The impacts of host association and perturbation on symbiont fitness.

Symbiosis can benefit hosts in numerous ways, but less is known about whether interactions with hosts benefit symbionts-the smaller species in the relationship. To determine the fitness impact of host association on symbionts in likely mutualisms, we conducted a meta-analysis across 91 unique host-symbiont pairings under a range of spatial and temporal contexts. Specifically, we assess the consequences to symbiont fitness when in and out of symbiosis, as well as when the symbiosis is under suboptimal or varying environments and biological conditions (e.g., host age). We find that some intracellular symbionts associated with protists tend to have greater fitness when the symbiosis is under stressful conditions. Symbionts of plants and animals did not exhibit this trend, suggesting that symbionts of multicellular hosts are more robust to perturbations. Symbiont fitness also generally increased with host age. Lastly, we show that symbionts able to proliferate in- and outside host cells exhibit greater fitness than those found exclusively inside or outside cells. The ability to grow in multiple locations may thus help symbionts thrive. We discuss these fitness patterns in light of host-driven factors, whereby hosts exert influence over symbionts to suit their own needs. Supplementary Information: The online version contains supplementary material available at 10.1007/s13199-024-00984-6.

Recent exposure to environmental stochasticity does not determine the demographic resilience of natural populations.

Escalating climatic and anthropogenic pressures expose ecosystems worldwide to increasingly stochastic environments. Yet, our ability to forecast the responses of natural populations to this increased environmental stochasticity is impeded by a limited understanding of how exposure to stochastic environments shapes demographic resilience. Here, we test the association between local environmental stochasticity and the resilience attributes (e.g. resistance, recovery) of 2242 natural populations across 369 animal and plant species. Contrary to the assumption that past exposure to frequent environmental shifts confers a greater ability to cope with current and future global change, we illustrate how recent environmental stochasticity regimes from the past 50 years do not predict the inherent resistance or recovery potential of natural populations. Instead, demographic resilience is strongly predicted by the phylogenetic relatedness among species, with survival and developmental investments shaping their responses to environmental stochasticity. Accordingly, our findings suggest that demographic resilience is a consequence of evolutionary processes and/or deep-time environmental regimes, rather than recent-past experiences.

Global gene flow releases invasive plants from environmental constraints on genetic diversity.

When plants establish outside their native range, their ability to adapt to the new environment is influenced by both demography and dispersal. However, the relative importance of these two factors is poorly understood. To quantify the influence of demography and dispersal on patterns of genetic diversity underlying adaptation, we used data from a globally distributed demographic research network comprising 35 native and 18 nonnative populations of Plantago lanceolata Species-specific simulation experiments showed that dispersal would dilute demographic influences on genetic diversity at local scales. Populations in the native European range had strong spatial genetic structure associated with geographic distance and precipitation seasonality. In contrast, nonnative populations had weaker spatial genetic structure that was not associated with environmental gradients but with higher within-population genetic diversity. Our findings show that dispersal caused by repeated, long-distance, human-mediated introductions has allowed invasive plant populations to overcome environmental constraints on genetic diversity, even without strong demographic changes. The impact of invasive plants may, therefore, increase with repeated introductions, highlighting the need to constrain future introductions of species even if they already exist in an area.

Life history adaptations to fluctuating environments: Combined effects of demographic buffering and lability.

Demographic buffering and lability have been identified as adaptive strategies to optimise fitness in a fluctuating environment. These are not mutually exclusive, however, we lack efficient methods to measure their relative importance for a given life history. Here, we decompose the stochastic growth rate (fitness) into components arising from nonlinear responses and variance-covariance of demographic parameters to an environmental driver, which allows studying joint effects of buffering and lability. We apply this decomposition for 154 animal matrix population models under different scenarios to explore how these main fitness components vary across life histories. Faster-living species appear more responsive to environmental fluctuations, either positively or negatively. They have the highest potential for strong adaptive demographic lability, while demographic buffering is a main strategy in slow-living species. Our decomposition provides a comprehensive framework to study how organisms adapt to variability through buffering and lability, and to predict species responses to climate change.

