Is phylogenetic diversity a useful measure of evolutionary potential for development of conservation strategy

Is phylogenetic diversity a useful measure
of evolutionary potential for development
of conservation strategy?
130000433
Word count: 2194 excluding figures and reference list
November 9, 2015

Is phylogenetic diversity a useful measure of
evolutionary potential for development of
conservation strategy? | 130000433
Page 1 of 17
Introduction to Phylogenetic Diversity (PD) and evolutionary potential
The original quantitative definition of PD was summarised by Faith & Baker (2006) as a measure of
“the minimum total length of all phylogenetic branches required to span a given set of taxa on the
phylogenetic tree” (Fig.1), as set out by Faith (1992a, 1992b) (although Vane-Wright et al.(1991)
may have first conceived PD). This gives a measure of the evolutionary distinctness of any one
species or selected groups of species that can act as a reflection of evolutionary potential – the
potential for a species or set of taxa to speciate in the future (Winter et al., 2013).
Figure 1 – (Adapted from (Crozier, 2005) in (Faith & Baker, 2006))
PD calculation from a simple phylogenetic tree.
In this tree PD can be found by measuring the branch lengths of a set of taxa. For example, the PD of species 1
and 2 to root R is (1+1+2) = 4, whilst for species 3 and 4 is (2+2+1) = 5. Species 1 and 4 would equal
(1+2+2+1) = 6, as would other combinations of species 2 & 4, 2 & 3 and 1 & 3. Therefore, the most optimal
solution for a conservationist interested in protecting maximal PD would be to save one of species 1 & 2 and
one of species 3 & 4 if resources were limited to saving just two species. If there were enough resources for
saving three species, both species 3 and 4 would be protected (PD=5) and one of species 1 & 2 (PD=4).
or
Selection
2-species 3-species

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Maximising PD is thought to maximise another type of diversity called ‘feature diversity’ that refers
to the diversity in traits within a given set of taxa (Fig.2) (Faith, 2002). In turn, this can represent
the ‘option value’ of taxa in terms of the probability that in the future there will be a correct,
selectable feature in taxa to enable adaptation to environmental change – thus evolutionary
potential (Forest et al., 2007; Crozier, 1997).
Figure 2 – (Adapted from Faith (1992b)) A demonstration of the connection between PD and feature diversity
Using imaginary data in a) (rows are taxa and columns are features) where an outgroup (o) has all 0-values for all
features whilst all other taxa show presence (1) or absence (0) of that feature. A hypothetical tree of these taxa then
has the most likely position of where each feature arose superimposed on the branches (bars across the branches)
(Faith, 2006). This shows that PD calculations that use the branch lengths of the tree directly correlate with the
numbers of features for different groups of taxa. For example, a taxa set of b and h (in orange) clearly represents a
much greater length for PD and has 15 features, as opposed to the set of i and j (in blue) with a smaller branch length
and only 5 features – in a) you can see there is far greater similarity in the feature matrix too.

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However, the theoretical connection between PD and evolutionary potential, as well as its use in
informing real-life conservation strategies, remains controversial (Faith & Baker, 2006; Winter et
al., 2013). Nonetheless, it is of paramount importance that this debate is resolved as species face a
future of unpredictable environmental change, caused by anthropogenic effects ranging from
invasive species and deforestation, to rising atmospheric carbon dioxide concentrations (Forest et
al., 2007). If evolutionary potential is not protected, the Tree of Life could be reduced to little more
than a dead trunk as species become extinct at rates faster than ever recorded (Erwin, 2008). So is
it possible that using PD to develop conservation strategies could useful in helping to avert this
biodiversity crisis?
Support for PD
Rodrigues & Gaston (2002) have suggested that PD is a superior ‘currency’ for feature diversity
over the commonly used measures of taxonomic richness (alpha, beta and gamma diversity) in
terms of conservation prioritisation. This is because any measure of taxonomic richness neglects to
account for the different values of taxa as conservation units – PD can reflect the fact that one
species can represent far more evolutionary potential than another (Faith, 1992a; May 1990).
Taxonomic richness also encounters the problem of scale-dependence, as Brown (1988) showed a
positive correlation between taxa found and sampling effort (area sampled) – whereas PD is less
prone to such biases (Erwin, 2008).
Arguments that taxonomic richness is an adequate surrogate for PD have been based on spatial
overlap between conservation areas selected by both measures (see Polasky et al. (2001)). These
have been dismissed by Rodrigues & Gaston (2002), as flawed comparisons used an unlimited

