Molecular Ecology (2008) 17, 3754–3774 doi: 10.1111/j.1365-294X.2008.03857.

INVITED REVIEW
Blackwell Publishing Ltd

Twenty years of phylogeography: the state of the field and

the challenges for the Southern Hemisphere
L U C I A N O B . B E H E R E G A R AY
Department of Biological Sciences, Macquarie University, Sydney, NSW 2109, Australia

Abstract
Phylogeography is a young, vigorous and integrative field of study that uses genetic data
to understand the history of populations. This field has recently expanded into many areas
of biology and also into several historical disciplines of Earth sciences. In this review, I
present a numerical synthesis of the phylogeography literature based on an examination of
over 3000 articles published during the first 20 years of the field (i.e. from 1987 to 2006).
Information from several topics needed to evaluate the progress, tendencies and deficiencies
of the field is summarized for 10 major groups of organisms and at a global scale. The topics
include the geography of phylogeographic surveys, comparative nature of studies, temporal
scales and major environments investigated, and genetic markers used. I also identify
disparities in research productivity between the developing and the developed world, and
propose ways to reduce some of the challenges faced by phylogeographers from less affluent
countries. Phylogeography has experienced explosive growth in recent years fuelled by
developments in DNA technology, theory and statistical analysis. I argue that the intellectual
maturation of the field will eventually depend not only on these recent developments, but
also on syntheses of comparative information across different regions of the globe. For this
to become a reality, many empirical phylogeographic surveys in regions of the Southern
Hemisphere (and in developing countries of the Northern Hemisphere) are needed. I
expect the information and views presented here will assist in promoting international
collaborative work in phylogeography and in guiding research efforts at both regional and
global levels.
Keywords: biogeography, conservation biology, evolutionary biology, global biodiversity,
population genetics, Quaternary science

Received 10 March 2008; revision accepted 30 May 2008

position to test biogeographic hypotheses, describe the

Introduction
evolution of reproductive isolation of population units,
Most species display some degree of population structure and infer processes underlying the origin, distribution and
that can be interpreted in geographic and chronological maintenance of biodiversity. Given that the structure of
contexts. Deciphering spatial and temporal components of population genealogies is influenced by demographic
population structure and interpreting the evolutionary and history, phylogeographers can also make inferences about
ecological processes responsible are major goals of phylo- temporal changes in the physical and biotic environment
geography. Phylogeography is an integrative field of science of a population using present-day genetic data. For these
that uses genetic information to study the geographic reasons phylogeography has provided valuable contributions
distribution of genealogical lineages, especially those found to several areas of study in biology and Earth sciences, such
within species (Avise 2000). Based on appropriate sampling as speciation (Avise et al. 1998; Moritz et al. 2000; Hewitt
of individuals and genes, phylogeographers can be in a 2001; Kohn 2005), historical biogeography (Avise 2000;
Riddle & Hafner 2006), human evolution (Beaumont 2004;
Correspondence: Luciano B. Beheregaray, Fax: +61 2 9850 8245; Templeton 2005; Torroni et al. 2006), conservation biology
E-mail: [email protected] (O’Brien 1994; Avise & Hamrick 1996; Smith & Wayne 1996;

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Fig. 1 Number of phylogeography articles

published between 1987 and 2006 and
corresponding number of citations.

Moritz & Faith 1998; Fraser & Bernatchez 2001; Frankham phylogeography between different regions of the world
et al. 2002), biodiversity research and taxonomy (Avise & and comment on the difficult task posed by researchers from
Ball 1990; Taberlet 1998; Beheregaray & Caccone 2007), less affluent institutions (such as those generally found in
palaeoecology (Cruzan & Templeton 2000), palaeoclimato- many Southern Hemisphere countries) to conduct studies
logy (Hewitt 2000) and volcanology (Emerson 2002). and publish their findings. I expect the information and
Last year marked the 20th anniversary of the formal views presented here will assist in promoting international
birth of phylogeography. The term was coined by John collaborative work in phylogeography and in guiding
Avise et al. in 1987 to describe a discipline with conceptual research efforts at both regional and global levels aimed at
and technical roots linked to the incipient field of molecular reducing gaps in our knowledge about spatial and tem-
genetics of the 1970s. Several reviews have described find- poral components of population history.
ings in phylogeography and evaluated its contribution to
ecology and evolutionary biology (e.g. Riddle 1996; Roderick
Methods
1996; Avise 1998, 2000; Taberlet 1998; Walker & Avise 1998;
Newton et al. 1999; Hewitt 2000; Beheregaray & Caccone
Review database and general statistics
2007). Other articles have assessed how recent advances in
DNA technology, coalescent theory and statistical analyses The database used for this review was compiled by
have prompted methodological and conceptual shifts in conducting searches in Web of Science®. Titles, abstracts
the field (e.g. Edwards & Beerli 2000; Sunnucks 2000; Hare and keywords of all articles published between 1987 and
2001; Templeton 2001, 2004; Hey & Machado 2003; Knowles 2006 were searched for two terms: ‘phylogeography’ and
2004; Emerson & Hewitt 2005). Despite the variety of topics ‘phylogeographic’. Web of Science is an online academic
reviewed, the literature contains only a few reviews reporting database from ISI Web of Knowledge® that provides access
data needed to evaluate the progress, tendencies and to information from over 8700 research journals. The following
deficiencies of the field at a global scale. The last publication general statistics were obtained through the ‘Analyse Results’
to present such information was the book of Avise (2000), option in Web of Science: subject categories, source titles
the benchmark contribution to the field published before (i.e. journal titles), document types, publication years,
the extraordinary growth of phylogeography observed in affiliations and countries. The mean number of publications
recent years (see Fig. 1). per year of each country was compared with its per capita
Here I provide a description about the state of phylo- gross domestic product (GDP) estimated based on the
geography based on a detailed examination of articles purchasing power parity calculation. For this I used the
published during the first 20 years of the field (i.e. from 1987 to most recent GDP statistics from The World Factbook published
2006). I have two broad objectives with this review. The first on the website of the Central Intelligence Agency.
one is to present a numerical synthesis of the phylogeography
literature with information on several topics, including
Review categories and specific statistics
the geographic distribution of surveys, biological groups
studied, genetic markers employed, number of taxa used Data from 40 selected categories and other specific statistics
and temporal scales investigated. My second objective is to were obtained by reading the abstract of each article
draw attention to disparities in research productivity in retrieved. If the required information was not available in