Life history mediates the trade-offs among different components of demographic resilience.

Accelerating rates of biodiversity loss underscore the need to understand how species achieve resilience-the ability to resist and recover from a/biotic disturbances. Yet, the factors determining the resilience of species remain poorly understood, due to disagreements on its definition and the lack of large-scale analyses. Here, we investigate how the life history of 910 natural populations of animals and plants predicts their intrinsic ability to be resilient. We show that demographic resilience can be achieved through different combinations of compensation, resistance and recovery after a disturbance. We demonstrate that these resilience components are highly correlated with life history traits related to the species' pace of life and reproductive strategy. Species with longer generation times require longer recovery times post-disturbance, whilst those with greater reproductive capacity have greater resistance and compensation. Our findings highlight the key role of life history traits to understand species resilience, improving our ability to predict how natural populations cope with disturbance regimes.

Data gaps and opportunities for comparative and conservation biology.

Biodiversity loss is a major challenge. Over the past century, the average rate of vertebrate extinction has been about 100-fold higher than the estimated background rate and population declines continue to increase globally. Birth and death rates determine the pace of population increase or decline, thus driving the expansion or extinction of a species. Design of species conservation policies hence depends on demographic data (e.g., for extinction risk assessments or estimation of harvesting quotas). However, an overview of the accessible data, even for better known taxa, is lacking. Here, we present the Demographic Species Knowledge Index, which classifies the available information for 32,144 (97%) of extant described mammals, birds, reptiles, and amphibians. We show that only 1.3% of the tetrapod species have comprehensive information on birth and death rates. We found no demographic measures, not even crude ones such as maximum life span or typical litter/clutch size, for 65% of threatened tetrapods. More field studies are needed; however, some progress can be made by digitalizing existing knowledge, by imputing data from related species with similar life histories, and by using information from captive populations. We show that data from zoos and aquariums in the Species360 network can significantly improve knowledge for an almost eightfold gain. Assessing the landscape of limited demographic knowledge is essential to prioritize ways to fill data gaps. Such information is urgently needed to implement management strategies to conserve at-risk taxa and to discover new unifying concepts and evolutionary relationships across thousands of tetrapod species.

Climatic and evolutionary contexts are required to infer plant life history strategies from functional traits at a global scale.

Life history strategies are fundamental to the ecology and evolution of organisms and are important for understanding extinction risk and responses to global change. Using global datasets and a multiple response modelling framework we show that trait-climate interactions are associated with life history strategies for a diverse range of plant species at the global scale. Our modelling framework informs our understanding of trade-offs and positive correlations between elements of life history after accounting for environmental context and evolutionary and trait-based constraints. Interactions between plant traits and climatic context were needed to explain variation in age at maturity, distribution of mortality across the lifespan and generation times of species. Mean age at maturity and the distribution of mortality across plants' lifespan were under evolutionary constraints. These findings provide empirical support for the theoretical expectation that climatic context is key to understanding trait to life history relationships globally.

Phenotypic plasticity masks range-wide genetic differentiation for vegetative but not reproductive traits in a short-lived plant.

Genetic differentiation and phenotypic plasticity jointly shape intraspecific trait variation, but their roles differ among traits. In short-lived plants, reproductive traits may be more genetically determined due to their impact on fitness, whereas vegetative traits may show higher plasticity to buffer short-term perturbations. Combining a multi-treatment greenhouse experiment with observational field data throughout the range of a widespread short-lived herb, Plantago lanceolata, we (1) disentangled genetic and plastic responses of functional traits to a set of environmental drivers and (2) assessed how genetic differentiation and plasticity shape observational trait-environment relationships. Reproductive traits showed distinct genetic differentiation that largely determined observational patterns, but only when correcting traits for differences in biomass. Vegetative traits showed higher plasticity and opposite genetic and plastic responses, masking the genetic component underlying field-observed trait variation. Our study suggests that genetic differentiation may be inferred from observational data only for the traits most closely related to fitness.

