Mammals on the EDGE: Conservation Priorities Based on Threat and Phylogeny — TEI-tagged view

Nick J.B. IsaacpersName, Samuel T. TurveypersName, Ben CollenpersName, Carly WatermanpersName, Jonathan E.M. BailliepersName (2007date). “Mammals on the EDGE: Conservation Priorities Based on Threat and Phylogeny.” PLoS ONEtitle·j.

Object of study — species contributions to mammalian phylogenetic diversityterm and extinction-risk-weighted conservation priority

Research question — can evolutionary distinctivenessterm be measured comparably and robustly across taxa and combined with extinction riskterm to set global conservation priorities

Contribution — defines Evolutionary Distinctivenessterm and EDGE scoresterm, corrects major phylogenetic uncertainties, tests robustness, and produces a global mammal priority list

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Mammals on the EDGE: Conservation Priorities Based on Threat and Phylogeny Abstract Conservation priority settingterm based on phylogenetic diversityterm has frequently been proposed but rarely implemented. Here, we define a simple index that measures the contribution made by different species to phylogenetic diversityterm and show how the index might contribute towards species-based conservation prioritiesterm. We describe procedures to control for missing speciesterm, incomplete phylogenetic resolution and uncertainty in node agesterm that make it possible to apply the method in poorly known clades. We also show that the index is independent of clade sizeterm 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 conceptsterm, 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 diversityterm and extinction riskterm. 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 speciesterm) do not benefit from existing conservation projects or protected areasterm. The results suggest that global conservation priorities may have to be reassessed in order to prevent a disproportionately large amount of mammalian evolutionary historyterm becoming extinct in the near future.

Introduction Our planet is currently experiencing a severe anthropogenically driven extinction event, comparable in magnitude to prehistoric mass extinctions. Global extinction rates are now elevated up to a thousand times higher than the background extinction rates shown by the fossil record, and may climb another order of magnitude in the near future [1] – [3] . The resources currently available for conservation are, unfortunately, insufficient to prevent the loss of much of the world's threatened biodiversityterm during this crisis, and conservation planners have been forced into the unenviable situation of having to prioritise which species should receive the most protection–this is ‘the agony of choice’ [4] or the ‘Noah’s Ark problem' [5] .

A range of methods for setting species-based conservation prioritiesterm have been advocated by different researchers or organisations, focusing variously on threatened species, restricted-range endemics, ‘flagship’, ‘umbrella’, ‘keystone’, ‘landscape’ or ‘indicator’ species, or species with significant economic, ecological, scientific or cultural value [6] – [8] . To date, global priority-setting exercises have tended to focus on endemic (or restricted range) species [6] , [9] , [10] , presumably because endemism is easier to measure than competing methods. However, recent data show that endemism is a poor predictor of total species richness or the number of threatened species [11] .

It has also been argued that maximising Phylogenetic Diversityterm (PD) should be a key component of conservation priority settingterm [4] , [12] – [14] . Species represent different amounts of evolutionary historyterm, reflecting the tempo and mode of divergence across the Tree of Lifeterm. The extinction of a species in an old, monotypic or species-poor cladeterm would therefore result in a greater loss of biodiversityterm than that of a young species with many close relatives [15] , [16] . However, conserving such lineages may be difficult, since there is some evidence that they are more likely to be threatened with extinction than expected by chance [17] . This clumping of extinction risk in species-poor cladesterm greatly increases the loss of PDterm compared with a null model of random extinction [18] and suggests that entire vertebrate orders may be lost within centuries [19] . Among mammals alone, at least 14 genera and three families have gone extinct since AD 1500 [20] , and all members of a further 19 families and three orders are considered to be in imminent danger of extinction [2] . Many academic papers have suggested ways to maximise the conservation of PD [e.g. 12] , [13] , [21] – [23] and measure species' contributions to PD [e.g. 4] , [23] – [25] , but these have rarely been incorporated into conservation strategies. Therefore, it is possible that evolutionary historyterm is being rapidly lost, yet the most distinct species are not being identified as high priorities in existing conservation frameworks.