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the abstract, then the text of the manuscript was consulted. (AFLPs), single nucleotide polymorphisms (SNPs), or ran-
This strategy, although time consuming and subject to domly amplified polymorphic DNA (RAPD); Class III,
human error, is preferred to using the ‘Analyse Results’ microsatellites; and Class IV, allozymes. Studies that used
option. It can provide information about phylogeography more than one class of marker were also classified in five
that is otherwise unavailable from automated searches and categories of marker combinations: combination of classes
overcomes problems about the way records are stored in the ‘I & II’, ‘I & III’, ‘I & IV’, ‘three or four markers combined’
database (see examples below). For this section I excluded or ‘other combinations’.
the following document types: review articles (n = 136),
meeting abstracts (n = 48), editorial material (n = 38) and
Results
correction or additions (n = 16). Technical notes (e.g. primer
and software notes) and articles with a purely taxonomic or
Section I: Global Scale
systematic focus were also excluded (n = 377). This pruning
was conducted after reading each abstract (as opposed to
The spectacular growth of a new field of science
conducting a priori sorting by document type in Web of
Science). The exclusion of such articles ensured that the A total of 3049 articles published between 1987 and 2006
statistics presented in this review are a reflection of the work were identified in the database searches. Phylogeography
conducted only by empirical phylogeographic studies, and has experienced exponential growth as measured by the
not of other scholarly outputs. number of articles published each year (Fig. 1). The large
After reading the abstract, information from each article number of papers retrieved probably barely reflects the
was classified in seven major clusters containing the 40 popularity of the field since it was not possible to identify
categories (listed below) and entered into an electronic a considerable proportion of phylogeographic studies.
data sheet for subsequent analysis. Importantly, these clas- These were surveys that might fall within the umbrella of
sifications were based on the locations where the organisms phylogeography but did not use the terms ‘phylogeography’
were sampled — as opposed to automatically sorting studies or ‘phylogeographic’ in abstracts, keywords or titles. I
using the affiliation of authors as implemented by Web of verified this discrepancy by comparing the results of my
Science. The latter creates biases in data analysis given that searches with the track record of four phylogeographers
in some regions (e.g. the Neotropics), several studies are for whom I had access to complete publication lists. On
conducted in collaboration or sometimes exclusively by average, the review’s searches detected 65% of the number
international institutions, and the location of the study of journal articles published in phylogeography by these
organism is often not recorded in the database. In the first four researchers (individual ‘success rate’ ranged from 40%
two clusters, studies were sorted by their global scope, to 92%). This apparent disparity is probably not influencing
hemisphere (Northern, Southern or transequatorial) and negatively the results of this review because most compari-
continent (and associated oceans). In another cluster, study sons and conclusions were made relative to the total
organisms were assigned to 10 groups: mammals, herps number of articles identified.
(i.e. reptiles and amphibians), birds, fishes, terrestrial plants,
aquatic plants, terrestrial invertebrates, aquatic invertebrates,
Citations numbers
fungi and micro-organisms. Study organisms were also
arranged by type of environment (terrestrial, marine or The number of citations of phylogeographic studies has
freshwater) and grouped on the basis of the nature of a also grown exponentially (Fig. 1). Citations climbed from
particular phylogeographic study. The latter included three 368 in 1997 to 10 835 in 2006, with an average annual
mutually exclusive categories: comparative phylogeography, number of citations of 3172 for the 20-year period. Below I
taxon-specific studies, and surveys that used more than provide a brief account of the main topics covered by the
one taxon but did not present the study in a comparative 20 or so most cited journal articles in phylogeography. The
manner. A perspective about the timescale of interest of paper that named the field and introduced its conceptual
phylogeographic studies was obtained by classifying arti- ideas (Avise et al. 1987) appears as the second most cited
cles that studied biogeographic scenarios of the Quaternary publication. Three articles by Godfrey Hewitt about the
Period (approximately the last 2 million years), Tertiary influence of Pleistocene ice ages on population genetic
Period (c. 2 to 65 million years ago), both Quaternary and structure (Hewitt 1996, 1999, 2000) are among the top seven
Tertiary, or undetermined (i.e. studies in which timescales papers with a combined total of over 2000 citations. This
were not explored). Finally, in the seventh cluster articles highlights well the impact of the interdisciplinary field of
were sorted on the basis of four major classes of genetic Quaternary science in phylogeographic research. Another
marker employed: Class I, mitochondrial DNA (mtDNA) popular topic is comparative phylogeography: empirical
or chloroplast DNA (cpDNA); Class II, nuclear DNA studies and reviews that used genealogical information
sequences, amplified fragment length polymorphisms from multiple codistributed species to identify commonalities

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in biogeographic history are the subject of five highly cited The globe and the continents. Study systems from the Northern
papers (Avise 1992; Dumolin-Lapegue et al. 1997; Avise & Hemisphere were the subject of 77% of all the articles,
Walker 1998; Bernatchez & Wilson 1998; Taberlet et al. whereas only 15% of publications focused on systems
1998). From all articles retrieved, a note published by from the Southern Hemisphere (Fig. 2a). A much smaller
Clement et al. (2000) describing TCS (a computer program to proportion (2%) used samples collected across both sides
estimate gene genealogies) is the one that tops the list with of the equator. On the other hand, a good proportion of
over 1000 citations. This and other articles related to the studies (6% or 146 papers) were considered of global scale
method of Nested-Clade Phylogeographic Analysis (e.g. since they included samples from multiple continents
Templeton 1998; Posada et al. 2000) are among the top 10 or oceans. The research done at the global scale almost
cited studies in phylogeography. The continuous popularity invariably included several authors and institutions. I also
of these three studies since their publication exemplifies identified studies that could not be classified as being of
well the central position of tree-based frameworks for global scope, but which nevertheless used samples collected
reconstructing genealogies and population histories. As a over vast continental regions. This class was represented in
comparison, recent years have seen the popularization 6.2% of all of the Northern and in 2.2% of all of the Southern
of studies using methodological developments related to Hemisphere studies.
statistical phylogeography and coalescent theory. Accord- When publications are classified based on the continental
ingly, two publications that advocate the use of statistical origin of the organisms (Fig. 3), Europe was the most inten-
models for parameter estimation in phylogeography — sively studied continent with 31% of all articles (779 papers)
the papers of Edwards & Beerli (2000) and Knowles & followed closely by North America with 30%. Within the
Maddison (2002) are among the top 25 most cited studies North American continent, the species-rich region of Cen-
in the field. tral America accounted for only 9.7% of studies. Asia, the
world’s largest and most populous continent ranked third in
this list with 16.4%. Similarly to North America, the species-
Subject categories and journals
rich region of Southeast Asia was represented by a relatively
The position of phylogeography as a far-reaching scientific small proportion (20%) of the Asian studies. Africa ranked
discipline is evident in Table 1, which lists the top 50 subject fourth and Australia fifth, with 8% and 7.4%, respectively.
categories in the field. Around 72% of phylogeographic Within the Australian continent, c. 5% of papers focused on
studies can be primarily classified in the fields of ecology the islands of Melanesia and nearby archipelagos (i.e. most
and evolution (41% of the total) and molecular biology and studies focused on Australia or New Zealand). Ironically,
genetics (31% of the total). Nonetheless, phylogeographic South America, the continental region generally recognized
studies have also addressed a multitude of additional as harbouring the greatest biodiversity on Earth, ranked
topics in life sciences (e.g. from biodiversity conservation last among all the human populated continents with only
to legal medicine), as well as in earth sciences (e.g. from 6.3% of the articles. Finally and predictably, a very small
physical geography to archaeology). Also listed in Table 1 proportion of studies (0.6%) focused primarily on the
are journal names, representing a great variety of scientific Antarctic continent.
disciplines. Although a large proportion of articles have
been published in journals of broad scope (e.g. Molecular Countries and the GDP. The top 100 most productive countries
Ecology, Molecular Phylogenetics and Evolution, and Evolution), in phylogeography are listed in the Appendix. A total of
phylogeography has also been very popular with topic- 124 countries had researchers involved with publications
oriented journals (e.g. Conservation Genetics, Biological in phylogeography. The USA appeared as the most produc-
Conservation and Conservation Biology). The same is true for tive nation in terms of absolute number of publications:
journals that focus on specific taxonomic groups, such as US-based researchers participated in 1250 articles, or 41%
plants, insects or mammals. In this category, vertebrates of the total. The other top 10 ranked countries were the UK
and in particular mammals (e.g. Journal of Mammalogy, (422 articles), France (289), Germany (279), Australia (237),
American Journal of Human Genetics and American Journal of Canada and Spain (each with 218 articles), Italy (163),
Physical Anthropology) are amongst the most popular. Japan (137) and Sweden (113). Out of the top 20 ranked
countries, only three are from the Southern Hemisphere:
Australia, Brazil and New Zealand. Unsurprisingly, affluent
The geography of publications
nations are responsible for the vast majority of articles in
Unless otherwise stated, the results of all subsequent phylogeography (Fig. 4), a pattern consistent with the
sections are based on data collected from reading the geographic distribution of publications in biomedical
abstracts of 2434 articles. This number was obtained by research (e.g. Benzer et al. 1993). Mean annual productivity
pruning the initial database of 3049 articles published appears to be broadly divided based on a threshold of
between 1987 and 2006 using criteria described above. around US$20 000. All countries with more than three

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Table 1 Number of publications in phylogeography for the top 50 subject categories and scientific journals

Subject category No. Journal No.

