Fitness trade-offs and the origins of endosymbiosis.

Endosymbiosis drives evolutionary innovation and underpins the function of diverse ecosystems. The mechanistic origins of symbioses, however, remain unclear, in part because early evolutionary events are obscured by subsequent evolution and genetic drift. This Essay highlights how experimental studies of facultative, host-switched, and synthetic symbioses are revealing the important role of fitness trade-offs between within-host and free-living niches during the early-stage evolution of new symbiotic associations. The mutational targets underpinning such trade-offs are commonly regulatory genes, such that single mutations have major phenotypic effects on multiple traits, thus enabling and reinforcing the transition to a symbiotic lifestyle.

The evolution of the traplining pollinator role in hummingbirds: specialization is not an evolutionary dead end.

Trapliners are pollinators that visit widely dispersed flowers along circuitous foraging routes. The evolution of traplining in hummingbirds is thought to entail morphological specialization through the reciprocal coevolution of longer bills with the long-tubed flowers of widely dispersed plant species. Specialization, such as that exhibited by traplining hummingbirds, is often viewed as both irreversible and an evolutionary dead end. We tested these predictions in a macroevolutionary framework. Specifically, we assessed the relationship between beak morphology and foraging and tested whether transitions to traplining are irreversible and lead to lower rates of diversification as predicted by the hypothesis that specialization is an evolutionary dead end. We find that there have been multiple independent transitions to traplining across the hummingbird phylogeny, but reversals have been rare or incomplete at best. Multiple independent lineages of trapliners have become morphologically specialized, convergently evolving relatively large bills for their body size. Traplining is not an evolutionary dead end however, since trapliners continue to give rise to new traplining species at a rate comparable to non-trapliners.

Climate change research and action must look beyond 2100.

Anthropogenic activity is changing Earth's climate and ecosystems in ways that are potentially dangerous and disruptive to humans. Greenhouse gas concentrations in the atmosphere continue to rise, ensuring that these changes will be felt for centuries beyond 2100, the current benchmark for projection. Estimating the effects of past, current, and potential future emissions to only 2100 is therefore short-sighted. Critical problems for food production and climate-forced human migration are projected to arise well before 2100, raising questions regarding the habitability of some regions of the Earth after the turn of the century. To highlight the need for more distant horizon scanning, we model climate change to 2500 under a suite of emission scenarios and quantify associated projections of crop viability and heat stress. Together, our projections show global climate impacts increase significantly after 2100 without rapid mitigation. As a result, we argue that projections of climate and its effects on human well-being and associated governance and policy must be framed beyond 2100.

The myriad of complex demographic responses of terrestrial mammals to climate change and gaps of knowledge: A global analysis.

Approximately 25% of mammals are currently threatened with extinction, a risk that is amplified under climate change. Species persistence under climate change is determined by the combined effects of climatic factors on multiple demographic rates (survival, development and reproduction), and hence, population dynamics. Thus, to quantify which species and regions on Earth are most vulnerable to climate-driven extinction, a global understanding of how different demographic rates respond to climate is urgently needed. Here, we perform a systematic review of literature on demographic responses to climate, focusing on terrestrial mammals, for which extensive demographic data are available. To assess the full spectrum of responses, we synthesize information from studies that quantitatively link climate to multiple demographic rates. We find only 106 such studies, corresponding to 87 mammal species. These 87 species constitute <1% of all terrestrial mammals. Our synthesis reveals a strong mismatch between the locations of demographic studies and the regions and taxa currently recognized as most vulnerable to climate change. Surprisingly, for most mammals and regions sensitive to climate change, holistic demographic responses to climate remain unknown. At the same time, we reveal that filling this knowledge gap is critical as the effects of climate change will operate via complex demographic mechanisms: a vast majority of mammal populations display projected increases in some demographic rates but declines in others, often depending on the specific environmental context, complicating simple projections of population fates. Assessments of population viability under climate change are in critical need to gather data that account for multiple demographic responses, and coordinated actions to assess demography holistically should be prioritized for mammals and other taxa.

