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Phylogenetic diversity in conservation: A brief history, critical overview, and challenges to progress

Published online by Cambridge University Press:  27 March 2023

Marcel Cardillo*
Affiliation:
Macroevolution and Macroecology Group, Research School of Biology, Australian National University, Canberra, ACT, Australia
*
Corresponding author: Marcel Cardillo; Email: marcel.cardillo@anu.edu.au
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Abstract

Species that are evolutionarily distinct have long been valued for their unique and irreplaceable contribution to biodiversity. About 30 years ago, this idea was extended to the concept of phylogenetic diversity (PD): a quantitative, continuous-scale index of conservation value for a set of species, calculated by summing the phylogenetic branch lengths that connect them. This way of capturing evolutionary history has opened new opportunities for analysis, and has therefore generated a huge academic literature, but to date has had only limited impact on conservation practice or policy. In this review, I present a brief historical overview of PD research. I then examine the empirical evidence for the primary rationale of PD that it is the best proxy for “feature diversity,” which includes both known and unknown phenotypic characters, contributing to utilitarian value, ecosystem function, future resilience, and evolutionary potential. Surprisingly, it is only relatively recently that this rationale has been subject to systematic empirical scrutiny, and to date, there are mixed results on the connection between PD and phenotypic diversity. Finally, I examine the least well-studied, but potentially greatest challenge for PD: its dependence on the reliability of phylogenetic inference itself. The very few studies that have investigated this so far show that the ranking of species assemblages by their PD values can vary substantially under alternative, routine, phylogenetic methods and assumptions. If PD is to become more widely adopted into conservation decision-making, it will be important to better understand the conditions under which it performs well, and those under which it performs poorly.

Type
Review
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Creative Common License - CCCreative Common License - BY
This is an Open Access article, distributed under the terms of the Creative Commons Attribution licence (http://creativecommons.org/licenses/by/4.0), which permits unrestricted re-use, distribution and reproduction, provided the original article is properly cited.
Copyright
© The Author(s), 2023. Published by Cambridge University Press

Impact statement

The concept of quantifying evolutionary history of assemblages of species, as a way of assessing the biodiversity value of different areas, has been advocated for the past 30 years. A large academic literature has developed, that applies evolutionary history (most frequently phylogenetic diversity, or PD) in a variety of ways to conservation problems. However, very little of this literature has examined PD from a critical perspective, and there is mixed evidence about whether PD reliably represents the biodiversity qualities that we expect it to. This review aims to summarize recent research that has begun to examine the rationale for PD empirically, and highlight the challenges that will need to be overcome for PD to become more widely adopted into conservation practice.

Introduction

Species are the primary currency of conservation, despite the inconsistency of species concepts, the ambiguity and taxonomic instability of many species, or the lack of a strong theoretical justification (Maclaurin and Sterelny, Reference Maclaurin and Sterelny2008). We mourn the loss of a species far more than the population decline that precedes it. The death of the last known individual of a species is considered a mark of humanity’s failure to safeguard biodiversity, even if that species had long since ceased playing a functional role in its ecosystem. Yet species are not all considered equal contributors to what we value about biodiversity. Large species tend to be more highly valued than small ones, mammals more than other vertebrates, primates and carnivores more than rodents (R.M. May noted, “As we move from the furries and featheries, down through the innumerable species of insects, and on down to bacteria and viruses, sentimental concern does not merely wane. It changes sign.”). And species that are evolutionarily distinct, with few close living relatives, are often regarded as more worthy of protection than those that are less evolutionarily distinct, with many close relatives to which they are genetically and phenotypically similar.

Some species are known to be the only representative of a higher taxon, a Family or even an Order, perhaps one that was more diverse in past ages (Figure 1). The ancestral lineage of these species may have diverged from that of their closest living relatives tens or hundreds of millions of years ago. The Albany Pitcher Plant (Cephalotus follicularis), for example, is the only species of its family (Cephalotaceae) and represents an origin of plant carnivory that is independent of that in other plant lineages from which it diverged in the mid-Cretaceous Period, over 100 million years ago. The Ganges and Indus River Dolphins (Platanista gangetica and P. minor) are the only species remaining in the once-diverse and geographically widespread family Platanistidae, of which six extinct genera are known from Miocene fossils. More widely known examples of evolutionarily distinct species include Welwitschia mirabilis, a gymnosperm endemic to the Namib Desert and the only species in the Order Welwitschiales; and the Coelacanths (Latimeria), the two surviving species of lobe-finned fish in the Order Actinistia.

Figure 1. Evolutionarily distinct species have long been valued for their unique and irreplaceable contribution to biodiversity. Left: Albany Pitcher Plant, Cephalotus follicularis (source: https://www.flickr.com/photos/7326810@N08/1555479035/in/photostream/ Attribution 2.0 Generic CC BY 2.0); Top right: African Coelacanth, Latimeria chalumnae (source: https://www.the-scientist.com/news-opinion/african-coelacanths-may-live-to-be-100-study-68911); Bottom right: Welwitschia mirabilis (source: https://commons.wikimedia.org/wiki/File:Welwitschia_mirabilis,_m%C3%A4nnl._Bl%C3%BCte,_Namibw%C3%BCste,Namibia.jpg Attribution-ShareAlike 3.0 Unported CC BY-SA 3.0).

The extinction of one of these evolutionarily distinct species would represent the loss of a unique and irreplaceable contribution to biodiversity. For this reason, species such as these have long been singled out for special conservation attention. In the past three decades, however, the traditional qualitative value afforded to particular evolutionarily distinct species has given rise to a more quantitative conception of evolutionary history in the context of conservation. This is expressed most commonly in the concept of “phylogenetic diversity” (PD). Essentially, PD amounts to the use of phylogenetic branch lengths as a continuous-scale index of conservation value for a set of taxa. The focus of this review is on PD, rather than single-species measures of evolutionary distinctness. This is because the extension of evolutionary history value from individual species to assemblages brought with it new assumptions and a new kind of rationale that may be less intuitively obvious to many people compared to the rationale for protecting individual species. The theoretical justification for PD and its claims to primacy as the currency of conservation have been given detailed treatment in recent years by philosophers (Maclaurin and Sterelny, Reference Maclaurin and Sterelny2008; Lean and Maclaurin, Reference Lean, Maclaurin, Pellens and Grandcolas2016), so I will touch only briefly on this aspect to provide context and background. I will not attempt to review exhaustively the extensive empirical literature on PD, which has been methodically summarized by Tucker et al. (Reference Tucker, Aze, Cadotte, Cantalapiedra, Chisholm, Díaz, Grenyer, Huang, Mazel, Pearse, Pennell, Winter and Mooers2019). Rather, after presenting a brief historical overview of PD research, I will focus on several questions that help to clarify the current position of PD within conservation biology and are important for the future of PD in conservation practice. How much empirical support is there for the claims made by the advocates of PD in conservation? In particular, I ask if (1) PD serves as a reliable indicator of phenotypic diversity; and (2) PD can be quantified consistently or reliably in the face of the variability, uncertainty, and arbitrary choices that characterize methods for estimating phylogenetic branch lengths.

Origins of the PD concept

Two seminal papers in the early 1990s mark the onset of a rapid rise in popularity of PD among conservation researchers. Among the first to suggest that phylogeny can be used to avoid treating all species as equal in measures of diversity were (Vane-Wright et al., Reference Vane-Wright, Humphries and Williams1991). Their measure of “taxonomic distinctness” was based on the cladistic information content of a cladogram: that is, the number of monophyletic groups (clades) in which each taxon can be placed, with a higher value for taxa with a more limited clade membership portfolio. In many phylogenetic trees, such taxa often belong to “basal” or early branching lineages. Vane-Wright et al. (Reference Vane-Wright, Humphries and Williams1991) showed how taxonomic distinctness weights might be used in complementarity-based algorithms to select priority areas for conservation that maximize the amount of evolutionary history represented by a given number of taxa protected within reserves.