Senescence: why and where selection gradients might not decline with age.

Patterns of ageing across the tree of life are much more diverse than previously thought. Yet, we still do not adequately understand how, why and where across the tree of life a particular pattern of ageing will evolve. An ability to predict ageing patterns requires a firmer understanding of how and why different ecological and evolutionary factors alter the sensitivity of fitness to age-related changes in mortality and reproduction. From this understanding, we can ask why and where selection gradients might not decline with age. Here, we begin by summarizing the recent breadth of literature that is unearthing, empirically and theoretically, the mechanisms that drive variation in patters of senescence. We focus on the relevance of two key parameters, population structure and reproductive value, as key to understanding selection gradients, and therefore senescence. We discuss how growth form, individual trade-offs, stage structure and social interactions may all facilitate differing distributions of these two key parameters than those predicted by classical theory. We argue that these four key aspects can help us understand why patterns of negligible and negative senescence can actually be explained under the same evolutionary framework as classical senescence.

Lagged and dormant season climate better predict plant vital rates than climate during the growing season.

Understanding the effects of climate on the vital rates (e.g., survival, development, reproduction) and dynamics of natural populations is a long-standing quest in ecology, with ever-increasing relevance in the face of climate change. However, linking climate drivers to demographic processes requires identifying the appropriate time windows during which climate influences vital rates. Researchers often do not have access to the long-term data required to test a large number of windows, and are thus forced to make a priori choices. In this study, we first synthesize the literature to assess current a priori choices employed in studies performed on 104 plant species that link climate drivers with demographic responses. Second, we use a sliding-window approach to investigate which combination of climate drivers and temporal window have the best predictive ability for vital rates of four perennial plant species that each have over a decade of demographic data (Helianthella quinquenervis, Frasera speciosa, Cylindriopuntia imbricata, and Cryptantha flava). Our literature review shows that most studies consider time windows in only the year preceding the measurement of the vital rate(s) of interest, and focus on annual or growing season temporal scales. In contrast, our sliding-window analysis shows that in only four out of 13 vital rates the selected climate drivers have time windows that align with, or are similar to, the growing season. For many vital rates, the best window lagged more than 1 year and up to 4 years before the measurement of the vital rate. Our results demonstrate that for the vital rates of these four species, climate drivers that are lagged or outside of the growing season are the norm. Our study suggests that considering climatic predictors that fall outside of the most recent growing season will improve our understanding of how climate affects population dynamics.

Four key challenges in the open-data revolution.

In Focus: Culina, A., Adriaensen, F., Bailey, L. D., et al. (2021) Connecting the data landscape of long-term ecological studies: The SPI-Birds data hub. Journal of Animal Ecology, https://doi.org/10.1111/1365-2656.13388. Long-term, individual-based datasets have been at the core of many key discoveries in ecology, and calls for the collection, curation and release of these kinds of ecological data are contributing to a flourishing open-data revolution in ecology. Birds, in particular, have been the focus of international research for decades, resulting in a number of uniquely long-term studies, but accessing these datasets has been historically challenging. Culina et al. (2021) introduce an online repository of individual-level, long-term bird records with ancillary data (e.g. genetics), which will enable key ecological questions to be answered on a global scale. As well as these opportunities, however, we argue that the ongoing open-data revolution comes with four key challenges relating to the (1) harmonisation of, (2) biases in, (3) expertise in and (4) communication of, open ecological data. Here, we discuss these challenges and how key efforts such as those by Culina et al. are using FAIR (Findable, Accessible, Interoperable and Reproducible) principles to overcome them. The open-data revolution will undoubtedly reshape our understanding of ecology, but with it the ecological community has a responsibility to ensure this revolution is ethical and effective.

