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.

Predicting Long Pendant Edges in Model Phylogenies, with Applications to Biodiversity and Tree Inference.

In the simplest phylogenetic diversification model (the pure-birth Yule process), lineages split independently at a constant rate $\lambda$ for time $t$. The length of a randomly chosen edge (either interior or pendant) in the resulting tree has an expected value that rapidly converges to $\frac{1}{2\lambda}$ as $t$ grows and thus is essentially independent of $t$. However, the behavior of the length $L$ of the longest pendant edge reveals remarkably different behavior: $L$ converges to $t/2$ as the expected number of leaves grows. Extending this model to allow an extinction rate $\mu$ (where $\mu<\lambda$), we also establish a similar result for birth-death trees, except that $t/2$ is replaced by $t/2 \cdot (1-\mu/\lambda)$. This "complete" tree may contain subtrees that have died out before time $t$; for the "reduced tree" that just involves the leaves present at time $t$ and their direct ancestors, the longest pendant edge length $L$ again converges to $t/2$. Thus, there is likely to be at least one extant species whose associated pendant branch attaches to the tree approximately half-way back in time to the origin of the entire clade. We also briefly consider the length of the shortest edges. Our results are relevant to phylogenetic diversity indices in biodiversity conservation, and to quantifying the length of aligned sequences required to correctly infer a tree. We compare our theoretical results with simulations and with the branch lengths from a recent phylogenetic tree of all mammals. [Birth-death process; phylogenetic diversification models; phylogenetic diversity.].

Pulse grazing by reindeer (Rangifer tarandus) can increase the phylogenetic diversity of vascular plant communities in the Fennoscandian tundra.

Herbivore grazing is an important determinant of plant community assemblages. Thus, it is essential to understand its impact to direct conservation efforts in regions where herbivores are managed. While the impacts of reindeer (Rangifer tarandus) grazing on plant biodiversity and community composition in the Fennoscandian tundra are well studied, the impact of reindeer grazing on phylogenetic community structure is not. We used data from a multiyear quasi-experimental study in northern Fennoscandia to analyze the effect of reindeer grazing on plant community diversity including its phylogenetic structure. Our study design used a permanent fence constructed in the 1960s and temporary fences constructed along the permanent fence to expose plant communities to three different grazing regimes: light (almost never grazed), pulse (grazed every other year), and press (chronic grazing for over 40 years). Similar to previous studies on low productivity ecosystems in this region, the species richness and evenness of plant communities with pulse and press grazing did not differ from communities with light grazing. Also consistent with previous studies in this region, we observed a transition from shrub-dominated communities with light grazing to graminoid-dominated communities with pulse and press grazing. Interestingly, communities with pulse, but not press, grazing were more phylogenetically dispersed than communities with light grazing. If grazing pulses can increase the phylogenetic diversity of plant communities, our result suggests changes in reindeer management allowing for pulses of grazing to increase phylogenetic diversity of plant communities.

Evolutionary legacies in contemporary tetrapod imperilment.

The Tree of Life will be irrevocably reshaped as anthropogenic extinctions continue to unfold. Theory suggests that lineage evolutionary dynamics, such as age since origination, historical extinction filters and speciation rates, have influenced ancient extinction patterns - but whether these factors also contribute to modern extinction risk is largely unknown. We examine evolutionary legacies in contemporary extinction risk for over 4000 genera, representing ~30,000 species, from the major tetrapod groups: amphibians, birds, turtles and crocodiles, squamate reptiles and mammals. We find consistent support for the hypothesis that extinction risk is elevated in lineages with higher recent speciation rates. We subsequently test, and find modest support for, a primary mechanism driving this pattern: that rapidly diversifying clades predominantly comprise range-restricted, and extinction-prone, species. These evolutionary patterns in current imperilment may have important consequences for how we manage the erosion of biological diversity across the Tree of Life.

The dynamics underlying avian extinction trajectories forecast a wave of extinctions.