Bridging gaps in demographic analysis with phylogenetic imputation.

Phylogenetically informed imputation methods have rarely been applied to estimate missing values in demographic data but may be a powerful tool for reconstructing vital rates of survival, maturation, and fecundity for species of conservation concern. Imputed vital rates could be used to parameterize demographic models to explore how populations respond when vital rates are perturbed. We used standardized vital rate estimates for 50 bird species to assess the use of phylogenetic imputation to fill gaps in demographic data. We calculated imputation accuracy for vital rates of focal species excluded from the data set either singly or in combination and with and without phylogeny, body mass, and life-history trait data. We used imputed vital rates to calculate demographic metrics, including generation time, to validate the use of imputation in demographic analyses. Covariance among vital rates and other trait data provided a strong basis to guide imputation of missing vital rates in birds, even in the absence of phylogenetic information. Mean NRMSE for null and phylogenetic models differed by <0.01 except when no vital rates were available or for vital rates with high phylogenetic signal (Pagel's λ > 0.8). In these cases, including body mass and life-history trait data compensated for lack of phylogenetic information: mean normalized root mean square error (NRMSE) for null and phylogenetic models differed by <0.01 for adult survival and <0.04 for maturation rate. Estimates of demographic metrics were sensitive to the accuracy of imputed vital rates. For example, mean error in generation time doubled in response to inaccurate estimates of maturation time. Accurate demographic data and metrics, such as generation time, are needed to inform conservation planning processes, for example through International Union for Conservation of Nature Red List assessments and population viability analysis. Imputed vital rates could be useful in this context but, as for any estimated model parameters, awareness of the sensitivities of demographic model outputs to the imputed vital rates is essential.

Cerrando Brechas en los Análisis Demográficos con Imputación Filogenética Resumen Los métodos de imputación guiados filogenéticamente se han aplicado con poca frecuencia para estimar los valores faltantes en los datos demográficos, aunque pueden ser una herramienta poderosa para la reconstrucción de tasas vitales de supervivencia, maduración y fecundidad de especies de importancia para la conservación. Las tasas vitales imputadas podrían usarse para generar parámetros en los modelos demográficos para explorar cómo responden las poblaciones cuando se perturban las tasas vitales. Utilizamos estimaciones de tasas vitales estandarizadas para 50 especies de aves para analizar el uso de la imputación filogenética para llenar los vacíos en los datos demográficos. Calculamos la certeza de imputación para las tasas vitales de las especies focales excluidas del conjunto de datos por sí solas o en combinación y con y sin datos de filogenia, masa corporal y características de historia de vida. Usamos las tasas vitales imputadas para calcular las medidas demográficas, incluyendo el tiempo de generación, y así validar el uso de la imputación en los análisis demográficos. La covarianza entre las tasas vitales y otros datos de características proporcionó una base sólida para orientar la imputación de tasas vitales faltantes en las aves, incluso la ausencia de información filogenética. El NRMSE medio para los modelos nulo y filogenético difirió por <0.01 salvo cuando no hubo tasas vitales disponibles o para tasas vitales con una señal filogenética alta (λ de Pagel > 0.8). En estos casos, la inclusión de la masa corporal y las características de historia de vida compensó la falta de información filogenética: el error cuadrático medio de la raíz normalizada media (NRMSE) para los modelos nulo y filogenéticos difirió por <0.01 para la supervivencia adulta y <0.04 para la tasa de maduración. Las estimaciones de las medidas demográficas fueron sensibles a la certeza de las tasas vitales imputadas. Por ejemplo, el error medio en el tiempo generacional se duplicó en respuesta a las estimaciones imprecisas del tiempo de maduración. Las medidas y datos demográficos certeros, como el tiempo generacional, son necesarios para orientar los procesos de planeación de la conservación; por ejemplo, a través de las valoraciones de la Lista Roja de la Unión Internacional para la Conservación de la Naturaleza y los análisis de viabilidad poblacional. Las tasas vitales imputadas podrían ser útiles en este contexto, pero como para cualquier tipo de parámetro de modelo estimado, el conocimiento de las sensibilidades del rendimiento del modelo demográfico es esencial para las tasas vitales imputadas.

