The scale of the ongoing biodiversity crisis requires both effective conservation prioritisation and urgent action. As extinction is non-random across the tree of life, it is important to prioritise threatened species which represent large amounts of evolutionary history. The EDGE metric prioritises species based on their Evolutionary Distinctiveness (ED), which measures the relative contribution of a species to the total evolutionary history of their taxonomic group, and Global Endangerment (GE), or extinction risk. EDGE prioritisations rely on adequate phylogenetic and extinction risk data to generate meaningful priorities for conservation. However, comprehensive phylogenetic trees of large taxonomic groups are extremely rare and, even when available, become quickly out-of-date due to the rapid rate of species descriptions and taxonomic revisions. Thus, it is important that conservationists can use the available data to incorporate evolutionary history into conservation prioritisation. We compared published and new methods to estimate missing ED scores for species absent from a phylogenetic tree whilst simultaneously correcting the ED scores of their close taxonomic relatives. We found that following artificial removal of species from a phylogenetic tree, the new method provided the closest estimates of their “true” ED score, differing from the true ED score by an average of less than 1%, compared to the 31% and 38% difference of the previous methods. The previous methods also substantially under- and over-estimated scores as more species were artificially removed from a phylogenetic tree. We therefore used the new method to estimate ED scores for all tetrapods. From these scores we updated EDGE prioritisation rankings for all tetrapod species with IUCN Red List assessments, including the first EDGE prioritisation for reptiles. Further, we identified criteria to identify robust priority species in an effort to further inform conservation action whilst limiting uncertainty and anticipating future phylogenetic advances.

Funding: RG is funded by the Natural Environment Research Council Science and Solutions for a Changing Planet Doctoral Training Programme (grant number NE/L002515/1), the CASE component of which is funded by the Zoological Society of London - https://www.imperial.ac.uk/grantham/education/science-and-solutions-for-achanging-planet-dtp/ . The Zoological Society of London paid the salary of NRO, ORW and CLG during the time period of the study - https://www.zsl.org/ . The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Introduction

We are currently in a period of unprecedented human-mediated biodiversity loss, often termed the ‘sixth mass extinction’ [1]. To achieve global commitments to halt the loss of biodiversity [2], the resources available for conservation must be targeted effectively. Several species-level conservation prioritisation schemes [3] have been developed, focussing on ‘charismatic’ species [4,5], threat levels [6], important ecosystem service providers [7], or some combination of these [8–11].

However, very few—if any—of these approaches explicitly focus on preserving unique evolutionary history, or Phylogenetic Diversity (PD) [12–14]. For a group of species comprising the extant descendants of a common ancestor (hereafter clade), the total PD of the clade is the sum of the lengths of the branches connecting all species on the phylogeny, and is measured in millions of years (Myr) [15,16]. Species with relatively few extant close relatives represent a disproportionate amount of the total PD of their clade [17]. Where these species are threatened with extinction, they often represent a significant amount of important functional trait diversity that could soon be lost [18,19].The conservation of functional trait diversity is important to maintain ecosystem functioning, the services provided by which—such as food production [20]—are vital to human survival [21–24].Therefore, current conservation prioritisation approaches that do not take PD into consideration may fail to prevent the loss of large amounts of both phylogenetic and functional trait diversity [13,19,25–27]. To date, several metrics have been proposed to integrate PD into the prioritisation of species and regions [12,17,28–31].

A number of these metrics measure the contribution of individual species to the total PD of a clade [32–37], and the Evolutionary Distinctiveness (ED) metric has received the most widespread use [12,14,17,38–43]. Whereas PD is the sum of all branch lengths of a phylogeny, ED is the ‘fair proportion’ of the total PD assigned to an individual species [35], with the length of each branch of the phylogeny divided equally amongst all species to which it is ancestral (see original formulation [12] for detailed description). This partitioning of PD amongst species facilitates prioritisation at the species, rather than clade, level.

