Predicting loss of evolutionary history: Where are we?

The Earth's evolutionary history is threatened by species loss in the current sixth mass extinction event in Earth's history. Such extinction events not only eliminate species but also their unique evolutionary histories. Here we review the expected loss of Earth's evolutionary history quantified by phylogenetic diversity (PD) and evolutionary distinctiveness (ED) at risk. Due to the general paucity of data, global evolutionary history losses have been predicted for only a few groups, such as mammals, birds, amphibians, plants, corals and fishes. Among these groups, there is now empirical support that extinction threats are clustered on the phylogeny; however this is not always a sufficient condition to cause higher loss of phylogenetic diversity in comparison to a scenario of random extinctions. Extinctions of the most evolutionarily distinct species and the shape of phylogenetic trees are additional factors that can elevate losses of evolutionary history. Consequently, impacts of species extinctions differ among groups and regions, and even if global losses are low within large groups, losses can be high among subgroups or within some regions. Further, we show that PD and ED are poorly protected by current conservation practices. While evolutionary history can be indirectly protected by current conservation schemes, optimizing its preservation requires integrating phylogenetic indices with those that capture rarity and extinction risk. Measures based on PD and ED could bring solutions to conservation issues, however they are still rarely used in practice, probably because the reasons to protect evolutionary history are not clear for practitioners or due to a lack of data. However, important advances have been made in the availability of phylogenetic trees and methods for their construction, as well as assessments of extinction risk. Some challenges remain, and looking forward, research should prioritize the assessment of expected PD and ED loss for more taxonomic groups and test the assumption that preserving ED and PD also protects rare species and ecosystem services. Such research will be useful to inform and guide the conservation of Earth's biodiversity and the services it provides.     

The future of evolutionary diversity in reef corals

One-third of the world''s reef-building corals are facing heightened extinction risk from climate change and other anthropogenic impacts. Previous studies have shown that such threats are not distributed randomly across the coral tree of life, and future extinctions have the potential to disproportionately reduce the phylogenetic diversity of this group on a global scale. However, the impact of such losses on a regional scale remains poorly known. In this study, we use phylogenetic metrics in conjunction with geographical distributions of living reef coral species to model how extinctions are likely to affect evolutionary diversity across different ecoregions. Based on two measures—phylogenetic diversity and phylogenetic species variability—we highlight regions with the largest losses of evolutionary diversity and hence of potential conservation interest. Notably, the projected loss of evolutionary diversity is relatively low in the most species-rich areas such as the Coral Triangle, while many regions with fewer species stand to lose much larger shares of their diversity. We also suggest that for complex ecosystems like coral reefs it is important to consider changes in phylogenetic species variability; areas with disproportionate declines in this measure should be of concern even if phylogenetic diversity is not as impacted. These findings underscore the importance of integrating evolutionary history into conservation planning for safeguarding the future diversity of coral reefs.     

云南被子植物菊类分支的系统发育多样性及其分布格局

全球气候变化与人为活动等因素导致的生物多样性丧失,引起了全球各界对生物多样性保护的高度关注。传统生物多样性保护主要对物种、特有种、受威胁物种的种类组成及其分布模式开展研究,忽视了进化历史在生物多样性保护中的作用。云南是全球生物多样性热点地区的交汇区,生物多样性的保护历来受到广泛关注,为了更好地探讨云南生物多样性的保护措施,该研究以云南被子植物菊类分支物种为研究对象,基于物种间的演化关系,结合其地理分布,从进化历史的角度探讨物种、特有种、受威胁物种的种类组成及系统发育组成的分布格局,并整合自然保护地的空间分布,识别生物多样性的重点保护区域。结果表明：云南被子植物菊类分支的物种、特有种及受威胁物种的物种密度与系统发育多样性均显著正相关;通过零模型分析发现,由南向北标准化系统发育多样性逐渐降低;云南南部、东南部、西北部是云南被子植物菊类分支的重点保护区域,加强这些区域的保护,将最大化地保护生物多样性的进化历史和进化潜能。由此可见,融合进化历史信息的植物多样性格局分析不仅有助于更加深入地理解植物多样性的形成与演变,也为生物多样性保护策略的制定提供更多的思路。     

Phylogenetic Patterns of Extinction Risk in the Eastern Arc Ecosystems,an African Biodiversity Hotspot

