High-throughput characterization of bacterial responses to complex mixtures of chemical pollutants.

Our understanding of how microbes respond to micropollutants, such as pesticides, is almost wholly based on single-species responses to individual chemicals. However, in natural environments, microbes experience multiple pollutants simultaneously. Here we perform a matrix of multi-stressor experiments by assaying the growth of model and non-model strains of bacteria in all 255 combinations of 8 chemical stressors (antibiotics, herbicides, fungicides and pesticides). We found that bacterial strains responded in different ways to stressor mixtures, which could not be predicted simply from their phylogenetic relatedness. Increasingly complex chemical mixtures were both more likely to negatively impact bacterial growth in monoculture and more likely to reveal net interactive effects. A mixed co-culture of strains proved more resilient to increasingly complex mixtures and revealed fewer interactions in the growth response. These results show predictability in microbial population responses to chemical stressors and could increase the utility of next-generation eco-toxicological assays.

Global conservation status of the jawed vertebrate Tree of Life.

Human-driven extinction threatens entire lineages across the Tree of Life. Here we assess the conservation status of jawed vertebrate evolutionary history, using three policy-relevant approaches. First, we calculate an index of threat to overall evolutionary history, showing that we expect to lose 86-150 billion years (11-19%) of jawed vertebrate evolutionary history over the next 50-500 years. Second, we rank jawed vertebrate species by their EDGE scores to identify the highest priorities for species-focused conservation of evolutionary history, finding that chondrichthyans, ray-finned fish and testudines rank highest of all jawed vertebrates. Third, we assess the conservation status of jawed vertebrate families. We found that species within monotypic families are more likely to be threatened and more likely to be in decline than other species. We provide a baseline for the status of families at risk of extinction to catalyse conservation action. This work continues a trend of highlighting neglected groups-such as testudines, crocodylians, amphibians and chondrichthyans-as conservation priorities from a phylogenetic perspective.

Phylogenetic Biodiversity Metrics Should Account for Both Accumulation and Attrition of Evolutionary Heritage.

Phylogenetic metrics are essential tools used in the study of ecology, evolution and conservation. Phylogenetic diversity (PD) in particular is one of the most prominent measures of biodiversity, and is based on the idea that biological features accumulate along the edges of phylogenetic trees that are summed. We argue that PD and many other phylogenetic biodiversity metrics fail to capture an essential process that we term attrition. Attrition is the gradual loss of features through causes other than extinction. Here we introduce 'EvoHeritage', a generalisation of PD that is founded on the joint processes of accumulation and attrition of features. We argue that whilst PD measures evolutionary history, EvoHeritage is required to capture a more pertinent subset of evolutionary history including only components that have survived attrition. We show that EvoHeritage is not the same as PD on a tree with scaled edges; instead, accumulation and attrition interact in a more complex non-monophyletic way that cannot be captured by edge lengths alone. This leads us to speculate that the one dimensional edge lengths of classic trees may be insufficiently flexible to capture the nuances of evolutionary processes. We derive a measure of EvoHeritage and show that it elegantly reproduces species richness and PD at opposite ends of a continuum based on the intensity of attrition. We demonstrate the utility of EvoHeritage in ecology as a predictor of community productivity compared with species richness and PD. We also show how EvoHeritage can quantify living fossils and resolve their associated controversy. We suggest how the existing calculus of PD-based metrics and other phylogenetic biodiversity metrics can and should be recast in terms of EvoHeritage accumulation and attrition.

Diversification of flowering plants in space and time.

