Phylogeny and Conservation Conservation Biology

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Phylogeny and Conservation
Phylogeny is a potentially powerful tool for conserving biodiversity. This book explores
how it can be used to tackle questions of great practical importance and urgency for
conservation. For example, what role should phylogeny play in delimiting units of
conservation? Does phylogeny provide a good surrogate measure of biodiversity? How
can phylogeny be incorporated into area-selection algorithms to maximise biodiversity
coverage, and how much difference does it make? Using case studies from many
different taxa and regions of the world, the volume evaluates how useful phylogeny is
in understanding the processes that have generated today’s diversity and the processes
that now threaten it. The novelty of many of the applications, the increasing ease with
which phylogenies can be generated, the urgency with which conservation decisions
have to be made and the need to make decisions that are as good as possible together
make this volume a timely and important synthesis, which will be of great value to
researchers, practitioners and policy-makers alike.
ANDY PURVIS is Reader in Biodiversity at Imperial College London. His research
interests focus on the use of phylogenies to study macroevolution and extinction.
JOHN L. GITTLEMAN is Professor of Biology at the University of Virginia. His
current research examines global patterns and processes of speciation and extinction
in mammals.
THOMAS BROOKS is head of the Conservation Synthesis Department in
Conservation International’s Center for Applied Biodiversity Science. His interests lie
in species conservation, particularly birds, and tropical forest biodiversity hotspots.
Conservation Biology
Conservation biology is a flourishing field, but there is still enormous potential for
making further use of the science that underpins it. This new series aims to present
internationally significant contributions from leading researchers in particularly active
areas of conservation biology. It will focus on topics where basic theory is strong and
where there are pressing problems for practical conservation. The series will include
both single-authored and edited volumes and will adopt a direct and accessible style
targeted at interested undergraduates, postgraduates, researchers and university
teachers. Books and chapters will be rounded, authoritative accounts of particular
areas with the emphasis on review rather than original data papers. The series is the
result of a collaboration between the Zoological Society of London and Cambridge
University Press. The series editors are Professor Morris Gosling, Professor of Animal
Behaviour at the University of Newcastle upon Tyne, Professor John Gittleman,
Professor of Biology at the University of Virginia, Charlottesville, Dr Rosie Woodroffe
of the University of California, Davis, and Dr Guy Cowlishaw of the Institute of
Zoology, Zoological Society of London. The series ethos is that there are unexploited
areas of basic science that can help define conservation biology and bring a radical new
agenda to the solution of pressing conservation problems.
Published Titles
1. Conservation in a Changing World, edited by Georgina Mace, Andrew Balmford and
Joshua Ginsberg 0 521 63270 6 (hardcover), 0 521 63445 8 (paperback)
2. Behaviour and Conservation, edited by Morris Gosling and William Sutherland
0 521 66230 3 (hardcover), 0 521 66539 6 (paperback)
3. Priorities for the Conservation of Mammalian Diversity, edited by Abigail Entwistle and
Nigel Dunstone 0 521 77279 6 (hardcover), 0 521 77536 1 (paperback)
4.Genetics, Demography and Viability of Fragmented Populations, edited by Andrew G.
Young and Geoffrey M. Clarke 0 521 78207 4 (hardcover), 0 521 794218 (paperback)
5. Carnivore Conservation, edited by John L. Gittleman, Stephan M. Funk,
David Macdonald and Robert K. Wayne 0 521 66232 X (hardcover),
0 521 66537 X (paperback)
6.Conservation of Exploited Species, edited by John D. Reynolds, Georgina M. Mace,
Kent H. Redford, and John G. Robinson 0 521 78216 3 (hardcover),
0 521 78733 5 (paperback)
7. Conserving Bird Biodiversity, edited by Ken Norris and Deborah J. Pain 0 521 78340 2
(hardcover), 0 521 78949 4 (paperback)
8. Reproductive Science and Integrated Conservation, edited by William V. Holt, Amanda
R. Pickard, John C. Rodger and David E. Wildt 0 521 81215 1 (hardcover),
0 521 01110 8 (paperback)
9.People and Wildlife: Conflict or Co-existence? edited by Rosie Woodroffe, Simon
Thirgood and Alan Rabinowitz 0 521 82505 9 (hardcover), 0 521 53203 5 (paperback)
Phylogeny and Conservation
Edited by
andy purvis
john l . gittleman
thomas brooks
cambridge university press
Cambridge, New York, Melbourne, Madrid, Cape Town, Singapore, São Paulo
Cambridge University Press
The Edinburgh Building, Cambridge cb2 2ru, UK
First published in print format
isbn-13 978-0-521-82502-3
isbn-13 978-0-521-53200-6
isbn-13 978-0-511-12869-1
© The Zoological Society of London 2005
2005
Information on this title: www.cambridge.org/9780521825023
This publication is in copyright. Subject to statutory exception and to the provision of
relevant collective licensing agreements, no reproduction of any part may take place
without the written permission of Cambridge University Press.
isbn-10 0-521-82502-4
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guarantee that any content on such websites is, or will remain, accurate or appropriate.
Published in the United States of America by Cambridge University Press, New York
www.cambridge.org
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Contents
List of contributors page [ix]
1 Phylogeny and conservation [1]
andy purvis , john l . gittleman and thomas
m. brooks
Part 1 Units and currencies
2 Molecular phylogenetics for conservation biology [19]
elizabeth a . s inclair , marcos p e´rez -losada
and keith a . crandall
3 Species: demarcation and diversity [57]
paul -michael agapow
4 Phylogenetic units and currencies above and below
the species level [76]
john c. avise
5 Integrating phylogenetic diversity in the selection of priority areas
for conservation: does it make a difference? [101]
ana s . l . rodrigues , thomas m. brooks
and kevin j . gaston
6 Evolutionary heritage as a metric for conservation [120]
arne ø. mooers , stephen b. heard
and eva chrostowski
Part 2 Inferring evolutionary processes
7 Age and area revisited: identifying global patterns and implications
for conservation [141]
kate e . jones , wes sechrest and john l . gittleman
vi Contents
8 Putting process on the map: why ecotones are important
for preserving biodiversity [166]
thomas b . smith, sassan saatchi , catherine graham,
hans slabbekoorn and greg spicer
9 The oldest rainforests in Africa: stability or resilience for survival
and diversity? [198]
jon c . lovett, rob marchant, james taplin and
wolfgang ku¨per
10 Late Tertiary and Quaternary climate change and centres of endemism
in the southern African flora [230]
guy f. midgley, gail reeves and cornelia klak
11 Historical biogeography, diversity and conservation of Australia’s
tropical rainforest herpetofauna [243]
craig moritz , conrad hoskin , catherine h. graham,
andrew hugall and adnan moussall i
Part 3 Effects of human processes
12 Conservation status and geographic distribution of avian evolutionary
history [267]
thomas m. brooks , john d. pilgrim,
ana s . l . rodrigues and gustavo a . b . da fonseca
13 Correlates of extinction risk: phylogeny, biology, threat and
scale [295]
andy purvis , marcel cardillo , richard grenyer