Evolutionary Biology 1419 Molecular Ecology 648

Ecology 1131 Molecular Phylogenetics and Evolution 229
Biochemistry and Molecular Biology 1008 Evolution 167
Genetics & Heredity 865 Biological Journal of the Linnean Society 96
Zoology 315 Heredity 84
Plant Sciences 248 Journal of Biogeography 78
Marine and Freshwater Biology 222 Conservation Genetics 58
Biodiversity Conservation 123 Proceedings of the Royal Society B 58
Biology 107 Journal of Mammalogy 46
Fisheries 95 Marine Biology 46
Geography, Physical 90 Journal of Evolutionary Biology 40
Multidisciplinary Sciences 67 Molecular Biology and Evolution 40
Entomology 55 Proceedings of the National Academy of Sciences, USA 38
Environmental Sciences 53 American Journal of Botany 37
Ornithology 52 Journal of Heredity 30
Biotechnology and Microbiology 31 Journal of Fish Biology 29
Forestry 28 Plant Systematics and Evolution 29
Oceanography 28 Molecular Ecology Notes 27
Agronomy 23 Zoological Science 26
Anthropology 23 Genetics 22
Parasitology 21 Taxon 22
Horticulture 20 Canadian Journal Fisheries and Aquatic Sciences 19
Microbiology 20 Integrative and Comparative Biology 19
Limnology 18 Journal of Zoological Systematics and Evolutionary Research 19
Mycology 13 Systematic Biology 19
Virology 12 Theoretical and Applied Genetics 19
Agriculture, Dairy and Animal Science 10 American Journal of Human Genetics 18
Veterinary Sciences 8 Annals Entomological Society of America 18
Cell Biology 7 Biological Conservation 18
Tropical Medicine 7 Forest Ecology and Management 17
Geosciences, Multidisciplinary 6 Auk 16
Paleontology 6 Genetica 15
Medicine, Legal 5 Journal of Plant Research 15
Biochemical Research Methods 4 Condor 14
Engineering, Environmental 4 Conservation Biology 14
Public and Occupational Health 4 Journal of Zoology 13
Environmental Studies 3 American Journal of Physical Anthropology 12
Medicine, General and Internal 3 Australian Journal of Zoology 12
Toxicology 3 Botanical Journal of the Linnean Society 12
Archaeology 2 Canadian Journal of Zoology 12
Geography 2 Copeia 12
Immunology 2 Hydrobiologia 12
Infectious Diseases 2 Marine Ecology-Progress Series 12
Urban Studies 2 Trends in Ecology & Evolution 12
Anatomy and Morphology 1 Annals of Human Genetics 11
Astronomy and Astrophysics 1 Genome 11
Industrial Relations and Labour 1 Journal of Phycology 11
Mathematical and Computational Biology 1 American Naturalist 10
Sociology 1 Animal Conservation 10
Urology and Nephrology 1 Herpetologica 10

publications per year have a GDP per capita higher than

Taxonomic coverage
US$20 000. The exception is the productivity of Russia,
Brazil, China and South Africa. These nations have GDP per The global publication effort in phylogeography is noticeably
capita below this threshold but had an annual publication biased towards vertebrates, which accounted for 57% of all
rate of 4.6, 4.3, 4.1 and 3.4 articles, respectively (Fig. 4). publications. Out of the 10 groups of organisms (Fig. 5),

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Fig. 2 Proportion of articles in phylogeography published between 1987 and 2006 according to (a) hemisphere or global scale, (b) type of
environment, (c) nature of study and (d) timescale (see text for details).

Fig. 3 Continental origin of articles in phylogeography published

between 1987 and 2006 based on the location of organisms studied.

mammals were the most popular taxon in phylogeographic

research (508 papers or 21% of all articles). Fishes and
terrestrial plants ranked second with an equal number of
Fig. 4 Research productivity and country’s wealth for the 100 most
392 articles each. The next most popular category was the productive nations in phylogeography (see text for details about
group of terrestrial invertebrates, followed by herps (reptiles highlighted countries). Productivity is measured by the mean
and amphibians), aquatic invertebrates and birds (the number of publications per year and wealth by the nation’s per
latter with 182 articles). The remaining categories in this list capita gross domestic product (GDP).

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Fig. 5 Taxonomic coverage of articles in

phylogeography published between 1987
and 2006.

were micro-organisms and aquatic plants, both accounting papers) did not explore temporal aspects of inferred bioge-
for less than 2% of the total number of publications (c. 40 ographic divergences, or lack thereof, and were therefore
articles each) and lastly the fungi with only 1.8% of the classified as ‘undetermined’.
total.

Genetic markers
Type of environment, nature of the study and timescale
Below I summarize results and trends observed at a global
Most studies in phylogeography focused on the terrestrial level — patterns and idiosyncrasies about marker use in
environment (65% of the total; Fig. 2b). Despite enormous taxonomic groups are presented in Section II. Genealogical
differences in surface area of habitats, a smaller proportion information derived from mtDNA was used in 1750 papers
of studies was conducted on marine organisms (17%) than (72% of all articles), whereas data from cpDNA appeared
on freshwater organisms (18%). in 217 papers (9%, Fig. 6). Together these two markers
The sorting of papers by nature of the study (Fig. 2c) comprise what I named Class I, a class represented in 81%
showed that 68% of the articles examined genealogical of all studies. Data from nuclear DNA sequence, SNPs, AFLP
relationships within one taxon. A large proportion of studies or RAPD (Class II) were represented in 536 publications.
(25% or 674 papers) described phylogeographic patterns Microsatellites (Class III) were used in 214 papers and
in more than one taxon but surprisingly did not explore allozymes (Class IV) in 179.
outcomes using a comparative framework. Although this Several interesting trends can be identified when a class
appeared to be related to sampling design in some studies, of marker is sorted according to the proportion of articles
others could probably have benefited from testing for con- published in a given year (Fig. 7). The proportion of studies
gruence in the evolutionary and demographic history based exclusively on uniparentally inherited markers (Class I)
of taxa (sensu Bermingham & Moritz 1998). Only 8% (188 decreased from around 90% to 62% during the last 10 years.
papers) explicitly compared patterns of multiple codistri- On the other hand, surveys based solely on Class II mark-
buted taxa and as such were classified in the category of ers increased in popularity during the 1990s and appar-
comparative phylogeography. Nevertheless, the populariza- ently stabilized around 13% during the last 5 years (the
tion of phylogeography in recent years resulted in an increase 50% value for Class II in 1989 is biased since only two
in absolute numbers of comparative studies, from 12 articles empirical surveys were published that year). Microsatel-
in 2000 to 54 in 2006. Comparative phylogeographic lites only started being used as the sole source of informa-
studies were more common in the Northern than in the tion in 1997, but in the last years they already accounted for
Southern Hemisphere (75% and 23%, respectively) and around 8% of publications. Allozymes on the other hand
were rarely conducted at global scales (2%). were quite popular in the 1990s (c. 10% of surveys) but in
The analysis according to timescale strongly supports recent years they were used in only c. 4% of studies. These
the position of phylogeography as a popular discipline in general trends are consistent with the way the information
Quaternary science (Fig. 2d). Around 69% of the output of from different genetic markers was combined. During the
the field (1679 papers) reported diversifications of biological 20-year period, the great majority of studies, or 89% of the
units temporally associated with the Quaternary Period. A total, used only one type of marker. This value dropped to
reasonable proportion (11% or 267 papers) reported deeper around 80% in the last 5 years, a reduction driven in part by
divergences probably related to geological events of the the rapid increase of studies combining markers from
Tertiary, whereas 2% suggested that the evolution of their Classes I and II. This was by far the most popular combina-
study groups spanned both geological periods. Unfortu- tion in the last 5 years, accounting for around 10% of all
nately, a considerable proportion of articles (18% or 438 studies. For the same period, combinations of Classes I and

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Fig. 6 Number of phylogeography articles

published per year sorted according to
genetic marker(s) used for data collection
(categories are not exclusive, see text for
details).