The rapid diversification and high species richness of flowering plants is regarded as 'Darwin's second abominable mystery'. Today the global spatiotemporal pattern of plant diversification remains elusive. Using a newly generated genus-level phylogeny and global distribution data for 14,244 flowering plant genera, we describe the diversification dynamics of angiosperms through space and time. Our analyses show that diversification rates increased throughout the early Cretaceous and then slightly decreased or remained mostly stable until the end of the Cretaceous-Paleogene mass extinction event 66 million years ago. After that, diversification rates increased again towards the present. Younger genera with high diversification rates dominate temperate and dryland regions, whereas old genera with low diversification dominate the tropics. This leads to a negative correlation between spatial patterns of diversification and genus diversity. Our findings suggest that global changes since the Cenozoic shaped the patterns of flowering plant diversity and support an emerging consensus that diversification rates are higher outside the tropics.

Mechanistic neutral models show that sampling biases drive the apparent explosion of early tetrapod diversity.

Estimates of deep-time biodiversity typically rely on statistical methods to mitigate the impacts of sampling biases in the fossil record. However, these methods are limited by the spatial and temporal scale of the underlying data. Here we use a spatially explicit mechanistic model, based on neutral theory, to test hypotheses of early tetrapod diversity change during the late Carboniferous and early Permian, critical intervals for the diversification of vertebrate life on land. Our simulations suggest that apparent increases in early tetrapod diversity were not driven by local endemism following the 'Carboniferous rainforest collapse'. Instead, changes in face-value diversity can be explained by variation in sampling intensity through time. Our results further demonstrate the importance of accounting for sampling biases in analyses of the fossil record and highlight the vast potential of mechanistic models, including neutral models, for testing hypotheses in palaeobiology.

Indicators to monitor the status of the tree of life.

Following the failure to fully achieve any of the 20 Aichi biodiversity targets, the future of biodiversity rests in the balance. The Convention on Biological Diversity's Kunming-Montreal Global Biodiversity Framework (GBF) presents the opportunity to preserve nature's contributions to people (NCPs) for current and future generations by conserving biodiversity and averting extinctions. There is a need to safeguard the tree of life-the unique and shared evolutionary history of life on Earth-to maintain the benefits it bestows into the future. Two indicators have been adopted within the GBF to monitor progress toward safeguarding the tree of life: the phylogenetic diversity (PD) indicator and the evolutionarily distinct and globally endangered (EDGE) index. We applied both to the world's mammals, birds, and cycads to show their utility at the global and national scale. The PD indicator can be used to monitor the overall conservation status of large parts of the evolutionary tree of life, a measure of biodiversity's capacity to maintain NCPs for future generations. The EDGE index is used to monitor the performance of efforts to conserve the most distinctive species. The risk to PD of birds, cycads, and mammals increased, and mammals exhibited the greatest relative increase in threatened PD over time. These trends appeared robust to the choice of extinction risk weighting. EDGE species had predominantly worsening extinction risk. A greater proportion of EDGE mammals (12%) had increased extinction risk compared with threatened mammals in general (7%). By strengthening commitments to safeguarding the tree of life, biodiversity loss can be reduced and thus nature's capacity to provide benefits to humanity now and in the future can be preserved.

Indicadores para monitorear el estado del árbol de la vida Resumen El futuro de la biodiversidad peligra tras no haberse logrado ninguno de los 20 Objetivos de Aichi. El Marco Global de Biodiversidad (GBF) de Kunming-Montreal del Convenio sobre la Diversidad Biológica (CDB) representa la oportunidad de preservar las contribuciones de la naturaleza a las personas (PNC) para las generaciones actuales y futuras mediante la conservación de la biodiversidad y la prevención de las extinciones. Es necesario salvaguardar el árbol de la vida -la historia evolutiva única y compartida de la vida en la Tierra- para mantener en el futuro los beneficios que aporta. En el GBF se han adoptado dos indicadores para supervisar los avances hacia el cuidado del árbol de la vida: el indicador de diversidad filogenética y el índice de especies evolutivamente distintas y globalmente amenazadas (EDGE). Aplicamos ambos a los mamíferos, las aves y las cícadas del mundo para demostrar su utilidad a escala mundial y nacional. El indicador de diversidad filogenética puede utilizarse para supervisar el estado de conservación general de grandes partes del árbol evolutivo de la vida, una medida de la capacidad de la biodiversidad para mantener los PNC para las generaciones futuras. El índice EDGE se utiliza para supervisar el rendimiento de los esfuerzos por conservar las especies más distintivas. El riesgo para la diversidad filogenética de aves, cícadas y mamíferos aumentó, y los mamíferos mostraron el mayor aumento relativo de la diversidad filogenética amenazada a lo largo del tiempo. Estas tendencias parecieron sólidas a la hora de elegir la valoración del riesgo de extinción. Las especies EDGE tuvieron un riesgo de extinción predominante cada vez peor. Una mayor proporción de mamíferos EDGE (12%) presentó un riesgo de extinción creciente en comparación con los mamíferos amenazados en general (7%). Si se refuerza el compromiso de salvaguardar el árbol de la vida, se puede reducir la pérdida de biodiversidad y preservar así la capacidad de la naturaleza para proporcionar beneficios a la humanidad ahora y en el futuro.

