Linking the spatial and genomic structure of adaptive potential for conservation management: a review.

We unified the recent literature with the goal to contribute to the discussion on how genetic diversity might best be conserved. We argue that this decision will be guided by how genomic variation is distributed among manageable populations (i.e. its spatial structure), the degree to which adaptive potential is best predicted by variation across the entire genome or the subset of that variation that is identified as putatively adaptive (i.e. its genomic structure), and whether we are managing species as single entities or as collections of diversifying lineages. The distribution of genetic variation and our ultimate goal will have practical implications for on-the-ground management. If adaptive variation is largely polygenic or responsive to change, its spatial structure might be broadly governed by the forces determining genome-wide variation (linked selection, drift, and gene flow), making measurement and prioritization straightforward. If we are managing species as single entities, then population-level prioritization schemes are possible so as to maximize future pooled genetic variation. We outline one such scheme based on the popular Shapley Value from cooperative game theory that considers the relative genetic contribution of a population to an unknown future collection of populations.

Capturing diversity: Split systems and circular approximations for conservation.

We investigated the implications of employing a circular approximation of split systems in the calculation of maximum diversity subsets of a set of taxa in a conservation biology context where diversity is measured using Split System Diversity (SSD). We conducted a comparative analysis between the maximum SSD score and the maximum SSD set(s) of size k, efficiently determined using a circular approximation, and the true results obtained through brute-force search based on the original data. Through experimentation on simulated datasets and SNP data across 50 Atlantic Salmon populations, our findings demonstrate that employing a circular approximation can lead to the generation of an incorrect max-SSD set(s). We built a graph-based split system whose circular approximation led to a max-SSD set of size k=4 that was less than the true max-SSD set by 17.6%. This discrepancy increased to 25% for k=11 when we used a hypergraph-based split system. The same comparison on the Atlantic salmon dataset revealed a mere 1% difference. However, noteworthy disparities emerged in the population composition between the two sets. These findings underscore the importance of assessing the suitability of circular approximations in conservation biology systems. Caution is advised when relying solely on circular approximations to determine sets of maximum diversity, and careful consideration of the data characteristics is crucial for accurate results in conservation biology applications.

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.

Observations on spindly leg syndrome in a captive population of Andinobates geminisae.

Amphibian health problems of unknown cause limit the success of the growing number of captive breeding programs. Spindly leg syndrome (SLS) is one such disease, where affected individuals with underdeveloped limbs often require euthanization. We experimentally evaluated husbandry-related factors of SLS in a captive population of the critically endangered frog, Andinobates geminisae. SLS has been linked to tadpole nutrition, vitamin B deficiency, water filtration methods, and water quality, but few of these have been experimentally tested. We tested the effects of water filtration method and vitamin supplementation (2017) and the effects of tadpole husbandry protocol intensity (2018) on time to metamorphosis and the occurrence of SLS. We found that vitamin supplementation and reconstituted reverse osmosis filtration of tadpole rearing water significantly reduced SLS prevalence and that reduced tadpole husbandry delayed time to metamorphosis. A fortuitous accident in 2018 resulted in a decrease in the phosphate content of rearing water, which afforded us an additional opportunity to assess the influence of phosphate on calcium sequestration. We found that tadpoles that had more time to sequester calcium for ossification during development had decreased the prevalence of SLS. Taken together, our results suggest that the qualities of the water used to rear tadpoles plays an important role in the development of SLS. Specifically, filtration method, vitamin supplementation, and calcium availability of tadpole rearing water may play important roles. Focused experiments are still needed, but our findings provide important information for amphibian captive rearing programs affected by high SLS prevalence.

Formal Links between Feature Diversity and Phylogenetic Diversity.

The extent to which phylogenetic diversity (PD) captures feature diversity (FD) is a topical and controversial question in biodiversity conservation. In this short paper, we formalize this question and establish a precise mathematical condition for FD (based on discrete characters) to coincide with PD. In this way, we make explicit the two main reasons why the two diversity measures might disagree for given data; namely, the presence of certain patterns of feature evolution and loss, and using temporal branch lengths for PD in settings that may not be appropriate (e.g., due to rapid evolution of certain features over short periods of time). Our article also explores the relationship between the "Fair Proportion" index of PD and a simple index of FD (both of which correspond to Shapley values in cooperative game theory). In a second mathematical result, we show that the two indices can take identical values for any phylogenetic tree, provided the branch lengths in the tree are chosen appropriately. [Evolutionary distinctiveness; feature diversity; phylogenetic diversity; shapley value.].

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.

Guiding the prioritization of the most endangered and evolutionary distinct birds for new zoo conservation programs.

Zoos have played a pivotal role in the successful reinforcement and reintroduction of species threatened with extinction, but prioritization is required in the face of increasing need and limited capacity. One means of prioritizing between species of equal threat status when establishing new breeding programs is the consideration of evolutionary distinctness (ED). More distinct species have fewer close relatives such that their extinction would result in a greater overall loss to the Tree of Life. Considering global ex situ holdings of birds (a group with a complete and well-detailed evolutionary tree), we investigate the representation of at-risk and highly evolutionarily distinct species in global zoo holdings. We identified a total of 2,236 bird species indicated by the Zoological Information Management System as being held in zoological institutions worldwide. As previously reported, imperiled species (defined as those possessing endangered or critically endangered threat status) in this database are less likely to be held in zoos than non-imperiled species. However, we find that species possessing ED scores within the top 10% of all bird species are more likely to be held in zoos than other species, possibly because they possess unique characteristics that have historically made them popular exhibits. To assist with the selection of high priority ED species for future zoo conservation programs, we provide a list of imperiled species currently not held in zoos, ranked by ED. This list highlights species representing particular priorities for ex situ conservation planners, and represents a practical tool for improving the conservation value of zoological collections.

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.

Corrigendum: Reductions in global biodiversity loss predicted from conservation spending.

This corrects the article DOI: 10.1038/nature24295.

Evolutionary isolation and phylogenetic diversity loss under random extinction events.

The extinction of species at the present leads to the loss of 'phylogenetic diversity' (PD) from the evolutionary tree in which these species lie. Prior to extinction, the total PD present can be divided up among the species in various ways using measures of evolutionary isolation (such as 'fair proportion' and 'equal splits'). However, the loss of PD when certain combinations of species become extinct can be either larger or smaller than the cumulative loss of the isolation values associated with the extinct species. In this paper, we show that for trees generated under neutral evolutionary models, the loss of PD under a null model of random extinction at the present can be predicted from the loss of the cumulative isolation values, by applying a non-linear transformation that is independent of the tree. Moreover, the error in the prediction provably converges to zero as the size of the tree grows, with simulations showing good agreement even for moderate sized trees (n=64).