Soon after, Faith (Reference Faith1992) presented PD: a measure of diversity in which taxa are weighted by the number of character-state changes along branches of a phylogeny. The PD for a set of taxa is simply the sum of the number of character changes (or the branch lengths) in the “minimum spanning tree” formed by those taxa and the phylogenetic branches that connect them (Figure 2). The key difference between PD and Vane-Wright et al.’s taxonomic diversity was that the amount of evolutionary change along branches, including the evolution of convergent characters (those that arose independently on several lineages) contributes to the PD value. For taxonomic diversity, the only characters that determine the value of the metric (implicitly) are the shared derived characters that define monophyletic clades. A number of alternative ways of quantifying evolutionary history, both for individual and multiple taxa, have been proposed over the years (e.g., Redding et al., Reference Redding, Hartmann, Mimoto, Bokal, DeVos and Mooers2008; Chao et al., Reference Chao, Chiu and Jost2010; Faith, Reference Faith2016), but Faith’s original PD measure is the one that has gained the most traction. Of course, in the years since the original PD paper was published, genomic data has taken over from phenotypic characters as the primary basis for inferring phylogeny, but PD can be calculated equally well from molecular branch lengths, whether in units of evolutionary change or of time.

Figure 2. Calculation of Faith’s phylogenetic diversity (PD) for a set of species g1–g6. PD is the sum of the branch lengths (indicated here by the division of branches into intervals) along the shortest paths connecting the set of species. The panel in the center shows how a small subset of species can capture a large proportion of the evolutionary history of the whole group (left panel), if the paths connecting them traverse the root of the phylogeny. In the panel on the right, a different set of three species has a much lower PD score because they are more closely related to one another. Source: Rodrigues and Gaston (Reference Rodrigues and Gaston2002).

The rationale for PD

It has been argued that evolutionarily distinct species (and biodiversity more generally) have intrinsic value; that is, a value in and of themselves that is independent of any rational agent doing the valuing, but this justification for biodiversity conservation has philosophical difficulties (Maclaurin and Sterelny, Reference Maclaurin and Sterelny2008; Lean and Maclaurin, Reference Lean, Maclaurin, Pellens and Grandcolas2016). In my view, the traditional regard for evolutionarily distinct species as being worth conserving is closer to what McNeely et al. (Reference McNeely, Miller, Reid, Mittermeier and Werner1990) called “existence value”: many people are happy knowing that such species exist, and would feel some kind of loss on an emotional level if they went extinct. The rationale for PD, on the other hand, has always tended to emphasize the instrumental, or utilitarian, values, of biodiversity. From the outset, PD was intended to be an indicator of “feature diversity”: the diversity of phenotypic characters (both known and unknown) represented by a set of species, which is the real target of conservation (Faith, Reference Faith1992).

Why is it considered desirable to conserve feature diversity? There are two basic arguments. The first is that maintaining enough phenotypic or ecological diversity allows ecological communities and ecosystems to continue to function and cope with changing and uncertain future conditions (Faith, Reference Faith1992, Reference Faith2016). A similar idea applied to intraspecific populations is that conserving genetic diversity, in particular adaptive genetic variation, is a means of maintaining adaptive evolutionary potential, which is regarded as critical for the resilience of populations to rapid environmental change (Moritz, Reference Moritz2002; Sgrò et al., Reference Sgrò, Lowe and Hoffmann2011). The second argument for conserving feature diversity is that it maximizes the utilitarian values of biodiversity, economic or otherwise. This includes values that can be “cashed in” immediately (demand value), but it also includes those values that are yet to be realized, or may not yet have been discovered. A frequent example provided for the latter is the future financial value of pharmacologically useful compounds that are likely to be discovered through bioprospecting (Crozier, Reference Crozier1997). Under both of these arguments, conserving maximum feature diversity increases “option value”: this is the additional value placed on a sample of biodiversity, over and above its immediate demand value, that derives from having the option of reaping future benefit left open (Maclaurin and Sterelny, Reference Maclaurin and Sterelny2008; Lean and Maclaurin, Reference Lean, Maclaurin, Pellens and Grandcolas2016).

The popularity of PD in academic studies

Academic interest in PD has flourished since the early 1990s, and it is worth a brief examination of the reasons for this. Firstly, perhaps, the rationale is compelling: there is an intuitive logic to the idea that if we have to choose between species to conserve (which we do, given the ubiquitous shortfall in conservation funding), then all else being equal, the ones that capture more evolutionary history ought be prioritized. Secondly, the concept itself is simple and quite elegant. The idea of summing branch lengths to represent the amount of evolutionary history captured by a set of species is just as intuitively easy to grasp as many other measures of diversity. PD is computationally undemanding to calculate, provided a representation of phylogeny is already available. The growing popularity of the R language has brought about an increased fluency in handling and analyzing phylogenetic data among ecology and conservation researchers. Tools provided in R packages such as APE and Picante have made it a simple matter to calculate PD and incorporate it into a wide range of analyses. The timing was probably also important: PD was introduced at a time when all things phylogenetic were being adopted into the mainstream of evolution and ecology research, driven by interest in phylogenetically informed comparative methods (Harvey and Pagel, Reference Harvey and Pagel1991), new macroevolutionary models (Nee et al., Reference Nee, Mooers and Harvey1992), and the integration of phylogeny into community ecology (Brooks et al., Reference Brooks, McLennan and McLennan1991; Haydon et al., Reference Haydon, Radtkey, Pianka, Ricklefs and Schluter1993). During the 1990s, the publication of molecular phylogenies increased rapidly, providing abundant new raw material for the calculation of PD and exploration of its patterns and nuances.

An overview of analyses of PD patterns

In the first decade after the introduction of PD, a major focus of interest was the effect of species extinctions on the loss of evolutionary history. Many of these studies focused on clade-level patterns (either hypothetical or real clades), rather than spatial patterns. One of the earliest of these studies showed that for a given proportion of species lost, a smaller proportion of the clade’s total branch length is lost, so that conserving a modest proportion of species should, in principle, protect much of a clade’s evolutionary history (Nee and May, Reference Nee and May1997). However, the relative amount of evolutionary history lost when species go extinct increases when there is substantial imbalance in the phylogeny, the legacy of heterogeneous speciation and extinction rates (Nee and May, Reference Nee and May1997; Purvis et al., Reference Purvis, Agapow, Gittleman and Mace2000; von Euler, Reference von Euler2001; Vamosi and Wilson, Reference Vamosi and Wilson2008). The amount of evolutionary history lost increases further still when species extinctions are phylogenetically nonrandom – which is a reasonable expectation, given that currently threatened species are more likely to be found in some higher taxa than others (Purvis et al., Reference Purvis, Agapow, Gittleman and Mace2000, von Euler, Reference von Euler2001, Vamosi and Wilson, Reference Vamosi and Wilson2008). All of these studies were couched in terms of conservation priorities, although none aimed to make specific or direct recommendations for conservation planning and management. They are what Cardillo and Meijaard (Reference Cardillo and Meijaard2012) termed “call to arms” studies that aimed primarily to draw attention to the consequences of the extinction crisis for the erosion of biodiversity at large scales.

These clade-level patterns were soon extended to spatial analyses of geographic assemblages, which aimed to connect PD more closely with practical conservation decision-making, in the way originally envisaged by Vane-Wright et al. (Reference Vane-Wright, Humphries and Williams1991) and Faith (Reference Faith1992). At large geographic scales, spatial patterns of PD are shaped by the history of speciation and extinction in different regions (Davies et al., Reference Davies, Fritz, Grenyer, Orme, Bielby, Bininda-Emonds, Cardillo, Jones, Gittleman, Mace and Purvis2008; Warren et al., Reference Warren, Cardillo, Rosauer and Bolnick2014). While measures of evolutionary history are generally correlated with species richness, the two do not always align closely and regions of highest aggregate evolutionary history can be very different from regions of highest species richness (Safi et al., Reference Safi, Cianciaruso, Loyola, Brito, Armour-Marshall and Diniz-Filho2011; Fritz et al., Reference Fritz, Rahbek and Linder2012; Honorio Coronado et al., Reference Honorio Coronado, Dexter, Pennington, Chave, Lewis, Alexiades, Alvarez, de Oliveira, Amaral and Araujo‐Murakami2015; Voskamp et al., Reference Voskamp, Baker, Stephens, Valdes and Willis2017; Rapacciuolo et al., Reference Rapacciuolo, Graham, Marin, Behm, Costa, Hedges, Helmus, Radeloff, Young and Brooks2019; Hu et al., Reference Hu, Fan, Chen, Chang, Zhan, Wu, Zhang, Wang, Zhang, Yang, Hou, Shen, Pan, Wu, Li, Hu and Wei2021). A common practice has been to map the component of variation in an evolutionary history measure that is independent of species richness, for example by using regression residuals or values that are standardized against a null model (Davies et al., Reference Davies, Fritz, Grenyer, Orme, Bielby, Bininda-Emonds, Cardillo, Jones, Gittleman, Mace and Purvis2008; Safi et al., Reference Safi, Cianciaruso, Loyola, Brito, Armour-Marshall and Diniz-Filho2011; Fritz et al., Reference Fritz, Rahbek and Linder2012; Honorio Coronado et al., Reference Honorio Coronado, Dexter, Pennington, Chave, Lewis, Alexiades, Alvarez, de Oliveira, Amaral and Araujo‐Murakami2015; Carvalho et al., Reference Carvalho, Velo-Antón, Tarroso, Portela, Barata, Carranza, Moritz and Possingham2017; Voskamp et al., Reference Voskamp, Baker, Stephens, Valdes and Willis2017; Rapacciuolo et al., Reference Rapacciuolo, Graham, Marin, Behm, Costa, Hedges, Helmus, Radeloff, Young and Brooks2019; Gumbs et al., Reference Gumbs, Gray, Böhm, Hoffmann, Grenyer, Jetz, Meiri, Roll, Owen and Rosindell2020; Hu et al., Reference Hu, Fan, Chen, Chang, Zhan, Wu, Zhang, Wang, Zhang, Yang, Hou, Shen, Pan, Wu, Li, Hu and Wei2021). However, the spatial patterns that result from this can be hard to interpret, because they are often heterogeneous or fragmented, or do not correspond in an obvious way to major climatic or biogeographic zones. It is also difficult to know what such patterns mean from a conservation perspective. Should regions of high PD relative to species richness be afforded higher value than regions of high total PD?