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number of sites and forgot that complementarity-based selection methods (an approach to protect
species not currently protected using reserves) produce multiple optimal solutions. Even so, strong,
positive and highly significant correlations between PD and taxonomic richness have given support
to the use of taxonomic richness as a reliable proxy for PD (Rodrigues & Gaston, 2002; Polasky et
al., 2001). However, decoupling can occur when heavily imbalanced phylogenetic trees (far more
or less monophyletic branches than highly split ones) or insular communities (with unique
phylogeographic structures due to high endemism and localised radiations) are studied (Rodrigues
& Gaston, 2002). Studies of plants in the Cape of South Africa, the lemurs of Madagascar and
bumblebees in South America versus in Asia are all examples of such decoupling (Rodrigues &
Gaston, 2002). This suggests PD might be a more reliable measure for use in wider conservation
initiatives without decoupling limitations.
Faith (1992a) also found that PD may even be able to measure feature diversity below the species
level (Fig.3), whilst at the other end of the spectrum, there is a theoretical basis at the community
level for increases in evolutionary potential with increases in PD. A range of studies support this,
from coral reefs (Bellwood et al., 2003), to bird diversity (Meynard et al., 2011) and evolutionary
resilience (Sgrò et al., 2011). However, there seems to be a lack of empirical evidence for these
theories at both the species and community-level (Winter et al., 2013).
However, there is evidence to support a clear relationship between PD and feature diversity, since
by considering branch lengths probabilistically using a Poisson distribution, a measure of feature
diversity (from Crozier (1992)) corresponds monotonically to PD (Faith, 1994).

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With a strong theoretical grounding, PD can recommend which actions, sites/regions and species
conservationists should prioritise to ensure the Tree of Life’s diversity persists into the future
(Rosauer & Mooers, 2013). The Zoological Society of London has already fully integrated PD into
their conservation efforts by creating the EDGE of Existence programme which aims to maintain a
list of ‘EDGE (Evolutionarily Distinct & Globally Endangered) species’ (Fig.4) in order to preserve
Figure 3 - PD calculated from a mtDNA phylogeny of Great Crested Newt (Triturus cristatus)
populations in Europe (from Faith, 1992a).
If one includes population genomes 1, 11, and 12, a length measure for PD of 19 is found. By including one of
the western populations (genomes 5-9) in conservation efforts, 7-10 could be added to the PD length
measure. Additionally saving a Turkish population site (with genomes 15, 16 and 17) will increase PD by 9.
Therefore protecting a population from Turkey or from Western Europe could improve the PD under
protection by at least 35% from the initial selection. Being able to work out the best course of action is an
invaluable tool for conservationists to use in terms of protecting fragmented populations and maintaining a
large enough effective population size and gene pool with high PD (Faith, 1992a).
Western
populations
Turkish
populations

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future evolutionary potential (Isaac et al., 2007). Such direct usage of PD is promising for advocates
of the usefulness of PD in developing conservation strategies, even if the EDGE programme
currently focuses on mammals.
Problems with PD and alternatives
Although PD has a broad base of support and there are some examples of its integration into
conservation strategies, many conservationists have been reluctant to use PD in developing
conservation strategies for several reasons (Winter et al., 2013).
In some cases, it has been disputed whether PD is a good proxy for other diversity measures such as
functional diversity (FD) (Jernvall & Wright, 1998; Fritz & Purvis, 2010; Hooper et al., 2005). If PD
does not represent FD well, then this could be a loss of information on an aspect controlling
evolutionary potential, since the functional role a species performs in an ecosystem could influence
not only its own evolutionary potential, but also those of other species – ecosystem engineers for
example, could determine the niches available for species to occupy and radiate among through
niche construction (Erwin, 2008). Fritz & Purvis (2010) found that for large mammals, a measure of
EDGE = ln(1+ED) + GE * ln(2)
Figure 4 – (From Isaac et al. 2007) The EDGE equation.
The EDGE equation gives a score for each species based on ED (a measure of their evolutionary
distinctiveness) and GE (a measure of the threat level they face from extinction obtained from the IUCN Red
List). Together these metrics not only prioritise species based on their ED, but also on the relative risk they
face of becoming extinct which helps target conservation efforts on species that not only warrant more
attention, but also those that require it.