The Chronic Effects of Copper and Cadmium on Life History Traits Across Cladocera Species: A Meta-analysis.

The effect of sublethal concentrations of heavy metals on cladoceran growth and reproduction is a cornerstone of modern ecotoxicology. However, the literature contains assays across numerous concentrations, on numerous species and genotypes, and conditions are far from consistent. We undertook a systematic review of the sublethal effects of copper and cadmium concentrations on Cladocera spp. life history (reproduction, maturation age, and somatic growth rate). Using meta-analysis, we tested the hypothesis that the effects of increasing Cu and Cd concentrations on traits may vary by species. We also evaluated where possible whether the effect of metal concentrations on traits vary by water hardness, exposure duration, or whether the metals were delivered in aqueous solution or via food. We surveyed > 200 papers, resulting in a set of 32 experimental studies representing 446 trials where the results were presented compared with Daphnia magna-the most commonly assayed species. We found qualitatively similar effects of Cu and Cd on life history traits that included reduction in reproduction and somatic growth rate and delay of maturation. Cladocera species showed marked variations in their susceptibility to metals, and D. magna was found to be the least sensitive species to sublethal changes in reproduction. The effects were largely consistent for aqueous vs. dietary food. Water hardness, where data were available, had no detectable effect. Available data indicate that exposure duration had no effect on the toxicity of Cu but did for D. magna reproductive response to Cd. Our study highlights the importance of including species identity when considering toxicological testing and regulation development.

The impact of intraspecific variation on food web structure.

Accounting for the variation that occurs within species in food webs can theoretically result in significant changes in both network structure and dynamics. However, there has been little work exploring their role with empirical data. In particular, the variation associated with species' life cycles, which is prevalent and represents both trait variation and taxonomic identity, has received little attention. Here, we characterize the structural consequences of life stage variation in five food webs, including a newly compiled web from the Arabian Gulf. We show that making life stage variation explicit in food webs results in larger food webs that possess consistent structural changes that are separate from the changes in structure that come simply from increasing the number of nodes in the webs. Furthermore, we show that the magnitude of these changes is related to ontogenetic specialism, the degree of overlap in the ecological niches of life stages. These results demonstrate the capacity of intraspecific variation to affect ecological networks and indicate the potential usefulness of stage-structured food webs, which capture size and taxonomic information, to represent variation below the species level.

Evolution of a predator-induced, nonlinear reaction norm.

Inducible, anti-predator traits are a classic example of phenotypic plasticity. Their evolutionary dynamics depend on their genetic basis, the historical pattern of predation risk that populations have experienced and current selection gradients. When populations experience predators with contrasting hunting strategies and size preferences, theory suggests contrasting micro-evolutionary responses to selection. Daphnia pulex is an ideal species to explore the micro-evolutionary response of anti-predator traits because they face heterogeneous predation regimes, sometimes experiencing only invertebrate midge predators and other times experiencing vertebrate fish and invertebrate midge predators. We explored plausible patterns of adaptive evolution of a predator-induced morphological reaction norm. We combined estimates of selection gradients that characterize the various habitats that D. pulex experiences with detail on the quantitative genetic architecture of inducible morphological defences. Our data reveal a fine scale description of daphnid defensive reaction norms, and a strong covariance between the sensitivity to cues and the maximum response to cues. By analysing the response of the reaction norm to plausible, predator-specific selection gradients, we show how in the context of this covariance, micro-evolution may be more uniform than predicted from size-selective predation theory. Our results show how covariance between the sensitivity to cues and the maximum response to cues for morphological defence can shape the evolutionary trajectory of predator-induced defences in D. pulex.

