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.

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 generalization of PD that is founded on the joint processes of accumulation and attrition of features. We argue that while 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.

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.

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 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.

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.

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.

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.

Unifying ecology and macroevolution with individual-based theory.

A contemporary goal in both ecology and evolutionary biology is to develop theory that transcends the boundary between the two disciplines, to understand phenomena that cannot be explained by either field in isolation. This is challenging because macroevolution typically uses lineage-based models, whereas ecology often focuses on individual organisms. Here, we develop a new parsimonious individual-based theory by adding mild selection to the neutral theory of biodiversity. We show that this model generates realistic phylogenies showing a slowdown in diversification and also improves on the ecological predictions of neutral theory by explaining the occurrence of very common species. Moreover, we find the distribution of individual fitness changes over time, with average fitness increasing at a pace that depends positively on community size. Consequently, large communities tend to produce fitter species than smaller communities. These findings have broad implications beyond biodiversity theory, potentially impacting, for example, invasion biology and paleontology.

Islands as model systems in ecology and evolution: prospects fifty years after MacArthur-Wilson.

The study of islands as model systems has played an important role in the development of evolutionary and ecological theory. The 50th anniversary of MacArthur and Wilson's (December 1963) article, 'An equilibrium theory of insular zoogeography', was a recent milestone for this theme. Since 1963, island systems have provided new insights into the formation of ecological communities. Here, building on such developments, we highlight prospects for research on islands to improve our understanding of the ecology and evolution of communities in general. Throughout, we emphasise how attributes of islands combine to provide unusual research opportunities, the implications of which stretch far beyond islands. Molecular tools and increasing data acquisition now permit re-assessment of some fundamental issues that interested MacArthur and Wilson. These include the formation of ecological networks, species abundance distributions, and the contribution of evolution to community assembly. We also extend our prospects to other fields of ecology and evolution - understanding ecosystem functioning, speciation and diversification - frequently employing assets of oceanic islands in inferring the geographic area within which evolution has occurred, and potential barriers to gene flow. Although island-based theory is continually being enriched, incorporating non-equilibrium dynamics is identified as a major challenge for the future.

Detecting the ecological footprint of selection.

The structure of communities is influenced by many ecological and evolutionary processes, but the way these manifest in classic biodiversity patterns often remains unclear. Here we aim to distinguish the ecological footprint of selection-through competition or environmental filtering-from that of neutral processes that are invariant to species identity. We build on existing Massive Eco-evolutionary Synthesis Simulations (MESS), which uses information from three biodiversity axes-species abundances, genetic diversity, and trait variation-to distinguish between mechanistic processes. To correctly detect and characterise competition, we add a new and more realistic form of competition that explicitly compares the traits of each pair of individuals. Our results are qualitatively different to those of previous work in which competition is based on the distance of each individual's trait to the community mean. We find that our new form of competition is easier to identify in empirical data compared to the alternatives. This is especially true when trait data are available and used in the inference procedure. Our findings hint that signatures in empirical data previously attributed to neutrality may in fact be the result of pairwise-acting selective forces. We conclude that gathering more different types of data, together with more advanced mechanistic models and inference as done here, could be the key to unravelling the mechanisms of community assembly and question the relative roles of neutral and selective processes.

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.

Prolonging the past counteracts the pull of the present: protracted speciation can explain observed slowdowns in diversification.

Phylogenetic trees show a remarkable slowdown in the increase of number of lineages towards the present, a phenomenon which cannot be explained by the standard birth-death model of diversification with constant speciation and extinction rates. The birth-death model instead predicts a constant or accelerating increase in the number of lineages, which has been called the pull of the present. The observed slowdown has been attributed to nonconstancy of the speciation and extinction rates due to some form of diversity dependence (i.e., species-level density dependence), but the mechanisms underlying this are still unclear. Here, we propose an alternative explanation based on the simple concept that speciation takes time to complete. We show that this idea of "protracted" speciation can be incorporated in the standard birth-death model of diversification. The protracted birth-death model predicts a realistic slowdown in the rate of increase of number of lineages in the phylogeny and provides a compelling fit to four bird phylogenies with realistic parameter values. Thus, the effect of recognizing the generally accepted fact that speciation is not an instantaneous event is significant; even if it cannot account for all the observed patterns, it certainly contributes substantially and should therefore be incorporated into future studies.

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.

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.

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.

A unified model of island biogeography sheds light on the zone of radiation.

Islands acquire species through immigration and speciation. Models of island biogeography should capture both processes; however quantitative island biogeography theory has either neglected speciation or treated it unrealistically. We introduce a model where the dominance of immigration on small and near islands gives way to an increasing role for speciation as island area and isolation increase. We examine the contribution of immigration and speciation to the avifauna of 35 archipelagoes and find, consistent with our model, that the zone of radiation comprises two regions: endemic species diverged from mainland sister-species at intermediate isolation and from insular sister-species at higher levels of isolation. Our model also predicts species-area curves in accord with existing research and makes new predictions about species ages and abundances. We argue that a paucity of data and theory on species abundances on isolated islands highlights the need for island biogeography to be reconnected with mainstream ecology.

Integrating ecology into macroevolutionary research.

On 9 March, over 150 biologists gathered in London for the Centre for Ecology and Evolution spring symposium, 'Integrating Ecology into Macroevolutionary Research'. The event brought together researchers from London-based institutions alongside others from across the UK, Europe and North America for a day of talks. The meeting highlighted methodological advances and recent analyses of exemplar datasets focusing on the exploration of the role of ecological processes in shaping macroevolutionary patterns.