and ben collen
14 Mechanisms of extinction in birds: phylogeny, ecology
and threats [317]
peterm. bennett, ian p. f. owens , daniel nussey,
stephen t. garnett and gabriel m. crowley
15 Primate diversity patterns and their conservation in Amazonia [337]
jos e´ maria cardoso da silva , anthony b . rylands ,
jos e´ s . s i lva j u´nior , claude gascon and
gustavo a . b . da fonseca
16 Predicting which species will become invasive: what’s taxonomy got to
do with it? [365]
julie lockwood
Contents vii
Part 4 Prognosis
17 Phylogenetic futures after the latest mass extinction [387]
sean nee
18 Predicting future speciation [400]
timothy g. barraclough and t. jonathan davies
Index [419]
Contributors
paul -michael agapow
Department of Biology
University College London
Darwin Building
Gower Street
London WC1E 6BT
UK
john c. avise
Department of Ecology and
Evolutionary Biology
University of California
Irvine, CA 92697
USA
timothy g barraclough
Department of Biological Sciences and
NERC Centre for Population Biology
Imperial College London
Silwood Park Campus
Ascot
Berks SL5 7PY
UK
peter m. bennett
Institute of Zoology
Zoological Society of London
Regent’s Park
London NW1 4RY
UK
thomas m. brooks
Conservation Synthesis Department
Center for Applied Biodiversity Science
Conservation International
1919 M St
NW Suite 600
Washington, DC 20036
USA
marcel cardillo
Department of Biological Sciences
Imperial College London
Silwood Park Campus
Ascot
Berks SL5 7PY
UK
and
Institute of Zoology
Zoological Society of London
Regent’s Park
London NW1 4RY
UK
jos e´ maria cardoso da silva
Conservation International do Brasil
Av Nazare 541/310
66035-170 Bele´m
Para´
Brazil
eva chrostowski
Department of Biological Sciences
Simon Fraser University
Burnaby
Canada V5A 1S6
ben collen
Department of Biological Sciences
Imperial College London
Silwood Park Campus
Ascot
Berks SL5 7PY
UK
and
x List of contributors
Institute of Zoology
Zoological Society of London
Regent’s Park
London NW1 4RY
UK
keith a . crandall
Department of Integrative Biology
Monte L. Bean Life Science Museum
Brigham Young University
Provo, UT 84602-5255
USA
gabriel m. crowley
Institute of Advanced Studies
Charles Darwin University
Northern Territory 0909
Australia
gustavo a . b . da fonseca
Center for Applied Biodiversity Science
Conservation International
1919 M St
NW Suite 600
Washington, DC 20036
USA
t. jonathan davies
Department of Biological Sciences and
NERC Centre for Population Biology
Imperial College London
Silwood Park Campus
Ascot
Berks SL5 7PY
UK
and
Jodrell Laboratory
Molecular Systematics Section
Royal Botanic Gardens Kew
Richmond
Surrey TW9 3DS
UK
stephen t. garnett
Institute of Advanced Studies
Charles Darwin University
Northern Territory 0909
Australia
claude gascon
Center for Applied Biodiversity Science
Conservation International
1919 M Street NW
Suite 600
Washington, DC 20036
USA
kevin j . gaston
Biodiversity and Macroecology Group
Department of Animal and Plant Sciences
University of Sheffield
Sheffield S10 2TN
UK
john l . gittleman
Department of Biology
Gilmer Hall
University of Virginia
Charlottesville, VA 22904
USA
catherine graham
Museum of Vertebrate Zoology
University of California at Berkeley
Berkeley, CA 94720
USA
and
Department of Ecology and Evolution
State University of New York
Stony Brook, NY 11794
USA
richard grenyer
Department of Biological Sciences
Imperial College London
Silwood Park Campus
Ascot
Berks SL5 7PY
UK
stephen b. heard
Department of Biology and
Canadian Rivers Institute
University of New Brunswick
Fredericton
Canada E3B 6E1
sheard@unb.ca
List of contributors xi
conrad hoskin
Department of Zoology and Entomology
The University of Queensland
QLD 4072
Australia
andrew hugall
Department of Zoology and Entomology
The University of Queensland
QLD 4072
Australia
and
Environmental Biology
University of Adelaide
SA 5005
Australia
kate e . jones
Department of Biology
Gilmer Hall
University of Virginia
Charlottesville, VA 22904
USA
cornelia klak
Bolus Herbarium
University of Cape Town
7701 Rondebosch
South Africa
wolfgang ku¨per
Botanical Institute
University of Bonn
Meckenheimer Allee 170
D-533115 Bonn
Germany
julie lockwood
Environmental Studies
University of California
Santa Cruz, CA 95064
USA
Present address:
Ecology, Evolution and Natural Resources
Rutgers University
New Brunswick, NJ 08902
USA
jon c . lovett
Environment Department
University of York
York YO10 5DD
UK
rob merchant
Department of Botany
Kruislaan 318
1098 SM Amsterdam
The Netherlands
and
Department of Botany
Trinity College Dublin
Dublin 2
Ireland
guy f. midgley
Climate Change Research Group
National Botanical Institute
Private Bag X7
Claremont 7735
Cape Town
South Africa
and
Center for Applied Biodiversity Science
Conservation International
1919 M Street
NW Suite 600
Washington, DC 20036
USA
arne ø. mooers
Department of Biological Sciences
Simon Fraser University
Burnaby
Canada V5A 1S6
craig moritz
Museum of Vertebrate Zoology
University of California at Berkeley
Berkeley, CA 94720
USA
and
xii List of contributors
Department of Zoology and Entomology
The University of Queensland
QLD 2072
Australia
adnan moussall i
Department of Zoology and Entomology
The University of Queensland
QLD 2072
Australia
sean nee
Institute of Cell, Animal and Population
Biology
University of Edinburgh
West Mains Road
Edinburgh EH9 3JT
UK
daniel nussey
Institute of Zoology
Zoological Society of London
Regent’s Park
London NW1 4RY
UK
and
School of Biology
University of Edinburgh
The King’s Buildings
West Mains Road
Edinburgh EH9 3JT
UK
ian p. f. owens
Department of Biological Sciences
Imperial College London
Silwood Park Campus
Ascot
Berks SL5 7PY
UK
marcos perez -losada
Department of Integrative Biology
School of Natural Sciences
Edith Cowan University
Perth, WA 6027
Australia
john d. pilgrim
Center for Applied Biodiversity Science
Conservation International
1919 M St
NW Suite 600
Washington, DC 20036
USA
andy purvis
Department of Biological Sciences
Imperial College London
Silwood Park Campus
Ascot
Berks SL5 7PY
UK
gail reeves
Leslie Hill Molecular Systematics
Laboratory
National Botanical Institute
Private Bag X7
Claremont 7735
Cape Town
South Africa
ana s . l . rodrigues
Conservation Synthesis Department
Center for Applied Biodiversity Science
Conservation International
1919 M St
NW Suite 600
Washington, DC 20036
USA
anthony b . rylands
Center for Applied Biodiversity Science
Conservation International
1919 M Street
NW Suite 600
Washington, DC 20036
USA
sassan saatchi
Radar Science Section
Jet Propulsion Laboratory
Pasadena, CA 91109
USA
wes sechrest
Department of Biology
Gilmer Hall
University of Virginia
Charlottesville, VA 22904
USA
jos e´ s . s i lva junior
Museu Paraense Emı´lio Goeldi
Departamento de Zoologia
C.P. 399
66017-970 Bele´m
Para´
Brazil
List of contributors xiii
elizabeth a . s inclair
Department of Integrative Biology
School of Natural Sciences
Edith Cowan University
Perth, WA 6027
Australia
hans slabbekoorn
Behavioural Biology
Institute of Evolutionary and Ecological
Sciences
Leiden University
2300 RA Leiden
The Netherlands
thomas b . smith
Center for Tropical Research
Institute of the Environment
University of California at Los Angeles
1609 Hershey Hall
Box 951496
Los Angeles, CA 90095-1496
USA
greg spicer
Department of Biology
San Francisco, State University
1600 Holloway
San Francisco, CA 94132
USA
james taplin
Environment Department
University of York
York YO10 5DD
UK
1
Phylogeny and conservation
A N D Y P U R V I S , J O H N L . G I T T L E M A N
A N D T H O M A S M . BR O O K S
W H Y A B O O K O N P H Y L O G E N Y A N D C O N S E R VAT I O N ?