Some of the attempts to use large-scale spatial patterns of PD or other evolutionary history measures to guide conservation decisions have taken a gap analysis approach, by asking whether the existing network of protected areas adequately captures PD for a given taxon. In this way, gaps in the protected area network can be identified and recommended as priority areas for future expansion of the network, although there is rarely any objective way of deciding on an “adequate” level of coverage. At a global scale, these kinds of studies have revealed that a high proportion of the priority conservation areas for terrestrial vertebrate and angiosperm PD are unrepresented within current protected areas (Daru et al., Reference Daru, le Roux, Gopalraj, Park, Holt and Greve2019; Robuchon et al., Reference Robuchon, Pavoine, Véron, Delli, Faith, Mandrici, Pellens, Dubois and Leroy2021). At regional scales, the results have been more case-specific, with some studies finding that PD is relatively well-represented within protected areas (Quan et al., Reference Quan, Che, Wu, Wu, Zhang, Zhang and Zou2018; Aguilar-Tomasini et al., Reference Aguilar-Tomasini, Martin and Speed2021; Llorente-Culebras et al., Reference Llorente-Culebras, Molina-Venegas, Barbosa, Carvalho, Rodríguez and Santos2021), and others finding that it is not (McCarthy and Pollock, Reference McCarthy and Pollock2016; Franke et al., Reference Franke, Brandl, Heibl, Mattivi, Müller, Pinkert and Thorn2020; Oliveira et al., Reference Oliveira, Peláez and Agostinho2021).

When the configuration of priority conservation areas needs to be optimized in the face of cost constraints, the “hotspot” approach of simply skimming off areas of highest diversity for protection is not a very efficient way to meet predefined conservation targets (Balmford and Gaston, Reference Balmford and Gaston1999; Margules and Pressey, Reference Margules and Pressey2000). For this reason, the past 20 years have seen the development of a substantial literature on the use of complementarity-based algorithms (which focus on marginal gains rather than hotspots) to select priority areas for PD conservation. This application of evolutionary history measures was discussed by Vane-Wright et al. (Reference Vane-Wright, Humphries and Williams1991) and Faith (Reference Faith1992), but it took some years before both phylogenetic data and computing power were sufficient to solve optimization problems involving PD (Rodrigues and Gaston, Reference Rodrigues and Gaston2002). The question most frequently asked by these studies is how closely priority areas selected using taxonomic richness criteria coincide with those selected using evolutionary history. Again, the answers seem to be mixed and case-specific. Some studies have found that species or higher-taxon richness are a good surrogate for PD and there is a high degree of overlap in priority areas selected under both criteria (Rodrigues and Gaston, Reference Rodrigues and Gaston2002; Strecker et al., Reference Strecker, Olden, Whittier and Paukert2011; Pollock et al., Reference Pollock, Rosauer, Thornhill, Kujala, Crisp, Miller and McCarthy2015; Pollock et al., Reference Pollock, Thuiller and Jetz2017; Rapacciuolo et al., Reference Rapacciuolo, Graham, Marin, Behm, Costa, Hedges, Helmus, Radeloff, Young and Brooks2019). Others have found that richness-based and PD-based priority areas differ substantially, so that a focus on protecting maximum taxonomic richness does not adequately protect evolutionary history (Forest et al., Reference Forest, Grenyer, Rouget, Davies, Cowling, Faith, Balmford, Manning, Procheş, Bank, Reeves, Hedderson and Savolainen2007; Pio et al., Reference Pio, Broennimann, Barraclough, Reeves, Rebelo, Thuiller, Guisan and Salamin2011; Carvalho et al., Reference Carvalho, Velo-Antón, Tarroso, Portela, Barata, Carranza, Moritz and Possingham2017).

How well does PD predict feature diversity and biodiversity values?

The vast majority of studies involving PD have focused on analyzing patterns of PD, rather than testing the basic assumptions that PD represents feature diversity, and that feature diversity represents utilitarian value, ecosystem function, or evolutionary resilience and potential. It is only fairly recently that some studies have begun to take a critical look at the empirical support for these assumptions (e.g., Kelly et al., Reference Kelly, Grenyer and Scotland2014; Mazel et al., Reference Mazel, Mooers, Riva and Pennell2017; Tucker et al., Reference Tucker, Davies, Cadotte and Pearse2018, Reference Tucker, Aze, Cadotte, Cantalapiedra, Chisholm, Díaz, Grenyer, Huang, Mazel, Pearse, Pennell, Winter and Mooers2019). One difficulty with evaluating the results of these analyses is that in the PD literature, there has been little clarity or consistency in the definition of feature diversity. Many studies seem to use the terms “feature diversity” and “functional diversity” (FD) synonymously, but Owen et al. (Reference Owen, Gumbs, Gray and Faith2019) caution against this, arguing that the two concepts are distinct and should not be conflated. In their view, feature diversity encompasses all of the diversity of traits – both known and unknown – possessed by a set of species, while FD is a more narrowly defined subset of feature diversity, based only on traits that have ecological function. For this reason, Owen et al. argue that recent tests of relationships between PD and FD (e.g., Mazel et al.,Reference Mazel, Pennell, Cadotte, Diaz, Riva, Grenyer, Leprieur, Mooers, Mouillot, Tucker and Pearse2018a) do not, in fact, test the ability of PD to act as a proxy for feature diversity. This raises the question of whether feature diversity, defined in this way, can be regarded as a scientifically tractable concept. It means that any empirical test of the relationship between PD and any aspect of phenotypic diversity potentially could be dismissed as not having adequately tested the concept of feature diversity, which by definition is unable to be quantified.

On the other hand, Tucker et al. (Reference Tucker, Aze, Cadotte, Cantalapiedra, Chisholm, Díaz, Grenyer, Huang, Mazel, Pearse, Pennell, Winter and Mooers2019) describe a more tractable conception of phenotypic diversity that prevails in the ecological literature, as the range of values of any measurable trait. Tucker et al. (Reference Tucker, Davies, Cadotte and Pearse2018) adopt a pragmatic working definition of phenotypic diversity as “the variation in all ecological or functional traits, which includes a wide variety of physiological, phenological, morphological, and behavioral measures,” which they refer to as “FD” to align with the general use of this term in the ecological literature. The advantages of this definition are that phenotypic diversity is measurable and thus testable, and expected associations between phylogenetic and phenotypic diversity can be derived from macroevolutionary models. In the following discussion, I will follow Tucker et al and use “FD” to represent all conceptions of phenotypic diversity that commonly appear in the PD literature, while acknowledging that these may not properly represent feature diversity in its strict sense.

