PATTERNS IN PHYLOGENETIC TREE BALANCE WITH VARIABLE AND EVOLVING SPECIATION RATES

Aspects of phylogenetic tree shape, and in particular tree balance, provide clues to the workings of the macroevolutionary process. I use a simulation approach to explore patterns in tree balance for several models of the evolutionary process under which speciation rates vary through the history of diversifying clades. I demonstrate that when speciation rates depend on an evolving trait of individuals, and are therefore “heritable” along evolutionary lineages, the resulting phylogenies become imbalanced. However, imbalance also results from some (but not all) models of “nonheritable” speciation rate variation. The degree of imbalance increases with the magnitude of speciation rate variation, and then for gradual evolution (but not punctuated equilibria) reaches an asymptote short of the theoretical maximum. Very high levels of rate variation are required to produce imbalance matching that found in real data (estimated phylogenies from the systematic literature). I discuss implications of the simulation results for our understanding of macroevolution.     

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.     

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.     

A Comprehensive Quantitative Assessment of Bird Extinction Risk in Brazil

In an effort to avoid species loss, scientists have focused their efforts on the mechanisms making some species more prone to extinction than others. However, species show different responses to threats given their evolutionary history, behavior, and intrinsic biological features. We used bird biological features and external threats to (1) understand the multiple pathways driving Brazilian bird species to extinction, (2) to investigate if and how extinction risk is geographically structured, and (3) to quantify how much diversity is currently represented inside protected areas. We modeled the extinction risk of 1557 birds using classification trees and evaluated the relative contribution of each biological feature and external threat in predicting extinction risk. We also quantified the proportion of species and their geographic range currently protected by the network of Brazilian protected areas. The optimal classification tree showed different pathways to bird extinction. Habitat conversion was the most important predictor driving extinction risk though other variables, such as geographic range size, type of habitat, hunting or trapping and trophic guild, were also relevant in our models. Species under higher extinction risk were concentrated mainly in the Cerrado Biodiversity Hotspot and were not quite represented inside protected areas, neither in richness nor range. Predictive models could assist conservation actions, and this study could contribute by highlighting the importance of natural history and ecology in these actions.     

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.     

Neutral biodiversity theory can explain the imbalance of phylogenetic trees but not the tempo of their diversification

Numerous evolutionary studies have sought to explain the distribution of diversity across the limbs of the tree of life. At the same time, ecological studies have sought to explain differences in diversity and relative abundance within and among ecological communities. Traditionally, these patterns have been considered separately, but models that consider processes operating at the level of individuals, such as neutral biodiversity theory (NBT), can provide a link between them. Here, we compare evolutionary dynamics across a suite of NBT models. We show that NBT can yield phylogenetic tree topologies with imbalance closely resembling empirical observations. In general, metacommunities that exhibit greater disparity in abundance are characterized by more imbalanced phylogenetic trees. However, NBT fails to capture the tempo of diversification as represented by the distribution of branching events through time. We suggest that population-level processes might therefore help explain the asymmetry of phylogenetic trees, but that tree shape might mislead estimates of evolutionary rates unless the diversification process is modeled explicitly.     

Exploring the phylogenetic history of mammal species richness

Aim At broad geographical scales, species richness is a product of three basic processes: speciation, extinction and migration. However, determining which of these processes predominates is a major challenge. Whilst palaeontological studies can provide information on speciation and extinction rates, data are frequently lacking. Here we use a recent dated phylogenetic tree of mammals to explore the relative importance of these three processes in structuring present‐day richness gradients. Location The global terrestrial biosphere. Methods We combine macroecological data with phylogenetic methods more typically used in community ecology to describe the phylogenetic history of regional faunas. Using simulations, we explore two simple phylogenetic metrics, the mean and variance in the pairwise distances between taxa, and describe their relationship to phylogenetic tree topology. We then use these two metrics to characterize the evolutionary relationships among mammal species assemblages across the terrestrial biome. Results We show that the mean and variance in the pairwise distances describe phylogenetic tree topology well, but are less sensitive to phylogenetic uncertainty than more direct measures of tree shape. We find the phylogeny for South American mammals is imbalanced and ‘stemmy’ (long branches towards the root), consistent with recent diversification within evolutionarily disparate lineages. In contrast, the phylogeny for African mammals is balanced and ‘tippy’ (long branches towards the tips), more consistent with the slow accumulation of diversity over long times, reflecting the Old World origin of many mammal clades. Main conclusions We show that phylogeny can accurately capture biogeographical processes operating at broad spatial scales and over long time periods. Our results support inferences from the fossil record – that the New World tropics are a diversity cradle whereas the Old World tropics are a museum of old diversity.     