Of the many sub-fields of biology, phylogenetics and conservation biology
are two of the fastest growing. On the one hand, the explosion of phylogenet-
ics – the study of evolutionary history – has been stimulated over the past
two decades by the emergence of new molecular methods and statistical
techniques for modelling the tree of life. DNA sequence data are now typ-
ically freely available through public-access databases such as GENBANK,
and much software for phylogeny estimation is cheap and easy to use. On
the other hand, the tree of life is being heavily pruned by human activities;
this pruning has helped to drive the emergence of the applied discipline of
conservation biology.
Bibliometric data provide a rough-and-ready way to summarise the
growth in the two disciplines. There was an exponential increase in the
number of papers in both fields between 1992 and 2003, as shown by a
search of the Science Citation Index with the keywords ‘conservation biol-
ogy’ and ‘phylogen∗’. According to these searches (other terms would give
slightly different results), numbers of papers in each discipline are growing
at about 12%. The growth rate of the intersection set – papers linking conser-
vation biology and phylogenetics – is slightly (although non-significantly)
lower at 10.4%. Numbers of papers found by a search for ‘phylogen∗’ in four
conservation journals (Conservation Biology, Biological Conservation, Biodi-
versity and Conservation and Animal Conservation) over the same period have
increased at about the same rate (13%) as phylogenetics papers overall.
These results all suggest that, although phylogenetics has been permeat-
ing conservation biology over the past decade, there has so far been little
synergy.
C© The Zoological Society of London 2005
2 A. Purvis, J. L. Gittleman and T. M. Brooks
Why, then, are we interested in the overlap between these historically
separate fields of biological endeavour? The main reason is the direction in
which both fields are growing, rather than the speed. As the magnitude of
the anthropogenic threat to biodiversity has become apparent, much con-
servation biology has focused on systematic conservation planning, priority-
setting and monitoring trends, and on the biodiversity assessment required
to provide the data for those activities. An effect of this transition is that con-
servation biologists are increasingly dealing with taxa whose natural history
and even species membership is poorly known. The increase of available
phylogenies is inversely related to the demise of basic descriptive taxonomy
(Wheeler 2004; Wheeler et al. 2004). Proposals to base species descriptions
upon DNA sequences instead of morphology, and even to build the com-
plete tree of life – both unthinkable a few years ago – must now be taken
seriously. Increasingly, an organism’s position in phylogeny will be one of
the few things we know about it with any precision (Mace et al. 2003). It
is therefore timely to explore the ways in which the wealth of new phyloge-
netic information can benefit conservation biology. This book is the result
of a Symposium of the Zoological Society of London, organised to investi-
gate these issues. The meeting was held on 6–7 February 2003.
We have structured this book around four areas where phylogeny should
give insights into conservation issues. First, phylogeny can help delimit the
units and currencies of biodiversity assessment and management (Cracraft
1983; Vane-Wright et al. 1991). Second, phylogeny is a record (albeit only a
partial one) of how biodiversity has come about: the evolutionary processes
responsible for it (Harvey et al. 1996). Understanding origins can assist in
the conservation of biodiversity by contrasting current versus historical pat-
terns, and of the processes that have generated these patterns. Third, phy-
logeny provides a statistical framework for the rigorous investigation of how
human processes – habitat loss, overexploitation, species introductions –
are affecting biodiversity (Fisher & Owens 2004). Fourth, it is possible
to extrapolate from the past and present into the phylogenetic future, in
order to predict what might happen to biodiversity under possible scenarios
(Rosenzweig 2001). We enlarge on each of these below.
U N I T S A N D C U R R E N C I E S
Traditionally, the units of conservation biology have been species (Agapow
et al. 2004). The severity of the current biodiversity crisis is often expressed
in terms of numbers of species that have gone, are going, or are in immi-
nent danger of going, extinct. Species provide an intuitive currency for
Phylogeny and conservation 3
comparing the biodiversity value of different locations. Management plans
often focus on particular species. However, species can be hard to demar-
cate, with a great many decision rules available from which to choose (Hey
2001; Mayden 1997; Sites & Marshall 2003). Further, many species harbour
considerable diversity among their populations, a fact with two important
and related implications: the species should perhaps not be managed as
a single entity (for example, translocating individuals among populations
may be harmful to the species), and conservation of a single population of
the species does not conserve all of the diversity. Phylogenetics made its first
impressions on conservation biology by providing possible extra units (e.g.
evolutionarily significant units (Avise 2000)) and currencies (e.g. phyloge-
netic distinctiveness (Faith 1992)) for conservation biology. The first two
chapters of this book consider phylogeny’s role in demarcating units; then
the subsequent three chapters consider the use of currencies derived from
phylogeny when trying to set conservation priorities.
Chapter 2 starts with an overview of how evolutionary relationships can
be inferred both among and within species, focusing on practical issues
of study design and on recent methodological developments (Felsenstein
(2004) provides a general review of the whole field). The chapter concludes
with two examples showing how the results of such analyses can help to
demarcate species and, by revealing the patterns of gene flow, manage-
ment units. Despite the rapid growth of phylogenetics, phylogenies of the
detail and sophistication described in this chapter are still very much the
exception. Many later chapters use less statistically justified phylogenies, or
taxonomies as surrogates for phylogeny. This lack-of-fit is a transient phe-
nomenon: phylogenies will improve, and it makes sense to use the best
surrogate we have at any given time, whatever it is.
The use of phylogenetics in conservation is sometimes controversial,
nowhere more so than in the application of the phylogenetic species concept
(PSC). Formulations differ in the detail, but the essence of the proposal is
that species are the least inclusive clades in phylogenies: they are the small-
est sets of populations that can be told apart from other sets. The PSC has
been gaining ground in recent years because of its ease of application: there
is no difficult decision about whether two distinct lineages are sufficiently
diverged to be recognised as separate species. In Chapter 3, Agapow reports
that, on average, species lists based on PSC contain about twice as many
species as lists for the same groups based on the biological species concept.
He goes on to explore some of the problematic consequences of this change,
and suggests ways in which conservation biologists might avoid such prob-
lems. Among these ways is the idea of using species’ unique evolutionary
4 A. Purvis, J. L. Gittleman and T. M. Brooks
history, or phylogenetic distinctiveness (PD), as a currency of biodiversity,
rather than focus on counting species (Faith 1992). The last three chapters
in Part 1 consider differentaspects of PD.
Based on the emerging science of conservation genetics, with a founda-
tion in phylogenetics, Avise (Chapter 4) considers two possibilities for how
phylogenies may be effective in management decisions. First, using earlier
work on comparing phylogenetic measures with trait or ecological diver-
sity (see, for example, Faith 1992; Vane-Wright et al. 1991), Avise develops
a ranking procedure for assessing how species in clades can be selected for
conservation management based on differences in phylogenetic diversity
relative to other measures such as rarity, endemism, ecology or charisma.
Some examples show that this priority-based system can isolate a species
such as the giant panda (Ailuropoda melanoleuca) because it has clearly high
values relative to other bear species. However, analyses of other groups,
such as horseshoe crabs or cats, are ambiguous. When ecological and phy-
logenetic diversity are relatively equal or, more often, when these measures
are poorly known, then such a priority analysis is limited (for example,
how can we decide between the polar bear (Ursus maritimus) and brown
bear (U. arctos)?). In general, Avise is sceptical as to whether phylogenetic
analysis has much to offer at the interspecific level. This conclusion can be
confounded by other factors, however: conservation prioritisation generally
considers areas rather than species (Margules & Pressey 2000), and com-
binatorial scoring of this kind will necessarily produce subjective results
(Williams & Arau´jo 2002).
Second, Avise emphasises that because phylogenetic analyses have been
successful at intraspecific levels for describing genetic diversity, adaptive
variability to habitat change and the consequences of population fragmenta-
tion, it is at this level that phylogenies are beneficial. For example, he argues
that the constructs of evolutionarily significant units (ESUs) and manage-
ment units (MUs) are relevant to conservation prioritisation, with phylo-
geographic analyses setting the primary criteria for establishing these units
for individual species (see Crandall et al. 2000). The future of phylogenies
in conservation rests, Avise argues, with how to use the kind of informa-
tion gleaned at intraspecific levels to inform conservation decisions at global
levels.