Studies of the links between PD and FD can be divided into two basic kinds: those that deal with phylogeny-based patterns, and those that deal with area-based patterns. The expectation that PD and FD should be correlated on a phylogeny follows from basic models of trait evolution. The simplest evolutionary model for continuous traits is Brownian Motion, which describes independent, random, nondirectional and unbounded drift in trait values along the branches of a phylogeny. The degree to which the variance in trait values among the tips of a phylogeny, given the lengths of the branches separating them, is consistent with a Brownian Motion model is known as phylogenetic signal. Many species traits (ecological, morphological, physiological, or otherwise) show phylogenetic signal, although it varies in strength among traits and among taxa (Freckleton et al., Reference Freckleton, Harvey and Pagel2002; Blomberg et al., Reference Blomberg, Garland and Ives2003). This fact suggests that phylogenetic distance among taxa should often correlate positively with trait distance.

However, this does not necessarily mean that PD will usually be a better predictor of FD than species richness, or that a subset of taxa chosen from a phylogeny to maximize PD will also maximize FD. The processes and history of trait evolution can be complex, and Brownian Motion is not always the model most consistent with the data. A trait may be subject to fitness constraints on extreme values; the speed of trait evolution may have varied through time, as a result of adaptive radiation or changing selective regimes; and the speed of trait evolution may have varied among lineages across different parts of the phylogeny. The different processes and patterns of trait evolution affect the PD–FD relationship. The correlation is predicted to be weaker, for example, when traits have evolved under an early burst model (faster evolutionary rates earlier in a clade’s diversification) compared to a Brownian Motion model, in which rates are homogeneous through time (Tucker et al., Reference Tucker, Davies, Cadotte and Pearse2018). Simulations and meta-analysis of real datasets have both revealed that positive correlations between phylogenetic and functional distance tend to be restricted to relatively short distances on phylogenies, an effect that becomes more marked as the degree of homoplasy increases (Kelly et al., Reference Kelly, Grenyer and Scotland2014). This means that as sets of taxa are expanded to include increasingly distant relatives, the capacity of PD to serve as a proxy for FD declines. Furthermore, because a subset of species that maximizes PD is usually distributed nonrandomly on the phylogeny, it can be possible for the maximum-PD set to be a worse predictor of FD than a random set of species (Mazel et al., Reference Mazel, Mooers, Riva and Pennell2017).

Perhaps more relevant to conservation planning are area-based patterns: correlations between PD and FD, or congruence between the maximum PD set and the maximum FD set, across geographically defined assemblages. In many case studies, there is a high degree of correlation between PD and measures of FD across assemblages, but because both are highly correlated with species richness it is difficult to infer a strong, direct association. This was demonstrated explicitly in a study of the spatial distribution of PD, FD and species richness of plant assemblages in the Pyrenees (Pardo et al., Reference Pardo, Roquet, Lavergne, Olesen, Gómez and García2017). In this study, there is a high degree of correlation among these three facets of diversity, with PD and species richness equally strongly associated with FD. However, the association between PD and FD largely disappears when the co-association with species richness is accounted for by calculating richness-independent measures of PD and FD.

On the other hand, results of some studies suggest that PD can serve as a useful proxy for diversity of phenotypic traits, including traits with utilitarian value. For the flora of South Africa’s Cape region, Forest et al. (Reference Forest, Grenyer, Rouget, Davies, Cowling, Faith, Balmford, Manning, Procheş, Bank, Reeves, Hedderson and Savolainen2007) showed that not only does prioritizing PD lead to different conservation decisions than prioritizing taxon richness, but PD does a better job of predicting the distribution of plants with economic or medicinal utility. On a global scale, Molina-Venegas et al. (Reference Molina-Venegas, Rodríguez, Pardo-de-Santayana, Ronquillo and Mabberley2021) also found that PD captures a greater range of recorded economic values associated with plant taxa, compared to randomly selected taxa. This was not a spatial analysis but was based on selecting taxa from global or continental phylogenies, which seems more consistent with conservation decision-making that emphasizes species rather than areas.

Perhaps the most compelling support for area-based conservation of maximum PD comes from studies of the links between PD, feature diversity, and ecosystem function. The response variables in these studies are the emergent properties of an ecosystem (such as biomass production), so by definition the sets of taxa chosen must be not just spatially congruent, but functionally part of the same ecosystem. The link between PD and ecosystem function is based on a complementarity effect: species with low niche overlap will access different resources and compete little, so that their combined performance when they co-occur (hence ecosystem function) should be greater than that of species with more overlapping resource use. Therefore, if PD predicts complementarity in resource use, it should also predict ecosystem function (Cadotte et al., Reference Cadotte, Cardinale and Oakley2008; Cadotte, Reference Cadotte2013). A number of studies of experimental plant communities have found that PD does indeed do a better job than species richness or FD of predicting biomass production (Cadotte et al., Reference Cadotte, Cardinale and Oakley2008; Flynn et al., Reference Flynn, Mirotchnick, Jain, Palmer and Naeem2011; Cadotte, Reference Cadotte2013). The scale and scope of such studies are necessarily limited by the need to measure ecosystem function in a controlled experimental situation, and it is unclear whether the ecosystem function rationale for PD could be tested for larger or more phylogenetically disparate assemblages across large geographic regions.

The elephant in the room: Reliability and uncertainty of phylogenetic inference

The final part of this review will focus on the aspect of PD that has received the least attention, but may turn out to be the most important: the dependence of PD measures on the reliability of phylogenetic inference itself. A phylogenetic tree is not really a “reconstruction” of the true, unobservable evolutionary history of a clade, but a hypothesis or inference, based on our assumptions about how evolution led to the data we can observe (Baum and Smith, Reference Baum and Smith2013; Bromham, Reference Bromham2019). Inferring phylogeny requires a large number of methodological decisions, some of which are theoretically well-supported, while others are chosen purely for tractability. The results of a phylogenetic analysis, including branching relationships among taxa, node ages, branch lengths, and measures of support or confidence, are sensitive to these decisions and assumptions, and to the suitability, quality, and completeness of the data. How all of these considerations affect phylogenetic inference is of course a huge field of research, but one that has, until very recently, failed to penetrate the PD literature. Although the potential sensitivity of PD values to the uncertainty of phylogenetic inference was recognized from the beginning (Faith, Reference Faith1992; Crozier, Reference Crozier1997), there has been very little systematic investigation of this in the three decades since.

Bromham (Reference Bromham2019) describes some of the ways in which assumptions and methodological decisions can lead to uncertainty or systematic bias in molecular date estimation. These include assumptions about the homology of sites in an alignment of DNA sequences; adequacy of substitution models to account for the data (as opposed to relative goodness of fit); whether variation in substitution rates across branches or over time can be adequately modeled; completeness and randomness of sampling among lineages; constancy of diversification rates; and the ability of new data to change prior beliefs in a Bayesian analysis. Violation of all of these assumptions is routine and can alter estimates of divergence times substantially. In some cases, divergence times have been shown to vary up to seven or eightfold across different fossil calibration scenarios (Sauquet et al., Reference Sauquet, Ho, Gandolfo, Jordan, Wilf, Cantrill, Bayly, Bromham, Brown and Carpenter2012), or under different molecular clock models (Crisp et al., Reference Crisp, Hardy and Cook2014; Figure 3).

Figure 3. Different specifications of models underlying molecular date estimates can lead to very different outcomes. In these simulated clades, alternative combinations of models of diversification through time (Yule vs. Birth-Death) and variation in substitution rates across branches (Uncorrelated Lognormal vs. Relaxed Local Clock) generate crown age estimates that vary from 3 to 30 million years. Source: Crisp et al. (Reference Crisp, Hardy and Cook2014).

From the point of view of PD, the important question is whether the degree of uncertainty that is typical in phylogenetic inference leads to unacceptably low consistency and reliability in PD estimates, and in conservation prioritization analyses that use PD. Few studies have explored this question so far. Park et al. (Reference Park, Worthington and Xi2018) showed that the common practice of constructing “community phylogenies” (i.e., a phylogeny including only members of geographically-defined assemblages rather than complete clades) leads to underestimation of PD because of under-sampling of the clades from which community members are drawn. Not surprisingly, this effect is more severe when ecological filtering processes (such as competition between close relatives) cause communities to be overdispersed, that is, where species are less closely related than expected from null models. Importantly for PD-based spatial prioritization, this does not simply lower PD values consistently across communities, but alters the rank order of communities by up to 50% when they are ranked by PD values. Ritchie et al. (Reference Ritchie, Hua, Cardillo, Yaxley, Dinnage and Bromham2021) used a similar approach to investigate the sensitivity of PD rankings to assumptions about variation in evolutionary rates between and along branches, and about timescale calibration methods. Again, it was found that PD values calculated from inferred phylogenies were prone to error (average of 6–14%, and up to 23–38%, difference from true, simulated phylogenies), that the degree of error varied depending on the assumptions, and that out of 100 simulated assemblages ranked by PD, 8–9 were incorrectly included or excluded from the top 10 positions. Ritchie et al. note that when it comes to conservation decision-making it is important to characterize the risk arising from possible worst-case scenarios, so that the maximum error values they report may be more consequential for conservation than the mean values.