Enfocado: Culina, A., Adriaensen, F., Bailey, L. D., et al. (2021) Connecting the data landscape of long-term ecological studies: the SPI-Birds data hub. Journal of Animal Ecology, https://doi.org/10.1111/1365-2656.13388. La información a largo plazo y a nivel de individuo ha cementado numerosos descubrimientos clave en la ecología, y las llamadas para la recopilación, conservación, y publicación de este tipo de datos ecológicos están contribuyendo a una revolución de información abierta en la ecología. Las aves, en particular, han sido el foco de la investigación internacional durante décadas, el cual ha resultado en una serie de estudios únicos a largo plazo. No obstante, historicamente el acceso libre a esta información ha representado un desafío importante. Culina y colegas (2021) presentan un repositorio online de registros de aves a nivel individual y de alta replicación temporal con metadatos (por ejemplo, genética) que permitirá explorar importantes preguntas ecológicas a grandes escalas espaciales. Sin embargo, además de las oportunidades presentadas en esta base de datos, argumentamos que la revolución de la información abierta viene con cuatro desafíos clave relacionados con (1) la armonización de, (2) los sesgos en, (3) la experiencia en y (4) la comunicación de información ecológica de forma abierta y transparente. Aquí discutimos estos desafíos y cómo esfuerzos clave como los de Culina y colaboradores están utilizando los principios FAIR (por sus siglas en inglés: Localizable, Accesible, Interoperable y Reproducible) para superarlos. La revolución de la información abierta sin duda remodelará nuestro entendimiento de la ecología. Sin embargo, la comunidad ecológica tiene la responsabilidad de garantizar que esta revolución sea ética y eficaz.

The projected degradation of subtropical coral assemblages by recurrent thermal stress.

Subtropical coral assemblages are threatened by similar extreme thermal stress events to their tropical counterparts. Yet, the mid- and long-term thermal stress responses of corals in subtropical environments remain largely unquantified, limiting our capacity to predict their future viability. The annual survival, growth and recruitment of 311 individual corals within the Solitary Islands Marine Park (Australia) was recorded over a 3-year period (2016-2018), including the 2015/2016 thermal stress event. These data were used to parameterise integral projection models quantifying the effect of thermal stress within a subtropical coral assemblage. Stochastic simulations were also applied to evaluate the implications of recurrent thermal stress scenarios predicted by four different Representative Concentration Pathways. We report differential shifts in population growth rates (λ) among coral populations during both stress and non-stress periods, confirming contrasting bleaching responses among taxa. However, even during non-stress periods, the observed dynamics for all taxa were unable to maintain current community composition, highlighting the need for external recruitment sources to support the community structure. Across all coral taxa, projected stochastic growth rates (λs ) were found to be lowest under higher emissions scenarios. Correspondingly, predicted increases in recurrent thermal stress regimes may accelerate the loss of coral coverage, species diversity and structural complexity within subtropical regions. We suggest that these trends are primarily due to the susceptibility of subtropical specialists and endemic species, such as Pocillopora aliciae, to thermal stress. Similarly, the viability of many tropical coral populations at higher latitudes is highly dependent on the persistence of up-current tropical systems. As such, the inherent dynamics of subtropical coral populations appear unable to support their future persistence under unprecedented thermal disturbance scenarios.

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.

Diversity of ageing across the tree of life.

Evolution drives, and is driven by, demography. A genotype moulds its phenotype's age patterns of mortality and fertility in an environment; these two patterns in turn determine the genotype's fitness in that environment. Hence, to understand the evolution of ageing, age patterns of mortality and reproduction need to be compared for species across the tree of life. However, few studies have done so and only for a limited range of taxa. Here we contrast standardized patterns over age for 11 mammals, 12 other vertebrates, 10 invertebrates, 12 vascular plants and a green alga. Although it has been predicted that evolution should inevitably lead to increasing mortality and declining fertility with age after maturity, there is great variation among these species, including increasing, constant, decreasing, humped and bowed trajectories for both long- and short-lived species. This diversity challenges theoreticians to develop broader perspectives on the evolution of ageing and empiricists to study the demography of more species.

Forecasting species range dynamics with process-explicit models: matching methods to applications.