In Chapter 5, Rodrigues et al. consider a separate question concerning
PD: if it is used for priority-setting, does it lead area-selection algorithms
to choose areas different from those selected solely on the basis of species
data? The extra information about evolutionary history that phylogeny con-
tains may suggest an efficiency gain, in terms of how much diversity is
Phylogeny and conservation 5
captured within a set of preferred areas. But is the gain large or small?
Their simulation study finds that the gain will not in general be large unless
four conditions are all met: the phylogeny must be unbalanced, the geog-
raphy must show a phylogenetic pattern, old species must tend to have
smaller geographic ranges, and these old species must tend to be endemic
to species-poor areas. The first condition is usually met (Mooers & Heard
1997; Stam 2002) and the second is so common it is even a prerequisite
for cladistic biogeography. Jones et al. (Chapter 7 below) report evidence for
the third. Little is so far known about how often old species are endemic
to species-poor areas, indicating that this is an important priority for future
research. Later chapters contain several case studies that bear on the issue
of whether phylogeny will affect choice of areas: some (e.g. Moritz, et al.
Chapter 11) suggest that it will, others (e.g. Brooks et al., Chapter 12) that it
will not.
Mooers et al. (Chapter 6) round off Part 1 by attempting to bridge the
gap between scientific precision and political reality with their discussion
of ‘evolutionary heritage’. Here, they propose measurements of PD at the
national level, in order to inspire conservation both in its own country
and through international aid. The idea of highlighting national heritage –
especially of endemism, for countries have ultimate responsibility for their
endemic species – is not a new one (Mittermeier et al. 1998). The novelty
here is in incorporating phylogenetic history. Two caveats face this, how-
ever. On the one hand, it is unclear how well evolutionary heritage will res-
onate with policy-makers, especially given that many of the nations identi-
fied as having the greatest evolutionary heritage retain creationist beliefs at
the state level. Second, the jury is still out as to how much the evolutionary
precision added by this metric changes the results of conservation planning
relative to consideration of species alone (Rodrigues et al., Chapter 5).
I N F E R R I N G E V O L U T I O N A R Y P R O C E S S E S
Knowing how diversity arose is important for at least three related reasons
in conservation. First, a process-based understanding of diversity patterns
provides a null expectation against which today’s state of play can be judged.
Such use of null models can help to identify lineages whose distribution is
narrower than might be expected, for example (see Webb et al. 2001). Sec-
ond, an understanding of the mechanisms that generate diversity is essen-
tial if we are to safeguard their future through conservation of evolutionary
process as well as of the pattern it has produced. Because phylogenies con-
tain information about how they grew – about how biodiversity arose – some
6 A. Purvis, J. L. Gittleman and T. M. Brooks
of the necessary understanding can be gleaned from careful analysis of phy-
logeny (Harvey et al. 1996). Lastly, knowledge of how particular lineages
have responded to challenges in the past may help us to understand how
they are now responding, or will soon respond, to anthropogenic changes.
The first chapter in Part 2 revisits one of the oldest conundrums in
evolutionary biology – the relationship between the age and the extent of
occurrence of a taxon (Willis 1922) – in an attempt to model the underlying
process. Jones et al. (Chapter 7) offer new insight into age–area relations,
using a remarkable dataset of the geographic distributions of all mammal
species (compiled at the University of Virginia and now comprising the
basis for the IUCN Global Mammal Assessment) plus two of the most com-
plete supertrees compiled to date, for primates (Purvis 1995) and carnivores
(Bininda-Emonds et al. 1999). For both taxa, Jones et al. tentatively support
a model of declines in species’ range sizes over time. Further, they find that,
contrary to previous evidence (see, for example, Webb & Gaston 2003), there
tends to be phylogenetic correlation across range sizes, for primates and car-
nivores at least. Based on these findings, they then ask whether currently
threatened species have smaller range sizes than would be expected by their
phylogeny, and, as expected, find that they do.
Although the importance of preserving pattern and process is readily
acknowledged, the pattern is difficult to achieve in practice. The next four
chapters in Part 2, however, illustrate ways of beginning to address evo-
lutionary process. The field studies of Smith and colleagues (Chapter 8)
on West African populations of the little greenbul (Andropadus virens) inves-
tigate the processes that cause differentiation resulting from isolation and
ecological selection. Using a combination of molecular, behavioural and
phylogenetic analyses at both intra and inter-specific levels, Smith et al.
show that divergence in fitness-related characters (body mass, wing length)
and parallel characters of male song types are mainly related to habi-
tat rather than to geographic isolation. Analysis of sister species across
the sunbird family are also consistent with gradients of speciation associ-
ated with different habitats. Different qualities of tree density and climatefound within ecotones suggest that ecologically they are extremely impor-
tant for areas of speciation, at least in the ecotones of West Africa. Unfor-
tunately, these areas are also attractive to human settlements. Future work
is needed to sort out how ecotones are structured worldwide, whether they
are also cradles of speciation and, if so, how to protect them from habitat
degradation.
What happens when a biodiverse area is shocked by climatic change or
habitat degradation? A triad of chapters, from the Eastern Arc of eastern
Phylogeny and conservation 7
Africa, the South African Fynbos and Succulent Karoo, and the wet tropics
of Australia, show the processes by which species respond to these changes.
Lovett et al. (Chapter 9) study geologically ancient rainforests in Africa, dat-
ing back perhaps to the Miocene, to assess the question of whether biodi-
versity can withstand change by community stability, or whether it is adapt-
able. The distributions of over 100 tree species along a gradient of 158 plots
through the elevational range of the forests suggest the former. Further,
these Eastern Arc rainforests appear more stable than other areas in sub-
Saharan Africa. The phylogenetic implication is that such areas of high
endemism hold numerous closely related species that respond in kind to
temperature and rainfall gradients. Further analyses adopting a more explic-
itly phylogenetic perspective should find out whether other global centres
of endemism hold closely related taxa.
It is commonly thought that Pleistocene climate change has dramatically
influenced the unusually high plant endemism in the Fynbos and Succulent
Karoo biomes of southern Africa. As with other species hotspots it is impor-
tant to disentangle such historic from current ecological effects influencing
regional differences in species richness. In Chapter 10, Midgley et al. pull
together palaeoecological data, present biogeographic maps and phyloge-
netic information to assess these patterns. The clearest explanation is that
climatic history produced shifts in geographic extents of the two biomes,
resulting in speciation through vicariance and allopatry. Midgley et al. indi-
cate that anthropogenic climatic change could result in a loss of 51–65% of
the extent of the Fynbos biome, resulting in potentially significant species
losses. Similar global effects have also been reported elsewhere (Thomas
et al. 2004). The next generation of global change studies could usefully
incorporate phylogenetic analyses in order to evaluate historical background
climatic shifts from current levels.
Finally in Part 2, a detailed analysis reveals how the Eastern Australian
rainforests are also under intense threat from predicted climate change
(Williams et al. 2003). In Chapter 11, Moritz et al. show how past climate
has influenced the diversification and present diversity of three reptile and
amphibian clades within this region. They use phylogeographic insights
from snails – whose low vagility and need for moisture make their current
distribution a likely pointer to past refugia – to provide a backdrop against
which to compare herpetofaunal patterns and processes. Interestingly, the
groups studied show different evolutionary processes in response to the
same environmental history. Such differences clearly complicate the use
of one lineage as a surrogate for another. Furthermore, old lineages do tend
to be restricted to small and species-poor locations: two of the requirements
8 A. Purvis, J. L. Gittleman and T. M. Brooks
for PD to show patterns different from those of species-richness (Rodrigues
et al., Chapter 5). The study nicely shows how past refugia leave imprints on
today’s diversity patterns, and how even small areas can contain important
phylogenetic diversity. The lineage-specificity of responses to a common
climatic history provides another layer of challenges in predicting and mit-
igating what may happen in response to climate change.