Another consideration is whether the phylogeny used for PD calculations is a phylogram (branch lengths in units of evolutionary change) or a chronogram (branch lengths calibrated to an absolute timescale). Both are commonly used to calculate PD (Elliott et al., Reference Elliott, Knerr and Schmidt-Lebuhn2018), although the phylogram is more in keeping with the original aim of PD to capture feature diversity, while the chronogram is perhaps more appropriate for questions about evolutionary history as something valuable for its own sake. Elliott et al. (Reference Elliott, Knerr and Schmidt-Lebuhn2018) have shown that the same data used to construct phylograms and chronograms can lead to very different spatial patterns of PD in Australian and New Zealand plant groups: in some cases, PD hotspots occupy entirely different parts of the Australian continent depending on the type of phylogeny used.

Although investigations of the sensitivity of PD to phylogenetic choices and uncertainty have only just begun, the early signs are that alternative, equally well-justified assumptions and methodological decisions about phylogenetic inference can lead to very different spatial patterns of PD and conservation priorities. However, it is still difficult to know how general these results are, and whether there are particular, easily identified conditions under which the uncertainty and variability in PD values can be limited to acceptable levels. Another thing that remains unexplored so far is the effect that variability in spatial patterns has on the outcomes of algorithmic conservation planning or reserve-selection analyses.

Conclusion: Where to for PD?

PD has received an enormous amount of academic attention for the past three decades: Faith’s original PD paper has been cited over 4,500 times. Yet the adoption of PD into conservation practice (including policy, legislation, planning, and management, at international, national, and subnational levels) appears still to be very limited. The most frequently cited example of a practical application of evolutionary history more generally is the Zoological Society of London’s EDGE (Evolutionarily Distinct, Globally Endangered) program (Isaac et al., Reference Isaac, Turvey, Collen, Waterman and Baillie2007). This program has had much success in raising public awareness of threatened species, including many that are not widely known, by highlighting the ones that are also evolutionarily distinct. EDGE or evolutionarily distinct species have been recognized as a high priority under IUCN Resolution WCC-2012-Res-019-EN (IUCN, 2012) and by the IUCN Species Survival Commission (https://www.iucn.org/our-union/commissions/species-survival-commission/partners-and-donors/ssc-edge-internal-grant), and some international charities such as On the Edge (https://www.ontheedge.org) have EDGE species as their focus. But although they both have origins in the concept of evolutionary distinctness, EDGE differs from PD in a way that is fundamentally important, because it is not a measure of diversity: it shifts the focus of conservation attention away from assemblages of species and back to the old idea of valuing individual species for their uniqueness. However, EDGE differs from the traditional, qualitative value placed on evolutionarily distinct species in assigning species a numeric score to indicate their value. EDGE also differs from PD in that it is only partly a measure of evolutionary distinctness, with threat status and evolutionary distinctness contributing equally to the score for each species.

Perhaps due to the wide success of EDGE in drawing attention to evolutionary distinctness, PD does appear to be making some inroads into international policy. The most prominent examples of this are the adoption of PD as an indicator under the Nature’s Contributions to People category of the IPBES Global Assessment on Biodiversity and Ecosystem Services (Brauman et al., Reference Brauman, Garibaldi, Polasky and Zayas2020), and the listing of PD as one of a number of Complementary Indicators of progress toward two goals under the draft Global Biodiversity Framework (Convention on Biological Diversity, 2022). International agreements such as these provide an increasingly important global context and framework that can shape conservation policy at the national level, and it may be that PD begins to find its way into conservation practice in some countries. As yet, however, there is little evidence that this has happened, and it cannot yet be said that PD is a prominent part of the prevailing conservation paradigm.

If PD is to be adopted into the mainstream of conservation practice, it will be all the more important to fully understand the connections between PD and the biodiversity qualities that we want it to represent. Assuming that PD always does an adequate job of representing these qualities could lead to poor outcomes for conservation, so we need to know when it does do an acceptable job and when it does not. Likewise, it is unwise to assume that phylogenetic branch lengths represent evolutionary history precisely and accurately. A better understanding of how phylogenetic error and uncertainty affect conservation decision-making involving PD is one of the most pressing current issues that needs to be addressed with further research. More than anything else, this particular issue highlights a key problem for the wider adoption of PD: considerable specialist expertise is required for a critical understanding of what phylogenetic branch lengths represent, and of the data, models, and methods of inference from which they are derived. The policymakers who decide on metrics and indicators for biodiversity goals do not necessarily have this expertise, and it is critical that the scientific advice provided to them on the utility and limitations of phylogenetic information is balanced, realistic, and free from advocacy.

There are two other important challenges to overcome in order for PD to become more widely applied. One of these is simply data availability: despite the massive growth in generation of molecular data and publication of phylogenetic trees, the majority of the world’s biodiversity is still unrepresented in genomic databases, and most of the tree of life remains unknown. This is especially true for some the world’s most biodiverse taxa, including arthropods and angiosperms. Although there are ambitious plans to sequence all described eukaryotic species, estimating PD for many assemblages will probably continue to be based on relationships between higher-level taxa or incomplete data for many years to come, and the possible limitations this imposes on PD estimates needs to be generally understood. While some degree of data incompleteness can be overcome using imputation methods (Gumbs et al., Reference Gumbs, Gray, Wearn and Owen2018), for poorly known taxa unrealistic data requirements may make it difficult for PD to compete with simple species richness as the primary, basic currency of conservation.

Finally, those of us who are familiar with PD as an academic concept should not assume that the practical conservation relevance of phylogenetic branch lengths is necessarily obvious to most conservation managers, policymakers, funding agencies, government departments, or the general public. How meaningful is the difference between 20 million years and 25 million years of evolutionary history? Do option value or “evolutionary potential” over the next few million years rate highly as priorities for many people, in the way that preventing the extinction of the Siberian tiger or Ganges River dolphin do? With its species-specific focus, the EDGE program has captured public imagination and continues a long tradition of valuing unique and distinct species. Doing the same for assemblages of species, especially when faced with uncertainty over what is being represented, is perhaps the biggest challenge that will need to be overcome for the conservation of PD.

Open peer review

To view the open peer review materials for this article, please visit http://doi.org/10.1017/ext.2023.8.

Acknowledgments

I thank Lindell Bromham, Ben Scheele, Alex Slavenko, and Sam Passmore for comments and feedback, and the two peer reviewers for their thoughtful and constructive reviews.

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Figure 0

Figure 1. Evolutionarily distinct species have long been valued for their unique and irreplaceable contribution to biodiversity. Left: Albany Pitcher Plant, Cephalotus follicularis (source:https://www.flickr.com/photos/7326810@N08/1555479035/in/photostream/ Attribution 2.0 Generic CC BY 2.0); Top right: African Coelacanth, Latimeria chalumnae (source:https://www.the-scientist.com/news-opinion/african-coelacanths-may-live-to-be-100-study-68911); Bottom right: Welwitschia mirabilis (source:https://commons.wikimedia.org/wiki/File:Welwitschia_mirabilis,_m%C3%A4nnl._Bl%C3%BCte,_Namibw%C3%BCste,Namibia.jpg Attribution-ShareAlike 3.0 Unported CC BY-SA 3.0).

Figure 1

Figure 2. Calculation of Faith’s phylogenetic diversity (PD) for a set of species g1–g6. PD is the sum of the branch lengths (indicated here by the division of branches into intervals) along the shortest paths connecting the set of species. The panel in the center shows how a small subset of species can capture a large proportion of the evolutionary history of the whole group (left panel), if the paths connecting them traverse the root of the phylogeny. In the panel on the right, a different set of three species has a much lower PD score because they are more closely related to one another. Source: Rodrigues and Gaston (2002).

Figure 2

Figure 3. Different specifications of models underlying molecular date estimates can lead to very different outcomes. In these simulated clades, alternative combinations of models of diversification through time (Yule vs. Birth-Death) and variation in substitution rates across branches (Uncorrelated Lognormal vs. Relaxed Local Clock) generate crown age estimates that vary from 3 to 30 million years. Source: Crisp et al. (2014).