Population decline is a process, yet estimates of current extinction rates often consider just the final step of that process by counting numbers of species lost in historical times. This neglects the increased extinction risk that affects a large proportion of species, and consequently underestimates the effective extinction rate. Here, we model observed trajectories through IUCN Red List extinction risk categories for all bird species globally over 28 years, and estimate an overall effective extinction rate of 2.17 × 10-4/species/year. This is six times higher than the rate of outright extinction since 1500, as a consequence of the large number of species whose status is deteriorating. We very conservatively estimate that global conservation efforts have reduced the effective extinction rate by 40%, but mostly through preventing critically endangered species from going extinct rather than by preventing species at low risk from moving into higher-risk categories. Our findings suggest that extinction risk in birds is accumulating much more than previously appreciated, but would be even greater without conservation efforts.

Ecological constraints associated with genome size across salamander lineages.

Salamanders have some of the largest, and most variable, genome sizes among the vertebrates. Larger genomes have been associated with larger cell sizes, lower metabolic rates, and longer embryonic and larval durations in many different taxonomic groups. These life-history traits are often important for dictating fitness under different environmental conditions, suggesting that a species' genome size may have the potential to constrain its ecological distribution. We test how genome size varies with the ephemerality of larval habitat across the salamanders, predicting that species with larger genomes will be constrained to more permanent habitats that permit slower development, while species with smaller genomes will be more broadly distributed across the gradient of habitat ephemerality. We found that salamanders with larger genomes are almost exclusively associated with permanent aquatic habitats. In addition, the evolutionary transition rate between permanent and ephemeral larval habitats is much higher in salamander lineages with smaller genome sizes. These patterns suggest that genome size may act as an evolutionary constraint on the ecological habitats of salamanders, restricting those species with large genomes and slower development to habitats with permanent sources of water.

Assessing the utility of conserving evolutionary history.

It is often claimed that conserving evolutionary history is more efficient than species-based approaches for capturing the attributes of biodiversity that benefit people. This claim underpins academic analyses and recommendations about the distribution and prioritization of species and areas for conservation, but evolutionary history is rarely considered in practical conservation activities. One impediment to implementation is that arguments related to the human-centric benefits of evolutionary history are often vague and the underlying mechanisms poorly explored. Herein we identify the arguments linking the prioritization of evolutionary history with benefits to people, and for each we explicate the purported mechanism, and evaluate its theoretical and empirical support. We find that, even after 25 years of academic research, the strength of evidence linking evolutionary history to human benefits is still fragile. Most - but not all - arguments rely on the assumption that evolutionary history is a useful surrogate for phenotypic diversity. This surrogacy relationship in turn underlies additional arguments, particularly that, by capturing more phenotypic diversity, evolutionary history will preserve greater ecosystem functioning, capture more of the natural variety that humans prefer, and allow the maintenance of future benefits to humans. A surrogate relationship between evolutionary history and phenotypic diversity appears reasonable given theoretical and empirical results, but the strength of this relationship varies greatly. To the extent that evolutionary history captures unmeasured phenotypic diversity, maximizing the representation of evolutionary history should capture variation in species characteristics that are otherwise unknown, supporting some of the existing arguments. However, there is great variation in the strength and availability of evidence for benefits associated with protecting phenotypic diversity. There are many studies finding positive biodiversity-ecosystem functioning relationships, but little work exists on the maintenance of future benefits or the degree to which humans prefer sets of species with high phenotypic diversity or evolutionary history. Although several arguments link the protection of evolutionary history directly with the reduction of extinction rates, and with the production of relatively greater future biodiversity via increased adaptation or diversification, there are few direct tests. Several of these putative benefits have mismatches between the relevant spatial scales for conservation actions and the spatial scales at which benefits to humans are realized. It will be important for future work to fill in some of these gaps through direct tests of the arguments we define here.

Author Correction: Prioritizing phylogenetic diversity captures functional diversity unreliably.

The original version of this Article contained a plotting error in Fig. 3g. The Serranidae and Siganidae families were misplaced in the plotted phylogeny. This error has now been corrected in the PDF and HTML versions of the Article. For comparison, the original, incorrect version of Fig. 3g is presented below as Fig. 1. The authors thank P. Cowman for identifying the plotting error.

Prioritizing phylogenetic diversity captures functional diversity unreliably.

In the face of the biodiversity crisis, it is argued that we should prioritize species in order to capture high functional diversity (FD). Because species traits often reflect shared evolutionary history, many researchers have assumed that maximizing phylogenetic diversity (PD) should indirectly capture FD, a hypothesis that we name the "phylogenetic gambit". Here, we empirically test this gambit using data on ecologically relevant traits from >15,000 vertebrate species. Specifically, we estimate a measure of surrogacy of PD for FD. We find that maximizing PD results in an average gain of 18% of FD relative to random choice. However, this average gain obscures the fact that in over one-third of the comparisons, maximum PD sets contain less FD than randomly chosen sets of species. These results suggest that, while maximizing PD protection can help to protect FD, it represents a risky conservation strategy.