There are several reasons why PD has not gained wider acceptance in the conservation community. First, although evolutionary historyterm consists of two distinct componentsterm (the branching pattern of a phylogenetic treeterm and the length of its branchesterm), complete dated species-level phylogeniesterm for large taxonomic groups have only recently become available [26] . Early implementations of PD-based approaches were therefore unable to incorporate branch lengthterm·var data, and focused solely on measurements of branching pattern [4] . Second, PD removes the focus from species and so may lack wider tangible appeal to the public; conserving PD may be seen as less important than the protection of endemic or threatened species [16] . However, the current instability in species taxonomy [27] means that decisions based on PD might be more objective than those based on different species conceptsterm [13] , [16] , [27] . Combining species' conservation status with a measure of their contribution to PD is therefore desirable, because species can be retained as units but weighted appropriately [5] , [22] . This would generate a useful and transparent means for setting global priorities for species-based conservation [25] .

This paper describes a new method for measuring species' relative contributions to phylogenetic diversityterm [the ‘originalityterm’ of species: ref 24] . We explore the statistical properties of the resulting measure, which we call Evolutionary Distinctivenessterm (ED), and test its robustness to changing species conceptsterm. ED scoresterm are calculated for the Class Mammalia, and combined with values for species' extinction riskterm to generate a list of species that are both evolutionarily distinct and globally endangered (‘EDGE speciesterm’). The resultant list provides a set of priorities for mammalian conservation based not only on the likelihood that a species will be lost, but also on its irreplaceabilityterm.

Evolutionary Distinctivenessterm and its use in priority-setting In order to calculate ED scoresterm for each species, we divide the total phylogenetic diversityterm of a clade amongst its members. This is achieved by applying a value to each branch equal to its length divided by the number of species subtending the branchterm. The ED of a species is simply the sum of these valuesterm for all branches from which the species is descended, to the root of the phylogeny. For the examples in this paper, we have measured ED in units of time, such that each million years of evolution receives equal weighting and the branches terminate at the same point (i.e. the phylogeny is ultrametric). The method could be applied to non-ultrametric phylogenies if the conservation of other units [e.g. character diversity 28] , [29] was prioritised [although see ref 30] .

The basic procedure for calculating ED scoresterm is illustrated in figure 1 , which describes a clade of seven species (A–G). The ED scoreterm of species A is given by the sum of the ED scoresterm for each of the four branches between A and the root. The terminal branchterm contains just one species (A) and is 1 million years (MY) long, so receives a score of 1 MY. The next two branches are both 1 MY long and contain two and three species, so each daughter species (A, B and C) receives 1/2 and 1/3 MY respectively. The deepest branch that is ancestral to species A is 2 MY long and is shared among five species (A to E), so the total ED scoreterm for species A is given by (1/1+1/2+1/3+2/5) = 2.23 MY. Species B is the sister taxon of A, so receives the same score. By the same arithmetic, C has a score of (2/1+1/3+2/5) = 2.73 MY, both D and E receive (1/1+2/2+2/5) = 2.4 MY, and both F and G receive (0.5/1+4.5/2) = 2.75 MY. The example illustrates that ED is not solely determined by a species' unique PDterm (i.e. the length of the terminal branchterm). Species F and G are the top-ranked species based on their ED scoresterm, even though each represents just a small amount of unique evolutionary historyterm (0.5 MY). This suggests that the conservation of both F and G should be prioritised, because the extinction of either would leave a single descendant of the oldest and most unusual lineage in the phylogeny [c.f. 15] , [24] . The ED calculation is similar to the Equal Splits measureterm [25] , which apportions branch lengthterm·var equally among daughter clades, rather than among descendent species.

Hypothetical phylogeny of seven species (A–G) with Evolutionary Distinctivenessterm (ED) scores. Numbers above each branch indicate the length; numbers below show the number of descendent species. MYBP, millions of years before present.