Fig. 7 Proportion of articles published per year in phylogeography sorted by classes of genetic marker or marker combinations (categories
are mutually exclusive, see text for details).

III appeared in c. 4% and of Classes I and IV in c. 2% of Section II: Taxonomic Groups

the studies. Other types of double marker combinations Here I summarize results for taxonomic groups listed in
(i.e. those not involving uniparentally inherited markers) decreasing order of popularity. The data presented are
accounted for a very small proportion of articles (1.4%). based on the geographic origin of the organisms studied
Finally, only 26 out of the 2424 articles analysed used three (i.e. they are not based on the origin of researchers who
or more marker types. conducted the work). I draw attention to group-specific

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Table 2 Distribution of phylogeographic studies published between 1987 and 2006 for 10 groups of organisms. Values are the proportion
of studies by continent and by hemisphere or global region based on the geographic origin of organisms (see text for details)

Continent Hemisphere

North South Across Northern

Organisms Europe America Asia Africa Australia America Northern Southern and Southern Global

Mammals 0.27 0.24 0.23 0.15 0.04 0.07 0.74 0.16 0.05 0.05
Fishes 0.32 0.36 0.14 0.06 0.07 0.06 0.77 0.16 0.02 0.06
Herps 0.22 0.42 0.09 0.10 0.12 0.10 0.70 0.26 0.01 0.03
Birds 0.25 0.37 0.15 0.06 0.08 0.09 0.76 0.17 0.01 0.05
Plants: terrestrial 0.43 0.23 0.21 0.04 0.05 0.04 0.88 0.08 0.01 0.03
Plants: aquatic 0.32 0.35 0.21 0.03 0 0.09 0.63 0.02 0.05 0.29
Invertebrates: terrestrial 0.34 0.32 0.12 0.06 0.08 0.08 0.79 0.15 0.02 0.04
Invertebrates: aquatic 0.35 0.29 0.14 0.04 0.16 0.02 0.71 0.16 0.04 0.10
Micro-organisms 0.09 0.43 0.23 0.11 0 0.14 0.40 0.16 0.04 0.40
Fungi 0.29 0.36 0.21 0.07 0.07 0 0.57 0 0.05 0.38

results that contrast with outcomes for all taxonomic groups studies (77% compared to an average of 68% for all taxonomic
described in Section I. I also use a few selected examples groups combined). Yet, most studies that did use more than
from the literature to illustrate general findings and topics one taxon explicitly compared patterns across taxa, resulting
of interest. Descriptions of empirical phylogeographic in an average of comparative phylogeographic studies of 8%.
findings are not within the scope of this review. These have A total of 86% of articles on mammals used data from mtDNA
been presented and discussed in detail elsewhere (e.g. (68% used mtDNA alone and 18% combined it with other
Avise 2000) using case studies spanning the diversity of life markers) (Table 4). Studies based exclusively on nuclear DNA
and a vast variety of phylogeographic scenarios. sequence data were much more popular in mammals (8%)
than in other vertebrate groups (2% to 3%), a difference attribut-
able to the availability of a large number of target loci in humans
Mammals
and other intensively studied mammals (e.g. Templeton
Mammals have been pivotal in the development of the 2005). The reverse is true regarding allozyme markers,
theory and practice of phylogeography. This has been in which were rarely used in mammals (c. 1% of the total).
part due to the extensive research investment in deciphering
the history of human populations at both global and regional
Fishes
levels (e.g. Cann et al. 1987; Bonatto & Salzano 1997;
Richards et al. 1998; Underhill et al. 2001; Templeton 2005). Fishes, the most abundant and species-rich vertebrate
Genealogical surveys of our own species have greatly group comprised, together with terrestrial plants, the second
benefited our understanding of patterns in other species, most frequently studied taxon in phylogeography. Fishes
especially those influenced by recent biogeographic scenarios. have for a long time fascinated natural historians and
Considerable achievements in the field have also been evolutionary biologists (Wallace 1876; Nelson 2006). Fresh-
made in several other groups of mammals at intraspecific water fishes often display marked phylogeographic structure
and interspecific levels (e.g. Morin et al. 1994; Eizirik et al. strongly connected to historical and ecological changes of
2001), as well as in analyses of comparative phylogeography the aquatic environment and landscapes (Bermingham
(Da Silva & Patton 1998; Lessa et al. 2003). & Avise 1986; Bernatchez & Wilson 1998; Rundle et al. 2000;
The number of publications by continent of origin in Waters et al. 2007). In contrast, notwithstanding examples
mammals is not as skewed towards Europe and North of remarkable philopatry (e.g. Taylor & Hellberg 2003),
America as in other taxonomic groups (Table 2). This is marine fishes usually show shallow phylogeographic
because Asia and Africa account for a relatively high per- structure associated with the general absence of dispersal
centage of mammal studies (23% and 15%, respectively). barriers and high levels of spatial connectivity (Bowen &
Studies on South American and Australian mammals, on the Grant 1997). Fish phylogeography has also expanded
other hand, accounted for comparatively few publications considerably our understanding of the role of ecology in
(7% and 4%, respectively). Globally, the effort concentrated the speciation process, especially in scenarios where adaptive
on terrestrial mammals (93%) as opposed to marine (6%) or divergence and reproductive isolation are associated (Orr
freshwater mammals (1% of all articles) (Table 3). Mammals & Smith 1998; Lu & Bernatchez 1999; Beheregaray &
were the group with the highest percentage of taxon-specific Sunnucks 2001; Schluter 2001).