There is an urgent need to reduce drastically the rate at which biodiversity is declining worldwide. Phylogenetic methods are increasingly being recognised as providing a useful framework for predicting future losses, and guiding efforts for pre-emptive conservation actions. In this study, we used a reconstructed phylogenetic tree of angiosperm species of the Eastern Arc Mountains – an important African biodiversity hotspot – and described the distribution of extinction risk across taxonomic ranks and phylogeny. We provide evidence for both taxonomic and phylogenetic selectivity in extinction risk. However, we found that selectivity varies with IUCN extinction risk category. Vulnerable species are more closely related than expected by chance, whereas endangered and critically endangered species are not significantly clustered on the phylogeny. We suggest that the general observation for taxonomic and phylogenetic selectivity (i.e. phylogenetic signal, the tendency of closely related species to share similar traits) in extinction risks is therefore largely driven by vulnerable species, and not necessarily the most highly threatened. We also used information on altitudinal distribution and climate to generate a predictive model of at-risk species richness, and found that greater threatened species richness is found at higher altitude, allowing for more informed conservation decision making. Our results indicate that evolutionary history can help predict plant susceptibility to extinction threats in the hyper-diverse but woefully-understudied Eastern Arc Mountains, and illustrate the contribution of phylogenetic approaches in conserving African floristic biodiversity where detailed ecological and evolutionary data are often lacking.     

Phylogenetic correlates of extinction risk in mammals: species in older lineages are not at greater risk

Phylogenetic information is becoming a recognized basis for evaluating conservation priorities, but associations between extinction risk and properties of a phylogeny such as diversification rates and phylogenetic lineage ages remain unclear. Limited taxon-specific analyses suggest that species in older lineages are at greater risk. We calculate quantitative properties of the mammalian phylogeny and model extinction risk as an ordinal index based on International Union for Conservation of Nature Red List categories. We test for associations between lineage age, clade size, evolutionary distinctiveness and extinction risk for 3308 species of terrestrial mammals. We show no significant global or regional associations, and three significant relationships within taxonomic groups. Extinction risk increases for evolutionarily distinctive primates and decreases with lineage age when lemurs are excluded. Lagomorph species (rabbits, hares and pikas) that have more close relatives are less threatened. We examine the relationship between net diversification rates and extinction risk for 173 genera and find no pattern. We conclude that despite being under-represented in the frequency distribution of lineage ages, species in older, slower evolving and distinct lineages are not more threatened or extinction-prone. Their extinction, however, would represent a disproportionate loss of unique evolutionary history.     

Threatened reef corals of the world

A substantial proportion of the world's living species, including one-third of the reef-building corals, are threatened with extinction and in pressing need of conservation action. In order to reduce biodiversity loss, it is important to consider species' contribution to evolutionary diversity along with their risk of extinction for the purpose of setting conservation priorities. Here I reconstruct the most comprehensive tree of life for the order Scleractinia (1,293 species) that includes all 837 living reef species, and employ a composite measure of phylogenetic distinctiveness and extinction risk to identify the most endangered lineages that would not be given top priority on the basis of risk alone. The preservation of these lineages, not just the threatened species, is vital for safeguarding evolutionary diversity. Tests for phylogeny-associated patterns show that corals facing elevated extinction risk are not clustered on the tree, but species that are susceptible, resistant or resilient to impacts such as bleaching and disease tend to be close relatives. Intensification of these threats or extirpation of the endangered lineages could therefore result in disproportionate pruning of the coral tree of life.     

Phylogenetic diversity does not capture body size variation at risk in the world's mammals

Mammals contribute to important ecosystem processes and services, but many mammalian species are threatened with extinction. We compare how global patterns in three measures of mammalian diversity—species richness, phylogenetic diversity (PD) and body mass variance (BMV)—would change if all currently threatened species were lost. Given that many facets of species'' ecology and life history scale predictably with body mass, the BMV in a region roughly reflects the diversity of species'' roles within ecosystems and so is a simple proxy for functional diversity (FD). PD is also often considered to be a proxy for FD, but our results suggest that BMV losses within ecoregions would be much more severe than losses of PD or species richness, and that its congruence with the latter two measures is low. Because of the disproportionate loss of large mammals, 65 per cent of ecoregions would lose significantly more BMV than under random extinction, while only 11 per cent would lose significantly more PD. Ecosystem consequences of these selective losses may be profound, especially throughout the tropics, but are not captured by PD. This low surrogacy stresses a need for conservation prioritization based on threatened trait diversity, and for conservation efforts to take an ecosystem perspective.     