Grayanotoxin I variation across tissues and species of Rhododendron suggests pollinator-herbivore defence trade-offs.

Grayanotoxin I (GTX I) is a major toxin in leaves of Rhododendron species, where it provides a defence against insect and vertebrate herbivores. Surprisingly, it is also present in R. ponticum nectar, and this can hold important implications for plant-pollinator mutualisms. However, knowledge of GTX I distributions across the genus Rhododendron and in different plant materials is currently limited, despite the important ecological function of this toxin. Here we characterise GTX I expression in the leaves, petals, and nectar of seven Rhododendron species. Our results indicated interspecific variation in GTX I concentration across all species. GTX I concentrations were consistently higher in leaves compared to petals and nectar. Our findings provide preliminary evidence for phenotypic correlation between GTX I concentrations in defensive tissues (leaves and petals) and floral rewards (nectar), suggesting that Rhododendron species may commonly experience functional trade-offs between herbivore defence and pollinator attraction.

The EDGE2 protocol: Advancing the prioritisation of Evolutionarily Distinct and Globally Endangered species for practical conservation action.

The conservation of evolutionary history has been linked to increased benefits for humanity and can be captured by phylogenetic diversity (PD). The Evolutionarily Distinct and Globally Endangered (EDGE) metric has, since 2007, been used to prioritise threatened species for practical conservation that embody large amounts of evolutionary history. While there have been important research advances since 2007, they have not been adopted in practice because of a lack of consensus in the conservation community. Here, building from an interdisciplinary workshop to update the existing EDGE approach, we present an "EDGE2" protocol that draws on a decade of research and innovation to develop an improved, consistent methodology for prioritising species conservation efforts. Key advances include methods for dealing with uncertainty and accounting for the extinction risk of closely related species. We describe EDGE2 in terms of distinct components to facilitate future revisions to its constituent parts without needing to reconsider the whole. We illustrate EDGE2 by applying it to the world's mammals. As we approach a crossroads for global biodiversity policy, this Consensus View shows how collaboration between academic and applied conservation biologists can guide effective and practical priority-setting to conserve biodiversity.

The distribution, ecology and predicted habitat use of the Critically Endangered angelshark (Squatina squatina) in coastal waters of Wales and the central Irish Sea.

