Research addressing the effects of global warming on the distribution and persistence of species generally assumes that population variation in thermal tolerance is spatially constant or overridden ...by interspecific variation. Typically, this rationale is implicit in sourcing one critical thermal maximum (CTmax) population estimate per species to model spatiotemporal cross‐taxa variation in heat tolerance. Theory suggests that such an approach could result in biased or imprecise estimates and forecasts of impact from climate warming, but limited empirical evidence in support of those expectations exists.
We experimentally quantify the magnitude of intraspecific variation in CTmax among lizard populations, and the extent to which incorporating such variability can alter estimates of climate impact through a biophysical model. To do so, we measured CTmax from 59 populations of 15 Iberian lizard species (304 individuals).
The overall median CTmax across all individuals from all species was 42.8°C and ranged from 40.5 to 48.3°C, with species medians decreasing through xeric, climate‐generalist and mesic taxa. We found strong statistical support for intraspecific differentiation in CTmax by up to a median of 3°C among populations. We show that annual restricted activity (operative temperature > CTmax) over the Iberian distribution of our study species differs by a median of >80 hr per 25‐km2 grid cell based on different population‐level CTmax estimates. This discrepancy leads to predictions of spatial variation in annual restricted activity to change by more than 20 days for six of the study species.
Considering that during restriction periods, reptiles should be unable to feed and reproduce, current projections of climate‐change impacts on the fitness of ectotherm fauna could be under‐ or over‐estimated depending on which population is chosen to represent the physiological spectra of the species in question. Mapping heat tolerance over the full geographical ranges of single species is thus critical to address cross‐taxa patterns and drivers of heat tolerance in a biologically comprehensive way.
En macroecología, cuando se evalúan los efectos del calentamiento global en la distribución y persistencia de las especies, generalmente se asume que la tolerancia térmica entre poblaciones es constante a lo largo de la distribución de las especies, o despreciable en comparación con su variación interespecífica. Tal planteamiento es implícito cuando se utiliza el máximo crítico termal (CTmax) de una población por especie para modelar la variación espacio‐temporal de la tolerancia termal entre especies. Teóricamente, esto puede sesgar o añadir imprecisión en las estimaciones y proyecciones de impacto por el calentamiento asociado al cambio global, pero la evidencia empírica de tales previsiones es limitada.
Cuantificamos experimentalmente la magnitud de la variación intraespecífica en CTmax entre poblaciones de lagartijas, y hasta qué punto la incorporación de esta variabilidad puede alterar la evaluación del impacto del clima a través de un modelo biofísico. Para ello, medimos el CTmax en 59 poblaciones de 15 especies de lagartijas ibéricas (304 individuos).
La mediana general del CTmax fue 42.8°C entre todos los individuos de todas las especies, y varió desde 40.5 hasta 48.3°C, mientras que las medianas por especie decrecieron de taxones de hábitats secos, pasando por generalistas, hasta taxones de hábitats húmedos. Encontramos un fuerte apoyo estadístico para la diferenciación intraespecífica del CTmax de hasta de 3°C (mediana) entre poblaciones. Mostramos que la actividad restringida anual (temperatura operativa > CTmax) en la distribución ibérica de las especies de estudio difirió en > 80 horas por celda espacial de 25‐km2 (mediana) en función del CTmax poblacional. Esta discrepancia conduce a que las predicciones de la variación espacial de la actividad restringida anual difieran en más de 20 días en seis de las especies investigadas.
Teniendo en cuenta que durante los periodos de restricción, los reptiles son incapaces de alimentarse y reproducirse, las proyecciones actuales de impactos del cambio climático sobre el fitness de la fauna ectotérmica pueden infra‐ o sobre‐estimarse dependiendo de la población elegida para representar el espectro fisiológico de cada especie. Cartografiar la tolerancia termal sobre el rango geográfico completo de especies individuales es por lo tanto crucial, antes de que podamos examinar patrones y mecanismos de variación entre múltiples especies de una manera biológicamente comprensiva.
In one of the largest field surveys of thermal tolerances undertaken to date (304 individuals, 59 populations, 15 species), the authors show that estimates of climate impact on Iberian lizards differ depending on which population estimate of heat tolerance is taken to represent this trait in a full species.
Principal component analysis (PCA) is a powerful tool for the analysis of population structure, a genetic property that is essential to understand the evolutionary processes driving biological ...diversification and (pre)historical colonizations, migrations and extinctions. In the current era of high‐throughput sequencing technologies, population structure can be quantified from scores of genetic markers across hundreds to thousands of genomes. However, these big genomic datasets pose substantial computing and analytical challenges.