Phylogenetic autocorrelation of extinction threat in globally imperilled amphibians

The global extinction crisis demands immediate action to conserve species at risk. However, if entire clades such as superfamilies are at risk due to shared evolutionary history, a shift towards conserving clades rather than individual species may be needed. Using phylogenetic autocorrelation analysis, we demonstrate that multiple kinds of extinction threat clump within the amphibian tree of life. Our study provides insight into how these threats may collectively influence the extinction risk of whole clades, consistent with the supposition that related species, with similar traits, share an intrinsic vulnerability to common kinds of threat. Most strikingly, we find a significant concentration of 'enigmatic' decline and critically endangered status within families of the hyloid frogs. This phylogenetic clumping of risk is also geographically concentrated, with most threats found in Central and South America, and Australia, coinciding with reported outbreaks of chytridiomycosis. We speculate that the phylogenetic clumping of threat represents, in part, shared extinction proneness due to shared evolutionary history. However, even if the phylogenetic clumping of threat were simply a by-product of shared geography, this concordance between phylogenetic and geographical patterns represents a prime opportunity. Where practical, we should implement conservation plans that focus on biogeographical regions where threatened clades occur, thereby improving our ability to conserve species. This approach could outperform the usual triage approach of saving individual species after they have become critically endangered.     

Palm economic and traditional uses,evolutionary history and the IUCN Red List

The growing demand for natural resources to sustain human population has increased the loss and modification of natural habitats, enhancing the number of species threatened with extinction. Commonly tools such as Red Lists guide conservation actions and policies. However, Red Lists are based in population parameters, and important aspects of biodiversity such as phylogenetic diversity are not considered. Here we evaluated the amount of economic and traditional uses and evolutionary history of palms captured by the global IUCN Red List and the national Red Lists of Colombia and Madagascar. We estimated palms plant use diversity (PUD) and phylogenetic diversity (PD) for all species in the IUCN Red List and for each threat category at global and national scale. We also investigated if the number of uses, PUD and PD predict palm threat level. Species covered by IUCN Red List have lower PUD and PD than expected by chance. At global scale, palms with higher extinction risk have lower number of uses, PUD and PD. However, whereas in Colombia least concern species had lower PUD and PD, in Madagascar only Data Deficient species had lower PUD than expected by chance. Our findings highlight the need of palm specialists to expand the list of palms they have assessed and submit them for inclusion in Red Lists, enabling Red Lists to capture a more random sample of palm evolutionary history and economic uses. That would improve the success of biodiversity conservation actions by taking into account other aspects of biodiversity rather than taxonomic identity.     

Extinction risk and diversification are linked in a plant biodiversity hotspot

It is widely recognized that we are entering an extinction event on a scale approaching the mass extinctions seen in the fossil record. Present-day rates of extinction are estimated to be several orders of magnitude greater than background rates and are projected to increase further if current trends continue. In vertebrates, species traits, such as body size, fecundity, and geographic range, are important predictors of vulnerability. Although plants are the basis for life on Earth, our knowledge of plant extinctions and vulnerabilities is lagging. Here, we disentangle the underlying drivers of extinction risk in plants, focusing on the Cape of South Africa, a global biodiversity hotspot. By comparing Red List data for the British and South African floras, we demonstrate that the taxonomic distribution of extinction risk differs significantly between regions, inconsistent with a simple, trait-based model of extinction. Using a comprehensive phylogenetic tree for the Cape, we reveal a phylogenetic signal in the distribution of plant extinction risks but show that the most threatened species cluster within short branches at the tips of the phylogeny--opposite to trends in mammals. From analyzing the distribution of threatened species across 11 exemplar clades, we suggest that mode of speciation best explains the unusual phylogenetic structure of extinction risks in plants of the Cape. Our results demonstrate that explanations for elevated extinction risk in plants of the Cape flora differ dramatically from those recognized for vertebrates. In the Cape, extinction risk is higher for young and fast-evolving plant lineages and cannot be explained by correlations with simple biological traits. Critically, we find that the most vulnerable plant species are nonetheless marching towards extinction at a more rapid pace but, surprisingly, independently from anthropogenic effects. Our results have important implications for conservation priorities and cast doubts on the utility of current Red List criteria for plants in regions such as the Cape, where speciation has been rapid, if our aim is to maximize the preservation of the tree-of-life.     

