The state of phylogeography
Phylogeography is an established, integrative and vigorous discipline. The field has experienced dramatic expansion over two decades, with the most noticeable growth spurt observed between 1997 and 2006 — a period when annual publication rates jumped from around 50 to 540 articles (Fig. 1). The number of published articles is still increasing considerably every year; 2007 experienced a growth rate of around 12% compared to 2006. Pinpointing specific reasons for this growth is probably an ineffective exercise since phylogeography has benefited in diverse ways from the constellation of technological, analytical and theoretical developments experienced in the last two decades by the field of molecular ecology (Hewitt 1996; Avise 1998, 2000, 2006; Templeton 1998; Sunnucks 2000; Rieseberg & Smith 2007). It is interesting to mention though that some noticeable annual increases (e.g. that of the year 2000) followed the publication of seminal work, such as the special issue of 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 of scientific journals that have featured phylogeographic studies in their pages (Table 1). Although most studies can be primarily classified in the subject categories of ecology and evolution, empirical findings have also had valuable ramifications to conservation biology, plant sciences, zoology, aquatic biology, parasitology, microbiology, genetics, animal behaviour and biotechnology. In other words, there seems to be growing awareness among biologists about the importance of adding historical perspectives derived from the distribution of genetic diversity in populations to understand organismal biology, conservation biology, ecology, and evolution.
Phylogeography has also expanded into several historical disciplines of Earth sciences, especially palaeoclimatology, palaeontology and geomorphology, with the majority of the field's output (69% of all papers) reporting scenarios of diversification temporally associated with the Quaternary Period. Here, however, I perceive ample room for more collaboration and a better integration between phylogeographers and Earth scientists (sensu Beheregaray & Caccone 2007). On one hand, phylogeographers have often inefficiently (and sometimes incorrectly) explored and interpreted data about Earth's history. These researchers generally lack formal training in Earth sciences and are not updated with recent advances in Late Quaternary dynamics (but several neat exceptions exist, e.g. Magri et al. 2006). On the other hand, Earth scientists seem to be generally unaware of the usefulness of genealogical reconstructions to address 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 communication is needed between these scientists. Earth scientists and phylogeographers can mutually benefit by integrating information to fill in temporal and spatial gaps when reconstructing the history of a particular region and its biota, a strategy that can guide and rationalize further genetic and geological sampling over the geographic and temporal landscapes (Beheregaray & Caccone 2007). Another possible corollary of such integration is a decrease of the overly large proportion of articles in phylogeography (18% of the total, or 438 papers) that did not explore or propose any temporal perspective when making inferences about population history. Adding a temporal component when interpreting biogeographic patterns should be a priority in the research agenda of phylogeographers.
In terms of taxonomic coverage, vertebrates were relatively well represented in the phylogeography literature, accounting for more than half of all publications (1387 papers). This was about twice the number of articles of terrestrial and aquatic invertebrates combined and over three times that of terrestrial and aquatic plants. When comparing across taxonomic groups, a taxonomic bias becomes evident for mammals, which accounted for 21% of all articles. This bias is in part due to the popular status that our own species and the charismatic mammalian megafauna have in phylogeography. In contrast, smaller and hard to notice nonvertebrates have been largely unstudied. Relative to their diversity, more phylogeographic surveys are needed for invertebrates, micro-organisms and fungi than for other biological groups. An increase in research effort in these groups would have wide-reaching ramifications. These would include an improved understating of population histories in poor-disperser species, which can be indicators of localized evolutionary and ecological processes and, therefore, represent conservative benchmarks for biological conservation. The recent ecological findings suggesting that both bacteria and microbial fungi exhibit predictable taxa–area relationships from centimetres up to whole continents (Green et al. 2004; Horner-Devine et al. 2004) open up an exciting avenue to study the relative roles of environmental heterogeneity and geography in shaping the demographic history and evolution of microbes. Further phylogeographic work with small life forms would also contribute to our understanding of the relationship between demography and species cohesiveness within predominantly asexual taxa (Avise 2000). Plants are another key group that was not well covered in the literature, especially during the 1990s. Fortunately, AFLPs (Bensch & Akesson 2005; Meudt & Clarke 2007) and microsatellites (Squirrell et al. 2003) have offered some solutions to initial problems of obtaining genealogical information in plants. This promoted a recent upsurge of phylogeographic surveys, with 92% of all plant articles published since 2000.