Author comment: Phylogenetic diversity in conservation: A brief history, critical overview, and challenges to progress — R0/PR1

Comments

No accompanying comment.

Review: Phylogenetic diversity in conservation: A brief history, critical overview, and challenges to progress — R0/PR2

Conflict of interest statement

Reviewer declares none.

Comments

Comments to Author: In principle, a review of the role of PD in conservation is a welcome piece, however this paper is in practice simply an opinion piece critiquing PD, it cannot be considered a review as it omits multiple important advances and applications that have happened in recent years. As well as general misunderstandings throughout, it also mis-represents the author’s previous work to fit the narrative agenda of framing PD in a negative light. The abstract and conclusion both use highly loaded, inflammatory language, unsupported by the limited evidence presented in the paper. This paper should, at the very least, be significantly revised to include the omitted aspects, as well as in presenting a more balanced view of progress. However, as it stands, the paper also does not seem to be in keeping with the stated aims and scope of the journal, and should also be reframed as such to proceed.

I present the key concerns as follows:

1. The paper claims that PD is not used or of any particular use for conservation, ignoring multiple applications, with a non-exhaustive list of applications as follows:

a) explicit recognition by IUCN of its importance with the establishment of the IUCN SSC Phylogenetic Diversity Task Force www.pdtf.org in 2019, as a consortium of experts aiming to do exactly what the author says is a challenge: “bridging the divide between academic conservation science and the scientific requirements of conservation policymakers and planners” (L381-383).

b) building on the 2012 IUCN Resolution on halting the loss of evolutionarily distinct lineages https://portals.iucn.org/library/sites/library/files/resrecfiles/WCC_2012_RES_19_EN.pdf

and recent call by Diaz et al. 2019 to prioritise the conservation of evolutionarily distinct lineages across the tree of life in the Convention for Biological Diversity’s Global Biodiversity Framework https://www.science.org/doi/abs/10.1126/science.abe1530.

c) PD’s increasing influence on conservation activities of the IUCN SSC, recognised as important in prioritising conservation activities in multiple Specialist Groups e.g. in the goals of the Small Mammal Specialist Group, the Amphibian Specialist Group; and the activities of many others funded through the SSC EDGE Grants https://www.iucn.org/our-union/commissions/species-survival-commission/partners-and-donors/ssc-edge-internal-grant.

d) Dedicated and increasing donor and practitioner support globally for conserving species important to maintaining PD, specifically EDGE species and Zones, by multiple organisations, e.g. ZSL, On the Edge, re:wild, Rainforest Trust among others.

e) the adoption of Phylogenetic Diversity by IPBES as an indicator for multiple aspects of Nature’s Contributions to People in their Global and Regional assessments https://ipbes.net/global-assessment.

f) The inclusion of Phylogenetic Diversity in the draft Global Biodiversity Framework as a Complementary indicator for Goal B, and the paired EDGE Index as a Component Indicator for Goal A, see here for technical submissions https://www.pdtf.org/publications leading to the most recent CBD COP15 draft document listing the indicators: https://www.cbd.int/doc/c/0524/cc9d/99da38b8be1522bd3fd97e43/cop-15-02-en.pdf, full details of the indicators as described in the pre-print https://www.biorxiv.org/content/10.1101/2021.03.03.433783v1.full.

These two indicators were even proposed by some Parties to be considered as Alternative Headline Indicators during the CBD technical meetings in Geneva, March 2022 https://www.cbd.int/doc/c/f191/8db7/17c0a45b42a5a4fcd0bbbb8c/sbstta-24-l-10-en.pdf.

g) The inclusion of Phylogenetic Diversity in the Multi-Dimensional Biodiversity Index developed by UNEP-WCMC and already incorporated by pilot countries, Soto-Navarro et al. 2021 https://www.nature.com/articles/s41893-021-00753-z.

h) Reporting on EDGE species by WDPA’s Protected Planet e.g. https://livereport.protectedplanet.net/pdf/Protected_Planet_Report_2018.pdf.

i) Systematic conservation planning in Australia using PD and associated metrics, e.g, Rosauer et al. 2018 https://conbio.onlinelibrary.wiley.com/doi/10.1111/conl.12438 ; Laity et al. 2015 https://geobon.org/downloads/scientific-publications/2015/1-s2.0-S0048969715300498-main.pdf

Unfortunately, the author does not seem to understand the principles of ZSL’s EDGE of Existence programme as the most widely cited application of PD in conservation, claiming that it is “quite far removed from PD…[shifting] focus back to the old idea of valuing individual species for their uniqueness” (L369-371). The EDGE programme, and the multiple papers presenting EDGE assessments across multiple taxonomic groups, clearly recognise PD as foundational to this work, and it is highlighted by the IUCN SSC PDTF as being a practical application of PD in conservation. It is quite a disjointed and somewhat contradictory narrative for the author to present the conservation of evolutionary history in species as then leading to the quantification of PD but then to distance the consequently developed EDGE metric from PD.

I would also suggest the author may like to undertake a more rigorous review of the applications of PD in conservation than post a request on twitter https://twitter.com/MarcelCardillo/status/1549624820316286981?t=qsro5ScTF9w_Ko64gc3Kug&s=31.

2. The paper neglects or downplays evidence in support of the application of PD in conservation, to support a negative and unbalanced narrative, in general there is a misunderstanding of the debate, evidence and findings to date, in a variety of ways.

PD is described by the author as “a continuous-scale index of conservation value for a set of species, calculated by summing the phylogenetic branch lengths that connect them.” L5 & 54. But PD is not an index of conservation value – it is a measure of biodiversity, that informs conservation. Conservation does not necessarily seek to maximise PD, but to conserve PD, an important distinction highlighted in Owen et al. 2019 https://pubmed.ncbi.nlm.nih.gov/30787282/.

No academics, practitioners or expert groups such as the IUCN SSC PDTF lay claim to PD’s “primacy as the currency of conservation” (L57) as the author asserts. This is especially important as conservation does not work this way in practice, with any single prioritisation scheme - in reality, the intention of PD-informed conservation such as the EDGE of Existence programme and other PD-initiatives (as outlined above) is to complement current conservation efforts and prioritisations, and seek to highlight where valuable species and areas may otherwise be overlooked.

The author does not seem to understand conservation practice, claiming “simple species richness as the primary, basic currency of conservation” (L378). For some time now, the literature has recognised that conservation efforts should not be based on species richness alone but on additional metrics, such as species composition, endemism, functional significance, and the severity of threats (and, increasingly, evolutionary distinctiveness). For example biodiversity hotspots are based on endemism, Key Biodiversity Areas on the presence of trigger (threatened) species, the IUCN Red List on extinction risk, and indeed efforts are typically made to control for species richness in spatial or species-based prioritisation analysis.

The author decides throughout that feature diversity equates to all work on PD / functional relationships, despite feature diversity having a specific definition and this being cautioned against repeatedly, e.g. in Owen et al. 2019.

The inference that feature diversity and option value (and hence PD) is solely a utilitarian value of biodiversity (L122 + L222) is not supported in practice, as it is contrary to the use of PD as an indicator for multiple NCPs by IPBES and in consideration throughout the CBD (see links above), both of which’s descriptions highlight its importance as a mechanism for ensuring intergenerational equity. Future benefits from biodiversity are of course not restricted to only utilitarian use and include benefits derived from non-utilitarian extrinsic values such as cultural, aesthetic, etc as well as intrinsic values.

The author critiques data limitations around PD analyses (L379), but has omitted efforts to overcome these, such as that presented in Gumbs et al. 2018 https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0194680; note that this area is also advanced extensively in the pre-print https://www.biorxiv.org/content/10.1101/2022.05.17.492313v1.abstract.

There is some mis-representation of previous findings, most notably being the author’s co-authored Ritchie et al. 2021 paper, but also Kelly et al. 2014 and Mazel et al. 2018 which actually do show strong support for the PD and feature / PD and function relationship in tree space and geographic space respectively. The author dismisses Molina-Venegas’s work and ignores the positive overall findings of Mazel et al. 2018; Tucker 2018,2019, and fails to cite Owen et al. 2019’s response to Mazel et al. 2018.

For Ritchie et al. 2021, specific examples are as follows:

The author claims: “Again, it was found that PD values calculated from inferred phylogenies were prone to error (23-38% difference from true, simulated phylogenies)...” L339-340.