In conjunction with any PD prioritisation, conservation actions must also be timely. Many species are at imminent risk of extinction, and those that are under greatest threat are widely considered to be the highest priority for immediate action. The EDGE metric, which combines the ED of a species with its extinction risk—or ‘Global Endangerment’ (GE) [12], has been implemented by the EDGE of Existence programme at the Zoological Society of London to prioritise species in a number of taxonomic groups (mammals [12,26], amphibians [38], birds [17], and corals [44]). The EDGE of Existence programme is the only global conservation initiative to focus on threatened species representing a significant amount of unique evolutionary history, raising awareness of these often poorly known species, and actively supporting conservation activities [45]. Research has shown the EDGE metric has the potential to not only preserve more PD than expected [19], but also preserve more functional trait diversity than expected if conserving threatened species without considering PD [18,19,27].

However, meaningful and credible prioritisation for conservation depends on the quality of data available. Metrics such as ED ideally require species-level phylogenies to calculate the individual contribution of each species to the total PD of a clade [12,40], yet no phylogeny exists that contains all known species of any tetrapod class. There are little, if any, genetic data available for many poorly-known species, precluding their inclusion in most phylogenetic analyses. In addition, given the high rate of tetrapod species descriptions, species-level phylogenies quickly become out of date; for example, almost 400 species were missing from the mammalian supertree [46] less than four years following publication [26]. Even though the exact phylogenetic position of these “missing species” is not known, in most cases they can be assigned to genus or family [44,47,48]. This provides an opportunity for their ED scores to be estimated based on the ED scores of congeneric or confamilial species.

The phylogenies currently available also have notable limitations. Of the tetrapods (amphibians, birds, mammals and reptiles), amphibians and testudines (turtles and tortoises) suffer from particularly poor phylogenetic coverage [49–52], reflecting the relatively low research investment in these taxa compared to birds and mammals [53–55]. For example, at the time of writing the largest published amphibian genetic phylogeny [49] omits more than 3,600 species (50% of known species). Recent species-level phylogenies published for birds [56], mammals [46,57,58], and squamates [43] represent advances in phylogenetic coverage for these groups, but many species are still missing (~1,000 birds, ~500 mammals, ~200 squamates respectively).

To overcome the paucity of genetic data, many incomplete genetic phylogenies are now combined with taxonomic information to infer phylogenetic relationships for species lacking available genetic data [48,56,59]. These phylogenies constrain missing species to regions of the tree to which they are thought to belong (e.g. within their family or genus) and are inherently uncertain. Typical phylogenetic reconstruction methods use various approaches to select a single, optimal phylogeny (numerous reviews are available covering the merits and limitations of the various phylogenetic reconstruction techniques, e.g.[60–62]). However, the taxonomically-augmented phylogenies generated for birds and squamates require the creation of a large distribution of equally likely phylogenetic trees, rather than a single consensus phylogeny, in an attempt to capture the uncertainty around the placement of missing species and their taxonomically-inferred relationships [48,59]. The reliance on taxonomic data to augment genetic phylogenies means they are susceptible to significant changes due to taxonomic revisions and more comprehensive genetic sampling [48,58,59]. See Rabosky 2015 [59] for a detailed review of the limitations when using taxonomically-augmented phylogenies for downstream analyses.

The uncertainty in available phylogenies must be accounted for and acknowledged when developing conservation priorities. Given the imminent biodiversity crisis [1], it is impractical and undesirable for conservationists to wait for completely inclusive phylogenies to be published before implementing PD-based conservation efforts [26]. We therefore required a reliable method for incorporating all known species when using incomplete or out-of-date phylogenies.

Two methods have previously been employed to estimate ED for species missing from phylogenies from their relatives in the phylogeny (hereafter ‘imputation methods’) [12,26,44], though the relative performance of these methods has not yet been examined. Here, we compare the accuracy of both of the existing imputation methods with that of a third, novel method when estimating ED scores for missing species. We show empirically that the ED, and also EDGE rank, of missing species can be accurately predicted from other species in the phylogeny using our new method. This produces a robust set of priority species, and deals effectively with the uncertainty inherent in phylogenetic data. Finally, we use the statistical imputation of ED scores to produce updated EDGE priority lists for all tetrapods, including the first EDGE list for reptiles.