Knowing where species occur is fundamental to many ecological and environmental applications. Species distribution models (SDMs) are typically based on correlations between species occurrence data and environmental predictors, with ecological processes captured only implicitly. However, there is a growing interest in approaches that explicitly model processes such as physiology, dispersal, demography and biotic interactions. These models are believed to offer more robust predictions, particularly when extrapolating to novel conditions. Many process-explicit approaches are now available, but it is not clear how we can best draw on this expanded modelling toolbox to address ecological problems and inform management decisions. Here, we review a range of process-explicit models to determine their strengths and limitations, as well as their current use. Focusing on four common applications of SDMs - regulatory planning, extinction risk, climate refugia and invasive species - we then explore which models best meet management needs. We identify barriers to more widespread and effective use of process-explicit models and outline how these might be overcome. As well as technical and data challenges, there is a pressing need for more thorough evaluation of model predictions to guide investment in method development and ensure the promise of these new approaches is fully realised.

Fast-slow continuum and reproductive strategies structure plant life-history variation worldwide.

The identification of patterns in life-history strategies across the tree of life is essential to our prediction of population persistence, extinction, and diversification. Plants exhibit a wide range of patterns of longevity, growth, and reproduction, but the general determinants of this enormous variation in life history are poorly understood. We use demographic data from 418 plant species in the wild, from annual herbs to supercentennial trees, to examine how growth form, habitat, and phylogenetic relationships structure plant life histories and to develop a framework to predict population performance. We show that 55% of the variation in plant life-history strategies is adequately characterized using two independent axes: the fast-slow continuum, including fast-growing, short-lived plant species at one end and slow-growing, long-lived species at the other, and a reproductive strategy axis, with highly reproductive, iteroparous species at one extreme and poorly reproductive, semelparous plants with frequent shrinkage at the other. Our findings remain consistent across major habitats and are minimally affected by plant growth form and phylogenetic ancestry, suggesting that the relative independence of the fast-slow and reproduction strategy axes is general in the plant kingdom. Our findings have similarities with how life-history strategies are structured in mammals, birds, and reptiles. The position of plant species populations in the 2D space produced by both axes predicts their rate of recovery from disturbances and population growth rate. This life-history framework may complement trait-based frameworks on leaf and wood economics; together these frameworks may allow prediction of responses of plants to anthropogenic disturbances and changing environments.

Interactive life-history traits predict sensitivity of plants and animals to temporal autocorrelation.

Temporal autocorrelation in demographic processes is an important aspect of population dynamics, but a comprehensive examination of its effects on different life-history strategies is lacking. We use matrix population models from 454 plant and animal populations to simulate stochastic population growth rates (log λs ) under different temporal autocorrelations in demographic rates, using simulated and observed covariation among rates. We then test for differences in sensitivities, or changes of log λs to changes in autocorrelation among two major axes of life-history strategies, obtained from phylogenetically informed principal component analysis: the fast-slow and reproductive-strategy continua. Fast life histories exhibit highest sensitivities to simulated autocorrelation in demographic rates across reproductive strategies. Slow life histories are less sensitive to temporal autocorrelation, but their sensitivities increase among highly iteroparous species. We provide cross-taxonomic evidence that changes in the autocorrelation of environmental variation may affect a wide range of species, depending on complex interactions of life-history strategies.

Less favourable climates constrain demographic strategies in plants.

Correlative species distribution models are based on the observed relationship between species' occurrence and macroclimate or other environmental variables. In climates predicted less favourable populations are expected to decline, and in favourable climates they are expected to persist. However, little comparative empirical support exists for a relationship between predicted climate suitability and population performance. We found that the performance of 93 populations of 34 plant species worldwide - as measured by in situ population growth rate, its temporal variation and extinction risk - was not correlated with climate suitability. However, correlations of demographic processes underpinning population performance with climate suitability indicated both resistance and vulnerability pathways of population responses to climate: in less suitable climates, plants experienced greater retrogression (resistance pathway) and greater variability in some demographic rates (vulnerability pathway). While a range of demographic strategies occur within species' climatic niches, demographic strategies are more constrained in climates predicted to be less suitable.