We present the r package smartsnp for fast and user‐friendly computation of PCA on single‐nucleotide polymorphism (SNP) data. Inspired by the current field‐standard software EIGENSOFT, smartsnp includes appropriate SNP scaling for genetic drift and allows projection of ancient samples onto a modern genetic space while also providing permutation‐based multivariate tests for population differences in genetic diversity (both location and dispersion).
Our extensive benchmarks show that smartsnp's PCA is 2–4 times faster than EIGENSOFT's SMARTPCA algorithm across a wide range of sample and SNP sizes. All four smartsnp functions (smart_pca, smart_permanova, smart_permdisp and smart_mva) process datasets with up to 100 samples and 1 million simulated SNPs in less than 30 s and accurately recreate previously published SMARTPCA of ancient‐human and wolf genotypes.
The package smartsnp provides fast and robust multivariate ordination and hypothesis testing for big genomic data that is also suitable for ancient and low‐coverage modern DNA. The simple implementation should appeal to biological conservation, evolutionary, ecological and (palaeo)genomic researchers, and be useful for phenotype, ancestry and lineage studies.
El Análisis de Componentes Principales (PCA) es una herramienta poderosa para el análisis de la estructura de las poblaciones, una propiedad genética esencial para entender procesos evolutivos que promueven la biodiversidad biológica, las colonizaciones (pre)históricas, las migraciones y las extinciones. En la era actual de las tecnologías de secuenciación de alto rendimiento, la estructura de las poblaciones se puede cuantificar mediante valores de marcadores genéticos de cientos a miles de genomas. Sin embargo, estas bases de datos genómicos son gigantescas y plantean grandes desafíos de computación y análisis.
Presentamos el paquete de R smartsnp para la computación rápida y sencilla de PCA sobre datos de polimorfismos de nucleótido único (SNP). Inspirado en el paquete informático de referencia EIGENSOFT, smartsnp incluye escalamiento de SNPs cuando existe deriva genética y permite la proyeccción de muestras antiguas a un espacio genético moderno, al tiempo que corre pruebas multivariadas basadas en permutaciones para evaluar diferencias de diversidad genética entre poblaciones (posición y dispersión).
El PCA de smartsnp es de 2 a 4 veces más rápido que el SMARTPCA de EIGENSOFT para una amplia variedad de datos con distinto número de muestras y SNPs. Las cuatro funciones de smartsnp (smart_pca, smart_permanova, smart_permdisp, smart_mva) procesan bases de datos simulados de hasta 100 muestras y 1 millón de SNPs en menos de 30 segundos y recrean con exactitud SMARTPCAs publicados sobre genotipos de lobos y poblaciones humanas ancestrales.
El paquete smartsnp proporciona ordenación multivariada y pruebas de hipótesis rápidas y robustas para datos genómicos masivos, y también es apropiado para ADN ancestral y moderno de baja cobertura. Su implementación sencilla debería ser atractiva para investigadores que trabajan en biología de la conservación, evolución, ecología y (paleo)genómica, y aplicable a estudios del fenotipo, la ancestría y el linaje.
The widespread observation that heat tolerance is less variable than cold tolerance (‘cold‐tolerance asymmetry’) leads to the prediction that species exposed to temperatures near their thermal maxima ...should have reduced evolutionary potential for adapting to climate warming. However, the prediction is largely supported by species‐level global studies based on single estimates of both physiological metrics per taxon.
We ask whether cold‐tolerance asymmetry holds for Iberian lizards after accounting for intraspecific variation in critical thermal maxima (CTmax) and minima (CTmin). To do so, we quantified CTmax and CTmin for 58 populations of 15 Iberian lizard species (299 individuals). Then, we randomly selected one population from each study species (population sample = 15 CTmax and CTmin values), tested for differences between the variance of both thermal metrics across species, and repeated the test for thousands of population samples as if we had undertaken the same study thousands of times, each time sampling one different population per species (as implemented in global studies).
The ratio of variances in CTmax to CTmin across species varied up to 16‐fold depending on the populations chosen. Variance ratios show how much CTmax departs from the cross‐species mean compared to CTmin, with a unitary ratio indicating equal variance of both thermal limits. Sampling one population per species was six times more likely to result in the observation of greater CTmax variance (‘heat‐tolerance asymmetry’) than cold‐tolerance asymmetry. The probability of obtaining the data (given the null hypothesis of equal variance being true) was twice as likely for cases of cold‐tolerance asymmetry than for the opposite scenario.