The establishment and the vigorous growth of phylogeography have been closely associated with analyses based on information from the mitochondrial genome (Avise 1998). Despite recent developments in gene marker technology and lower genotyping costs, it can be concluded that organellar DNA (particularly mtDNA) still stands as the powerhouse of phylogeography. This was by far the most popular class of marker in the 20-year period, used both in combination with other markers (81% of all articles) or alone (75% of the total, this stabilized in around 62% since 2002). Related to this, recent years have seen a rapid increase in the amount of animal mtDNA data generated as result of DNA barcoding, which offers a single mtDNA gene approach for large-scale biodiversity survey and discovery (Hebert et al. 2003). Although the primary impetus of DNA barcoding is global bio-identification, and its merit is justifiably controversial (e.g. Will et al. 2005; Hickerson et al. 2006), the barcode data can be considered phylogeographic in its nature since it places specimens in one or another reciprocally monophyletic groups. As such, it represents a large and growing mtDNA database that is amenable to phylogeographic analysis.
Notwithstanding the supremacy of mtDNA, results of this review also illustrate important changes in the way researchers have used genetic markers. Perhaps the most relevant is the escalation of surveys using multilocus DNA data (particularly from introns and microsatellites) that occurred during the late 1990s. The initial boom was short-lived though (Fig. 7) and since 2002 the percentage of studies using nuclear DNA has stabilized in around 31%. Only c. 16% of these studies combined nuclear with organellar DNA data. It was also surprising to note that some combinations are not as popular as one would expect. This is the case for the combo ‘organelle and microsatellites’, which can offer insights about phylogeographic patterns and processes acting at different scales of the evolutionary landscape. For instance, despite the shorter coalescence time of mtDNA, the higher mutation rates of microsatellites create more twigs on the ends of genealogical branches that can be useful to disclose fine-scale structure, cryptic species, and rapid speciation events (e.g. Takezaki & Nei 1996; Petren et al. 1999; Beheregaray et al. 2002). Most importantly, it is well documented that the analysis of multiple unlinked loci is critical for accommodating coalescent stochasticity and improving the accuracy of inferences about demographic history and estimates of divergence times (Edwards & Beerli 2000; Hare 2001; Templeton 2002; Knowles 2004; Garrick et al. 2008). Putting it simply, if the question concerns processes (as opposed to patterns only), the study should be a multilocus endeavour. The unfortunate reality is that many present-day phylogeographers do not have the means to generate multilocus data sets that can be used to statistically assess uncertainty in genealogical estimates. Although it is unlikely that mtDNA will loose its special status as the marker of choice in phylogeography, the number of studies combining multiple loci looks set to increase as new generations of phylogeographers start to experience the benefits of the genomic era and become more familiar with advances in multilocus coalescent theory and analysis. However, I argue below that these benefits and advances might, unfortunately, not be fully available to the phylogeographers who actually have the most difficult job at hand.
The challenges for developing countries of the Southern Hemisphere (and other regions)
A wealth of phylogeographic data is available for many terrestrial and aquatic organisms of the Northern Hemisphere. In fact, a disproportionately 77% of all empirical surveys of the field (or 1874 papers) have focused exclusively on Northern Hemisphere study systems. Postglacially colonized regions of Europe and North America have been particularly well covered, resulting in increasingly coherent explanations (e.g. Hewitt 2000) about the influence of global climate fluctuations on range shifts, extinctions, and speciation of Northern Hemisphere biotas. This contrasts dramatically with the poorly studied Southern Hemisphere, which was represented in only 15% of the publications (or 365 papers) (Fig. 2a). Considerable differences in geomorphologic and climatic history exist between the two hemispheres and much more data are needed before generalizations proposed to Europe and North America can be extended to other parts of the world. Phylogeographic information is currently either inadequate or simply nonexisting for biotas inhabiting many regions of the Southern Hemisphere, such as Patagonia, Amazonia, Brazil's Atlantic Forest, Brazil's Cerrado, Wallacea, Sundaland, New Guinea, Polynesia-Micronesia, Northern and Central Australia, Madagascar, East Africa, and the bulk of marine bioregions. Most of these are found in developing countries, which is consistent with the positive correlation found in this review between research productivity and country's wealth. Several regions from developing countries of the Northern Hemisphere are also data deficient in phylogeography, including Sri Lanka, mountains of Central Asia, Irano-Anatolian region, Himalayas, mountains of Southwest China, and the Philippines.