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Table 3 Association with types of environment, and whether studies focused on single or multiple taxa or were of comparative nature for
10 groups of organisms. Values represent the proportion of phylogeographic studies published across the globe between 1987 and 2006 for
each category (see text for details)

Environment Nature of the study

More than one taxon Comparative

Organisms Terrestrial Marine Freshwater Single taxon but not comparative phylogeography

Mammals 0.93 0.06 0.01 0.77 0.15 0.08

Fishes — 0.45 0.55 0.64 0.26 0.10
Herps 0.61 0.07 0.32 0.67 0.26 0.07
Birds 0.94 0.06 — 0.64 0.23 0.13
Plants: terrestrial 1.0 — — 0.67 0.26 0.07
Plants: aquatic – 0.73 0.27 0.61 0.34 0.05
Invertebrates: terrestrial 1.0 — — 0.60 0.32 0.08
Invertebrates: aquatic — 0.60 0.40 0.62 0.28 0.11
Micro-organisms 0.73 0.09 0.18 0.60 0.31 0.09
Fungi 1.0 — — 0.71 0.24 0.05

Table 4 Application of different classes of genetic marker for 10 groups of organisms. Values represent the proportion of phylogeographic
studies published across the globe between 1987 and 2006 that used only one class of genetic marker or combinations of genetic markers
(categories are mutually exclusive, see text for details)

Class of genetic marker (only one class used) Combination of genetic markers

II nuclear DNA Other Three or

I mtDNA sequence, SNP, III IV I and I and double four markers
Organisms or cpDNA AFLP or RAPD Microsatellite Allozyme I and II III IV combinations combined

Mammals 0.68 0.08 0.04 0.01 0.08 0.08 0.02 0.01 0.01
Fishes 0.69 0.03 0.05 0.04 0.09 0.05 0.05 0 0.01
Herps 0.77 0.02 0.03 0.02 0.07 0.04 0.04 0.01 0
Birds 0.81 0.02 0.04 0.01 0.07 0.04 0.01 0 0.01
Plants: terrestrial 0.46 0.28 0.03 0.07 0.09 0.02 0.02 0.03 0.01
Plants: aquatic 0.22 0.39 0.07 0 0.27 0 0 0.05 0.03
Invertebrates: terrestrial 0.66 0.07 0.02 0.06 0.10 0.03 0.05 0 0.05
Invertebrates: aquatic 0.64 0.07 0.01 0.03 0.13 0.02 0.07 0 0.02
Micro-organisms 0.11 0.78 0 0 0.11 0 0 0 0
Fungi 0 0.85 0.05 0 0.05 0 0 0.05 0

The wealth of existing phylogeographic information noncomparative (26% of the total) as well as comparative
about fishes is essentially restricted to teleosts, which phylogeographic studies (10%). In terms of genetic markers,
accounted for 98.5% of all articles. Elasmobranchs, on the 88% of fish articles (344 studies) included data from
other hand, were represented by only six articles, a very mtDNA. Around 20% of this value was represented by
imbalanced number given that sharks and rays comprise surveys that combined mtDNA with other markers. The
over 1100 known species (Compagno et al. 2005). Over two- proportion of fish studies based on allozymes (either alone
thirds of all fish studies (68%) came from North America or in combination with other markers) was the highest
and Europe, two regions with relatively impoverished among vertebrates since obtaining fresh or frozen tissue is
ichthyofaunas. On the other hand, South America, the con- possible for many species targeted by commercial fisheries.
tinental region with the highest diversity of freshwater fish
on Earth (Reis et al. 2004) accounted for only 6% of the
Plants
studies. Overall, despite the higher diversity of marine fishes,
freshwater fishes were more intensively studied accounting Phylogeographic surveys have been notoriously difficult
for 55% of all articles. Many fish surveys were based on to conduct in plants because of the difficulties involved in
more than one species and included a good proportion of finding genetic markers with resolving power comparable

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to animal mtDNA (Schaal et al. 1998; Newton et al. 1999). Nonetheless, many studies have provided consequential
Nonetheless, plant phylogeography has come a long way information about the role of historical and contemporary
in the last few years with the popularization of nuclear factors influencing the evolutionary history of invertebrate
markers for analyses of gene flow, especially microsatellites populations (Roderick 1996; Avise 2000). Phylogeographic
and AFLPs, and with the collection of data from larger studies have informed on the chronologies of adaptive
sections of cpDNA. This has resulted in a rapid increase in radiations of island arthropods (Fleischer et al. 1998; Roderick
publications reporting genetic variation in plants related & Gillespie 1998), the delineation of biogeographic breaks
to historical events of fragmentation, range expansion, in copepods (Burton & Lee 1994), in estuarine crustaceans
bottlenecks and speciation (Byrne et al. 2002; Petit et al. (Teske et al. 2006), and in springtails (Garrick et al. 2007),
2002, 2005; Abbot & Brochmann 2003; Miller & Schaal and the development of extrinsic hypotheses to understand
2005). For example, around 92% of all articles in terrestrial the effects of climatic changes in land snails (Hugall et al.
plants were published since 2000. In comparison, the propor- 2002) and flatworms (Sunnucks et al. 2006). Historical
tion of recently published articles is much lower in other considerations about the distribution of genetic diversity
popular groups such as mammals and fishes (84% and have also contributed to our understanding of invasion
82%, respectively). Research in phylogeography has also biology (Hall & Muralidharan 1989), epidemiology (Rich
advanced considerably our knowledge about the conserva- et al. 1995), and to address issues about cryptic biodiversity
tion of tree species (Newton et al. 1999) and the consequences (Knowlton 1993).
of species invasion (Saltonstall 2002; Koehler-Santos et al. Studies of terrestrial and aquatic invertebrates showed
2006) and Quaternary dynamics (Demesure et al. 1996; similar trends with regard to the geography of phylogeo-
Dumolin-Lapegue et al. 1997; Magri et al. 2006) on ecology graphic surveys, nature of study and genetic markers used.
and evolution of plant populations. Europe and North America accounted for the majority of
Terrestrial plants from the Southern Hemisphere have publications but Australian freshwater invertebrates were
been largely left behind in phylogeographic research, with relatively well represented (Table 2). This remarkable
a massive proportion of 88% of studies coming from the result (Australia is the driest inhabited continent on the
Northern Hemisphere. This represents the largest disparity planet) can be partially explained because of the work of
across taxonomic groups analysed in this review (Table 2). one productive group at Griffith University. On the other
Europe dominates the stage with 43% of all publications; hand, Africa and South America were poorly represented
North America and Asia are also well represented with in the invertebrate literature. The prospect that the relative
23% and 21% of the articles, respectively. South America, ease with which multiple codistributed terrestrial inverte-
the continent with the highest diversity of plant species brates can be collected would result in a good number of
(Myers et al. 2000), was represented by only 15 surveys, comparative studies was not met — only 8% of phylogeo-
around 4% of the total. Only 11 studies of terrestrial plants graphic surveys were classified as comparative, a value
have analysed patterns at a global scale, the lowest fraction lower than those found for fishes and birds. The proportion
among all taxonomic groups. For aquatic plants, 30 of the of global studies followed expectations based on general
41 studies identified were in the marine environment and differences in patterns of organism distribution, being
the proportion of articles of global scale was relatively greater for aquatic than for terrestrial invertebrates (10%
large (29%). The continents of North America, Europe and and 4%, respectively). Despite the supremacy of mtDNA
Asia accounted for 88% of all publications. Only a few for invertebrates (in particular the popular mitochondrial
studies on aquatic plants (5%) compared phylogeographic COI gene), the number of studies using Classes II and IV
patterns across species. The research in terrestrial and was greater than in other animal taxa. Conversely, research
aquatic plants showed similar trends in the use of genetic on invertebrates based on microsatellites (Class III) is still
markers. Plant studies relied much less on uniparentally in its infancy compared to any other animal group: only
inherited DNA information and used more information 1.5% and 2.5% of articles used these markers alone or in
from nuclear markers of Class II (28% for terrestrial and 39% combination, respectively. This could be in part explained
for aquatic plants) than most of the other taxonomic groups. by the propensity of phylogeographers to work on more
than one invertebrate taxon for which cross-species ampli-
fication of microsatellites is often not feasible, coupled with
Invertebrates
complications concerning the isolation of microsatellite
For practical reasons the extraordinary diversity found in loci for several invertebrate groups (e.g. Piggott et al. 2006).
invertebrates was divided into two groups: terrestrial
(includes aerial taxa) and aquatic species. The myriad of
Herpetofauna
life histories and evolutionary ecologies found in terrestrial
and aquatic invertebrates was represented in the phylogeo- Reptiles and amphibians have been the focus of increasing
graphy literature by only 313 and 253 articles, respectively. phylogeographic research in recent years: from the 292