Integrating biogeography,threat and evolutionary data to explore extinction crisis in the taxonomic group of cycads

Will the ongoing extinction crisis cause a severe loss of evolutionary information accumulated over millions of years on the tree of life? This question has been largely explored, particularly for vertebrates and angiosperms. However, no equivalent effort has been devoted to gymnosperms. Here, we address this question focusing on cycads, the gymnosperm group exhibiting the highest proportion of threatened species in the plant kingdom. We assembled the first complete phylogeny of cycads and assessed how species loss under three scenarios would impact the cycad tree of life. These scenarios are as follows: (1) All top 50% of evolutionarily distinct (ED ) species are lost; (2) all threatened species are lost; and (3) only all threatened species in each IUCN category are lost. Finally, we analyzed the biogeographical pattern of cycad diversity hotspots and tested for gaps in the current global conservation network. First, we showed that threatened species are not significantly clustered on the cycad tree of life. Second, we showed that the loss of all vulnerable or endangered species does not depart significantly from random loss. In contrast, the loss of all top 50% ED , all threatened or all critically endangered species, would result in a greater loss of PD (Phylogenetic Diversity) than expected. To inform conservation decisions, we defined five hotpots of diversity, and depending on the diversity metric used, these hotspots are located in Southern Africa, Australia, Indo‐Pacific, and Mexico and all are found within protected areas. We conclude that the phylogenetic diversity accumulated over millions of years in the cycad tree of life would not survive the current extinction crisis. As such, prioritizing efforts based on ED and concentrating efforts on critically endangered species particularly in southern Africa, Australia, Indo‐Pacific, and Mexico are required to safeguarding the evolutionary diversity in the cycad tree of life.     

Mammals on the EDGE: conservation priorities based on threat and phylogeny

Conservation priority setting based on phylogenetic diversity has frequently been proposed but rarely implemented. Here, we define a simple index that measures the contribution made by different species to phylogenetic diversity and show how the index might contribute towards species-based conservation priorities. We describe procedures to control for missing species, incomplete phylogenetic resolution and uncertainty in node ages that make it possible to apply the method in poorly known clades. We also show that the index is independent of clade size in phylogenies of more than 100 species, indicating that scores from unrelated taxonomic groups are likely to be comparable. Similar scores are returned under two different species concepts, suggesting that the index is robust to taxonomic changes. The approach is applied to a near-complete species-level phylogeny of the Mammalia to generate a global priority list incorporating both phylogenetic diversity and extinction risk. The 100 highest-ranking species represent a high proportion of total mammalian diversity and include many species not usually recognised as conservation priorities. Many species that are both evolutionarily distinct and globally endangered (EDGE species) do not benefit from existing conservation projects or protected areas. The results suggest that global conservation priorities may have to be reassessed in order to prevent a disproportionately large amount of mammalian evolutionary history becoming extinct in the near future.     

Investing in evolutionary history: implementing a phylogenetic approach for mammal conservation

Under the impact of human activity, global extinction rates have risen a thousand times higher than shown in the fossil record. The resources available for conservation are insufficient to prevent the loss of much of the world's threatened biodiversity during this crisis. Conservation planners have been forced to prioritize their protective activities, in the context of great uncertainty. This has become known as 'the agony of choice'. A range of methods have been proposed for prioritizing species for conservation attention; one of the most strongly supported is prioritizing those species that maximize phylogenetic distinctiveness (PD). We evaluate how a composite measure of extinction risk and phylogenetic isolation (EDGE) has been used to prioritize species according to their degree of unique evolutionary history (evolutionary distinctiveness, ED) weighted by conservation urgency (global endangerment, GE). We review PD-based approaches and provide an updated list of EDGE mammals using the 2010 IUCN Red List. We evaluate how robust this method is to changes in phylogenetic uncertainty, knowledge of taxonomy and extinction risk, and examine how mammalian species that rank highly in EDGE score are representative of the collective from which they are drawn.     

Biological correlates of extinction risk in bats

We investigated patterns and processes of extinction and threat in bats using a multivariate phylogenetic comparative approach. Of nearly 1,000 species worldwide, 239 are considered threatened by the International Union for Conservation of Nature and Natural Resources (IUCN) and 12 are extinct. Small geographic ranges and low wing aspect ratios are independently found to predict extinction risk in bats, which explains 48% of the total variance in IUCN assessments of threat. The pattern and correlates of extinction risk in the two bat suborders are significantly different. A higher proportion (4%) of megachiropteran species have gone extinct in the last 500 years than microchiropteran bats (0.3%), and a higher proportion is currently at risk of extinction (Megachiroptera: 34%; Microchiroptera: 22%). While correlates of microchiropteran extinction risk are the same as in the order as a whole, megachiropteran extinction is correlated more with reproductive rate and less with wing morphology. Bat extinction risk is not randomly distributed phylogenetically: closely related species have more similar levels of threat than would be expected if extinction risk were random. Given the unbalanced nature of the evolutionary diversification of bats, it is probable that the amount of phylogenetic diversity lost if currently threatened taxa disappear may be greater than in other clades with numerically more threatened species.     