Micro‐evolutionary diversification among Indian Ocean parrots: temporal and spatial changes in phylogenetic diversity as a consequence of extinction and invasion

Almost 90% of global bird extinctions have occurred on islands. The loss of endemic species from island systems can dramatically alter evolutionary trajectories of insular species biodiversity, resulting in a loss of evolutionary diversity important for species adaptation to changing environments. The Western Indian Ocean islands have been the scene of evolution for a large number of endemic parrots. Since their discovery in the 16th century, many of these parrots have become extinct or have declined in numbers. Alongside the extinction of species, a number of the Indian Ocean islands have experienced colonization by highly invasive parrots, such as the Ring‐necked Parakeet Psittacula krameri. Such extinctions and invasions can, on an evolutionary timescale, drive changes in species composition, genetic diversity and turnover in phylogenetic diversity, all of which can have important impacts on species potential for adaptation to changing environmental and climatic conditions. Using mtDNA cytochrome b data, we resolve the taxonomic placement of three extinct Indian Ocean parrots: the Rodrigues Psittacula exsul, Seychelles Psittacula wardi and Reunion Parakeets Psittacula eques. This case study quantifies how the extinction of these species has resulted in lost historical endemic phylogenetic diversity and reduced levels of species richness, and illustrates how it is being replaced by non‐endemic invasive forms such as the Ring‐necked Parakeet. Finally, we use our phylogenetic framework to identify and recommend a number of phylogenetically appropriate ecological replacements for the extinct parrots. Such replacements may be introduced once invasive forms have been cleared, to rejuvenate ecosystem function and restore lost phylogenetic diversity.     

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.     

Phylogenetically patterned speciation rates and extinction risks change the loss of evolutionary history during extinctions

If we are to plan conservation strategies that minimize the loss of evolutionary history through human-caused extinctions, we must understand how this loss is related to phylogenetic patterns in current extinction risks and past speciation rates. Nee & May (1997, Science 278, 692-694) showed that for a randomly evolving clade (i) a single round of random extinction removed relatively little evolutionary history, and (ii) extinction management (choosing which taxa to sacrifice) offered only marginal improvement. However, both speciation rates and extinction risks vary across lineages within real clades. We simulated evolutionary trees with phylogenetically patterned speciation rates and extinction risks (closely related lineages having similar rates and risks) and then subjected them to several biologically informed models of extinction. Increasing speciation rate variation increases the extinction-management pay-off. When extinction risks vary among lineages but are uncorrelated with speciation rates, extinction removes more history (compared with random trees), but the difference is small. When extinction risks vary and are correlated with speciation rates, history loss can dramatically increase (negative correlation) or decrease (positive correlation) with speciation rate variation. The loss of evolutionary history via human-caused extinctions may therefore be more severe, yet more manageable, than first suggested.     

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.     

Urbanisation and the loss of phylogenetic diversity in birds

Despite the recognised conservation value of phylogenetic diversity, little is known about how it is affected by the urbanisation process. Combining a complete avian phylogeny with surveys along urbanisation gradients from five continents, we show that highly urbanised environments supported on average 450 million fewer years of evolutionary history than the surrounding natural environments. This loss was primarily caused by species loss and could have been higher had not been partially compensated by the addition of urban exploiters and some exotic species. Highly urbanised environments also supported fewer evolutionary distinctive species, implying a disproportionate loss of evolutionary history. Compared with highly urbanised environments, changes in phylogenetic richness and evolutionary distinctiveness were less substantial in moderately urbanised environments. Protecting pristine environments is therefore essential for maintaining phylogenetic diversity, but moderate levels of urbanisation still preserve much of the original diversity.     