In order to represent a useful tool in priority setting, ED scoresterm must be applicable in real phylogenies of large taxonomic groups. To do this, we modified the basic procedure described above to control for missing speciesterm, incomplete phylogenetic resolution and uncertainty in node agesterm (see Materials and Methods ). The approach is implemented using a dated phylogeny of the Class Mammalia that is nearly complete (>99%) at the species level [31] . We then combined ED and extinction riskterm to identify species that are both evolutionarily distinct and globally endangered (‘EDGE speciesterm’). We measured extinction riskterm using the quantitative and objective framework provided by the World Conservation Union (IUCN) Red List Categoriesterm [2] . We follow previous researchers in treating the Red List categoriesterm as intervals of extinction riskterm and by assuming equivalence among criteria [32] , [33] , [but see 34] . The resulting list of conservation priorities (‘EDGE scoresterm’) was calculated as follows: 1 where GEterm·def is the Red List category weightterm [Least Concern = 0, Near Threatened and Conservation Dependent = 1, Vulnerable = 2, Endangered = 3, Critically Endangered = 4, ref 32] , here representing extinction riskterm on a log scale. EDGE scoresterm are therefore equivalent to a log e -transformation of the species-specific expected loss of evolutionary historyterm [5] , [25] in which each increment of Red List categoryterm·var represents a doubling ( e ln(2) ) of extinction riskterm. For the purposes of these analyses, we did not calculate EDGE scoresterm for species listed as Extinct in the Wild (n = 4), domesticated populations of threatened species and 34 species (mostly of dubious taxonomic status) for which an evaluation has not been made.

Results Statistical properties of ED We measured ED in clades of different sizes to test whether ED scoresterm from different taxonomic groups are likely to be comparable. We found that most ED is derived from a few branches near the tips (i.e. those shared with few other species) and that virtually no ED is gained in clades above ∼180 species ( figure 2 ). Median ED in clades of 60 species is 88% of the total accumulated using the whole tree (n = 10, figure 2 ). Moreover, the rank order of ED scoresterm is unaffected by the size of the clade under consideration, except in very small clades and among species with low overall ED (i.e. few of the lines in figure 2 cross one another). These findings suggest that ED scoresterm of different taxonomic groups measured on separate phylogenies (i.e. with no nodes in common) will be comparable, so long as each phylogeny is larger than a threshold size. Based on the scaling observed in figure 2 , we suggest a minimum species richness of 100 as a useful rule of thumb to ensure comparability among taxa.

Scaling of ED scoresterm with clade sizeterm for ten Critically Endangered mammal species. ED scoresterm were calculated at each node between the tips and root for ten species in different orders. Species chosen are: the baiji ( Lipotes vexillifer ), sumatran rhino ( Dicerorhinus sumatrensis ), northern hairy-nosed wombat ( Lasiorhinus krefftii ), persian mole ( Talpa streeti ), Omiltemi rabbit ( Sylvilagus insonus ), Przewalski's gazelle ( Procapra przewalskii ), black-faced lion tamarin ( Leontopithecus caissara ), Livingstone's flying fox ( Pteropus livingstonii ), red wolf ( Canis rufus ) and northern Luzon shrew rat ( Crunomys fallax ). See Materials and Methods for further details.

Although most species (90% in figure 2 ) derive at least two-thirds of their total ED from the terminal branchterm (which is not shared with others), this branch lengthterm·var is a poor predictor of total ED (r 2 = 0.03 on a log-log scale). For species on short branches, there is an order of magnitude difference between the length of the terminal branchterm and ED. For example, the pale-throated and brown-throated three-toed sloths ( Bradypus tridactylus and B. variegatus ) share a common ancestor thought to be just over a million years old, but the total ED of both species is 20.4 MY ( Table S1 ) since they have few close living relatives.

ED scoresterm are also robust to taxonomic changes. For example, ED scoresterm in primates under the biological species conceptterm [35] are tightly correlated with ED scoresterm under the phylogenetic species conceptterm [36] (r 2 = 0.65 on a log-log scale), in spite of the fact that there are substantial differences between the two: the number of primate species differs by 50%. Furthermore, the highest-ranking species do not change their identity: 45 of 58 biological species in the upper quartile of ED scoresterm are also in the upper quartile as phylogenetic species. However, species that have been split into three or more species do tend to lose a large portion of their ED. For example, the fork-marked lemur ( Phaner furcifer ) is the second most distinct biological species of primate, with an ED scoreterm of 38.33. It was split into four phylogenetic species [36] with an ED scoreterm of 10.45 ( Table S2 ), which is just inside the upper quartile.