Global species richness of hydrobiid snails determined by climate and evolutionary history

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Multiple drivers of decline in the global status of freshwater crayfish (Decapoda: Astacidea)

Rates of biodiversity loss are higher in freshwater ecosystems than in most terrestrial or marine ecosystems, making freshwater conservation a priority. However, prioritization methods are impeded by insufficient knowledge on the distribution and conservation status of freshwater taxa, particularly invertebrates. We evaluated the extinction risk of the world''s 590 freshwater crayfish species using the IUCN Categories and Criteria and found 32% of all species are threatened with extinction. The level of extinction risk differed between families, with proportionally more threatened species in the Parastacidae and Astacidae than in the Cambaridae. Four described species were Extinct and 21% were assessed as Data Deficient. There was geographical variation in the dominant threats affecting the main centres of crayfish diversity. The majority of threatened US and Mexican species face threats associated with urban development, pollution, damming and water management. Conversely, the majority of Australian threatened species are affected by climate change, harvesting, agriculture and invasive species. Only a small proportion of crayfish are found within the boundaries of protected areas, suggesting that alternative means of long-term protection will be required. Our study highlights many of the significant challenges yet to come for freshwater biodiversity unless conservation planning shifts from a reactive to proactive approach.     

Ecological and socio-economic factors affecting extinction risk in parrots

Parrots (Psittaciformes) are among the most threatened bird orders with 28 % (111 of 398) of extant species classified as threatened under IUCN criteria. We confirmed that parrots have a lower Red List Index (higher aggregate extinction risk) than other comparable bird groups, and modeled the factors associated with extinction risk. Our analyses included intrinsic biological, life history and ecological attributes, external anthropogenic threats, and socio-economic variables associated with the countries where the parrot species occur, while we controlled for phylogenetic dependence among species. We found that the likelihood of parrot species being classified as threatened was less for species with larger historical distribution size, but was greater for species with high forest dependency, large body size, long generation time, and greater proportion of the human population living in urban areas in the countries encompassing the parrots’ home ranges. The severity of extinction risk (from vulnerable to critically endangered) was positively related to the per capita gross domestic product (GDP) of the countries of occurrence, endemism to a single country, and lower for species used as pets. A disproportionate number of 16 extinct parrot species were endemic to islands and single countries, and were large bodied, habitat specialists. Agriculture, hunting, trapping, and logging are the most frequent threats to parrots worldwide, with variation in importance among regions. We use multiple methods to rank countries with disproportionately high numbers of threatened parrot species. Our results promote understanding of global and regional factors associated with endangerment in this highly threatened taxonomic group, and will enhance the prioritization of conservation actions.     

Rate of lineage origin explains the diversity anomaly in the world's mangrove vegetation

The contribution of nonecological factors to global patterns in diversity is evident when species richness differs between regions with similar habitats and geographic area. Mangrove environments in the Eastern Hemisphere harbor six times as many species of trees and shrubs as similar environments in the New World. Genetic divergence of mangrove lineages from terrestrial relatives, in combination with fossil evidence, suggests that mangrove diversity is limited by evolutionary transition into the stressful marine environment, the number of mangrove lineages has increased steadily over the Tertiary with little global extinction, and the diversity anomaly in mangrove vegetation reflects regional differences in the rate of origin of new mangrove lineages.     

Integrating data‐deficient species in analyses of evolutionary history loss

There is an increasing interest in measuring loss of phylogenetic diversity and evolutionary distinctiveness which together depict the evolutionary history of conservation interest. Those losses are assessed through the evolutionary relationships between species and species threat status or extinction probabilities. Yet, available information is not always sufficient to quantify the threat status of species that are then classified as data deficient. Data‐deficient species are a crucial issue as they cause incomplete assessments of the loss of phylogenetic diversity and evolutionary distinctiveness. We aimed to explore the potential bias caused by data‐deficient species in estimating four widely used indices: HEDGE, EDGE, PDloss, and Expected PDloss. Second, we tested four different widely applicable and multitaxa imputation methods and their potential to minimize the bias for those four indices. Two methods are based on a best‐ vs. worst‐case extinction scenarios, one is based on the frequency distribution of threat status within a taxonomic group and one is based on correlates of extinction risks. We showed that data‐deficient species led to important bias in predictions of evolutionary history loss (especially high underestimation when they were removed). This issue was particularly important when data‐deficient species tended to be clustered in the tree of life. The imputation method based on correlates of extinction risks, especially geographic range size, had the best performance and enabled us to improve risk assessments. Solving threat status of DD species can fundamentally change our understanding of loss of phylogenetic diversity. We found that this loss could be substantially higher than previously found in amphibians, squamate reptiles, and carnivores. We also identified species that are of high priority for the conservation of evolutionary distinctiveness.     

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.