A Global Trend towards the Loss of Evolutionarily Unique Species in Mangrove Ecosystems

The mangrove biome stands out as a distinct forest type at the interface between terrestrial, estuarine, and near-shore marine ecosystems. However, mangrove species are increasingly threatened and experiencing range contraction across the globe that requires urgent conservation action. Here, we assess the spatial distribution of mangrove species richness and evolutionary diversity, and evaluate potential predictors of global declines and risk of extinction. We found that human pressure, measured as the number of different uses associated with mangroves, correlated strongly, but negatively, with extinction probability, whereas species ages were the best predictor of global decline, explaining 15% of variation in extinction risk. Although the majority of mangrove species are categorised by the IUCN as Least Concern, our finding that the more threatened species also tend to be those that are more evolutionarily unique is of concern because their extinction would result in a greater loss of phylogenetic diversity. Finally, we identified biogeographic regions that are relatively species-poor but rich in evolutionary history, and suggest these regions deserve greater conservation priority. Our study provides phylogenetic information that is important for developing a unified management plan for mangrove ecosystems worldwide.     

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.     

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.     

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.     

Phylogenetic extinction rates and comparative methodology

Species are not independent points for comparative analyses because closely related species share more evolutionary history and are therefore more similar to each other than distantly related species. The extent to which independent-contrast analysis reduces type I and type II statistical error in comparison with cross-species analysis depends on the relative branch lengths in the phylogenetic tree: as deeper branches get relatively long, cross-species analyses have more statistical type I and type II error. Phylogenetic trees reconstructed from extant species, under the assumptions of a branching process with speciation (branching) and extinction rates remaining constant through time, will have relatively longer deep branches as the extinction rate increases relative to the speciation rate. We compare the statistical performance of cross-species and independent-contrast analyses with varying relative extinction rates, and conclude that cross-species comparisons have unacceptable statistical performance, particularly when extinction rates are relatively high.     

Comparing strategies to preserve evolutionary diversity

The likely future extinction of various species will result in a decline of two quantities: species richness and phylogenetic diversity (PD, or ‘evolutionary history’). Under a simple stochastic model of extinction, we can estimate the expected loss of these quantities under two conservation strategies: An ‘egalitarian’ approach, which reduces the extinction risk of all species, and a ‘targeted’ approach that concentrates conservation effort on the most endangered taxa. For two such strategies that are constrained to experience the same expected loss of species richness, we ask which strategy results in a greater expected loss of PD. Using mathematical analysis and simulation, we describe how the strategy (egalitarian versus targeted) that minimizes the expected loss of PD depends on the distribution of endangered status across the tips of the tree, and the interaction of this status with the branch lengths. For a particular data set consisting of a phylogenetic tree of 62 lemur species, with extinction risks estimated from the IUCN ‘Red List’, we show that both strategies are virtually equivalent, though randomizing these extinction risks across the tip taxa can cause either strategy to outperform the other. In the second part of the paper, we describe an algorithm to determine how extreme the loss of PD for a given decline in species richness can be. We illustrate the use of this algorithm on the lemur tree.     

Inferring phylogenetic relationships avoiding forbidden rooted triplets

To construct a phylogenetic tree or phylogenetic network for describing the evolutionary history of a set of species is a well-studied problem in computational biology. One previously proposed method to infer a phylogenetic tree/network for a large set of species is by merging a collection of known smaller phylogenetic trees on overlapping sets of species so that no (or as little as possible) branching information is lost. However, little work has been done so far on inferring a phylogenetic tree/network from a specified set of trees when in addition, certain evolutionary relationships among the species are known to be highly unlikely. In this paper, we consider the problem of constructing a phylogenetic tree/network which is consistent with all of the rooted triplets in a given set C and none of the rooted triplets in another given set F. Although NP-hard in the general case, we provide some efficient exact and approximation algorithms for a number of biologically meaningful variants of the problem.     

PATTERNS IN TREE BALANCE AMONG CLADISTIC,PHENETIC, AND RANDOMLY GENERATED PHYLOGENETIC TREES

I examine patterns in tree balance for a sample of 208 cladograms and phenograms from the recent literature. I provide an expression for expected imbalance under a simple, uniform-rate random speciation model, and I estimate variances by simulation for the same model. Imbalance decreases with tree size (number of included taxa) in both theoretical and literature trees. In contrast to previous suggestions, I find cladistic trees to be no more imbalanced than phenetic trees when confounding variables are appropriately controlled. The degree of imbalance found in literature trees is inconsistent with the uniform-rate speciation model; this is most likely a result of variability in speciation and extinction rates among real lineages. The existence of such variation is a necessary (but not sufficient) condition for the operation of the macroevolutionary processes of species sorting and species selection.