ED and EDGE scoresterm in mammals Mammal ED scoresterm range from 0.0582 MY (19 murid rodents) to 97.6 MY (duck-billed platypus, Ornithorhynchus anatinus ). Scores are approximately log-normally distributed, with a median of 7.86 MY and geometric meanterm of 6.28 MY.

Evolutionary Distinctivenessterm is not evenly distributed among the Red List categoriesterm. Least Concern species have significantly lower ED than the other categories (F 1,4180 = 26.3, p <0.0001, using log e transformed scores); there are no significant differences among the remaining categories. This suggests that species with low ED scoresterm tend to suffer from low levels of extinction riskterm, although the explanatory power of this model is extremely low (r 2 = 0.006).

EDGE scoresterm range from 0.0565 (10 murid rodents) to 6.48 (Yangtze River dolphin or baiji, Lipotes vexillifer ) and are approximately normally distributed around a mean of 2.63 (±0.017; figure 3 ). The 100 highest priority (EDGE) species includes several large-bodied and charismatic mammals, including the giant and lesser pandas, the orang-utan, African and Asian elephants, four rhinoceroses, two tapirs, two baleen whales, a dugong and a manatee. However, many smaller and less appreciated species also receive high priority, including sixteen rodents, thirteen eulipotyphlans, twelve bats, four lagomorphs and an elephant shrew ( Table S1 ). The top 100 also includes at least 37 species that would not qualify for most area-based definitions of endemism, since they are listed as threatened under Red List criterion A (reduction in population size) without qualifying for criteria B–D, which are based on population size or geographical range. Whilst the highest-ranked species, by definition, are all highly threatened (44 of the top 100 species are Critically Endangered, a further 47 are Endangered), threat status alone does not guarantee a high priority. For example, 10 Critically Endangered species (in the genera Gerbillus, Peromyscus and Crocidura ), as well as 32 Endangered species, fail to make the top 1000, whilst 130 Near Threatened species do.

Histogram of EDGE scoresterm for 4182 mammal species, by threat category. Colours indicate the Red List categoryterm·var: Least Concern (green), Near Threatened and Conservation Dependent (brown), Vulnerable (yellow), Endangered (orange) and Critically Endangered (red).

Discussion It is important that conservation priority-setting approaches are able to satisfy two conditions: they capture biodiversity and are robust to uncertainty. The method described herein satisfies the first condition because EDGE scoresterm incorporate species value (in terms of originalityterm, or irreplaceabilityterm) weighted by urgency of action (i.e. risk of extinction). Our approach satisfies the second condition because the scores are also robust to clade sizeterm, missing speciesterm and poor phylogenetic resolution. EDGE scoresterm are also easy to calculate, as all that is required is a set of Red List assessments and a near-complete phylogeny containing at least 100 species.

In particular, EDGE priorities are much less sensitive to taxonomic uncertaintyterm than alternate methods. The current trend towards the adoption of the phylogenetic species conceptterm among biologists [27] is likely to produce a large number of ‘new’ threatened and endemic species [37] , potentially altering the distribution of hotspots [38] and distorting other biodiversity patterns [27] . The EDGE approach is robust to such distortion because any increase in extinction riskterm due to splitting is balanced by a decrease in ED. A good example is that of the ruffed lemurs ( Varecia spp.), which consist of one Endangered biological species (ED = 19.8; EDGE = 5.11) or two phylogenetic species (Endangered and Critically Endangered; ED = 10.3; EDGE = 4.50 and 5.20). Using the same approach, we estimate that the long-beaked echidna ( Zaglossus bruijni ) would fall from the second-ranked priority to the 20 th after the addition of two new congeners [suggested by 39] . Thus, EDGE scoresterm for existing species are robust to the ongoing discovery of new species.