Global priorities for conserving the evolutionary history of sharks, rays and chimaeras.

In an era of accelerated biodiversity loss and limited conservation resources, systematic prioritization of species and places is essential. In terrestrial vertebrates, evolutionary distinctness has been used to identify species and locations that embody the greatest share of evolutionary history. We estimate evolutionary distinctness for a large marine vertebrate radiation on a dated taxon-complete tree for all 1,192 chondrichthyan fishes (sharks, rays and chimaeras) by augmenting a new 610-species molecular phylogeny using taxonomic constraints. Chondrichthyans are by far the most evolutionarily distinct of all major radiations of jawed vertebrates-the average species embodies 26 million years of unique evolutionary history. With this metric, we identify 21 countries with the highest richness, endemism and evolutionary distinctness of threatened species as targets for conservation prioritization. On average, threatened chondrichthyans are more evolutionarily distinct-further motivating improved conservation, fisheries management and trade regulation to avoid significant pruning of the chondrichthyan tree of life.

Amphibian species traits, evolutionary history and environment predict Batrachochytrium dendrobatidis infection patterns, but not extinction risk.

The fungal pathogen Batrachochytrium dendrobatidis (B. dendrobatidis) has emerged as a major agent of amphibian extinction, requiring conservation intervention for many susceptible species. Identifying susceptible species is challenging, but many aspects of species biology are predicted to influence the evolution of host resistance, tolerance, or avoidance strategies towards disease. In turn, we may expect species exhibiting these distinct strategies to differ in their ability to survive epizootic disease outbreaks. Here, we test for phylogenetic and trait-based patterns of B. dendrobatidis infection risk and infection intensity among 302 amphibian species by compiling a global data set of B. dendrobatidis infection surveys across 95 sites. We then use best-fit models that associate traits, taxonomy and environment with B. dendrobatidis infection risk and intensity to predict host disease mitigation strategies (tolerance, resistance, avoidance) for 122 Neotropical amphibian species that experienced epizootic B. dendrobatidis outbreaks, and noted species persistence or extinction from these events. Aspects of amphibian species life history, habitat use and climatic niche were consistently linked to variation in B. dendrobatidis infection patterns across sites around the world. However, predicted B. dendrobatidis infection risk and intensity based on site environment and species traits did not reveal a consistent pattern between the predicted host disease mitigation strategy and extinction outcome. This suggests that either tolerant or resistant species may have no advantage in ameliorating disease during epizootic events, or that other factors drive the persistence of amphibian populations during chytridiomycosis outbreaks. These results suggest that using a trait-based approach may allow us to identify species with resistance or tolerance to endemic B. dendrobatidis infections, but that this approach may be insufficient to ultimately identify species at risk of extinction from epizootics.

Conserving Phylogenetic Diversity Can Be a Poor Strategy for Conserving Functional Diversity.

For decades, academic biologists have advocated for making conservation decisions in light of evolutionary history. Specifically, they suggest that policy makers should prioritize conserving phylogenetically diverse assemblages. The most prominent argument is that conserving phylogenetic diversity (PD) will also conserve diversity in traits and features (functional diversity [FD]), which may be valuable for a number of reasons. The claim that PD-maximized ("maxPD") sets of taxa will also have high FD is often taken at face value and in cases where researchers have actually tested it, they have done so by measuring the phylogenetic signal in ecologically important functional traits. The rationale is that if traits closely mirror phylogeny, then saving the maxPD set of taxa will tend to maximize FD and if traits do not have phylogenetic structure, then saving the maxPD set of taxa will be no better at capturing FD than criteria that ignore PD. Here, we suggest that measuring the phylogenetic signal in traits is uninformative for evaluating the effectiveness of using PD in conservation. We evolve traits under several different models and, for the first time, directly compare the FD of a set of taxa that maximize PD to the FD of a random set of the same size. Under many common models of trait evolution and tree shapes, conserving the maxPD set of taxa will conserve more FD than conserving a random set of the same size. However, this result cannot be generalized to other classes of models. We find that under biologically plausible scenarios, using PD to select species can actually lead to less FD compared with a random set. Critically, this can occur even when there is phylogenetic signal in the traits. Predicting exactly when we expect using PD to be a good strategy for conserving FD is challenging, as it depends on complex interactions between tree shape and the assumptions of the evolutionary model. Nonetheless, if our goal is to maintain trait diversity, the fact that conserving taxa based on PD will not reliably conserve at least as much FD as choosing randomly raises serious concerns about the general utility of PD in conservation.