Antagonistic interactions between an invasive alien and a native coccinellid species may promote coexistence.

Despite the capacity of invasive alien species to alter ecosystems, the mechanisms underlying their impact remain only partly understood. Invasive alien predators, for example, can significantly disrupt recipient communities by consuming prey species or acting as an intraguild predator (IGP). Behavioural interactions are key components of interspecific competition between predators, yet these are often overlooked invasion processes. Here, we show how behavioural, non-lethal IGP interactions might facilitate the establishment success of an invading alien species. We experimentally assessed changes in feeding behaviour (prey preference and consumption rate) of native UK coccinellid species (Adalia bipunctata and Coccinella septempunctata), whose populations are, respectively, declining and stable, when exposed to the invasive intraguild predator, Harmonia axyridis. Using a population dynamics model parameterized with these experimental data, we predicted how intraguild predation, accommodating interspecific behavioural interactions, might impact the abundance of the native and invasive alien species over time. When competing for the same aphid resource, the feeding rate of A. bipunctata significantly increased compared to the feeding in isolation, while the feeding rate of H. axyridis significantly decreased. This suggests that despite significant declines in the UK, A. bipunctata is a superior competitor to the intraguild predator H. axyridis. In contrast, the behaviour of non-declining C. septempunctata was unaltered by the presence of H. axyridis. Our experimental data show the differential behavioural plasticity of competing native and invasive alien predators, but do not explain A. bipunctata declines observed in the UK. Using behavioural plasticity as a parameter in a population dynamic model for A. bipunctata and H. axyridis, coexistence is predicted between the native and invasive alien following an initial period of decline in the native species. We demonstrate how empirical and theoretical techniques can be combined to understand better the processes and consequences of alien species invasions for native biodiversity.

The use of natural infochemicals for sustainable and efficient harvesting of the microalgae Scenedesmus spp. for biotechnology: insights from a meta-analysis.

Open raceway ponds are regarded as the most economically viable option for large-scale cultivation of microalgae for low to mid-value bio-products, such as biodiesel. However, improvements are required including reducing the costs associated with harvesting biomass. There is now a growing interest in exploiting natural ecological processes within biotechnology. We review how chemical cues produced by algal grazers induce colony formation in algal cells, which subsequently leads to their sedimentation. A statistical meta-analysis of more than 80 studies reveals that Daphnia grazers can induce high levels of colony formation and sedimentation in Scenedesmus obliquus and that these natural, infochemical induced sedimentation rates are comparable to using commercial chemical equivalents. These data suggest that natural ecological interactions can be co-opted in biotechnology as part of a promising, low energy and clean harvesting method for use in large raceway systems.

The ecological forecast horizon, and examples of its uses and determinants.

Forecasts of ecological dynamics in changing environments are increasingly important, and are available for a plethora of variables, such as species abundance and distribution, community structure and ecosystem processes. There is, however, a general absence of knowledge about how far into the future, or other dimensions (space, temperature, phylogenetic distance), useful ecological forecasts can be made, and about how features of ecological systems relate to these distances. The ecological forecast horizon is the dimensional distance for which useful forecasts can be made. Five case studies illustrate the influence of various sources of uncertainty (e.g. parameter uncertainty, environmental variation, demographic stochasticity and evolution), level of ecological organisation (e.g. population or community), and organismal properties (e.g. body size or number of trophic links) on temporal, spatial and phylogenetic forecast horizons. Insights from these case studies demonstrate that the ecological forecast horizon is a flexible and powerful tool for researching and communicating ecological predictability. It also has potential for motivating and guiding agenda setting for ecological forecasting research and development.

The alignment between phenotypic plasticity, the major axis of genetic variation and the response to selection.