EDGE priorities are also robust to several other forms of uncertainty. Like all phylogenetic methods, the precise EDGE scoresterm are dependent on the topologyterm and branch lengthsterm of the phylogeny. However, errors in the phylogeny are unlikely to alter the identity of high-ranking species, particularly for clades of several hundred species. Topological uncertainty is usually expressed in supertrees as polytomiesterm, which are accounted for using simple correction factors. Likewise, branch lengthterm·var uncertainty has been incorporated into the scoring system to down-weight the priority of species descended from nodes with imprecisely estimated ages (see Materials and Methods ). These developments make it possible to estimate robustly the contribution to phylogenetic diversityterm of species in poorly known clades. The other major source of uncertainty is in estimating extinction riskterm: most recent changes in Red List categoryterm·var have come about through improvements in knowledge, rather than genuine changes in status [32] . EDGE scoresterm will inevitably be affected by future changes in extinction riskterm, although no more so than other approaches using the Red List categoriesterm.

A minority of mammal species could not be assigned EDGE scoresterm. Around 300 species are classified as Data Deficientterm and could not be meaningfully included, although in reality they may have a high risk of extinction [17] . By far the most likely candidate for high EDGE status following future Red List re-assessment is the franciscana or La Plata River dolphin Pontoporia blainvillei (ED = 36.3 MY). In addition, fifty extant species are missing from the phylogeny. The highest ranked of these are probably a pair of Critically Endangered shrews ( Sorex cansulus and S. kizlovi ); median and maximum ED scoresterm for the genus are 4.55 and 14.6 MY, giving potential respective EDGE scoresterm of 4.49 and 5.52 for these species (cf. figure 3 ). A further 260 species have been described since the chosen taxonomy was published [40] . Of these, the recently described Annamite striped rabbit Nesolagus timminsi [41] is the sister species to the tenth-ranked Sumatran rabbit N. netscheri , so would be a high priority if similarly threatened.

It has been suggested that species with few close relatives (i.e. high ED) are ‘relicts’ or ‘living fossils’ that have limited ability to generate novel diversity. This view implies that conservation efforts should instead be focused on recent radiations containing species with low ED scoresterm (e.g. murid rodents), which represent ‘cradles’ rather than ‘museums’ of diversity [e.g. 16] , [42] . However, the assumption that we are able to predict future evolutionary potential is dubious and no general relationships between phylogeny and diversity over geological time have yet been established [43] , [44] . Furthermore, phylogenetic diversityterm is clearly related to character diversity [30] , and so ED may be a useful predictor of divergent properties and hence potential utilitarian value [14] . Moreover, because species with low ED scoresterm tend to suffer from low levels of extinction riskterm, phylogenetic cradles of mammalian diversity are likely to survive the current extinction crisis even without specific interventions. Focusing on lower risk species, at the expense of EDGE priorities, would therefore result in a severe pruning of major branches of the Tree of Lifeterm comparable to that seen in previous mass extinction events [45] , [46] .

The top 100 EDGE speciesterm span all the major mammalian clades [being distributed among 18 orders and 52 families recognised by ref 35] and display a comparable range of morphological and ecological disparity, including the largest and smallest mammals, most of the world's freshwater cetaceans, an oviparous mammal and the only species capable of injecting venom using their teeth. However, around three-quarters of species-based mammal conservation projects are specifically aimed at charismatic megafaunaterm [47] , so conventional priority-setting toolsterm may not be sufficient to protect high priority EDGE speciesterm. This concern is supported by two additional lines of evidence. First, we found that species not found in protected areasterm [‘gap speciesterm’ defined by ref 48] tended to have higher EDGE scoresterm than those found inside protected areasterm (logistic regression: χ 2 1,3994 = 69.46, p<0.0001). Second, an assessment of published conservation strategies and recommendations (including IUCN Specialist Group Conservation Action Plans, captive breeding protocols and the wider scientific literature listed in the 1978–2005 Zoological Record database) reveals that no species-specific conservation actions have even been suggested for 42 of the top 100 EDGE speciesterm. Most of these species are from poorly known regions or taxonomic groups and until now have rarely been highlighted as conservation priorities. Little conservation action is actually being implemented for many other top EDGE speciesterm, despite frequent recommendations in the conservation literature. Indeed, the top-scoring EDGE speciesterm, the Yangtze River dolphin ( Lipotes vexillifer ), is now possibly the world's most threatened mammal despite two decades of debate over a potential ex situ breeding programme, and may number fewer than 13 surviving individuals [49] . The lack of conservation attention for priority EDGE speciesterm is a serious problem for mammalian biodiversity and suggests that large amounts of evolutionary historyterm are likely to be lost in the near future. This phenomenon of diversity slipping quietly towards extinction is likely to be much more severe in less charismatic groups than mammals.