Linking speciation to extinction: Diversification raises contemporary extinction risk in amphibians.

Many of the traits associated with elevated rates of speciation, including niche specialization and having small and isolated populations, are similarly linked with an elevated risk of extinction. This suggests that rapidly speciating lineages may also be more extinction prone. Empirical tests of a speciation-extinction correlation are rare because assessing paleontological extinction rates is difficult. However, the modern biodiversity crisis allows us to observe patterns of extinction in real time, and if this hypothesis is true then we would expect young clades that have recently diversified to have high contemporary extinction risk. Here, we examine evolutionary patterns of modern extinction risk across over 300 genera within one of the most threatened vertebrate classes, the Amphibia. Consistent with predictions, rapidly diversifying amphibian clades also had a greater share of threatened species. Curiously, this pattern is not reflected in other tetrapod classes and may reflect a greater propensity to speciate through peripheral isolation in amphibians, which is partly supported by a negative correlation between diversification rate and mean geographic range size. This clustered threat in rapidly diversifying amphibian genera means that protecting a small number of species can achieve large gains in preserving amphibian phylogenetic diversity. Nonindependence between speciation and extinction rates has many consequences for patterns of biodiversity and how we may choose to conserve it.

A guide to phylogenetic metrics for conservation, community ecology and macroecology.

The use of phylogenies in ecology is increasingly common and has broadened our understanding of biological diversity. Ecological sub-disciplines, particularly conservation, community ecology and macroecology, all recognize the value of evolutionary relationships but the resulting development of phylogenetic approaches has led to a proliferation of phylogenetic diversity metrics. The use of many metrics across the sub-disciplines hampers potential meta-analyses, syntheses, and generalizations of existing results. Further, there is no guide for selecting the appropriate metric for a given question, and different metrics are frequently used to address similar questions. To improve the choice, application, and interpretation of phylo-diversity metrics, we organize existing metrics by expanding on a unifying framework for phylogenetic information. Generally, questions about phylogenetic relationships within or between assemblages tend to ask three types of question: how much; how different; or how regular? We show that these questions reflect three dimensions of a phylogenetic tree: richness, divergence, and regularity. We classify 70 existing phylo-diversity metrics based on their mathematical form within these three dimensions and identify 'anchor' representatives: for α-diversity metrics these are PD (Faith's phylogenetic diversity), MPD (mean pairwise distance), and VPD (variation of pairwise distances). By analysing mathematical formulae and using simulations, we use this framework to identify metrics that mix dimensions, and we provide a guide to choosing and using the most appropriate metrics. We show that metric choice requires connecting the research question with the correct dimension of the framework and that there are logical approaches to selecting and interpreting metrics. The guide outlined herein will help researchers navigate the current jungle of indices.

I-HEDGE: determining the optimum complementary sets of taxa for conservation using evolutionary isolation.

In the midst of the current biodiversity crisis, conservation efforts might profitably be directed towards ensuring that extinctions do not result in inordinate losses of evolutionary history. Numerous methods have been developed to evaluate the importance of species based on their contribution to total phylogenetic diversity on trees and networks, but existing methods fail to take complementarity into account, and thus cannot identify the best order or subset of taxa to protect. Here, we develop a novel iterative calculation of the heightened evolutionary distinctiveness and globally endangered metric (I-HEDGE) that produces the optimal ranked list for conservation prioritization, taking into account complementarity and based on both phylogenetic diversity and extinction probability. We applied this metric to a phylogenetic network based on mitochondrial control region data from extant and recently extinct giant Galápagos tortoises, a highly endangered group of closely related species. We found that the restoration of two extinct species (a project currently underway) will contribute the greatest gain in phylogenetic diversity, and present an ordered list of rankings that is the optimum complementarity set for conservation prioritization.