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Body Mass Variance (BMV) was better at estimating losses in FD compared to PD, whilst Jernvall &
Wright (1998) also suggested PD poorly captures FD of primates as phylogenetically clustered and
distinct taxa can be equally ecologically different. However, Flynn et al. (2011) suggested PD did not
perform as poorly in capturing functional roles in plants, implying PD might just be decoupled from
FD for certain clades – although, as with taxonomic richness and PD, this is not ideal.
There may also be fundamental problems with using PD as a proxy for feature diversity, since
Davies (2015) points out that results will depend upon whether one assumes features diverge
gradually or via punctuated equilibrium. Moreover, Kelly et al. (2014) found that a saturation point
is reached in phylogenetic trees where divergence in feature similarity stops increasing as species
become more evolutionarily distinct, thus suggesting a poorer correlation between feature
diversity and PD than first suggested.
Another problem Nee & May (1997) highlight is that there is no empirical evidence to determine
whether a more evolutionarily distinct species (such as a tuatara (Sphenodon punctatus), river
dolphin or long-beaked echidna (Zaglossus spp.)) has more or less evolutionary potential than a less
evolutionarily distinct species (such as a grass snake (Natrix natrix)) (Fig.5).

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Figure 5 – (Adapted from Erwin, 2008) Comparison between the impacts of extinction of two species with very different
levels of evolutionary distinctiveness. Dotted arrows reflect relative amount of loss of evolutionary history.
If one considers the grass snake (Natrix natrix) as being one of the terminal branches that could be lost from
extinctions shown in scenario A, the overall structure of the phylogenetic tree is relatively intact – 3 taxa are lost at
the tips but the branch lengths represent a small amount of evolutionary history. In scenario B, 7 taxa are lost from
losing one clade but again the overall structure of the tree remains relatively the same but there is slightly more loss
of evolutionary history. In scenario C, the single extinction of the tuatara (Sphenodon punctatus) removes the deepest
branch of the phylogenetic tree and consequently a large amount of evolutionary history, even far more than losing a
whole clade of 7 more closely related snake species.
However, even though the tuatara might represent more evolutionary history than the grass snake, but there is still
no consensus on whether it acts as a relic of its evolutionary history (no longer speciates) or a cradle of evolutionary
potential (Erwin, 2008).
Photos: (Garrod, n.d.) and (Marris, n.d.)

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Winter et al. (2013) suggest this means species-based conservation strategies cannot consider PD if
there is no knowledge of the relationship between a species’ position in the phylogenetic tree and
its evolutionary potential. Community-based approaches however, can consider PD if one assumes
closely related species have more similar evolutionary potentials than distantly related species, so
by maximising PD, one maximises the probability a clade will be present in the future with a high
level of evolutionary potential (Winter et al., 2013). Isaac et al. (2007) dismiss the relevance of
these arguments from a practical conservation perspective, since mammalian species with lower
ED scores (lower PD) tend to be less threatened with extinction and so are more likely to survive
the current biodiversity crisis, necessitating that species with higher ED scores are in greater need
of protection, regardless of evolutionary potential.
On the other hand, Nee & May (1997) claim that calculating PD to prioritise conservation efforts is
pointless because not only would a loss of 95% of species still leave 80% of the Tree of Life intact,
but also that random selection of species has the same effect of preserving feature diversity as
selecting species using PD. However, the authors ignored the phenomena of coextinctions
(extinctions of species are intricately linked through their ecological dependence on others) and
phylogenetic clustering of extinction risk which will result in more extensive losses in PD and the
Tree of Life (Koh et al., 2004; Davies, 2015)). Nevertheless, Parhar & Mooers (2011) reported
results that evidenced Nee & May (1997) as PD losses did not differ significantly from that expected
“Do we save the branches of the tree of life…or do we save the
twigs?”
Krajewski 1991