The approach described in this paper can be used for conservation in a number of ways. First, conservation managers with limited resources at their disposal typically need to conserve populations of several threatened species. If all other factors were equal, the management of the most evolutionarily distinct species should be prioritized. Second, a list of high-priority species requiring urgent conservation action can be generated easily. In this paper, we have selected the 100 highest-ranking species, but one might equally choose all threatened (Vulnerable and above) species with above average ED. This would result in a list of 521 (using median) or 630 (using geometric meanterm) ‘EDGE speciesterm’ that are both evolutionarily distinct and globally endangered. Third, EDGE scoresterm could also be used to weight species' importance in selecting reserve networks, building on previous studies that have used phylogenetic diversityterm [50] – [52] or threatened species [11] to identify priority areas for conservation. The statistical properties of EDGE scoresterm (they are both normally-distributed and bounded at zero) make them especially suitable for these kinds of analysis. In this way, the EDGE approach is not an alternative to existing conservation frameworks [e.g. 6] but complements them.

The EDGE approach identifies the species representing most evolutionary historyterm from among those in imminent danger of extinction. Our methods extend the application of PD-based conservation to a wider range of taxa and situations than previous approaches [4] , [5] , [13] , [22] , [24] , [25] . Future work might incorporate socioeconomic considerationsterm [5] , [14] and the fact that a species' value depends also on the extinction riskterm of its close relatives [53] . However, our results suggest that large numbers of evolutionarily distinct species are inadequately served by existing conservation measures, and that more work is carried out to prevent the imminent loss of large quantities of our evolutionary heritageterm. It is hoped that this approach will serve to highlight their importance to biodiversity and emphasize the need for urgent conservation action.

Materials and Methods Implementing ED scoresterm for mammals We used a composite ‘supertree’ phylogenyterm [31] to calculate ED scoresterm for mammals. The supertree presents several challenges to the estimation of ED when compared with the (unknown) true phylogeny: poor resolution, missing speciesterm and uncertainty in node agesterm. Accordingly, we modified the basic procedure to control for these problems.

Phylogenetic information is poor in many mammalian clades (especially bats and rodents, which together make up >60% of species) and the whole supertree contains only 47% of all possible nodes, many of which are polytomiesterm (nodes with more than two daughter branches). Across the whole phylogeny, ∼40% of species are immediately descended from bifurcations, ∼20% from small polytomiesterm (3–5 daughters), ∼15% from medium-sized polytomiesterm (6–10 daughters) and the remainder from large polytomiesterm with >10 daughters. Polytomiesterm in supertrees result from poor or conflicting data rather than a true representation of the speciation process, so the distinctiveness of branches subtending them is overestimatedterm [54] , thus leading to biased ED scoresterm. For example, the common ancestor of species X, Y and Z is believed to be 1 MY old, but the branching pattern within the clade is unknown. The polytomy appears to show that each species represents 1 MY of unique evolutionary historyterm. In reality, the phylogeny is bifurcating, with one species aged 1 MY and the others sharing a more recent common ancestor. The bias induced by polytomiesterm can be corrected by estimating the expected ED of descendant species under an appropriate null model of diversification. We achieved this by applying a scaling factorterm based on the empirical distribution of ED scoresterm in a randomly generated phylogeny of 5000 species grown under constant rates of speciation (0.1) and extinction (0.08). The mean ED scoreterm of species in 819 clades of three species was 0.81 of the clade age; ED scoresterm for nodes of 2–20 species scale according to (branch lengthterm·var) * (1.081–0.267 * ln{d}), where d is the number of descendent branches (n = 2873 clades, r 2 = 0.69). Quantitatively similar values were obtained in bifurcating clades of primates [1.117–0.246 * ln{d}, n = 78, ref 55] and carnivores [1.139–0.269 * ln{d}, n = 101, ref 56] .