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articles identified in this review, over 50% were published species (Baker et al. 1995), and reported on deviation from
between 2004 and 2006. Many of these species are specialists linearity of molecular evolution (Saetre et al. 2001) and on
found in patchy habitat or rely on disconnected water prehistoric decline of diversity in endangered species
bodies and as a result have shown strong phylogeographic (Paxinos et al. 2002). Phylogeographic studies, including
structure (Avise 2000). Some groups, such as the speciose comparative analyses, have also generated fruitful debates
frogs, have been the subject of a relatively small number of about the effects of the Pleistocene on bird speciation (Zink
surveys, whereas others, such as marine turtles, have been 1996; Avise & Walker 1998; Klicka & Zink 1999; Weir &
intensively studied (e.g. Bowen et al. 1991; Laurent et al. Schluter 2004) and about the significance of subspecies
1998). Research on herpetofauna have investigated speci- designations in ornithology for the fields of conservation
ation processes using environmental niche models (Graham and evolutionary biology (Ball & Avise 1992; Zink 2004).
et al. 2004), clarified Pleistocene population histories A large proportion of bird publications (37%) came from
(Phillips 1994; Alexandrino et al. 2000), and assessed recent North America, whereas the species-rich region of South
anthropogenic fragmentation (Cunningham & Moritz 1998) America accounted for a minor fraction (9%). Marine birds
and competing scenarios of evolutionary diversification represented 6% of all articles and most of these studies
(Walker & Avise 1998; Lougheed et al. 1999; Garcia-Paris were conducted in Polar Regions. Interestingly, considerable
et al. 2000). Other studies have investigated the roles of effort was allocated to compare phylogeographic patterns
volcano emergence, activity, and island ecology in driving in codistributed birds — this was the group with the highest
evolutionary diversification (Malhotra & Thorpe 2000; proportion of comparative studies (13%). Given the great
Caccone et al. 2002; Beheregaray et al. 2003, 2004; Keogh et al. potential for birds to disperse and their propensity to
2005) and provided essential information for taxonomy and migrate, this was also the group with more work con-
systematics (Zamudio et al. 1997; Ashton & de Queiroz 2001). ducted at hemispheric (but not global) scale, with 11% of
North America accounted for an amazingly high propor- studies falling into this category. In terms of genetic markers,
tion of the global productivity on reptiles and amphibians no other group relied so much on information based on
(42%) whereas Asia was represented by only 9% of the matrilineal diversity: 81% of the studies used only data
studies (the lowest value across all taxa for this continent, from the mtDNA genome and another 13% used these data
Table 2). Research in the Southern Hemisphere was pro- in combination with other markers. Very little work has
portionally more prolific for the herpetofauna (26% of been published based solely on allozymes and nuclear
all articles) than for any other taxonomic group, a result DNA data from Class II or based on combinations of these
attributable to numerous papers from Australia and the markers with mtDNA (2% and 7% of the total, respectively).
Galápagos Islands. Very small proportions of global and In contrast, recent years have seen an escalation in the
comparative phylogeographic studies were identified for number of bird articles using microsatellites, with 12 out of
reptiles and amphibians (3% and 7%, respectively), the the 17 papers that used these markers published between
lowest values among all animals. Compared to the general 2004 and 2006.
pattern detected across animal groups, there was less effort
in terms of obtaining multilocus data for reptiles and
Micro-organisms
amphibians and a much greater dependence on mtDNA
(77% of the studies used mtDNA alone and 16% combined Ecological studies about spatial scaling of microbial diversity
it with other markers). These values are only lower than have demonstrated that, like macro-organisms, both bacteria
those found for birds. and microbial eukaryotes exhibit spatially predictable
distributions from local to regional scales (Green et al. 2004;
Horner-Devine et al. 2004). However, the application of tools
Birds
and concepts to study the spatial distribution of genetic
The wealth of information about distribution and diversity variation in the highly heterogeneous and diverse group of
on birds is unrivalled among most biological groups. Yet, micro-organisms is a fairly novel endeavour: 31 out of the
birds represented the less studied animal group in this 45 identified articles were published between 2004 and 2006.
review with only 187 publications. Studies on birds have Despite the very low number of publications, the topics
revealed a great variety of phylogeographic patterns, both addressed were wide-ranging and included phylogeographic
in space and time, revolutionizing the knowledge about analyses of human viruses (Holmes 2004) and sulfate-
avian population structure and providing insight into the reducing bacteria in contaminated sediments (Perez-Jimenez
temporal durations of behavioural and morphological & Kerkhof 2005), a study of how interactions between
specializations (Avise & Ball 1991; Zink 1994, 1996; Avise symbiotic organisms can shape population genetic structure
2000). Studies have characterized breeding–overwintering (Jones et al. 2006), phylogeographic insights into the process
connectivity on broad geographic scales (Kimura et al. of host-race formation (Simon et al. 2003), and the proposal
2002), detected extreme population subdivision and cryptic of a model of evolutionary history of human and simian

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3766 L . B . B E H E R E G A R AY

T-cell leukaemia/lymphotropic viruses (Slattery et al. publication rates jumped from around 50 to 540 articles
1999). In addition, advances in the field of Environmental (Fig. 1). The number of published articles is still increasing
Microbiology have created potentially rich sources of considerably every year; 2007 experienced a growth rate of
phylogeographic data about bacterial diversity in soil and around 12% compared to 2006. Pinpointing specific reasons
aquatic samples (e.g. Voytek & Ward 1995). for this growth is probably an ineffective exercise since
The majority of the studies on micro-organisms were phylogeography has benefited in diverse ways from the
conducted in terrestrial environments (73%). The contin- constellation of technological, analytical and theoretical
ents of North America and Asia accounted for a large developments experienced in the last two decades by the
fraction of the articles (43% and 23%, respectively) and the field of molecular ecology (Hewitt 1996; Avise 1998, 2000,
proportion of surveys of global scope was the highest 2006; Templeton 1998; Sunnucks 2000; Rieseberg & Smith
among taxonomic groups (40%). As observed for the fungi, 2007). It is interesting to mention though that some noticeable
the most popular marker in micro-organism phylogeography annual increases (e.g. that of the year 2000) followed the
was nuclear DNA from Class II, which was used in 89% of publication of seminal work, such as the special issue of
the publications. Molecular Ecology (1998) about Comparative Phylogeography.
The integrative nature of the field can be illustrated by
the far-reaching topics addressed and by the great variety
Fungi
of scientific journals that have featured phylogeographic
Lastly we have the fungi, which were represented in the studies in their pages (Table 1). Although most studies can
phylogeographic arena by an exceptionally small number be primarily classified in the subject categories of ecology
of 21 articles. As stated by Kohn (2005), the variety of life- and evolution, empirical findings have also had valuable
history factors and species of fungi eagerly deserve more ramifications to conservation biology, plant sciences, zoology,
attention from the evolutionary biological community. aquatic biology, parasitology, microbiology, genetics,
Phylogeographic studies in fungi have the potential to animal behaviour and biotechnology. In other words, there
inform on consequential issues about disease control, seems to be growing awareness among biologists about
quarantine, free-trade and conservation (Kohn 2005). From the importance of adding historical perspectives derived
the limited number of surveys conducted I highlight the from the distribution of genetic diversity in populations to
contributions to taxonomy and biogeography of a multilocus understand organismal biology, conservation biology,
analysis of a phytopathogenic species complex (O’Donnell ecology, and evolution.
et al. 1998), a study of cryptic speciation and long-distance Phylogeography has also expanded into several historical
dispersal in a nonpathogenic fungus (Kauserud et al. 2006), disciplines of Earth sciences, especially palaeoclimatology,
inferences on population history and cryptic speciation palaeontology and geomorphology, with the majority of
in the fly agaric (Geml et al. 2006), and the role of local the field’s output (69% of all papers) reporting scenarios of
landscape to understand dispersal and gene flow in lichens diversification temporally associated with the Quaternary
(Walser et al. 2005). Period. Here, however, I perceive ample room for more
Most of the work on phylogeography of fungi comes collaboration and a better integration between phylogeo-
from the Northern Hemisphere, with North America, graphers and Earth scientists (sensu Beheregaray & Caccone
Europe and Asia accounting for 86% of the studies. Not a 2007). On one hand, phylogeographers have often ineffi-
single study carried out exclusively in the Southern Hemi- ciently (and sometimes incorrectly) explored and interpreted
sphere was retrieved in the database searches (Table 2). data about Earth’s history. These researchers generally lack
Most fungi surveys concentrated on one taxon or on species formal training in Earth sciences and are not updated with
complexes and only one study was classified as compara- recent advances in Late Quaternary dynamics (but several
tive phylogeography. Nuclear DNA markers from Class neat exceptions exist, e.g. Magri et al. 2006). On the other
I were the preferred source of genetic information for hand, Earth scientists seem to be generally unaware of
phylogeographic analyses in fungi, being used in 95% of the usefulness of genealogical reconstructions to address
the articles. questions concerning the interaction between physical and
biological systems (but a few elegant exceptions also exist
in geology, e.g. Craw et al. 2008). Clearly, more commun-
Concluding remarks, challenges, and prospects
ication is needed between these scientists. Earth scientists
and phylogeographers can mutually benefit by integrating
The state of phylogeography
information to fill in temporal and spatial gaps when
Phylogeography is an established, integrative and vigorous reconstructing the history of a particular region and its
discipline. The field has experienced dramatic expansion biota, a strategy that can guide and rationalize further
over two decades, with the most noticeable growth spurt genetic and geological sampling over the geographic and
observed between 1997 and 2006 — a period when annual temporal landscapes (Beheregaray & Caccone 2007). Another