E F F E C T S O F H U M A N P R O C E S S E S
Evolutionary processes such as those considered in the previous section
mean that diversity is not spread evenly over the globe. Most clades show lat-
itudinal gradients, with more species in tropical than in temperate regions
(Gaston 2000), as well as more complex non-random patterns of richness
(Davies et al. 2004). People also have more impact in some parts of the
world than in others: densities, land use and technological advancement
show complex patterns too. In the first chapter in Part 3, Brooks et al. (Chap-
ter 12) examine the spatial concordance between the fruits of natural diver-
sification processes and the threats caused by human actions. Their review
and analyses of birds illustrate how threats to species, threats to habitats,
evolutionary distinctness and endemism are all positively intercorrelated.
The authors argue that an important consequence is that conservation strat-
egy is quite tightly proscribed: arguments about whether to focus on areas
of greatest biodiversity value or those facing the severest threat lose impor-
tance if these areas are one and the same.
As well as providing the backdrop against which human actions play
out, phylogeny also gives a statistical and logical framework for analysing
the pattern of casualties, survivors and beneficiaries of those actions (Fisher
& Owens 2004). Because species biology tends to mirror phylogeny – i.e.
close relatives tend to be similar – evolutionary relationships should be con-
sidered in any comparative study of present-day conservation patterns. The
next two chapters use phylogeny in this way.
Using the primate and carnivore datasets discussed earlier, Purvis et al.
(Chapter 13) find selectivity of threat status in phylogeny and geography so
strong as to require consideration of phylogeny in all analyses of correlates
of extinction risk. They then go on to tease apart the impacts of threat inten-
sity per se from the interaction between biological characteristics and threat
intensity in determining threat status (as Purvis et al. point out, intrinsic
characteristics alone have a near-negligible impact on threat status). Two
particularly important results emerge. First is the importance of an addi-
tional parameter – scale – in determining the relative strengths of these
Phylogeny and conservation 9
factors. This notwithstanding, however, their second key result is the impor-
tance of incorporating biological characteristics in assessments of the deter-
minants of extinction risk, rejecting recent suggestions that measurements
of threat intensity such as human population density alone are relevant.
This chapter does not differentiate among the different ways in which peo-
ple endanger species; the remaining chapters in Part 3 probe more deeply
into particular threatening processes.
A multitude of causal factors such as small population size, habitat
depletion, and reduction in geographic range size all contribute to pop-
ulation decline in birds, with around 12% of species currently listed by
IUCN as threatened. Can an explicit phylogenetic approach help in under-
standing the current processes of extinction, and will this aid in staving off
levels of threat? In the face of many hypotheses, Bennett et al. (Chapter 14)
begin by showing that the distribution of extinction risk is not random
among birds: some families (e.g. parrots, Psittacidae, and cranes, Gruidae)
face a significantly higher prevalence of extinction risk than would be
expected under the ‘hail of bullets’ scenario. Similar patterns are known
throughout most animal and plant taxa (Purvis et al. 2000; Russell et al.
1998; Schwartz & Simberloff 2001). A comparative phylogenetic approach
reveals that threatened lineages have particular biological characteristics
that may predispose them to a higher risk of extinction. Specifically, larger
body mass and lower fecundity ratchetup threatened status as measured
from the IUCN Red List. Such biological characteristics vary considerably,
so the interesting problem is: how do species with divergent life histo-
ries respond to various human-related threats? Interestingly, the lineages
for which larger body mass is associated with greater threat status are
more vulnerable to human persecution or introduced predators, whereas
breeding specialisations are more influenced by habitat loss. Further, there
is evidence that ecological flexibility in diet and clutch size may allow
some species with ‘risky traits’ such as large size to overcome sources
of threat. The study by Bennett et al., along with other recent work (e.g.
that of Cardillo et al. 2004; Isaac & Cowlishaw 2004; Jones et al. 2003),
clearly shows multiple routes to the biological underpinnings of extinc-
tion risk. Future comparative work is needed, based on multivariate anal-
yses across large phylogenetic clades, to assess why some traits are more
risky than others and whether these are traits that have been historically
critical to adaptive radiations. In this way, speciation and extinction could
be tied together and phylogenetic analyses would be increasingly valuable
to conservation. The growing number of complete phylogenies and mas-
sive bioinformatic databases, together with the increasing sophistication
10 A. Purvis, J. L. Gittleman and T. M. Brooks
of methods for dealing with missing data in comparative analyses (Fisher
et al. 2003), give reason to be optimistic about the value of phylogenies for
conservation.
In Chapter 15, Cardoso da Silva et al. focus on habitat loss, the most
important single threatening process (Mace & Balmford 2000), at a finer
scale of phylogenetic and geographic resolution. They consider a single
taxon, primates, in a single region (albeit biologically the richest on the
planet), Amazonia. Based on claims initially made by Wallace in the 1850s,
they subdivide Amazonia into eight ‘areas of endemism’ and then exam-
ine primate diversity (including PD), likely deforestation around roads, and
protected-area coverage among these eight regions. They find a strong trend
in primate diversity from east to west (although this is at least partly driven
by the fact that the western ‘areas of endemism’ are much larger than those
in the east), but find that the eastern regions (especially Bele´m) are much
the most threatened and least protected. The contrast between these results
and those reported elsewhere in this volume (e.g. Brooks et al., Chapter 12)
of correlations between phylogeny and threat emphasise the result found
by Purvis et al. (Chapter 13) that these correlations can swing in unexpected
directions at fine scales.
Most biodiversity conservation attention focuses on diversity loss
through the loss of species and habitats, but diversity is also lost through
biotic homogenisation: the spread of invasive species reduces biological
differences between places. Lockwood (Chapter 16) provides an important
review of the literature on invasive success. She shows that, across a range
of plants and animals, the fact that one species is a successful invader much
increases the likelihood that a closely related species will also be. This does
not mean that phylogeny alone can be used as a predictor of invasion suc-
cess, but rather that phylogeny should be considered along with geography
and extrinsic factors in the science of pre-empting likely biotic invasion, a
result mirrored by that of Purvis et al. (Chapter 13) in considering extinction
risk.
P R O G N O S I S
Phylogeny helps us to understand both the distant and the recent past,
putting present-day diversity and extinction patterns into context. What can
we say of the future of phylogeny, given the intensity and breadth of anthro-
pogenic disturbance?
The first problem that the chapters in Part 4 raise is how a phyloge-
netic perspective shows that we may be looking at the wrong biodiversity:
Phylogeny and conservation 11
microscopic taxa are rarely discussed in general studies of biodiversity and
conservation, and yet they comprise the most abundant organisms on the
planet (Wilson 2002). In Chapter 17, Nee assesses how our views of con-
servation are skewed towards those few twigs of the tree of life that we can
see and comprehend. Would it really matter to the tree of life if all of the
macroscopic life became extinct? Nee’s unabashed answer is no: organisms
such as the Archaea or Apicomplexia, representing much of the tree of life,
will probably not be harmed by extinctions of large-scale organisms. Most of
our understanding of these organisms is taken from the medical literature,
thus if anything it would be more likely that the microscopic world that we
know is biased toward anthropomorphism. Nee then considers what we do
know about: extinctions of macroscopic life. Theory (Nee & May 1997) has
shown that losses of phylogenetic history may not be devastating if sister
lineages survive. Follow-up work grounded the theory by revealing that the
distribution of real-world extinctions, at least in birds, primates and carni-
vores (Purvis et al. 2000; von Euler 2001), are unfortunately much more
severe than predicted by theory. Nee emphasises that a useful phylogenetic
approach requires better models for what is an expected amount of evolu-
tionary history in a clade and how a null expectation is influenced by losses
of species.
