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.].

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.

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.

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.

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.

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.

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.

Targeting global conservation funding to limit immediate biodiversity declines.

Inadequate funding levels are a major impediment to effective global biodiversity conservation and are likely associated with recent failures to meet United Nations biodiversity targets. Some countries are more severely underfunded than others and therefore represent urgent financial priorities. However, attempts to identify these highly underfunded countries have been hampered for decades by poor and incomplete data on actual spending, coupled with uncertainty and lack of consensus over the relative size of spending gaps. Here, we assemble a global database of annual conservation spending. We then develop a statistical model that explains 86% of variation in conservation expenditures, and use this to identify countries where funding is robustly below expected levels. The 40 most severely underfunded countries contain 32% of all threatened mammalian diversity and include neighbors in some of the world's most biodiversity-rich areas (Sundaland, Wallacea, and Near Oceania). However, very modest increases in international assistance would achieve a large improvement in the relative adequacy of global conservation finance. Our results could therefore be quickly applied to limit immediate biodiversity losses at relatively little cost.

Bayesian analysis of a morphological supermatrix sheds light on controversial fossil hominin relationships.

The phylogenetic relationships of several hominin species remain controversial. Two methodological issues contribute to the uncertainty-use of partial, inconsistent datasets and reliance on phylogenetic methods that are ill-suited to testing competing hypotheses. Here, we report a study designed to overcome these issues. We first compiled a supermatrix of craniodental characters for all widely accepted hominin species. We then took advantage of recently developed Bayesian methods for building trees of serially sampled tips to test among hypotheses that have been put forward in three of the most important current debates in hominin phylogenetics--the relationship between Australopithecus sediba and Homo, the taxonomic status of the Dmanisi hominins, and the place of the so-called hobbit fossils from Flores, Indonesia, in the hominin tree. Based on our results, several published hypotheses can be statistically rejected. For example, the data do not support the claim that Dmanisi hominins and all other early Homo specimens represent a single species, nor that the hobbit fossils are the remains of small-bodied modern humans, one of whom had Down syndrome. More broadly, our study provides a new baseline dataset for future work on hominin phylogeny and illustrates the promise of Bayesian approaches for understanding hominin phylogenetic relationships.

A molecular genetic time scale demonstrates Cretaceous origins and multiple diversification rate shifts within the order Galliformes (Aves).

The phylogeny of Galliformes (landfowl) has been studied extensively; however, the associated chronologies have been criticized recently due to misplaced or misidentified fossil calibrations. As a consequence, it is unclear whether any crown-group lineages arose in the Cretaceous and survived the Cretaceous-Paleogene (K-Pg; 65.5 Ma) mass extinction. Using Bayesian phylogenetic inference on an alignment spanning 14,539 bp of mitochondrial and nuclear DNA sequence data, four fossil calibrations, and a combination of uncorrelated lognormally distributed relaxed-clock and strict-clock models, we inferred a time-calibrated molecular phylogeny for 225 of the 291 extant Galliform taxa. These analyses suggest that crown Galliformes diversified in the Cretaceous and that three-stem lineages survived the K-Pg mass extinction. Ideally, characterizing the tempo and mode of diversification involves a taxonomically complete phylogenetic hypothesis. We used simple constraint structures to incorporate 66 data-deficient taxa and inferred the first taxon-complete phylogenetic hypothesis for the Galliformes. Diversification analyses conducted on 10,000 timetrees sampled from the posterior distribution of candidate trees show that the evolutionary history of the Galliformes is best explained by a rate-shift model including 1-3 clade-specific increases in diversification rate. We further show that the tempo and mode of diversification in the Galliformes conforms to a three-pulse model, with three-stem lineages arising in the Cretaceous and inter and intrafamilial diversification occurring after the K-Pg mass extinction, in the Paleocene-Eocene (65.5-33.9 Ma) or in association with the Eocene-Oligocene transition (33.9 Ma).

Inferring ancestral states without assuming neutrality or gradualism using a stable model of continuous character evolution.

BACKGROUND: The value of a continuous character evolving on a phylogenetic tree is commonly modelled as the location of a particle moving under one-dimensional Brownian motion with constant rate. The Brownian motion model is best suited to characters evolving under neutral drift or tracking an optimum that drifts neutrally. We present a generalization of the Brownian motion model which relaxes assumptions of neutrality and gradualism by considering increments to evolving characters to be drawn from a heavy-tailed stable distribution (of which the normal distribution is a specialized form). RESULTS: We describe Markov chain Monte Carlo methods for fitting the model to biological data paying special attention to ancestral state reconstruction, and study the performance of the model in comparison with a selection of existing comparative methods, using both simulated data and a database of body mass in 1,679 mammalian species. We discuss hypothesis testing and model selection. The stable model outperforms Brownian and Ornstein-Uhlenbeck approaches under simulations in which traits evolve with occasional large "jumps" in their value, but does not perform markedly worse for traits evolving under a truly Brownian process. CONCLUSIONS: The stable model is well suited to a stochastic process with a volatile rate of change in which biological characters undergo a mixture of neutral drift and occasional evolutionary events of large magnitude.

Basal metabolic rate and maternal energetic investment durations in mammals.