Range‐wide, population‐level studies that quantify heat and cold tolerance of individual species are urgently needed to ascertain the global prevalence of cold‐tolerance asymmetry. While broad latitudinal clines of cold tolerance have been strongly supported, heat tolerance might respond to smaller‐scale climatic and habitat factors hence go unnoticed in global studies. Studies investigating physiological responses to climate change should incorporate the extent to which thermal traits are characteristic of individuals, populations and/or species.
A free Plain Language Summary can be found within the Supporting Information of this article.
A free Plain Language Summary can be found within the Supporting Information of this article.
Radiocarbon (
C) analysis of skeletal remains by accelerator mass spectrometry is an essential tool in multiple branches of science. However, bone
C dating results can be inconsistent and not ...comparable due to disparate laboratory pretreatment protocols that remove contamination. And, pretreatments are rarely discussed or reported by end-users, making it an 'elephant in the room' for Quaternary scientists. Through a questionnaire survey, I quantified consensus on the reliability of collagen pretreatments for
C dating across 132 experts (25 countries). I discovered that while more than 95% of the audience was wary of contamination and would avoid gelatinization alone (minimum pretreatment used by most
C facilities), 52% asked laboratories to choose the pretreatment method for them, and 58% could not rank the reliability of at least one pretreatment. Ultrafiltration was highly popular, and purification by XAD resins seemed restricted to American researchers. Isolating and dating the amino acid hydroxyproline was perceived as the most reliable pretreatment, but is expensive, time-consuming and not widely available. Solid evidence supports that only molecular-level dating accommodates all known bone contaminants and guarantees complete removal of humic and fulvic acids and conservation substances, with three key areas of progress: (i) innovation and more funded research is required to develop affordable analytical chemistry that can handle low-mass samples of collagen amino acids, (ii) a certification agency overseeing dating-quality control is needed to enhance methodological reproducibility and dating accuracy among laboratories, and (iii) more cross-disciplinary work with better
C reporting etiquette will promote the integration of
C dating across disciplines. Those developments could conclude long-standing debates based on low-accuracy data used to build chronologies for animal domestications, human/megafauna extirpations and migrations, archaeology, palaeoecology, palaeontology and palaeoclimate models.
Studies examining the underlying causes of the distributions of species and their future trajectories under climate change have benefitted from the accumulation of measurements of thermal tolerance ...across the tree of life. However, gaps in the global coverage of heat-tolerance data for ectotherms persist on four critical fronts. First, most large-scale analyses treat heat tolerance as a fixed species trait despite that population-level variation can equal or exceed cross-species variation. Second, terrestrial non-arthropod invertebrates and aquatic ectotherms other than bony fish have been poorly sampled, particularly in boreal and tropical regions, the Indian Ocean and the mesopelagic-deep ocean. Third, the study of climate impacts on the heat tolerance of terrestrial ectotherms has often neglected the interaction of environmental temperatures with water availability. And fourth, the mechanisms driving the dependence of heat tolerance on oxygen supply-demand remain largely unknown. We contend that filling those data and knowledge gaps requires novel strategies for the ecophysiological sampling of the range of understudied populations and species that occupy the length of climatic gradients globally. Such developments are essential for comprehensively predicting species responses to climate change across aquatic and terrestrial biomes.
Analysis of long‐term trends in abundance of animal populations provides insights into population dynamics. Population growth rates are the emergent interplay of inter alia fertility, survival, and ...dispersal. However, the density feedbacks operating on some vital rates (“component feedback”) can be decoupled from density feedbacks on population growth rates estimated using abundance time series (“ensemble feedback”). Many of the mechanisms responsible for this decoupling are poorly understood, thereby questioning the validity of using logistic‐growth models versus vital rates to infer long‐term population trends. To examine which conditions lead to decoupling, we simulated age‐structured populations of long‐lived vertebrates experiencing component density feedbacks on survival. We then quantified how imposed stochasticity in survival rates, density‐independent mortality (catastrophes, harvest‐like removal of individuals) and variation in carrying capacity modified the ensemble feedback in abundance time series simulated from age‐structured populations. The statistical detection of ensemble density feedback from census data was largely unaffected by density‐independent processes. Long‐term population decline caused from density‐independent mortality was the main mechanism decoupling the strength of component versus ensemble density feedbacks. Our study supports the use of simple logistic‐growth models to capture long‐term population trends, mediated by changes in population abundance, when survival rates are stochastic, carrying capacity fluctuates, and populations experience moderate catastrophic mortality over time.