But in Ritchie et al. 2021 the average % error is 6-14% (i.e. an average of 86-94% accuracy), which in fact is very positive, particularly for true PD estimation from reconstructed trees. The values quoted here are actually the max error, and this should be represented correctly.

The following phrase is also incorrect “…and that the ranked positions of 100 communities differed between true and inferred community PD by an average of 10-11 places” (L341-342).

In fact, these figures are about species ED rankings (not community PD rankings), and the Ritchie et al 2021 paper says, quite positively by comparison:

"Looking at how the position of each taxon changed when we used reconstructed ED, we found that taxa were mis-ranked by 10-11 positions on average and 20-40 positions at the 95th percentile compared to their rankings based on true ED values (BEAST, Figure 6; NPRS, Figure S4 available as Supplementary Information). Taxa that were top-ranked in the true tree were substantially more likely to be correctly ranked than those that had ED values in the middle of the ranking. An alternative way to interpret this data is to compare the proportion of the top 10, 50 (and so on) ranked species that are correctly identified under estimation. The above results are then equivalent to saying that 83-87% of the top 10 or top 50 species are correctly identified by estimation, whereas about 90% of the top 80 are correctly identified.”

3. Inflammatory language

The abstract is highly editorialised and does not match the content. This is also the case in the conclusion, claiming that PD currently has no impact on conservation decision making after omitting the multiple (and non-exhaustive) list of advances outlined above.

In particular, extremely loaded language unreflective of the advances that have already been made appears in the following sentences, which should be entirely revised on the basis of the evidence above:

L8 “has had virtually no impact on conservation practice or policy.”

L19-20 “it will be difficult to envisage a major role for PD in conservation policy and real-world decision making.”

L385-386 “…if that is ever to happen.”

L386-389 “The second will serve as a reality check on the value of PD for conservation…and help to identify the conditions under which PD might be considered to represent whatever it is that we value about biodiversity.”

Finally, the dramatically increasing interest in PD-informed conservation over recent years, spearheaded by concerted, cohesive and truly collaborative efforts from scientists, practitioners, donors and policy-makers highlighting the need to incorporate PD in conservation (but not as an exclusive goal), would seem to undermine the author’s claim that “ PD is certainly not a prominent part of the prevailing conservation paradigm.” (L373).

Review: Phylogenetic diversity in conservation: A brief history, critical overview, and challenges to progress — R0/PR3

Conflict of interest statement

Reviewer declares none.

Comments

Comments to Author: This opinion piece presents an overview of some of the debates and potential problems with approaches based on the concept of phylogenetic diversity. It is an interesting read, while I don’t necessarily agree with all the points that are made here.

The section exploring why PD is popular in academic studies argue that it is caused by two factors, the ease of compiling PD and the fortuitous rise of molecular systematics in the 1990s coinciding with the introduction of PD in 1992. While that may be somewhat the case, the way it’s presented makes is a bit disingenuous. Putting the conservation aspects aside, PD and associated metric have proven to be useful tools in deciphering biodiversity patterns and exploring the potential processes behind these patterns.

The ability of PD to predict feature diversity is certainly a topic that has been widely debated in recent years. It would be important to mention that some of the publication cited here use a narrow view of feature diversity, as pointed out for example by Owen et al 2019 (not cited here; https://www.nature.com/articles/s41467-019-08600-8) in the case of Mazel et al 2018a. In some of these papers, functional diversity is equal to feature diversity, which are in fact, as pointed out by the author, two different concepts. The examples reported in lines 275 to 283 are more in line with the concept of feature diversity (i.e. usefulness of plants), which is broader than functional diversity.

The last section of the manuscript focuses on the uncertainty in the phylogenetic inference itself, which is certainly not an issue for PD alone. Most of the points raised here are valid and I agree that additional research in this field would be necessary, especially studies using rarefication approach of real, near-complete data, rather than simulated data (such as Ritxchie et al 2021), which have value, but might not be capturing all the complexities of phylogenetic inference. The data needed for rarefication analyses are not readily available, but hopefully these will become more common in the future.

While I would not necessarily advocate that PD is the silver bullet that can provide all the answers we need in conservation science, it is certainly important to capture the evolutionary dimension of biodiversity, an important contributor to the diversity of life on Earth, when planning conservation actions. PD should be seen as representing one of the many components of biodiversity and should be considered in conservation planning where possible. I feel that this review/opinion piece is rather dismissive in that regard, but maybe it’s the way I interpreted it. In any case, it is, of course, an opinion that the author is entitled to have and several interesting points are made here.

Minor points:

L36: Family and order don’t need to be capitalised

L124: I don’t think that option values generally refer to financial value, so this example (i.e. pharmacologically-useful compound) might not be entirely representative of the general concept of option values.

L143: I don’t think the R package ape has functions to compile PD.

Figure 2: Faith’s definition of PD includes the root. The PD calculation using the tree on the right excludes the root, so this is not strictly Faith’s PD and more what some have called “local PD”. It doesn’t affect the point that the author is attempting to make here, however.

Recommendation: Phylogenetic diversity in conservation: A brief history, critical overview, and challenges to progress — R0/PR4

Comments

Comments to Author: Thanks for submitting your review of phylogenetic diversity. I found it interesting to read, and I’ve sought the opinions of two referees. Both referees note some aspects of communication that could be tempered, albeit that they differ in their recommendations and the length of their reviews. And one is very positive.

I did another editorial read to evaluate the comments you have here in the longer review. In particular, I was interested whether the manuscript, in its current form, is written in a suitably objective tone. Having done that, I do have some sympathy for the comments in the longer review, and I think this is something you could address in a revised version of the manuscript.

To illustrate my impressions, I’ve given a few quick examples below. I only give a few examples, but I’d like you to pay attention to phrasing and accuracy throughout the ms. The paper will have a bigger influence on the field if the phrasing is fair and objective, and does not alienate people who have a different view to the one presented here. I’d also like you to address the points of scholarship and accuracy from the longer review, and to respond to each of the referees' comments in a reponse letter, explaing what you did to the ms (also, doing your changes using coloured text).

--“...accepted, almost uncritically” [we don’t know whether people think critically or not, just by reading the text they wrote, strictly-speaking]

--“...adds nothing to...” [’adds nothing‘ is a strong statement from a statistical perspective. Of example, it could ’add something' even if it added a small amount of additional information]

--“...suffers from the same vulnerability to phylogenetic branch-length uncertainty” [this is a quantitative issue that is tackled only qualitatively. There is a question of effect size. For example, many of the samples given concern unequivocally very long brand distinct lineages (e.g. coelacanths). For these, the effect size of the uncertainties will be small].

In summary, I’m happy to consider a raised submission of the manuscript that addresses the referees' comments. Please do use the information they have given in a constructive way.

When you do resubmit, please provide me with a list of suggested referees in your cover letter. I would like to broaden the range of invited referees here, to ensure the best quality of outcome.

Decision: Phylogenetic diversity in conservation: A brief history, critical overview, and challenges to progress — R0/PR5

Comments

No accompanying comment.

Author comment: Phylogenetic diversity in conservation: A brief history, critical overview, and challenges to progress — R1/PR6

Comments

Many thanks for the opportunity to revise and resubmit my manuscript. My detailed response to the editors and reviewers comments are outlined in the response section.

As requested by the handling editor, below are some suggested additional reviewers who would be well qualified to review this manuscript:

Caroline Tucker, University of North Carolina

William Pearse, Imperial College London (will.pearse@imperial.ac.uk)

Florent Mazel, University of Lausanne (florent.mazel@unil.ch)

Marcel Cardillo

Review: Phylogenetic diversity in conservation: A brief history, critical overview, and challenges to progress — R1/PR7

Conflict of interest statement

I am Chair of the IUCN SSC Phylogenetic Diversity Task Force. I do not believe this to be a competing interest but declare it for transparency.

Comments

Comments to Author: I continue to welcome the principle of an objective review of the role of PD in conservation. However, despite some acknowledgements of the issues raised being made in the response to reviewers, this hasn’t been sufficiently brought through to the manuscript revisions. This version is written more neutrally, and there are sections which present good insights and value, particularly the phylogenetic inference section. However, the overall paper is still somewhat jumbled, and lacks internal consistency. There are two major areas of concern, plus a few other elements that could be better addressed.