Importantly, many of the regions named above have been classified as hotspots of biodiversity. These are areas where exceptional concentrations of endemics (e.g. 44% of the world's plant species and 35% of its vertebrate species) are undergoing exceptional loss of habitat (Myers et al. 2000). Most of the 25 identified hotspots are located in tropical regions of developing countries where threats to biodiversity are greatest and conservation resources are scarcest (Myers et al. 2000). One of such countries is Brazil. Despite being generally considered the world's most biodiverse nation, Brazil ranked only 15th in terms of productivity in phylogeography. Indonesia and Colombia also top the list of Earth's biologically wealthiest countries (Mittermeier et al. 2000) but ranked, respectively, a mere 38th and 62nd in the phylogeography ranking (Appendix). Phylogeographic studies, particularly those using large data sets from codistributed species, provide a valuable framework for developing conservation strategies aimed at protecting historical dimensions of biodiversity and the evolutionary processes that sustain it (Moritz & Faith 1998; Riddle et al. 2000; Moritz 2002). These comparative studies, such as the California Hotspots Project, can explore the performance of environmental drivers of diversification to identify regions that maintain rapid adaptive evolution, concentrations of historically isolated populations, or both (Davis et al. 2008). However, the limited phylogeographic data available for species-rich regions from most developing countries is essentially precluding the use of comparative phylogeography to inform on biodiversity conservation and management.
In addition to these problems, I also perceive technological challenges for phylogeographers in the developing world. This relates to the arrival of the new era of functional genomics, which has the exciting opportunity of changing the way we make inferences about population history. Mechanistic insights about the geographic distribution of adaptive genetic variation are expected to expand the intellectual horizons of phylogeography and establish a more integrated field (Emerson & Hewitt 2005; Avise 2006). The potential impact of functional genomics in the field can be seen in recent editorials of key journals such as Molecular Ecology and Proceedings of the Royal Society of London B, which actively encourage submissions of articles describing patterns of genetic diversity in populations related to ecological adaptations and the functioning of organisms. Despite the fruitful consequences of integrating functional genomics with more traditional fields of organismal biology, I anticipate an intensification of some disparities identified here between researchers from the developed and the developing world. My point is that whereas some researchers will benefit from an understanding of the adaptive value of historically partitioned genetic variation (especially that found in well-characterized postglacial populations), others will still face the difficult task of describing (and publishing) patterns of population history in understudied biotas. The latter is especially true for researchers working in species-rich areas with inadequate sampling and taxonomy, such as tropical marine regions and tropical rainforests of the developing world.
What can the phylogeographic community do to ameliorate these problems? One possibility is to establish international collaborations and research networks that will make available resources to rapidly document and compare species phylogeographies in poorly studied regions. Incipient collaborative efforts in developing countries will no doubt face numerous barriers, especially in terms of financial support, infrastructure, linguistics, and licensing for exporting tissue samples and specimens. One way to circumvent some of these barriers is to advocate the development of in situ capacity. Research institutions and scientific societies from the developed world could offer more workshops and training opportunities in regional areas of developing countries. They could also foster communication between individuals by increasing travel support for postgraduate students and young scientists from developing countries to attend international conferences. By creating strategies for developing in situ capacity our community will help building intellectual and practical expertise necessary to improve the quantity and quality of research in phylogeography and biodiversity. In addition, this will eventually lead to formal agreements between research institutions that should not fail to generate synergies and rationalize resources. Although several pre-eminent phylogeographers are based in the developing world, they usually do not attract enough funding for conducting large-scale screening of populations using multigene approaches. The contrary is probably true in several developed countries, where funding agencies tend to support scientists that use the latest (and often more expensive) molecular tools. One potential avenue for reducing the technological gap between these two types of scientists is to assess the role of less expensive approaches (e.g. genomic scans using AFLPs; Meudt & Clarke 2007) for disclosing information about the geographic distribution of both neutral and adaptive genetic variation. These approaches can potentially offer insights into the genotype–phenotype interface (e.g. Luikart et al. 2003; Bonin et al. 2006) in groups of organisms for which it is still unthinkable to use more canonical genomic methods.
Although collaborative efforts similar to those proposed above already exist in a few places, many species and biotas of our natural world still await to be surveyed and compared. The building up of regional comparative phylogeographic syntheses in the Southern Hemisphere (and in developing countries of the Northern Hemisphere) is crucial for the expansion of the field. This would enable testing for differences and generalities in the histories of biotas of the two hemispheres, contribute with regional conservation efforts, and facilitate the integration between phylogeographers and Earth scientists. Phylogeography is a young and integrative field within biological and historical sciences that has experienced fast growth in recent years. Although the growing popularity of the field is set to continue, the intellectual maturation of phylogeography will eventually depend not only on developments in DNA technology, theory, and statistical analysis, but also on syntheses of comparative information across different regions of the globe. For this to become a reality many empirical phylogeographic surveys in developing countries are needed.