The angelshark (Squatina squatina) has the northernmost range of any angel shark species, but there is limited information on its distribution, habitat use and ecology at higher latitudes. To address this, Angel Shark Project: Wales gathered 2231 S. squatina records and 142 anecdotal resources from fishers, coastal communities and archives. These spanned the coastal waters of Wales and the central Irish Sea and were dated from 1812 to 2020, with 97.62% of records within 11.1 km (6 nm) of the coast. Commercial, recreational and charter boat fishers provided the majority of S. squatina records (97.18%), with significantly more sightings from three decades (1970s, 1980s and 1990s) and in the months of September, June, August and July (in descending order). The coastal area between Bardsey Island and Strumble Head had the most S. squatina records (n = 1279), with notable concentrations also found in Carmarthen Bay, Conwy Bay and the Outer Severn Estuary. Species distribution models (SDM) identified four environmental variables that had significant influence on S. squatina distribution, depth, chlorophyll-a concentration, sea surface temperature (SST) and salinity, and these varied between the quarters (Q) of the year. SDM model outputs predicted a larger congruous area of suitable habitat in Q3 (3176 km2 ) compared to Q2 (2051 km2 ), with suitability along the three glacial moraines (Sarn Badrig, Sarn-y-Bwch and Sarn Cynfelyn) strongly presented. Comparison of modelled environmental variables at the location of S. squatina records for each Q identified reductions in depth and salinity, and increases in chlorophyll-a and SST when comparing Q2 or Q3 with Q1 or Q4. This shift may suggest S. squatina are making seasonal movements to shallow coastal waters in Q2 and Q3. This is supported by 23 anecdotal resources and may be driven by reproductive behaviour, as there were 85 records of S. squatina individuals ≤60 cm in the dataset, inferred as recently born or juvenile life-history stages. The results have helped fill significant evidence gaps identified in the Wales Angelshark Action Plan and immediate next research steps are suggested.

A unified model of species abundance, genetic diversity, and functional diversity reveals the mechanisms structuring ecological communities.

Biodiversity accumulates hierarchically by means of ecological and evolutionary processes and feedbacks. Within ecological communities drift, dispersal, speciation, and selection operate simultaneously to shape patterns of biodiversity. Reconciling the relative importance of these is hindered by current models and inference methods, which tend to focus on a subset of processes and their resulting predictions. Here we introduce massive ecoevolutionary synthesis simulations (MESS), a unified mechanistic model of community assembly, rooted in classic island biogeography theory, which makes temporally explicit joint predictions across three biodiversity data axes: (i) species richness and abundances, (ii) population genetic diversities, and (iii) trait variation in a phylogenetic context. Using simulations we demonstrate that each data axis captures information at different timescales, and that integrating these axes enables discriminating among previously unidentifiable community assembly models. MESS is unique in generating predictions of community-scale genetic diversity, and in characterizing joint patterns of genetic diversity, abundance, and trait values. MESS unlocks the full potential for investigation of biodiversity processes using multidimensional community data including a genetic component, such as might be produced by contemporary eDNA or metabarcoding studies. We combine MESS with supervised machine learning to fit the parameters of the model to real data and infer processes underlying how biodiversity accumulates, using communities of tropical trees, arthropods, and gastropods as case studies that span a range of data availability scenarios, and spatial and taxonomic scales.

Neutral syndrome.

Neutral models of evolution assume the absence of natural selection. Formerly confined to ecology and evolutionary biology, neutral models are spreading. In recent years they've been applied to explaining the diversity of baby names, scientific citations, cryptocurrencies, pot decorations, literary lexica, tumour variants and much more besides. Here, we survey important neutral models and highlight their similarities. We investigate the most widely used tests of neutrality, show that they are weak and suggest more powerful methods. We conclude by discussing the role of neutral models in the explanation of diversity. We suggest that the ability of neutral models to fit low-information distributions should not be taken as evidence for the absence of selection. Nevertheless, many studies, in increasingly diverse fields, make just such claims. We call this tendency 'neutral syndrome'.

Global priorities for conservation of reptilian phylogenetic diversity in the face of human impacts.

Phylogenetic diversity measures are increasingly used in conservation planning to represent aspects of biodiversity beyond that captured by species richness. Here we develop two new metrics that combine phylogenetic diversity and the extent of human pressure across the spatial distribution of species - one metric valuing regions and another prioritising species. We evaluate these metrics for reptiles, which have been largely neglected in previous studies, and contrast these results with equivalent calculations for all terrestrial vertebrate groups. We find that regions under high human pressure coincide with the most irreplaceable areas of reptilian diversity, and more than expected by chance. The highest priority reptile species score far above the top mammal and bird species, and reptiles include a disproportionate number of species with insufficient extinction risk data. Data Deficient species are, in terms of our species-level metric, comparable to Critically Endangered species and therefore may require urgent conservation attention.