1. Firstly, in general the paper’s approach falls into the trap of conflating research into a biodiversity metric (PD) with conservation that utilises PD along with measures of vulnerability, as is the main approach for conservation e.g. Brooks et al. 2006, and it is not appropriate to solely use the former to question the latter.

L63 “I ask if 1) PD serves as a reliable indicator of conservation-relevant phenotypic diversity". This is certainly an ambitious question, but the author does not define ‘conservation-relevant phenotypic diversity’ satisfactorily, and I’m uncertain if this is even possible, thus raising the question of how the author can come to a judgement. The review does not seem to adequately answer this question.

L223-226 “Most authors of papers on PD seem to regard feature diversity implicitly as the variety or richness of phenotypic traits of any measurable kind, including physiological, phenological, morphological, and behavioural traits (Tucker et al. 2019), without explicit consideration of whether the traits are of relevance to the goals of PD.”

It is unclear what is meant here: what exactly are “the goals of PD”? The goal of maximising PD (vs conserving PD, which is different and should be clearly differentiated in this review) is to retain the broad suite of features precisely because we don’t know what will be useful in the future, so how can it be stated (and by whom?) that any one trait is or is not of conservation relevance? However, in terms of conservation strategies, conserving PD, or maximising threatened PD, becomes the objective, and this needs to be clear if assessing the role of PD in conservation.

As part of this concern, although feature diversity is a central concept, within the manuscript feature diversity is repeatedly used interchangeably with functional diversity, which is a fundamental inaccuracy in this paper and has been cautioned against in the literature – functional diversity is only a subset of feature diversity, and this needs to be made clearer throughout. Since most of the review hinges on this point, they should both be separately defined, especially in relation to their differential use in the various studies cited. Otherwise, the review continues to misrepresent PD as a proxy for a selection of functional traits, rather than representing overall feature diversity. Specific examples as follows:

L109-111 “…PD was presented as a proxy for the diversity of unknown characters. In the age of genomic phylogenetics and open data, this is still the primary rationale for PD.”

The rationale is that it is impossible to know and measure all features of all species, and PD indicates that overall diversity of features. This is not the same thing as the diversity of unknown characters that were withheld from the public domain by scientists, or that can shift in meaning as more data become available.

L229 – “I will not dwell on the issue of definitions, but will use the term feature diversity to represent all conceptions of functional, trait, or phenotypic richness or diversity that appear in the PD literature.”

Please do dwell on the issue of definitions, because this seems critical to the entire point of the review. For example, feature diversity when the target of PD conservation is often defined as the variety of different features, measured and unmeasured, represented among species or other taxa, and it is widely acknowledged that studying the link between PD and a narrow selection of traits (i.e. functional diversity) does not represent a test of the PD-feature relationship (e.g. ”It is important to recognise that PD-based prioritisation aims to capture the diversity of evolutionary features of species, both measurable and unmeasurable…FD is just one part of this diversity.” - Griffith et al. 2023; and see Owen et al. 2019 and related articles). By conflating studies focusing on functional trait diversity (a la Mazel et al. 2018) with tests of PD-FD relationship (a la Kelly et al. 2014), the author fails to accurately reflect the literature. This could easily be remedied by spending the necessary effort to clearly define the terms used by the author and in the papers referenced, e.g.:

L257-258 “Furthermore, because a subset of species that maximizes PD is usually distributed non randomly on the phylogeny, it can be possible for the maximum-PD set to be a worse predictor of feature diversity than a random set of species (Mazel et al. 2017).”

Mazel et al 2017 was referring to functional diversity, not feature diversity. The two are not interchangeable.

L263-265 “This was demonstrated explicitly in a study of the spatial distribution of PD, functional diversity and species richness of plant assemblages in the Pyrenees (Pardo et al. 2017).”

The author is now talking about functional diversity, but it is not clear whether he considers this to be a component of feature diversity, or is using the terms interchangeably.

2. Secondly, the author continues to provide a contradictory perception of EDGE and the link to PD. They say that “the EDGE approach represents the current primary practical method to apply PD to conservation” in the response to reviewers, and in the paper outline how PD emerged from work on evolutionary distinctiveness, but then still distance EDGE (Evolutionary distinctiveness weighted by extinction risk) from PD when discussing PD’s uptake in conservation. This arbitrary distancing is the opinion of the author, and is in opposition to the original stated aim of EDGE (from Isaac et al. 2007):

“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.”

“This paper describes a new method for measuring species' relative contributions to phylogenetic diversity”

“The EDGE approach identifies the species representing most evolutionary history 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“.

And also contradictory to empirical data (e.g. see Redding and Mooers 2015, PLOS ONE). If the author’s point is that EDGE is a species-focused approach and their personal concern is only with assemblage-based measures, this is not clearly stated in the review and needs to be brought to the fore.

Whilst being unclear when critiquing assemblage PD and species-based measures, the author thus chooses to exclude elements such as the paired EDGE indicator, a component indicator in the CBD’s GBF (explicitly linked to—and derived from–the PD indicator), from being classed as advances in PD-informed conservation, which is misleading.

3. Other points

The correction of the misrepresentations of other research is improved, though still ambiguously worded in a way that could be misconstrued, or selectively presenting certain results, e.g. L334-337. Ritchie et al. 2021 provides stimulating and insightful findings, yet only a narrow set of these findings are highlighted in this review. e.g. choosing to highlight areas of relatively weaker performance of PD while ignoring areas of strong performance, with the previously erroneously cited (and positive, from my perspective) ED results now removed entirely from the review.

Regarding the author’s arguments that the researchers in the field are not concerned with the importance of uncertainty and phylogenetic inference and its implications for measuring PD and its link to feature diversity (e.g. L396-399), while the author highlights some areas that are indeed in need of greater interest, there are multiple examples to the contrary for various aspects of phylogenetic uncertainty/error – this is a very active area that is well-recognised in the literature and was even discussed in early literature around the EDGE metric (e.g. Isaac et al. 2007).

L354 – the author fails to note here the increased exploration of the impact of different phylogenetic hypotheses in phylogenetic-based work and how to incorporate or address uncertainty where possible (e.g. Jetz et al. 2014 Current Biology, Pollock et al 2017 Nature, Stein et al 2018 Nature Ecol Evo, Rabosky et al. 2015 Evolution, Weedop et al. 2019 Animal Conservation).

L357 – this sentence is good and should be a call to arms to phylogeneticists to tackle these issues to provide more robust PD calculations.

L42 – now classified as two species, P. gangetica and P. minor

Positively, I do agree with several of the author’s points: around phylogenetic inference and how increased research into the conditions under which PD works best are exciting avenues, and that PD performs variably at capturing sets of functional traits, and including clarity on both points (for the former: people do care and are working on some aspects of it; for the latter: greater clarity on function vs feature diversity as mentioned above) would go a long way to helping this transition from an opinion piece to a review. These positive elements are being overshadowed by the lack of clarity and conflation, and addressing these aspects will solve the issues outlined above.

Review: Phylogenetic diversity in conservation: A brief history, critical overview, and challenges to progress — R1/PR8

Conflict of interest statement

Reviewer declares none.

Comments

Comments to Author: I have no further comments. Thank you.

Recommendation: Phylogenetic diversity in conservation: A brief history, critical overview, and challenges to progress — R1/PR9

Comments

Comments to Author: Thanks for resubmitting your manuscript. You will see that one referee has some further comments for you to consider, but that those comments are now more constrained in scope than before. I would welcome a resubmission of the manuscript that considers these points.

Decision: Phylogenetic diversity in conservation: A brief history, critical overview, and challenges to progress — R1/PR10

Comments

No accompanying comment.

Author comment: Phylogenetic diversity in conservation: A brief history, critical overview, and challenges to progress — R2/PR11

Comments

Please note that permission to reproduce the figures from other journals (Figures 2 & 3) has not yet been sought. I’m not sure if that is my responsibility - please let me know if it is.

Recommendation: Phylogenetic diversity in conservation: A brief history, critical overview, and challenges to progress — R2/PR12

Comments

Comments to Author: Thanks for your considered participation in he peer review process for this paper. I appreciate the seriousness with which you have gone abou incorporating suggestions from both referees. I’m satisfied that you have done essentially a complete job with this and am happy for the paper to be published in it’s current form (pending any input from the technical editorial team of the journal). Thanks again, I look forward to seeing the work published.

Decision: Phylogenetic diversity in conservation: A brief history, critical overview, and challenges to progress — R2/PR13

Comments

No accompanying comment.