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possible corollary of such integration is a decrease of the alone (75% of the total, this stabilized in around 62% since
overly large proportion of articles in phylogeography (18% 2002). Related to this, recent years have seen a rapid increase
of the total, or 438 papers) that did not explore or propose in the amount of animal mtDNA data generated as result
any temporal perspective when making inferences about of DNA barcoding, which offers a single mtDNA gene
population history. Adding a temporal component when approach for large-scale biodiversity survey and discovery
interpreting biogeographic patterns should be a priority in (Hebert et al. 2003). Although the primary impetus of DNA
the research agenda of phylogeographers. barcoding is global bio-identification, and its merit is justi-
In terms of taxonomic coverage, vertebrates were rela- fiably controversial (e.g. Will et al. 2005; Hickerson et al.
tively well represented in the phylogeography literature, 2006), the barcode data can be considered phylogeographic
accounting for more than half of all publications (1387 in its nature since it places specimens in one or another
papers). This was about twice the number of articles of ter- reciprocally monophyletic groups. As such, it represents a
restrial and aquatic invertebrates combined and over three large and growing mtDNA database that is amenable to
times that of terrestrial and aquatic plants. When comparing phylogeographic analysis.
across taxonomic groups, a taxonomic bias becomes evident Notwithstanding the supremacy of mtDNA, results of
for mammals, which accounted for 21% of all articles. This this review also illustrate important changes in the way
bias is in part due to the popular status that our own species researchers have used genetic markers. Perhaps the most
and the charismatic mammalian megafauna have in relevant is the escalation of surveys using multilocus DNA
phylogeography. In contrast, smaller and hard to notice data (particularly from introns and microsatellites) that
nonvertebrates have been largely unstudied. Relative to occurred during the late 1990s. The initial boom was
their diversity, more phylogeographic surveys are needed short-lived though (Fig. 7) and since 2002 the percentage
for invertebrates, micro-organisms and fungi than for other of studies using nuclear DNA has stabilized in around
biological groups. An increase in research effort in these 31%. Only c. 16% of these studies combined nuclear with
groups would have wide-reaching ramifications. These organellar DNA data. It was also surprising to note that
would include an improved understating of population some combinations are not as popular as one would
histories in poor-disperser species, which can be indicators expect. This is the case for the combo ‘organelle and micro-
of localized evolutionary and ecological processes and, satellites’, which can offer insights about phylogeographic
therefore, represent conservative benchmarks for biological patterns and processes acting at different scales of the
conservation. The recent ecological findings suggesting that evolutionary landscape. For instance, despite the shorter
both bacteria and microbial fungi exhibit predictable taxa– coalescence time of mtDNA, the higher mutation rates of
area relationships from centimetres up to whole continents microsatellites create more twigs on the ends of genealogical
(Green et al. 2004; Horner-Devine et al. 2004) open up an branches that can be useful to disclose fine-scale structure,
exciting avenue to study the relative roles of environmental cryptic species, and rapid speciation events (e.g. Takezaki
heterogeneity and geography in shaping the demographic & Nei 1996; Petren et al. 1999; Beheregaray et al. 2002). Most
history and evolution of microbes. Further phylogeographic importantly, it is well documented that the analysis of
work with small life forms would also contribute to our multiple unlinked loci is critical for accommodating coales-
understanding of the relationship between demography cent stochasticity and improving the accuracy of inferences
and species cohesiveness within predominantly asexual about demographic history and estimates of divergence
taxa (Avise 2000). Plants are another key group that was times (Edwards & Beerli 2000; Hare 2001; Templeton 2002;
not well covered in the literature, especially during the Knowles 2004; Garrick et al. 2008). Putting it simply, if the
1990s. Fortunately, AFLPs (Bensch & Akesson 2005; Meudt question concerns processes (as opposed to patterns only),
& Clarke 2007) and microsatellites (Squirrell et al. 2003) the study should be a multilocus endeavour. The unfortunate
have offered some solutions to initial problems of obtaining reality is that many present-day phylogeographers do not
genealogical information in plants. This promoted a recent have the means to generate multilocus data sets that can
upsurge of phylogeographic surveys, with 92% of all plant be used to statistically assess uncertainty in genealogical
articles published since 2000. estimates. Although it is unlikely that mtDNA will loose its
The establishment and the vigorous growth of phylo- special status as the marker of choice in phylogeography,
geography have been closely associated with analyses based the number of studies combining multiple loci looks set to
on information from the mitochondrial genome (Avise 1998). increase as new generations of phylogeographers start to
Despite recent developments in gene marker technology experience the benefits of the genomic era and become
and lower genotyping costs, it can be concluded that more familiar with advances in multilocus coalescent theory
organellar DNA (particularly mtDNA) still stands as the and analysis. However, I argue below that these benefits
powerhouse of phylogeography. This was by far the most and advances might, unfortunately, not be fully available
popular class of marker in the 20-year period, used both in to the phylogeographers who actually have the most difficult
combination with other markers (81% of all articles) or job at hand.