Perhaps the greatest futuristic problem for phylogenies is where and
why new species are generated; if phylogenies can reveal how current
human activities are changing the evolutionary processes of speciation then
this could be a tremendous contribution toward preserving biodiversity.
Barraclough & Davies (Chapter 18) are pessimistic, however. First, our
methods and databases of trees for studying speciation mainly use recon-
struction techniques that are not very informative about the future of
speciation; most models are either not formalised sufficiently or the empiri-
cal data required to test them (e.g. detailed species distributional data to test
for allopatric vs. sympatric speciation) are unavailable, making it difficult
to compare differences in speciation across clades. Analytical issues aside,
after reviewing candidate factors that seem to correlate with high speciation
rates, Barraclough & Davies do not see that the typical empirical variables
such as body size, habitat or climate change explain many patterns. A more
optimistic suggestion is that, once combined effects of many variables are
placed in a single analysis, then it may be possible to see how changes in
habitat or climate change will interact with these multiple factors to alter the
process of speciation. As these authors admit, direct conservation applica-
tions of this work are limited, because the process of speciation takes place
over time periods much longer than those of conservation management.
12 A. Purvis, J. L. Gittleman and T. M. Brooks
Perhaps as we better understand the patterns of extinction and work
towards reducing species losses, then we will in turn preserve more species
of the future.
T H E S C O P E O F T H I S B O O K
Of perhaps ten million species in the world, hardly any are vertebrates, yet
vertebrates provide most of the case studies in this book. The approaches
used here are data-hungry, requiring phylogenetic information often in
addition to natural history data, and sometimes even requiring that
the information be available for all species. Such requirements force
researchers’ attention towards a few well-studied taxa: generally the large,
the obvious, and the charismatic. These taxa may not be typical, so the
gain in precision may be at the cost of a loss of generality (Mace et al.
2003). In this book, we have tried to keep the taxonomic scope as broad
as we could within the constraints imposed by the data (although,as Nee
points out in Chapter 17, most biologists work within a very narrow set of
taxa). In the longer term, progress on large-scale biotic sequencing projects
might increase the scope for using the approaches described and devel-
oped in this book, and will equally surely lead to the development of new
approaches.
The geographic scope of this book is also deliberately broad, reflecting
the fact that the approaches used here are applicable anywhere. Some of
the analyses in the book are global; those that are not are spread around the
world and relate to a range of biomes.
We have interpreted ‘phylogeny’ very broadly. Some chapters use state-
of-the-art phylogenies (or networks) generated from sequence data collected
to order. Some use ‘supertrees’: inclusive composite phylogenies produced
by combining algorithmically many less inclusive estimates of relationships
(Bininda-Emonds 2004; Sanderson et al. 1998). Some use taxonomies as
the best available surrogate – however flawed – for phylogeny. We are
sanguine about this heterogeneity. This is not a book about phylogenet-
ics or phylogenies; it is a book about how phylogenetic information can
be synthesised and used in conservation biology. As better information
becomes available, it should supersede that used here, and will in turn lead
to further methodological developments. Some likely directions can be seen
already. At present, analyses are usually conditioned on a single estimate
of phylogeny. Sensitivity analyses, in which analyses are repeated across a
range of plausible phylogenies, are becoming widespread in phylogenetic
Phylogeny and conservation 13
comparative biology, and are sure to do so here too. Another approach that
is permeating phylogenetics (and many other areas in biology) is the use of
Markov Chain Monte Carlo (MCMC) methods for implementing Bayesian
analyses (see Sinclair et al., Chapter 2). Such methods permit the simulta-
neous and relatively quick estimation of many parameters of interest, and
so are well suited to the analysis of real-world complexities. A strictly hier-
archical phylogeny is a conceptually simple framework for analysis, but the
hierarchy may not do a good job of representing relationships around and
below the species level: network-based methods of analysis need to be devel-
oped further to deal with such cases.
In the end how will phylogenies impact conservation? Some of the evi-
dence presented in this book suggests that their impact may be small. Incor-
poration of phylogenetic information into the establishment of geographic
conservation priorities is expected to make a difference only if certain con-
ditions are met. Human impact on the overall tree of life may be minor,
even if the branches nearest to us are to be heavily pruned. The time nec-
essary for recovery of current phylogenetic diversity may be far too great to
be relevant, relative to time scale relevant for conservation. In other ways,
phylogenetics may provide considerable benefits to conservation. Thus, for
example, it may provide resolutions to the species concept debates that oth-
erwise stand to destabilise conservation planning. Phylogenies will give pre-
dictive insights into patterns of extinction and invasion and ultimately may
allow for the explicit consideration of evolutionary process in conservation.
We hope that the chapters in this volume increase the veracity and speed of
tackling these issues.
A C K N O W L E D G E M E N T S
We are grateful to the many people and institutions that contributed to the organ-
isation of the ZSL Meeting at which the papers included were first presented.
In particular, we thank Deborah Body for actually organising the conference. Ini-
tially, Morris Gosling and Georgina Mace gave us the idea for putting together
a group around the topic of phylogeny and conservation. Russ Mittermeier and
Gustavo Fonseca supported the idea from the start. Guy Cowlishaw and two anony-
mous reviewers provided insightful comments on our first proposal. The interna-
tional participation at the symposium itself would not have been possible with-
out the financial assistance from the Zoological Society of London and the Center
for Applied Biodiversity Science at Conservation International. This edited volume
is the result of prompt, thorough and insightful reviews by John Avise, Tim
Barraclough, John Bates, Olaf Bininda-Emonds, Tim Blackburn, Jose´ Maria
Cardoso da Silva, Ben Collen, Richard Cowling, Keith Crandall, Dan Faith, Lincoln
Fishpool, Jon Fjeldsa˚, Richard Grenyer, Kate Jones, Julie Lockwood, Jon Lovett,
14 A. Purvis, J. L. Gittleman and T. M. Brooks
Georgina Mace, Pablo Marquet, Mike McKinney, Guy Midgley, Arne Mooers, Craig
Moritz, Norman Myers, Sean Nee, Ian Owens, John Reynolds, Ana Rodrigues,
Sergio Roig-Jun˜ent, Anthony Rylands, Jack Sites, Tom Smith, Alfried Vogler, Robert
Wayne, Tom Webb and Paul Williams. We appreciate the guidance through publica-
tion from Cambridge University Press, especially Tracey Sanderson, Alan Crowden,
Carol Miller, Lynn Davy and Maria Murphy.
R E F E R E N C E S
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by combining phylogenetic information: a complete phylogeny of the extant
Carnivora (Mammalia). Biological Reviews 74, 143–75.
Cardillo, M., Purvis, A., Sechrest, W., Gittleman, J. L., Bielby, J. & Mace, G. M.
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P A R T 1
Units and currencies
2
Molecular phylogenetics for conservation biology
E L I Z A B E T H A . S I N C L A I R , M A R C O S P E´ R E Z - L O S A D A
A N D K E I T H A . C R A N D A L L
Phylogeny reconstruction has been historically used as a tool in systematics
and taxonomy, examining relationships among species and at higher level
taxonomic classifications. However, with recent advances in our ability to
collect nucleotide sequence data from a wide variety of organisms, coupled
with advances in phylogenetic methodology and their comparative testing,
there has been a broader application of phylogeny reconstruction into areas
such as describing biodiversity to assign regional conservation priorities
(Crozier 1992; Faith 1992), defining critical habitat areas (see, for example,
Crandall 1998), and for understanding genetic patterns and processes at or
below the species level (see, for example, Fetzner & Crandall 2003; Morando
et al. 2003). There is also an increasing awareness among those involved in
the development of conservation programmes that molecular data can be
usefully combined for integrated conservation planning from the broader
landscape or community level, to biogeographic subregions, and to individ-
ual species (Moritz 2002).