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when one considered phylogenetically clustered extinctions – despite greater absolute losses. Such
results remain contentious, although they may imply a need for an integration of more aspects of
diversity – particularly FD – into future metrics for use in conservation.
Integrating diversity measures for conservation strategies
A stronger integration of FD into measures of PD seems to be supported by current evidence, also
since ‘functional redundancy’ is not always borne out in reality which could cause greater than
expected losses in PD (Hector & Bagchi, 2007; McCann, 2000; Fritz & Purvis, 2010). Indeed, Erwin
(2008) also highlights the importance of considering architectural diversity, reflecting ecosystem
engineers’ importance in niche construction in the ecosystem. It would also be helpful to integrate
the possible consequences of a species’ extinction into PD, since if there is an early loss of
architectural diversity in this biodiversity crisis, there could be a positive feedback effect on
extinctions, reducing PD further and limiting species’ evolutionary potentials (Erwin, 2008; Davies,
2015). However, such integrations will increase the complexity and cost of PD greatly, which in the
time- and resource-limited world of conservation is probably not viable (Winter et al., 2013).
Pardi & Goldman (2007) have also suggested that as the easiest and cheapest diversity measure to
calculate, taxonomic richness could be used as an auxiliary criterion in conservation planning if PD
finds two or more equally optimal solutions for complementarity-based approaches – although in
practice, financial viability of recommendations is likely to be a bigger factor in decision-making.
The staggering number of indices for PD also calls for a unification of PD measures, with 8 alone
listed in Winter et al. (2013) as well as confusingly similar PD in Faith (1992a) and taxic diversity in
Vane-Wright et al. (1991). Worryingly, these two yielded very different results when used to find
which species of bumblebee (Apidae) to protect (Faith, 1992a). A consensus decision on a

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standardised set of measures, much like physical SI units, for different aspects of conservation
(from species to community level) must be reached to guide conservationists with limited
theoretical knowledge of these measures (Winter et al., 2013; Rosauer & Mooers, 2013).
To use or not to use?
PD has had limited use in the conservation sector due to many of the controversies and lack of
empirical evidence backing up its credentials for estimating evolutionary potential (Winter et al.,
2013). However fundamentally, PD has been found to be a valid measure that captures many
aspects of biodiversity very well – although it may lose information on the functional roles of
species in their ecosystem, the greater difficulty in calculating FD probably makes this unrealistic
(Winter et al., 2013). Unlike FD, Rosauer & Mooers (2013) suggest the time and cost of calculating
PD is decreasing quickly because of new tools such as Biodiverse (Laffan et al., 2010), as well as the
development of rigorously sampled and taxonomically-broad trees (for instance, the bird
phylogeny by Jetz et al. (2012)).
Despite this however, from a conservationist’s perspective most measures of taxonomic richness
are still far less complicated, costly and time-consuming to use (Winter et al., 2013). Therefore, as
long as the limitations of such proxy measures are known, using taxonomic richness as a surrogate
for PD could be a far more viable option for developing conservation strategies.
Ultimately, it comes down to choosing between delaying concerted action (through time-consuming
arguments over which diversity measures to use) versus taking coordinated action based on the
best evidence available, even if this turns out to be suboptimal in the future. If PD is to be used, a
unifying framework of PD measures with consensus amongst conservationists in the field and

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theoretical evolutionary ecologists needs to be made – a reasonable action to take could be the
expansion of the EDGE programme.
If multiple diversity measures are continued to be used in an uncoordinated fashion,
conservationists will lack the guidance and direction on how and why to use PD in the field and
thus how to preserve evolutionary potential. With a race against the ticking clock of species
extinctions, if it can be agreed that taxonomic richness can be a reasonable proxy for PD, then its
advantages as being simpler, faster and more resource-effective probably mean that PD might not
be the most useful measure of evolutionary potential for developing conservation strategies in the
coming century.

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