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

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

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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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