BACKGROUND: The Metabolic Theory of Ecology (MTE) predicts that gestation duration, lactation duration, and their sum, total development time, are constrained by mass-specific basal metabolic rate such that they should scale with body mass with an exponent of 0.25. However, tests of the MTE's predictions have yielded mixed results. In an effort to resolve this uncertainty, we used phylogenetically-controlled regression to investigate the allometries of gestation duration, lactation duration, and total development time in four well-studied mammalian orders, Artiodactyla, Carnivora, Primates, and Rodentia. RESULTS: The results we obtained are not consistent with the predictions of the MTE. Gestation duration scaling exponents are below 0.25 in all four orders. The scaling exponent for lactation duration is below 0.25 in Carnivora and Rodentia, indistinguishable from 0.25 in Artiodactyls, and steeper than 0.25 in Primates. Total development time scales with body mass as predicted by the MTE in Primates, but not in artiodactyls, carnivores, and rodents. In the latter three orders, the exponent is 0.15. CONCLUSIONS: Together, these results indicate that the influence of basal metabolic rate on mammalian maternal investment durations must be more complicated than the MTE envisages, and that other factors must play an important role. Future research needs to allow for the possibility that different factors drive gestation duration and lactation duration, and that the drivers of the two durations may differ among orders.

Dietary innovations spurred the diversification of ruminants during the Caenozoic.

Global climate shifts and ecological flexibility are two major factors that may affect rates of speciation and extinction across clades. Here, we connect past climate to changes in diet and diversification dynamics of ruminant mammals. Using novel versions of Multi-State Speciation and Extinction models, we explore the most likely scenarios for evolutionary transitions among diets in this clade and ask whether ruminant lineages with different feeding styles (browsing, grazing and mixed feeding) underwent differential rates of diversification concomitant with global temperature change. The best model of trait change had transitions from browsers to grazers via mixed feeding, with appreciable rates of transition to and from grazing and mixed feeding. Diversification rates in mixed-feeder and grazer lineages tracked the palaeotemperature curve, exhibiting higher rates during the Miocene thermal maxima. The origination of facultative mixed diet and grazing states may have triggered two adaptive radiations--one during the Oligocene-Miocene transition and the other during Middle-to-Late Miocene. Our estimate of mixed diets for basal lineages of both bovids and cervids is congruent with fossil evidence, while the reconstruction of browser ancestors for some impoverished clades--Giraffidae and Tragulidae--is not. Our results offer model-based neontological support to previous palaeontological findings and fossil-based hypothesis highlighting the importance of dietary innovations--especially mixed feeding--in the success of ruminants during the Neogene.

Evidence that gestation duration and lactation duration are coupled traits in primates.

Gestation duration and lactation duration are usually treated as independently evolving traits in primates, but the metabolic theory of ecology (MTE) suggests both durations should be determined by metabolic rate. We used phylogenetic generalized least-squares linear regression to test these different perspectives. We found that the allometries of the durations are divergent from each other and different from the scaling exponent predicted by the MTE (0.25). Gestation duration increases much more slowly (0.06 < m < 0.12), and lactation duration much more quickly (0.36 < m < 0.52) with body mass than the MTE predicts. By contrast, we found that the combined duration of gestation and lactation is consistent with the MTE's predictions (0.22 < m < 0.35). These results suggest that gestation duration and lactation duration might best be viewed as distinct but coupled adaptations. When transferring energy to their offspring, primate mothers must meet metabolically dictated physiological requirements while optimizing the timing of the switch from gestation to lactation in relation to some as-yet-unidentified body-size-related factor.

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.

Missing saiga on the taiga.

Conservation biologists understand that linking demographic histories of species at risk with causal biotic and abiotic events should help us predict the effects of ongoing biotic and abiotic change. In parallel, researchers have started to use ancient genetic information (aDNA) to explore the demographic histories of a number of species present in the Pleistocene fossil record (see, e.g. Shapiro et al. 2004). However, aDNA studies have primarily focused on identifying long-term population trends, linked to climate variability and the role of early human activity. Population trends over more recent time, e.g. during the Holocene, have been poorly explored, partly owing to analytical limitations. In this issue, Campos et al. (2010a) highlight the potential of aDNA to investigate demographic patterns over such recent time periods for the compelling and endangered saiga antelope Saiga tatarica (Fig. 1). The time may come when past and current demography can be combined to produce a seamless record. [Figure: see text].

Modern and ancient DNA reveal recent partial replacement of caribou in the southwest Yukon.

The long-term persistence of forest-dwelling caribou (Rangifer tarandus caribou) will probably be determined by management and conservation decisions. Understanding the evolutionary relationships between modern caribou herds, and how these relationships have changed through time will provide key information for the design of appropriate management strategies. To explore these relationships, we amplified microsatellite and mitochondrial markers from modern caribou from across the Southern Yukon, Canada, as well as mitochondrial DNA from Holocene specimens recovered from alpine ice patches in the same region. Our analyses identify a genetically distinct group of caribou composed of herds from the Southern Lakes region that may warrant special management consideration. We also identify a partial genetic replacement event occurring 1000 years before present, coincident with the deposition of the White River tephra and the Medieval Warm Period. These results suggest that, in the face of increasing anthropogenic pressures and climate variability, maintaining the ability of caribou herds to expand in numbers and range may be more important than protecting the survival of any individual, isolated sedentary forest-dwelling herd.