The evolutionary relationships and age of Homo naledi: An assessment using dated Bayesian phylogenetic methods.

Homo naledi is a recently discovered species of fossil hominin from South Africa. A considerable amount is already known about H. naledi but some important questions remain unanswered. Here we report a study that addressed two of them: "Where does H. naledi fit in the hominin evolutionary tree?" and "How old is it?" We used a large supermatrix of craniodental characters for both early and late hominin species and Bayesian phylogenetic techniques to carry out three analyses. First, we performed a dated Bayesian analysis to generate estimates of the evolutionary relationships of fossil hominins including H. naledi. Then we employed Bayes factor tests to compare the strength of support for hypotheses about the relationships of H. naledi suggested by the best-estimate trees. Lastly, we carried out a resampling analysis to assess the accuracy of the age estimate for H. naledi yielded by the dated Bayesian analysis. The analyses strongly supported the hypothesis that H. naledi forms a clade with the other Homo species and Australopithecus sediba. The analyses were more ambiguous regarding the position of H. naledi within the (Homo, Au. sediba) clade. A number of hypotheses were rejected, but several others were not. Based on the available craniodental data, Homo antecessor, Asian Homo erectus, Homo habilis, Homo floresiensis, Homo sapiens, and Au. sediba could all be the sister taxon of H. naledi. According to the dated Bayesian analysis, the most likely age for H. naledi is 912 ka. This age estimate was supported by the resampling analysis. Our findings have a number of implications. Most notably, they support the assignment of the new specimens to Homo, cast doubt on the claim that H. naledi is simply a variant of H. erectus, and suggest H. naledi is younger than has been previously proposed.

Salmon nutrients are associated with the phylogenetic dispersion of riparian flowering-plant assemblages.

A signature of nonrandom phylogenetic community structure has been interpreted as indicating community assembly processes. Significant clustering within the phylogenetic structure of a community can be caused by habitat filtering due to low nutrient availability. Nutrient limitation in temperate Pacific coastal rainforests can be alleviated to some extent by marine nutrient subsidies introduced by migrating salmon, which leave a quantitative signature on the makeup of plant communities near spawning streams. Thus, nutrient-mediated habitat filtering could be reduced by salmon nutrients. Here, we ask how salmon abundance affects the phylogenetic structure of riparian flowering plant assemblages across 50 watersheds in the Great Bear Rainforest of British Columbia, Canada. Based on a regional pool of 60 plant species, we found that assemblages become more phylogenetically dispersed and species poor adjacent to streams with higher salmon spawning density. In contrast, increased phylogenetic clumping and species richness was seen in sites with low salmon density, with steeper slopes, further from the stream edge, and within smaller watersheds. These observations are all consistent with abiotic habitat filtering and biotic competitive exclusion acting together across local and landscape-scale gradients in nutrient availability to structure assembly of riparian flowering plants. In this case, rich salmon nutrients appear to release riparian flowering-plant assemblages from the confines of a low-nutrient habitat filter that drives phylogenetic clustering.

Ranking Mammal Species for Conservation and the Loss of Both Phylogenetic and Trait Diversity.

The 'edge of existence' (EDGE) prioritisation scheme is a new approach to rank species for conservation attention that aims to identify species that are both isolated on the tree of life and at imminent risk of extinction as defined by the World Conservation Union (IUCN). The self-stated benefit of the EDGE system is that it effectively captures unusual 'unique' species, and doing so will preserve the total evolutionary history of a group into the future. Given the EDGE metric was not designed to capture total evolutionary history, we tested this claim. Our analyses show that the total evolutionary history of mammals preserved is indeed much higher if EDGE species are protected than if at-risk species are chosen randomly. More of the total tree is also protected by EDGE species than if solely threat status or solely evolutionary distinctiveness were used for prioritisation. When considering how much trait diversity is captured by IUCN and EDGE prioritisation rankings, interestingly, preserving the highest-ranked EDGE species, or indeed just the most threatened species, captures more total trait diversity compared to sets of randomly-selected at-risk species. These results suggest that, as advertised, EDGE mammal species contribute evolutionary history to the evolutionary tree of mammals non-randomly, and EDGE-style rankings among endangered species can also capture important trait diversity. If this pattern holds for other groups, the EDGE prioritisation scheme has greater potential to be an efficient method to allocate scarce conservation effort.