Phenotypic plasticity is the ability of a genotype to produce more than one phenotype in order to match the environment. Recent theory proposes that the major axis of genetic variation in a phenotypically plastic population can align with the direction of selection. Therefore, theory predicts that plasticity directly aids adaptation by increasing genetic variation in the direction favoured by selection and reflected in plasticity. We evaluated this theory in the freshwater crustacean Daphnia pulex, facing predation risk from two contrasting size-selective predators. We estimated plasticity in several life-history traits, the G matrix of these traits, the selection gradients on reproduction and survival, and the predicted responses to selection. Using these data, we tested whether the genetic lines of least resistance and the predicted response to selection aligned with plasticity. We found predator environment-specific G matrices, but shared genetic architecture across environments resulted in more constraint in the G matrix than in the plasticity of the traits, sometimes preventing alignment of the two. However, as the importance of survival selection increased, the difference between environments in their predicted response to selection increased and resulted in closer alignment between the plasticity and the predicted selection response. Therefore, plasticity may indeed aid adaptation to new environments.

Endocrine regulation of predator-induced phenotypic plasticity.

Elucidating the developmental and genetic control of phenotypic plasticity remains a central agenda in evolutionary ecology. Here, we investigate the physiological regulation of phenotypic plasticity induced by another organism, specifically predator-induced phenotypic plasticity in the model ecological and evolutionary organism Daphnia pulex. Our research centres on using molecular tools to test among alternative mechanisms of developmental control tied to hormone titres, receptors and their timing in the life cycle. First, we synthesize detail about predator-induced defenses and the physiological regulation of arthropod somatic growth and morphology, leading to a clear prediction that morphological defences are regulated by juvenile hormone and life-history plasticity by ecdysone and juvenile hormone. We then show how a small network of genes can differentiate phenotype expression between the two primary developmental control pathways in arthropods: juvenoid and ecdysteroid hormone signalling. Then, by applying an experimental gradient of predation risk, we show dose-dependent gene expression linking predator-induced plasticity to the juvenoid hormone pathway. Our data support three conclusions: (1) the juvenoid signalling pathway regulates predator-induced phenotypic plasticity; (2) the hormone titre (ligand), rather than receptor, regulates predator-induced developmental plasticity; (3) evolution has favoured the harnessing of a major, highly conserved endocrine pathway in arthropod development to regulate the response to cues about changing environments (risk) from another organism (predator).

Accelerating the open research agenda to solve global challenges.

Harnessing science-based policy is key to addressing global challenges like the biodiversity and climate crises. Open research principles underpin effective science-based policy, but the uptake of these principles is likely constrained by the politicisation, commoditisation and conflicting motives of stakeholders in the research landscape. Here, using the mission and vision statements from 129 stakeholders from across the research landscape, we explore alignment in open research principles between stakeholders. We find poor alignment between stakeholders, largely focussed around journals, societies and funders, all of which have low open research language-use. We argue that this poor alignment stifles knowledge flow within the research landscape, ultimately limiting the mobilisation of impactful science-based policy. We offer recommendations on how the research landscape could embrace open research principles to accelerate societies' ability to solve global challenges.

Predator-induced shape plasticity in Daphnia pulex.

All animals and plants respond to changes in the environment during their life cycle. This flexibility is known as phenotypic plasticity and allows organisms to cope with variable environments. A common source of environmental variation is predation risk, which describes the likelihood of being attacked and killed by a predator. Some species can respond to the level of predation risk by producing morphological defences against predation. A classic example is the production of so-called 'neckteeth' in the water flea, Daphnia pulex, which defend against predation from Chaoborus midge larvae. Previous studies of this defence have focussed on changes in pedestal size and the number of spikes along a gradient of predation risk. Although these studies have provided a model for continuous phenotypic plasticity, they do not capture the whole-organism shape response to predation risk. In contrast, studies in fish and amphibians focus on shape as a complex, multi-faceted trait made up of different variables. In this study, we analyse how multiple aspects of shape change in D. pulex along a gradient of predation risk from Chaoborus flavicans. These changes are dominated by the neckteeth defence, but there are also changes in the size and shape of the head and the body. We detected change in specific modules of the body plan and a level of integration among modules. These results are indicative of a complex, multi-faceted response to predation and provide insight into how predation risk drives variation in shape and size at the level of the whole organism.