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Riddle et al. 2000; Moritz 2002). These comparative studies,

The challenges for developing countries of the Southern
such as the California Hotspots Project, can explore the
Hemisphere (and other regions)
performance of environmental drivers of diversification to
A wealth of phylogeographic data is available for many identify regions that maintain rapid adaptive evolution,
terrestrial and aquatic organisms of the Northern Hemisp- concentrations of historically isolated populations, or both
here. In fact, a disproportionately 77% of all empirical (Davis et al. 2008). However, the limited phylogeographic
surveys of the field (or 1874 papers) have focused exclusively data available for species-rich regions from most developing
on Northern Hemisphere study systems. Postglacially countries is essentially precluding the use of comparative
colonized regions of Europe and North America have been phylogeography to inform on biodiversity conservation
particularly well covered, resulting in increasingly coherent and management.
explanations (e.g. Hewitt 2000) about the influence of global In addition to these problems, I also perceive technological
climate fluctuations on range shifts, extinctions, and challenges for phylogeographers in the developing world.
speciation of Northern Hemisphere biotas. This contrasts This relates to the arrival of the new era of functional
dramatically with the poorly studied Southern Hemisphere, genomics, which has the exciting opportunity of changing
which was represented in only 15% of the publications the way we make inferences about population history.
(or 365 papers) (Fig. 2a). Considerable differences in geo- Mechanistic insights about the geographic distribution
morphologic and climatic history exist between the two of adaptive genetic variation are expected to expand the
hemispheres and much more data are needed before intellectual horizons of phylogeography and establish a
generalizations proposed to Europe and North America more integrated field (Emerson & Hewitt 2005; Avise 2006).
can be extended to other parts of the world. Phylogeographic The potential impact of functional genomics in the field can
information is currently either inadequate or simply be seen in recent editorials of key journals such as Molecular
nonexisting for biotas inhabiting many regions of the Ecology and Proceedings of the Royal Society of London B,
Southern Hemisphere, such as Patagonia, Amazonia, Brazil’s which actively encourage submissions of articles describing
Atlantic Forest, Brazil’s Cerrado, Wallacea, Sundaland, patterns of genetic diversity in populations related to
New Guinea, Polynesia-Micronesia, Northern and Central ecological adaptations and the functioning of organisms.
Australia, Madagascar, East Africa, and the bulk of marine Despite the fruitful consequences of integrating functional
bioregions. Most of these are found in developing countries, genomics with more traditional fields of organismal
which is consistent with the positive correlation found in biology, I anticipate an intensification of some disparities
this review between research productivity and country’s identified here between researchers from the developed
wealth. Several regions from developing countries of the and the developing world. My point is that whereas some
Northern Hemisphere are also data deficient in phylogeo- researchers will benefit from an understanding of the
graphy, including Sri Lanka, mountains of Central Asia, adaptive value of historically partitioned genetic variation
Irano-Anatolian region, Himalayas, mountains of Southwest (especially that found in well-characterized postglacial
China, and the Philippines. populations), others will still face the difficult task of
Importantly, many of the regions named above have describing (and publishing) patterns of population history
been classified as hotspots of biodiversity. These are areas in understudied biotas. The latter is especially true for
where exceptional concentrations of endemics (e.g. 44% of researchers working in species-rich areas with inadequate
the world’s plant species and 35% of its vertebrate species) sampling and taxonomy, such as tropical marine regions
are undergoing exceptional loss of habitat (Myers et al. and tropical rainforests of the developing world.
2000). Most of the 25 identified hotspots are located in What can the phylogeographic community do to amel-
tropical regions of developing countries where threats to iorate these problems? One possibility is to establish
biodiversity are greatest and conservation resources are international collaborations and research networks that will
scarcest (Myers et al. 2000). One of such countries is Brazil. make available resources to rapidly document and compare
Despite being generally considered the world’s most species phylogeographies in poorly studied regions. Incipient
biodiverse nation, Brazil ranked only 15th in terms of pro- collaborative efforts in developing countries will no doubt
ductivity in phylogeography. Indonesia and Colombia also face numerous barriers, especially in terms of financial sup-
top the list of Earth’s biologically wealthiest countries port, infrastructure, linguistics, and licensing for exporting
(Mittermeier et al. 2000) but ranked, respectively, a mere tissue samples and specimens. One way to circumvent
38th and 62nd in the phylogeography ranking (Appendix). some of these barriers is to advocate the development of in
Phylogeographic studies, particularly those using large situ capacity. Research institutions and scientific societies
data sets from codistributed species, provide a valuable from the developed world could offer more workshops
framework for developing conservation strategies aimed and training opportunities in regional areas of developing
at protecting historical dimensions of biodiversity and the countries. They could also foster communication between
evolutionary processes that sustain it (Moritz & Faith 1998; individuals by increasing travel support for postgraduate

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 T W E N T Y Y E A R S O F P H Y L O G E O G R A P H Y 3769

students and young scientists from developing countries work conducted at the Molecular Ecology Laboratory at Mac-
to attend international conferences. By creating strategies quarie University (MELMU).
for developing in situ capacity our community will help
building intellectual and practical expertise necessary to
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lead to formal agreements between research institutions flora: in the footsteps of Eric Hulten. Molecular Ecology, 12, 299–
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Alexandrino J, Froufe E, Arntzen JW, Ferrand N (2000) Genetic
resources. Although several pre-eminent phylogeographers
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Appendix
The top 100 most productive countries in phylogeography (period 1987–2006)

Ranking/Country No. of articles Ranking/Country No. of articles

1 USA 1250 51 Costa Rica 7

2 United Kingdom* 422 52 Madagascar 7
3 France 289 53 Peru 7
4 Germany 279 54 Singapore 7
5 Australia 237 55 Tunisia 7
6 Canada 218 56 Ecuador 6
7 Spain 218 57 Uganda 6
8 Italy 163 58 Iceland 5
9 Japan 137 59 Saudi Arabia 5
10 Sweden 113 60 Bolivia 4
11 Switzerland 96 61 Bulgaria 4
12 Russia 93 62 Colombia 4
13 Austria 90 63 Iran 4
14 Portugal 90 64 Latvia 4
15 Brazil 85 65 Luxembourg 4
16 People’s Republic of China 82 66 Mali 4
17 Norway 81 67 Mongolia 4
18 Belgium 78 68 Senegal 4
19 New Zealand 76 69 Ukraine 4
20 Netherlands 69 70 Albania 3
21 South Africa 68 71 Bosnia and Herzegovina 3
22 Taiwan 63 72 Burkina Faso 3
23 Finland 45 73 Côte d’Ivoire 3
24 Denmark 43 74 Cuba 3
25 Mexico 39 75 French Polynesia 3
26 Panama 37 76 Ghana 3
27 Argentina 33 77 Kuwait 3
28 Greece 31 78 Lithuania 3
29 Czech Republic 28 79 Niger 3
30 Poland 27 80 Nigeria 3
31 Estonia 26 81 Palau 3
32 Hungary 21 82 Papua New Guinea 3
33 India 20 83 Serbia and Montenegro 3
34 South Korea 19 84 Sri Lanka 3
35 Croatia 18 85 Tanzania 3
36 Chile 17 86 United Arab Emirates 3
37 Turkey 16 87 Zambia 3
38 Indonesia 14 88 Bangladesh 2
39 Malaysia 14 89 Botswana 2
40 Ireland 13 90 Cambodia 2
41 Thailand 12 91 Cyprus 2
42 Uruguay 12 92 French Guiana 2
43 Morocco 11 93 Gabon 2
44 Venezuela 11 94 Guatemala 2
45 Israel 10 95 Namibia 2
46 Kenya 10 96 Réunion 2
47 Romania 10 97 Yemen 2
48 Slovakia 10 98 Armenia 1
49 Slovenia 10 99 Benin 1
50 Vietnam 9 100 Bermuda 1

*Includes 293 articles by English, 79 by Scottish, 43 by Welsh and 7 by northern Irish researchers.

© 2008 The Author

Journal compilation © 2008 Blackwell Publishing Ltd