In cases where morphology is unable to resolve relationships among
closely related taxa or particularly at the population level (intraspecific rela-
tionships), molecular approaches provide the much-needed resolution to
interpret evolutionary histories. Defining species still remains an extremely
contentious issue among scientists; however, criteria may be defined to test
(morphologically cryptic) species boundaries, phylogenies may be statisti-
cally tested according to these criteria (see below), and outcomes compared
between different phylogenetic reconstruction methods or different data
sets (e.g. morphology versus molecular, different gene regions). Traditional
phylogenies used for describing hierarchical relationships among species or
higher-level classifications can be combined with a Nested Clade Analysis
C© The Zoological Society of London 2005
Emanuell
Realce
Emanuell
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Emanuell
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Emanuell
Realce
Emanuell
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20 E. A. Sinclair, M. Pe´rez-Losada and K. A. Crandall
(NCA) (Templeton et al. 1992) to examine the lower-level reticulating rela-
tionships among closely related sequences. The NCA is extremely useful
in explaining observed genetic patterns relative to historical and contempo-
rary population processes. The combination of these two methods provides
a very powerful tool particularly for understanding lower-level relationships
required in species-specific conservation programmes. Some of the sorts
of questions that can be addressed by using phylogenies include testing
hypotheses on the geographic origins of a particular group (see, for example,
Crandall et al. 2000a,b; Templeton 2002), examining relationships among
species or species complexes (see, for example, Taylor & Hardman 2002;
Sinclair et al. 2004a), providing a systematic framework for taxonomic revi-
sions in unresolved groups (see, for example, Hansen et al. 2003; Sinclair
et al. 2004b), setting conservation priorities for biogeographic regions
based on genetic and phylogenetic diversity within taxonomic groups (see,
for example, Crandall 1998; Whiting et al. 2000; Pe´rez-Losada et al. 2002),
and individual species conservation plans (see, for example, Gonza´les et al.
1998; Sinclair 2001). Once relationships among taxa or populations are
established through a well-supported phylogeny with good sampling, many
different questions may be resolved, or at least it will be possible to refocus
additional work. Indeed, this volume demonstrates the broad applicability
of phylogenies to conservation questions.
Given this broad application of phylogenies to conservation, it is crit-
ical to understand the diverse approaches to estimating robust phyloge-
nies. In this chapter, we outline the major steps involved in collecting sam-
ples, sequence alignment and different theoretical approaches to phylogeny
reconstruction for molecular data, show methods by which we can compare
results from these different approaches, and give two examples to demon-
strate the application of molecular data in conservation and management.
We focus on recent advances in this field, but for a more extensive descrip-
tion of traditional phylogenetic methodology see Swofford etal. (1996).
S A M P L I N G C O N S I D E R AT I O N S
Geographic sampling strategies and choice of gene regions (number and
length) must be carefully considered before beginning any research project.
Geographic sampling of individuals must be considered initially. Infer-
ences of population structure and history will depend critically on an appro-
priate geographic sampling strategy that incorporates random sampling
throughout the geographic distribution (Templeton et al. 1995), but also
encompasses as much of the previously documented variation as possible
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Molecular phylogenetics for conservation biology 21
Box 2.1 Definitions
Bootstrap (non-parametric): a statistical method based on repeated
random sampling with replacement from an original sample.
Codon: triplet of bases of DNA sequence that makes up a single
amino acid (e.g. AGA = arginine).
Convergence: the process by which a similar character evolves more
than once independently in different lineages or species. The
character will be absent from the common ancestor.
Haplotype: unique DNA sequence.
Homology: state in which two or more sequences share a common
ancestry
Markov Chain Monte Carlo (MCMC): describes an algorithm in
which the probability of a change from one (nucleotide) state to
another does not depend on the previous history of the state.
Metapopulation: a network of semi-isolated populations with some
level of regular or intermittent migration and gene flow among
them; individual populations may become extinct but be recolo-
nised from other populations.
Optimality criteria: how well the data fit a model or phylogeny.
Positional homology: the relationship among columns of nucleo-
tides or amino acids ‘correctly’ aligned. It is assumed that nucleo-
tides or amino acids in the same column are derived from a single
ancestral nucleotide or amino acid, with or without intermediate
substitutions.
Rate heterogeneity: differential mutation rates between nucleotide
positions in a sequence, and between transitions and transver-
sions.
Recombination: process of exchange of genetic material (genes or
segments) by crossing-over during meiosis.
Tokogenetic: describes non-hierarchical genetic relationships among
individuals arising through sexual reproduction (pedigree).
Tree bisection reconnections (TBR): method of rearranging
branches on a tree during the process of searching for a globally
optimal tree.
Transition: a nucleotide substitution from a purine to a purine
(A ↔ G) or a pyrimidine to a pyrimidine (C ↔ T).
Transversion: a nucleotide substitution between a purine and a
pyrimidine or vice versa (e.g. A ↔ C).
22 E. A. Sinclair, M. Pe´rez-Losada and K. A. Crandall
(for example, including all morphotypes or subspecies). In designing con-
servation genetic studies, careful consideration is warranted for the justi-
fication of sampling strategy in terms of numbers of sequences, length of
sequences, and geographic distribution of samples relative to the hypothe-
ses being tested. It is widely accepted that both taxon and character sampling
are important for improving phylogenetic accuracy, despite the ongoing
debate over which is more important (Graybeal 1998; Kim 1998; Poe 1998;
Poe & Swofford 1999; Rosenberg & Kumar 2001, 2003; Pollock et al. 2002;
Hillis et al. 2003). An appropriate sampling strategy becomes a key consid-
eration for the accuracy of phylogeny reconstruction (Hillis 1998), of param-
eter estimates associated with models of evolution (Sullivan et al. 1999),
and of the inferences made relative to conservation assessment (Sites &
Crandall 1997; Crandall et al. 2000c). Sampling considerations typically
entail two components: the first is the number of ‘taxa’ or sequences needed
for a given study relative to the geographic distribution of the species, and
the second is the number of ‘characters’ or nucleotides required. Given that
most studies have limited resources, there is no simple answer to ‘more taxa
or more characters?’. However, if lots of sequence data have been collected
for a few taxa, then it is often better to add more taxa than characters, and
vice versa (Hillis et al. 2003).
For lower-level population studies, knowledge of the distribution and
biology of the organism of study is key to selecting an appropriate sam-
pling density. For example, in low-vagility species, sampling density should
be higher than for a wide-ranging species. Sampling at geographic scales
that greatly exceed individual dispersal distances or metapopulation con-
nectivity is likely to mislead or confound inferences from many methods.
Hedin (1997) has suggested that a dense sampling of many geographically
close populations and the inclusion of three to five individuals per locality
would be adequate to discriminate between an absence of gene flow and very
limited gene flow in low-vagility species (see also Hedin & Wood 2002).