Quantifying multivariate plasticity: genetic variation in resource acquisition drives plasticity in resource allocation to components of life history.

Acquisition and allocation of resources are central to life-history theory. However, empirical work typically focuses only on allocation despite the fact that relationships between fitness components may be governed by differences in the ability of individuals to acquire resources across environments. Here, we outline a statistical framework to partition the genetic basis of multivariate plasticity into independent axes of genetic variation, and quantify for the first time, the extent to which specific traits drive multitrait genotype-environment interactions. Our framework generalises to analyses of plasticity, growth and ageing. We apply this approach to a unique, large-scale, multivariate study of acquisition, allocation and plasticity in the life history of the cricket, Gryllus firmus. We demonstrate that resource acquisition and allocation are genetically correlated, and that plasticity in trade-offs between allocation to components of fitness is 90% dependent on genetic variance for total resource acquisition. These results suggest that genotype-environment effects for resource acquisition can maintain variation in life-history components that are typically observed in the wild.

Ecological and demographic correlates of helping behaviour in a cooperatively breeding bird.

The evolution of cooperation is a persistent problem for evolutionary biologists. In particular, understanding of the factors that promote the expression of helping behaviour in cooperatively breeding species remains weak, presumably because of the diverse nature of ecological and demographic drivers that promote sociality. In this study, we use data from a long-term study of a facultative cooperative breeder, the long-tailed tit Aegithalos caudatus, to investigate the factors influencing annual variation in helping behaviour. Long-tailed tits exhibit redirected helping in which failed breeders may become helpers, usually at a relative's nest; thus, helping is hypothesised to be associated with causes of nest failure and opportunities to renest or help. We tested predictions regarding the relationship between annual measures of cooperative behaviour and four explanatory variables: nest predation rate, length of the breeding season, population-level relatedness and population density. We found that the degree of helping was determined principally by two factors that constrain successful independent reproduction. First, as predicted, cooperative behaviour peaked at intermediate levels of nest predation, when there are both failed breeders (i.e. potential helpers) and active nests (i.e. potential recipients) available. Second, there were more helpers in shorter breeding seasons when opportunities for renesting by failed breeders are more limited. These are novel drivers of helping behaviour in avian cooperative breeding systems, and this study illustrates the difficulty of identifying common ecological or demographic factors underlying the evolution of such systems.

Innovation and elaboration on the avian tree of life.

Widely documented, megaevolutionary jumps in phenotypic diversity continue to perplex researchers because it remains unclear whether these marked changes can emerge from microevolutionary processes. Here, we tackle this question using new approaches for modeling multivariate traits to evaluate the magnitude and distribution of elaboration and innovation in the evolution of bird beaks. We find that elaboration, evolution along the major axis of phenotypic change, is common at both macro- and megaevolutionary scales, whereas innovation, evolution away from the major axis of phenotypic change, is more prominent at megaevolutionary scales. The major axis of phenotypic change among species beak shapes at megaevolutionary scales is an emergent property of innovation across clades. Our analyses suggest that the reorientation of phenotypes via innovation is a ubiquitous route for divergence that can arise through gradual change alone, opening up further avenues for evolution to explore.

Reproducibility in ecology and evolution: Minimum standards for data and code.

We call for journals to commit to requiring open data be archived in a format that will be simple and clear for readers to understand and use. If applied consistently, these requirements will allow contributors to be acknowledged for their work through citation of open data, and facilitate scientific progress.