Relationship between conservation biology and ecology shown through machine reading of 32,000 articles.

Conservation biology was founded on the idea that efforts to save nature depend on a scientific understanding of how it works. It sought to apply ecological principles to conservation problems. We investigated whether the relationship between these fields has changed over time through machine reading the full texts of 32,000 research articles published in 16 ecology and conservation biology journals. We examined changes in research topics in both fields and how the fields have evolved from 2000 to 2014. As conservation biology matured, its focus shifted from ecology to social and political aspects of conservation. The 2 fields diverged and now occupy distinct niches in modern science. We hypothesize this pattern resulted from increasing recognition that social, economic, and political factors are critical for successful conservation and possibly from rising skepticism about the relevance of contemporary ecological theory to practical conservation.

Relaciones entre la Biología de la Conservación y la Ecología Mostradas a través de la Lectura Mediante Máquina de 32,000 Artículos Resumen La biología de la conservación se fundó a partir de la idea de que los esfuerzos para salvar a la naturaleza dependen del entendimiento científico de cómo funciona. La biología de la conservación buscaba aplicar los principios ecológicos a los problemas de conservación. En este trabajo investigamos si la relación entre estos ámbitos ha cambiado con el tiempo al realizar una lectura mediante máquina de 32,000 textos completos de artículos de investigación publicados en 16 revistas sobre ecología y biología de la conservación. También examinamos los cambios en los temas de investigación en ambos ámbitos y cómo éstos han evolucionado desde el año 2000 hasta el 2014. Conforme ha madurado la biología de la conservación, su enfoque se ha movido de los aspectos ecológicos de la conservación a los aspectos políticos y sociales. La ecología y la biología de la conservación se han separado y ahora ocupan nichos distintos dentro de la ciencia moderna. Nuestra hipótesis considera que este patrón resultó de incrementar el reconocimiento de que los factores sociales, económicos y políticos son muy importantes para una conservación exitosa. Posiblemente el patrón también proviene del creciente escepticismo acerca de la relevancia que la teoría ecológica contemporánea tiene para la conservación en práctica.

A phylogenomic analysis of Nepenthes (Nepenthaceae).

Nepenthaceae is one of the largest carnivorous plant families and features ecological and morphological adaptations indicating an impressive adaptive radiation. However, investigation of evolutionary and taxonomic questions is hindered by poor phylogenetic understanding, with previous molecular studies based on limited loci and taxa. We use high-throughput sequencing with a target-capture methodology based on a 353-loci, probe set to recover sequences for 197 samples, representing 151 described or putative Nepenthes species. Phylogenetic analyses were performed using supermatrix and maximum quartet species tree approaches. Our analyses confirm five Western outlier taxa, followed by N. danseri, as successively sister to the remainder of the group. We also find mostly consistent recovery of two major Southeast Asian clades. The first contains common or widespread lowland species plus a Wallacean-New Guinean clade. Within the second clade, sects. Insignes and Tentaculatae are well supported, while geographically defined clades representing Sumatra, Indochina, Peninsular Malaysia, Palawan, Mindanao and Borneo are also consistently recovered. However, we find considerable conflicting signal at the site and locus level, and often unstable backbone relationships. A handful of Bornean taxa are inconsistently placed and require further investigation. We make further suggestions for a modified infra-generic classification of genus Nepenthes.

Characterising extinction debt following habitat fragmentation using neutral theory.