Gene selection
Selection of appropriate genes is also critical to how well relationships
among sequences (populations or species) can be resolved, to the infer-
ences made, and hence to the long-term conservation and management
decisions being based on the data. Rates of mutation vary considerably
among genes (mitochondrial, nuclear, and across taxonomic groups). Note
that mitochondrial DNA (mtDNA) is normally non-recombining and essen-
tially behaves as a single locus. The amount of variation in genes will vary
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Molecular phylogenetics for conservation biology 23
depending on the taxonomic group, so it is important to look at the level of
variation in genes already available for related organisms and then screen
for variation by sequencing a representative subset of samples. If one is
examining intraspecific relationships among closely related groups of indi-
viduals, then more rapidly evolving genes, such as in the mtDNA control
region, will be more informative than nuclear coding genes. However, if
one is examining relationships among more distantly related taxa, at genus
level or above, then more slowly evolving genes (e.g. mtDNA 12S, COI,
ND4) are preferred. This minimises analytical problems posed by multiple
changes or hits at individual nucleotide positions and by sequence align-
ment. The discovery of nuclear copies of mtDNA genes (Lopez et al. 1994;
Zhang & Hewitt 1996a,b; Cracraft et al. 1998; Nguyen et al. 2002) has com-
plicated the use of mitochondrial sequences in phylogenetic studies. How-
ever, there are several methods to detect this, including translation of cod-
ing sequences into amino acid sequences (e.g. cyt b, ND2, ND4, COI) and
looking for the initiation and stop codons, blast searching by using Genbank
(www.ncbi.nlm.nih.gov/) and aligning sequences to other sequences for
closely related species for which the gene has been identified. Finally, the
phylogeny may not match that for other gene regions and/or make geo-
graphic sense (see, for example, Nguyen et al. 2002); this may be evidence
of recombination (reviewed by Rokas et al. 2003), or the gene tree does not
match the species tree owing to different histories (Avise 1994).
In conservation genetics, the use of nuclear gene information to com-
plement the inferences from mtDNA sequence data is becoming necessary
for a complete picture of the evolutionary forces shaping populations and
species (Antunes et al. 2002; Hare 2001; Shaw 2002). This combination can
be informative where the histories of the genes differ through modes of spe-
ciation or philopatry (differential movement between males and females)
(see, for example, Palumbi & Baker 1994; Ellegren et al. 1996; Shaw 2002).
For example, if females are philopatric and malesdisperse, then the mtDNA
will be highly structured and the nuclear DNA may show a pattern of pan-
mixia. Nuclear genes are made up of coding regions (exons) and non-coding
regions (introns), so it is possible to target the sequencing of introns that
will be more likely to exhibit intraspecific sequence variation, because they
are ‘junk’ DNA and are essentially not under selection. However, nuclear
genes are subject to recombination, although it should be noted that recom-
bination in mitochondrial DNA is also common in some groups (Gillham
1994). Recombination can affect our ability to accurately reconstruct evo-
lutionary relationships (Posada & Crandall 2002) and adversely affect
our ability to accurately estimate parameters associated with molecular
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24 E. A. Sinclair, M. Pe´rez-Losada and K. A. Crandall
evolution and population dynamics (Schierup & Hein 2000). Therefore,
it is desirable to test for recombination in a set of aligned sequences before
phylogenetic analyses are performed. There are a great number of meth-
ods to choose from for detecting recombination (reviewed in Crandall &
Templeton, 1999) with new methods being developed continuously (see,
for example, Dorman et al. 2002). Unfortunately, it is not a trivial task to
choose an appropriate tool.
Three different research groups have recently explored the ability of var-
ious methods to detect recombination. The first group studied the statistical
power (the probability that a statistical test will reject the false null hypoth-
esis) of four distinct methods: compatibility, phylogenetic, substitution dis-
tribution, and distance methods. They used simulated sequences under a
coalescent model with recombination. The simulation results showed clear
differences in statistical power among these four classes of methods, with
the compatibility approaches having the highest power and the phyloge-
netic approaches having lower power (Brown et al. 2001). The next group
also investigated the statistical power of the four classes of methods
to detect recombination, but added variation in the mutation rate as well
as the recombination rate. This is of interest because some methods may
perform differentially well at different divergences. Again, compatibility
approaches performed better than phylogenetic methods and all methods
detected fewer recombination events than theoretically possible (Wiuf et al.
2001). These papers set the foundation for the third group, which capital-
ised on the theoretical contributions of this earlier work to perform more
extensive simulation studies that examined the ability of fourteen different
methods to detect recombination while varying recombination rate, muta-
tion rate, and rate variation across sites. Here, there was no clearly supe-
rior method; different methods performed best at different levels of diver-
sity (mutation rates), but compatibility methods outperformed phylogenetic
methods (Posada & Crandall 2001b). All studies showed that the use of
multiple techniques is a reasonable approach, as the success of methods
for detecting recombination depends heavily on the level of sequence diver-
gence in the dataset. Methods to detect recombination, methods to estimate
recombination rates, and the impact of recombination on phylogenetics
were recently reviewed in detail (Posada et al. 2002). A number of software
packages are available for detecting recombination (see Posada & Crandall
2001b; Rokas et al. 2003). Although one should be aware of the potential
confounding effects of recombination on phylogeny reconstruction, recom-
bination will be far more common in rapidly evolving organisms, such as
viruses and bacteria, which are rarely the focus for conservation biologists.
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Molecular phylogenetics for conservation biology 25
Nevertheless, it is important to test for recombination, as there is increasing
evidence for recombination in mitochondrial DNA (see, for example, Lunt
& Hyman 1997; Maynard Smith & Smith 2002; Burzynski et al. 2003).
S E Q U E N C E A L I G N M E N T
Sequence alignment is performed to determine positional homology. It is
the process by which nucleotide or amino acid sequences from homologous
molecules are lined up so as to maximise similarity or minimise the num-
ber of inferred changes among the sequences. Alignments may be simple
for closely related individuals and coding genes, but become increasingly
difficult with more distantly related taxa or from non-coding gene regions.
Sequence alignment is, however, a central part of any phylogenetic analysis
and will have a profound effect on one’s results. Indeed, ideally one would
like to estimate a phylogeny and adjust the alignment simultaneously,
applying the same optimality criterion (see below) to both endeavours,
simultaneously improving both the alignment and phylogeny. However,
alignment algorithms today allow this only on a limited basis with a limited
range of optimality criteria (but see Giribet 2001). Therefore, the standard
approach to sequence alignment is to use generally available software, such
as Clustal (Thompson et al. 1997) and adjust by eye. Clustal is a pairwise
alignment algorithm that is relatively quick and easy to use, but alignments
should always be checked by eye as this program does not guarantee maxi-
mum similarity among sequences. Computer programs such as MALIGN
(Wheeler & Gladstein 1994) and POY (Gladstein & Wheeler 1999) use opti-
mality criteria to minimise the cost of guide trees based on weighting of
nucleotide changes and gap insertions. These programs are computation-
ally more intensive and often not intuitive in their methodology. One impor-
tant distinction is that Clustal uses a single guide tree, whereas MALIGN
and POY search heuristically across multiple guide trees and hence are not
algorithmic. MALIGN searches for a globally optimal alignment (or set of
alignments) in much the same way that we search for trees (see below).
POY provides a tree topology with a set of alignments for each node on the
tree, thus eliminating the need for a separate phylogeny search. No com-
plete alignment for the data set is produced and it is not possible to exclude
regions of questionable homology without a preliminary look at the data
through another alignment program or searching for common motifs. For
closely related sequences and coding genes, alignments are generally not
complex and can be adequately generated by using Clustal or Sequencher,
with some editing by eye. For more distantly related sequences where there
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26 E. A. Sinclair, M. Pe´rez-Losada and K. A. Crandall
is considerable sequence length variation (e.g. ribosomal genes), better
alignments may be obtained with the aid of more complex programs and
structural models (rDNAs and tRNAs).
The amino acid alphabet is made of 20 characters (Ala, Phe, Val, Iso,
Leu, etc.) whereas the DNA alphabet is made of only four (A, C, G, T), mak-
ing alignment of amino acids easier and more reliable than the alignment
of nucleotide sequences. Therefore, when working with coding sequences it
is to our advantage to align the corresponding amino acids first and subse-
quently return to the original nucleotides as they often have greater informa-
tion content for phylogeny reconstruction, provide better models of evolu-
tion, and hence give better parameter estimation. Unfortunately, programs
such as Clustal do not automate this procedure, so the usual method is to
align the nucleotides, translate them to amino acids, and check the quality
of the implied amino-acid alignment. Once the final alignment is settled
on, often there are still regions of ambiguity.