We simulated component density feedbacks on survival in age‐structured populations of long‐lived vertebrates and quantified how imposed density‐independent mortality and variation in carryingcapacity modified the ensemble density feedback strength estimated from logistic‐growth models to the simulated abundance time series. Catastrophic and proportional mortality eroded the effect of density‐dependent survival on ensemble‐feedback strength more strongly than variation in carrying capacity. Thus, phenomenological models offer a robust approach to capture the strength of density feedbacks from nonstationary census data when density‐independent mortality is low.
Marine sedimentary ancient DNA (sedaDNA) provides a powerful means to reconstruct marine palaeo‐communities across the food web. However, currently there are few optimized sedaDNA extraction ...protocols available to maximize the yield of small DNA fragments typical of ancient DNA (aDNA) across a broad diversity of eukaryotes. We compared seven combinations of sedaDNA extraction treatments and sequencing library preparations using marine sediments collected at a water depth of 104 m off Maria Island, Tasmania, in 2018. These seven methods contrasted frozen versus refrigerated sediment, bead‐beating induced cell lysis versus ethylenediaminetetraacetic acid (EDTA) incubation, DNA binding in silica spin columns versus in silica‐solution, diluted versus undiluted DNA in shotgun library preparations to test potential inhibition issues during amplification steps, and size‐selection of low molecular‐weight (LMW) DNA to increase the extraction efficiency of sedaDNA. Maximum efficiency was obtained from frozen sediments subjected to a combination of EDTA incubation and bead‐beating, DNA binding in silica‐solution, and undiluted DNA in shotgun libraries, across 45 marine eukaryotic taxa. We present an optimized extraction protocol integrating these steps, with an optional post‐library LMW size‐selection step to retain DNA fragments of ≤500 base pairs. We also describe a stringent bioinformatic filtering approach for metagenomic data and provide a comprehensive list of contaminants as a reference for future sedaDNA studies. The new extraction and data‐processing protocol should improve quantitative paleo‐monitoring of eukaryotes from marine sediments, as well as other studies relying on the detection of highly fragmented and degraded eukaryote DNA in sediments.
The scientific evidence for anthropogenic climate change is empirically settled, but communicating it to nonscientific audiences remains challenging. To be explicit about the state of knowledge on ...climate science, the Intergovernmental Panel on Climate Change (IPCC) has adopted a vocabulary that ranks climate findings through certainty-calibrated qualifiers of confidence and likelihood. In this article, we quantified the occurrence of knowns and unknowns about “The Physical Science Basis” of the IPCC’s Fifth Assessment Report by counting the frequency of calibrated qualifiers. We found that the tone of the IPCC’s probabilistic language is remarkably conservative (mean confidence is medium, and mean likelihood is 66%–100% or 0–33%), and emanates from the IPCC recommendations themselves, complexity of climate research, and exposure to politically motivated debates. Leveraging communication of uncertainty with overwhelming scientific consensus about anthropogenic climate change should be one element of a wider reform, whereby the creation of an IPCC outreach working group could enhance the transmission of climate science to the panel’s audiences.
Genetic data are a crucial and exponentially growing resource across all biological sciences, yet curated databases are scarce. The widespread occurrence of sequence and (meta)data errors in public ...repositories calls for comprehensive improvements of curation protocols leading to robust research and downstream analyses. We collated and curated all available GenBank cytochrome-b sequences for amphibians, a benchmark marker in this globally declining vertebrate clade. The Amphibia's Curated Database of Cytochrome-b (ACDC) consists of 36,514 sequences representing 2,309 species from 398 genera (median = 2 with 50% interquartile ranges of 1-7 species/genus). We updated the taxonomic identity of >4,800 sequences (ca. 13%) and found 2,359 (6%) conflicting sequences with 84% of the errors originating from taxonomic misidentifications. The database (accessible at https://doi.org/10.6084/m9.figshare.9944759 ) also includes an R script to replicate our study for other loci and taxonomic groups. We provide recommendations to improve genetic-data quality in public repositories and flag species for which there is a need for taxonomic refinement in the face of increased rate of amphibian extinctions in the Anthropocene.
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