Habitat loss leads to species extinctions, both immediately and over the long term as 'extinction debt' is repaid. The same quantity of habitat can be lost in different spatial patterns with varying habitat fragmentation. How this translates to species loss remains an open problem requiring an understanding of the interplay between community dynamics and habitat structure across temporal and spatial scales. Here we develop formulas that characterise extinction debt in a spatial neutral model after habitat loss and fragmentation. Central to our formulas are two new metrics, which depend on properties of the taxa and landscape: 'effective area', measuring the remaining number of individuals and 'effective connectivity', measuring individuals' ability to disperse through fragmented habitat. This formalises the conventional wisdom that habitat area and habitat connectivity are the two critical requirements for long-term preservation of biodiversity. Our approach suggests that mechanistic fragmentation metrics help resolve debates about fragmentation and species loss.

Reconciling the contribution of environmental and stochastic structuring of tropical forest diversity through the lens of imaging spectroscopy.

Both niche and stochastic dispersal processes structure the extraordinary diversity of tropical plants, but determining their relative contributions has proven challenging. We address this question using airborne imaging spectroscopy to estimate canopy ß-diversity for an extensive region of a Bornean rainforest and challenge these data with models incorporating niches and dispersal. We show that remotely sensed and field-derived estimates of pairwise dissimilarity in community composition are closely matched, proving the applicability of imaging spectroscopy to provide ß-diversity data for entire landscapes of over 1000 ha containing contrasting forest types. Our model reproduces the empirical data well and shows that the ecological processes maintaining tropical forest diversity are scale dependent. Patterns of ß-diversity are shaped by stochastic dispersal processes acting locally whilst environmental processes act over a wider range of scales.

Uncovering the rules of microbial community invasions.

Understanding the ecological and evolutionary processes determining the outcome of biological invasions has been the subject of decades of research with most work focusing on macro-organisms. In the context of microbes, invasions remain poorly understood despite being increasingly recognized as important. To shed light on the factors affecting the success of microbial community invasions, we perform simulations using an individual-based nearly neutral model that combines ecological and evolutionary processes. Our simulations qualitatively recreate many empirical patterns and lead to a description of five general rules of invasion: (1) larger communities evolve better invaders and better defenders; (2) where invader and resident fitness difference is large, invasion success is essentially deterministic; (3) propagule pressure contributes to invasion success, if and only if, invaders and residents are competitively similar; (4) increasing the diversity of invaders has a similar effect to increasing the number of invaders; and (5) more diverse communities more successfully resist invasion.

Species-area relationships and biodiversity loss in fragmented landscapes.

To estimate species loss from habitat destruction, ecologists typically use species-area relationships, but this approach neglects the spatial pattern of habitat fragmentation. Here, we provide new, easily applied, analytical methods that place upper and lower bounds on immediate species loss at any spatial scale and for any spatial pattern of habitat loss. Our formulas are expressed in terms of what we name the 'Preston function', which describes triphasic species-area relationships for contiguous regions. We apply our method to case studies of deforestation and tropical tree species loss at three different scales: a 50 ha forest plot in Panama, the tropical city-state of Singapore and the Brazilian Amazon. Our results show that immediate species loss is somewhat insensitive to fragmentation pattern at small scales but highly sensitive at larger scales: predicted species loss in the Amazon varies by a factor of 16 across different spatial structures of habitat loss.

Quantifying the effects of the break up of Pangaea on global terrestrial diversification with neutral theory.

The historic richness of most taxonomic groups increases substantially over geological time. Explanations for this fall broadly into two categories: bias in the fossil record and elevated net rates of diversification in recent periods. For example, the break up of Pangaea and isolation between continents might have increased net diversification rates. In this study, we investigate the effect on terrestrial diversification rates of the increased isolation between land masses brought about by continental drift. We use ecological neutral theory as a means to study geologically complex scenarios tractably. Our models show the effects of simulated geological events that affect all species equally, without the added complexity of further ecological processes. We find that continental drift leads to an increase in diversity only where isolation between continents leads to additional speciation through vicariance, and where higher taxa with very low global diversity are considered. We conclude that continental drift by itself is not sufficient to account for the increase in terrestrial species richness observed in the fossil record.