Molecular Ecology (1998) 7, 367–369 Comparative phylogeography: concepts and applications E. BERMINGHAM* and C. MORITZ† *Smithsonian Tropical Research Institute, Apartado 2072, Balboa, Republic of Panama, †Department of Zoology, The University of Queensland, Qld. 4072, Australia Introduction extinction; in other words, investigation of the funda- mental links between population processes and regional This special issue of Molecular Ecology celebrates the birth patterns of diversity and biogeography. The (typically) of phylogeography 10 years ago (Avise et al. 1987). slower evolutionary rate of chloroplast DNA (Schaal et al. Because the discipline has deep roots in historical bio- 1998) has limited the contribution of plants to phylo- geography and population genetics, phylogeography was geography and our nascent knowledge of landscape heralded as a bridge linking the study of micro- and evolution. We anticipate that plant phylogeography will macroevolutionary processes. The initial and still domi- increase in importance, thus refining our interpretation of nant infrastructure for this bridge has been mitochondrial historical landscape assembly and maintenance, as our DNA (mtDNA) analyses which have permitted genealog- understanding of the mutational basis of microsatellite ical traces to be followed across the genetic boundaries evolution improves and permits this class of molecular between populations, species and higher taxonomic markers to be used in comparative context. levels. In his personal reflection, Avise (1998) documents Certainly one clear empirical success of mtDNA-based the explosive growth of phylogeography in the decade phylogeography has been the improved description of the since its inception and notes many of the hallmark studies geographical distribution, phylogenetic relationships and that have provided the empirical and conceptual link genetic distances among evolutionary lineages of animals, between systematics and population genetics. leading, in turn, to a better understanding of regional bio- Celebrations are often times of renewal, and thus this geography and areas of endemism. Articles presented in special issue of Molecular Ecology aims not only to review this issue summarize and discuss the evolutionary land- the past but also to present a blend of theoretical and scapes of North America (Bernatchez & Wilson 1998), empirical papers with the hope of invigorating the field. lower Central America (Bermingham & Martin 1998), Phylogeography and its predominant reliance on Amazonia (da Silva & Patton 1998), Europe (Taberlet et al. (animal) mtDNA has led to a body of descriptive data that 1998), the Australian Wet Tropics (Schneider et al. 1998) are impressive in terms of their sheer comparative scope. and Hawaii (Roderick & Gillespie 1998; see also Fleischer For example, comparisons of mtDNA divergence et al. 1998). These studies demonstrate the importance of between sister taxa of North American birds combining molecular phylogeographic evidence with (Bermingham et al. 1992; Klicka & Zink 1997), South independent information on landscape history obtained American rodents and marsupials (da Silva & Patton from geology, palaeopalynology, etc. Of course there is a 1998) and frogs and reptiles across the Australian Wet long way to go. One of the many challenges lying ahead is Tropics (Schneider et al. 1998) have significantly dis- the comparative phylogeographic description of marine counted Late Pleistocene models of speciation and species, owing in part to the vast and disjunct geographi- suggested that many species pairs are older than previ- cal scale of many marine populations (Shulman & ously appreciated. Several articles in this issue presage Bermingham 1995; Palumbi 1997). Meeting this challenge the potential of comparative phylogeographic analyses and will undoubtedly provide contrasts and insights as sharp demonstrate that the shift from RFLP-based assays to as those emerging from comparisons of temperate and direct determination of DNA nucleotide sequence has tropical terrestrial evolutionary landscapes. permitted increasingly fruitful cross-taxa comparisons of Comparative phylogeographic analyses can con- evolutionary history. In turn, we project that comparative tribute to broader studies of ecology and evolution in a phylogeographic analysis will permit detailed studies of number of ways. First, phylogeographic analysis can landscape evolution, including the dispersal of taxa identify historically and evolutionarily independent through a region, speciation, adaptive radiation, and regions that can be considered as natural replicates amongst which generalizations about specific processes Correspondence: E. Bermingham. Tel.: +01-507-228-4339; Fax: can be tested statistically. For