of Crithidia, and Crithidia infection did not alter anabasine consumption. Our novel results highlight that although secondary metabolites may not rescue survival in infected bees, they may play a vital role in mediating Crithidia transmission within and between colonies by reducing Crithidia infection intensities.

Journal ArticleDOI
TL;DR: The results demonstrate that a posteriori approaches can lead to the selection of erroneous calibrations in divergence time analyses and suggest the most effective means of establishing the quality of fossil-based calibrations is through a priori evaluation of the intrinsic palaeontological, stratigraphic, geochronological and phylogenetic data.
Abstract: Calibration is the rate-determining step in every molecular clock analysis and, hence, considerable effort has been expended in the development of approaches to distinguish good from bad calibrations. These can be categorized into a priori evaluation of the intrinsic fossil evidence, and a posteriori evaluation of congruence through cross-validation. We contrasted these competing approaches and explored the impact of different interpretations of the fossil evidence upon Bayesian divergence time estimation. The results demonstrate that a posteriori approaches can lead to the selection of erroneous calibrations. Bayesian posterior estimates are also shown to be extremely sensitive to the probabilistic interpretation of temporal constraints. Furthermore, the effective time priors implemented within an analysis differ for individual calibrations when employed alone and in differing combination with others. This compromises the implicit assumption of all calibration consistency methods, that the impact of an individual calibration is the same when used alone or in unison with others. Thus, the most effective means of establishing the quality of fossil-based calibrations is through a priori evaluation of the intrinsic palaeontological, stratigraphic, geochronological and phylogenetic data. However, effort expended in establishing calibrations will not be rewarded unless they are implemented faithfully in divergence time analyses.

Journal ArticleDOI
TL;DR: This study demonstrates a high effectiveness of annual flower strips in promoting pest control, reducing CLB pest levels below the economic threshold and hence, the studied flower strip offers a viable alternative to insecticides.
Abstract: Providing key resources to animals may enhance both their biodiversity and the ecosystem services they provide. We examined the performance of annual flower strips targeted at the promotion of natural pest control in winter wheat. Flower strips were experimentally sown along 10 winter wheat fields across a gradient of landscape complexity (i.e. proportion non-crop area within 750 m around focal fields) and compared with 15 fields with wheat control strips. We found strong reductions in cereal leaf beetle (CLB) density (larvae: 40%; adults of the second generation: 53%) and plant damage caused by CLB (61%) in fields with flower strips compared with control fields. Natural enemies of CLB were strongly increased in flower strips and in part also in adjacent wheat fields. Flower strip effects on natural enemies, pests and crop damage were largely independent of landscape complexity (8–75% non-crop area). Our study demonstrates a high effectiveness of annual flower strips in promoting pest control, reducing CLB pest levels below the economic threshold. Hence, the studied flower strip offers a viable alternative to insecticides. This highlights the high potential of tailored agri-environment schemes to contribute to ecological intensification and may encourage more farmers to adopt such schemes.

Journal ArticleDOI
TL;DR: A summary is provided of recent advances in the natural science evidence base concerning the effects of neonicotinoid insecticides on insect pollinators in a format (a ‘restatement') intended to be accessible to informed but not expert policymakers and stakeholders.
Abstract: A summary is provided of recent advances in the natural science evidence base concerning the effects of neonicotinoid insecticides on insect pollinators in a format (a ‘restatement') intended to be accessible to informed but not expert policymakers and stakeholders Important new studies have been published since our recent review of this field (Godfray et al 2014 Proc R Soc B 281, 20140558 (doi:101098/rspb20140558)) and the subject continues to be an area of very active research and high policy relevance

Journal ArticleDOI
TL;DR: It is shown that by focusing on linkages to ecological impacts rather than the presence of debris and its sublethal impacts, it could reduce threats posed by debris.
Abstract: Accelerated contamination of habitats with debris has caused increased effort to determine ecological impacts. Strikingly, most work on organisms focuses on sublethal responses to plastic debris. This is controversial because (i) researchers have ignored medical insights about the mechanisms that link effects of debris across lower levels of biological organization to disease and mortality, and (ii) debris is considered non-hazardous by policy-makers, possibly because individuals can be injured or removed from populations and assemblages without ecological impacts. We reviewed the mechanisms that link effects of debris across lower levels of biological organization to assemblages and populations. Using plastic, we show microplastics reduce the ‘health’, feeding, growth and survival of ecosystem engineers. Larger debris alters assemblages because fishing-gear and tyres kill animals and damage habitat-forming plants, and because floating bottles facilitate recruitment and survival of novel taxa. Where ecological linkages are not known, we show how to establish hypothetical links by synthesizing studies to assess the likelihood of impacts. We also consider how population models examine ecological linkages and guide management of ecological impacts. We show that by focusing on linkages to ecological impacts rather than the presence of debris and its sublethal impacts, we could reduce threats posed by debris.

Journal ArticleDOI
TL;DR: Assessment of the effect of conventional pesticide use on the wild bee community visiting apple within a gradient of percentage natural area in the landscape demonstrates extended benefits of natural areas for wild pollinators and highlights the importance of considering the landscape context when weighing up the costs of pest management on crop pollination services.
Abstract: Wild bee communities provide underappreciated but critical agricultural pollination services. Given predicted global shortages in pollination services, managing agroecosystems to support thriving wild bee communities is, therefore, central to ensuring sustainable food production. Benefits of natural (including semi-natural) habitat for wild bee abundance and diversity on farms are well documented. By contrast, few studies have examined toxicity of pesticides on wild bees, let alone effects of farm-level pesticide exposure on entire bee communities. Whether beneficial natural areas could mediate effects of harmful pesticides on wild bees is also unknown. Here, we assess the effect of conventional pesticide use on the wild bee community visiting apple (Malus domestica) within a gradient of percentage natural area in the landscape. Wild bee community abundance and species richness decreased linearly with increasing pesticide use in orchards one year after application; however, pesticide effects on wild bees were buffered by increasing proportion of natural habitat in the surrounding landscape. A significant contribution of fungicides to observed pesticide effects suggests deleterious properties of a class of pesticides that was, until recently, considered benign to bees. Our results demonstrate extended benefits of natural areas for wild pollinators and highlight the importance of considering the landscape context when weighing up the costs of pest management on crop pollination services.

Journal ArticleDOI
TL;DR: The technological and analytical advances that have enabled genome-wide association studies to be successful in identifying a large number of genetic variants robustly associated with common disease are described and the biological insights that these genetic associations are beginning to produce are examined.
Abstract: Susceptibility to common human diseases is influenced by both genetic and environmental factors. The explosive growth of genetic data, and the knowledge that it is generating, are transforming our biological understanding of these diseases. In this review, we describe the technological and analytical advances that have enabled genome-wide association studies to be successful in identifying a large number of genetic variants robustly associated with common disease. We examine the biological insights that these genetic associations are beginning to produce, from functional mechanisms involving individual genes to biological pathways linking associated genes, and the identification of functional annotations, some of which are cell-type-specific, enriched in disease associations. Although most efforts have focused on identifying and interpreting genetic variants that are irrefutably associated with disease, it is increasingly clear that—even at large sample sizes—these represent only the tip of the iceberg of genetic signal, motivating polygenic analyses that consider the effects of genetic variants throughout the genome, including modest effects that are not individually statistically significant. As data from an increasingly large number of diseases and traits are analysed, pleiotropic effects (defined as genetic loci affecting multiple phenotypes) can help integrate our biological understanding. Looking forward, the next generation of population-scale data resources, linking genomic information with health outcomes, will lead to another step-change in our ability to understand, and treat, common diseases.