The mammal supertree contains 4510 of the 4548 (>99%) extant species listed in Wilson & Reeder [35] . Although few in number, the missing speciesterm need to be taken into account because their absenceterm will tend to inflate the ED scores of close relativesterm. For example, omitting species A from the phylogeny in figure 1 would elevate B from the joint lowest ranking species (with A) to the joint highest-ranking (with C), with an ED scoreterm of (2/1+1/2+2/4) = 3.5 MY. The problem is acute in real datasets since missing speciesterm tend not to be a random sample: 22 of the 38 missing mammals are from the genus Sorex . We account for this problem using a simple correction factor that allocates the missing speciesterm among their presumed closest relatives. For example, we correct for the omission of the bare-bellied hedgehog ( Hemiechinus nudiventris ) by treating the other five Hemiechinus spp. as 6/5 = 1.2 species, and we correct for the omission of both Cryptochloris species by spreading the two missing speciesterm evenly between other Chrysochloridae.

Variation among morphological and molecular estimates of divergence timesterm (node agesterm) can lead to considerable uncertainty in ED scoresterm. To reduce the effects of this uncertainty, we estimated ED using three sets of branch lengthsterm. One set was based on the best (i.e. mean) estimates of node ageterm; the others were derived from the upper and lower 95% confidence intervals around these dates. Species values of ED were calculated as the geometric meanterm of scores under the three sets of branch lengthsterm. The geometric meanterm was preferred since it down-weights speciesterm whose scores are based on nodes with symmetrical but wide confidence intervals in estimate age, and is therefore more conservative than the arithmetic mean.

Tests of robustness To test whether ED scoresterm are comparable among taxonomic groups, we examined how species' ED accumulates as progressively larger clades are considered. If ED scoresterm are truly comparable, their rank order will be independent of the size of the clade considered. We randomly selected one Critically Endangered species from each of ten mammal orders and measured the cumulative ED scoreterm at each node between the species and the root of the mammal supertree, thus redefining and enlarging the clade (and so increasing the number of species it contained) at each step.

Taxonomic changes have the potential to dramatically alter the ED scoresterm of individual species. Splitting a species in twoterm reduces the distinctiveness of all branches ancestral to the splitterm, particularly those near the tips. If ED scoresterm are highly sensitive to taxonomic changes then it may be meaningless to apply them in setting conservation priorities. The effects of taxonomic changes on ED scoresterm were therefore investigated in the primates, which have recently experienced considerable taxonomic inflation [27] . We compared primate ED scoresterm under a biological species conceptterm [35: 233 species] and a phylogenetic species conceptterm [36: 358 species] . We employed a single phylogeny [31] , but changed the number of species represented by each tip. We calculated the expected ED for multi-species tips by treating them as if they were descended from a polytomy of {n+r+1} descendent branches, where n is the actual number of descendent branches and r is the number of species represented by the tip.

Supporting Information Evolutionary Distinctivenessterm and EDGE scoresterm for mammals. This table shows Evolutionary Distinctivenessterm (ED) and EDGE scoresterm for all species included in the mammal supertree [31] ranked by their EDGE scoreterm. Species that could not be assigned EDGE scoresterm are appended to the bottom of the list, sorted by status and ED scoreterm. Species taxonomy follows Wilson & Reeder [35] . Red List categoriesterm follow the 2006 IUCN Red List [2] : CR = Critically Endangered, EN = Endangered, VU = Vulnerable, NT = Near Threatened, LC = Least Concern, CD = Conservation Dependent, DD = Data Deficientterm, NE = Not Evaluated. The NE category includes species in Wilson & Reeder [35] that could not be matched with any species or subspecies names in the Red List.

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Evolutionary Distinctivenessterm for primates under two species conceptsterm. This table lists ED scoresterm for primates under the biological species conceptterm i [.e. the taxonomy of ref 35] , the number of phylogenetic species into which the biological species was split [36] and the estimated ED scoreterm of each phylogenetic species. See Materials and Methods for further information. ED scoresterm are lower for phylogenetic species than biological species, even for taxa whose taxonomic status is the same under both concepts (i.e. the number of phylogenetic species is one). This occurs because the total number of species in the phylogeny is greater, so each receives a smaller share of the distinctiveness of ancestral branches. ED scoresterm were calculated using just one set of branch lengthsterm (the ‘best’ set), so differ from those in table S1 .

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