example, the evolutionary +01-507-228-0516; E-mail: [email protected] response to selection gradients can be compared across © 1998 Blackwell Science Ltd 368 E. BERMINGHAM AND C. MORITZ different historical isolates. Second, phylogeography can distributed across the K–Ar-aged Hawaiian Islands provide an evolutionary and geographical context for (Fleischer et al. 1998). More typically, phylogeographers the species comprising ecological communities, thus have extrapolated molecular rates from point estimates permitting determination of historical and spatial influ- relating a presumed date of separation with molecular ences on patterns of species richness (Ricklefs & Schluter divergence between taxa. The faith that many phylogeog- 1993). Third, an understanding of historical reponses to raphers appear to place in molecular clocks would be dis- changes in the landscape and the identification of evolu- quieting were it not for the advent of a number of tionarily isolated areas can inform conservation strate- statistical and phylogenetic approaches that permit gies (Moritz & Faith 1998). measures of molecular divergence to be tested for rate Phylogeography can be (and has been) criticized for heterogeneity. Notwithstanding these tests, robust tempo- being overly reliant on a single gene system, mtDNA, as a ral estimation in phylogeographic reconstructions would marker of evolutionary descent. The pitfalls, including be improved by utilizing two or more unlinked genetic effects of selection, inadvertent amplification of pseudo- markers and determining from each set of data whether genes, interspecific hybridization etc., can often be the relative times since cladogenesis are congruent. avoided by thoughtful molecular and numerical analyses Therefore, the major challenges that we see in the future and by testing for phylogenetic congruence across nuclear are: and mitochondrial genes. However, the utility of nuclear 1 To utilize unlinked molecular markers and develop gene (e.g. intron) sequences in population-level phyloge- improved analytical approaches for testing for evolution- netics appears to be limited by the substantially greater ary congruence, or lack thereof, between nuclear and coalescent time (and associated variance) of nuclear genes organelle genes. as compared to mitochondrial genes, and the potential for 2 To incorporate new developments in coalescence the- reticulate evolution among nuclear alleles due to recombi- ory, particularly as they apply to nonequilibrium popula- nation. Nonetheless, phylogeographers will come to rely tions, into phylogeography and, more generally, to increasingly on nuclear markers, and statistical in addition increase the statistical rigour of the field. to phylogenetic analyses, as attention turns to joint study 3 To increase the precision with which the timing of of the demographic and phylogenetic histories of species. cladogenetic (separation) events can be estimated. Under some conditions, particularly where genetic divergence is limited and there is substantial homoplasy Improvements in these areas, some of which are evident and among-site rate variation, or both, it may be inappro- from studies in this issue, will improve substantially the priate to use tree-based analytical methods even for power of phylogeography to test hypotheses derived from mtDNA (Smouse 1998). But where even part of a tree or species biogeography, speciation, earth history, etc. network can be estimated reliably, overlaying the tree on In conclusion, phylogeography seeks to test the congru- geography can provide insights into history that are diffi- ence between the evolutionary, demographic and distri- cult to obtain in any other way (Templeton 1998). The butional histories of taxa against the particular geological obvious link between coalescence models (Hudson 1998) and ecological setting of a region and to determine the and empirically estimated gene trees has refined phyloge- chronology of evolutionary diversification. Comparative netic analysis as the field increasingly incorporates this phylogeography describes the evolution of landscapes rapidly developing area of population genetics theory. and permits analysis of the effects of history and geogra- Already, it is apparent that gene trees can provide esti- phy on organismal community structure at both local and mates of (long-term) effective population size, mutation regional levels. Knowledge concerning the different ages rate and gene flow (see papers in Harvey et al. 1996). The of biotas and their areas of extent and the different rates of result should be strong inference regarding the history of species origin and extinction will enhance our under- a taxon’s spread across a landscape and the presence of standing of the processes responsible