Progress in Physical Geography

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The role of molecular genetics in sculpting the future of integrative biogeography Brett R. Riddle, Michael N. Dawson, Elizabeth A. Hadly, David J. Hafner, Michael J. Hickerson, Stacy J. Mantooth and Anne D. Yoder Progress in Physical Geography 2008; 32; 173 DOI: 10.1177/0309133308093822

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The role of molecular genetics in sculpting the future of integrative biogeography

Brett R. Riddle,1* Michael N. Dawson,2 Elizabeth A. Hadly,3 David J. Hafner,4 Michael J. Hickerson,5 Stacy J. Mantooth1 and Anne D. Yoder6

1School of Life Sciences, University of Nevada Las Vegas, 4505 Maryland Parkway, Las Vegas, Nevada 89154-4004, USA 2School of Natural Sciences, University of California at Merced, 5200 North Lake Road, Merced, California 95344, USA 3Department of Biology, Stanford University, Stanford, California 94305-5020, USA 4Biosciences Department, New Mexico Museum of Natural History, 1801 Mountain Road NW, Albuquerque, New Mexico 87104, USA 5Biology Department, Queens College, CUNY, 65030 Kissena Boulevard, Flushing, New York 11367-1597, USA 6Department of Biology, Duke University, Durham, North Carolina, USA 27706

Abstract: We review the expanding role of molecular genetics in the emergence of a vibrant and vital integrative biogeography. The enormous growth over the past several decades in the number and variety of molecular-based phylogenetic and population genetics studies has become the core information used by biogeographers to reconstruct the causal connections between historical evolutionary and ecological attributes of taxa and biotas, and the landscapes and seascapes that contain them. A proliferation of different approaches, sequences, and genomes have provided for the integration of a ‘biogeography of the Late Neogene’ with other Earth and biological sciences under the rubrics of phylogeography, landscape genetics, and phylochronology. Approaches designed explicitly to take advantage of unique properties of molecular genetic information have led to the re-emergence of dispersal as an analytically tractable process that historical biogeographers can now use, along with vicariance, to reconstruct the geographical context of diversiﬁ cation. Concomitant with the expanding amount of information available, molecular data sets often provide for estimates of lineage divergence dates, and analytical tools for doing so continue to improve. The comparability of molecular-based estimates of phylogenetic and population genetic histories across non-related

*Author for correspondence. Email: [email protected]

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taxa has stimulated deployment of new methods to test for spatial and temporal congruence across co-distributed taxa and ecosystems, and thus increased rigour in hypothesis-testing. We illustrate how a molecular genetics framework has provided robust and novel reconstructions of historical biogeographical pattern and process in three different systems, and ﬁ nish with some thoughts on the role a molecular genetic-based biogeography will play in predicting alternative futures of biodiversity.

Key words: biodiversity, congruence, dispersal, historical biogeography, phylochronology, phylogeny, phylogeography, vicariance.

I Introduction – the emergence of a and population genetics were conjoined to dynamic historical biogeography create phylogeography (Avise et al., 1987), ‘a Biogeography aims to decipher the geo- ﬁ eld of study concerned with the principles graphy of speciation, dispersal, and extinction and processes governing the geographical of lineages and clades and, in combination distributions of genealogical lineages, espe- with increasing knowledge of Earth history, cially those within and among closely related to reconstruct the assembly and disassembly species’ (Avise, 2000). A February 2008 of biotas through time. The vast scope of bio- topic search of the ISI Web of Science using geography requires integration across an ‘phylogeograph*’ revealed 4,800 studies to equally vast array of disciplines – including date with phylogeography as a topic. With ecology and evolutionary biology, systematics the advent of phylogeography, we can ex- and phylogenetic biology, population biology plore recent and ongoing distributional and and demography, organismal physiology and demographic changes within contemporary functional biology, geology, biogeochemistry, populations, including the processes of range climatology, and all of palaeontology. Indeed, contraction and expansion, hybridization and an increasingly integrative and revitalized introgression, and metapopulation structure. biogeography (Arbogast and Kenagy, 2001; Roughly coincident with the origins of Donoghue and Moore, 2003; Richards molecular systematics, the emergence of et al., 2007; Roy and Goldberg, 2007) is poised the theory of plate tectonics (Dietz, 1961; to provide a critical service to society. This Hess, 1962) provided historical biogeography integrative biogeography is uniquely pos- with a testable model of causal association itioned to make robust predictions about the between Earth history and the geographical consequences of human impacts on Earth’s history of distribution and divergence in biological diversity, including invasive species, plants and animals (Brundin, 1966), which habitat fragmentation and destruction, and motivated the development of vicariance global climate change (Whittaker et al., 2005) biogeography (Nelson, 1974; Platnick and in ways that cut across more typical species Nelson, 1978; Rosen, 1978). Vicariance bio- or area-based studies and which promise to geography is an approach and method high- reveal insights not otherwise possible. lighting the passive transport of species and To a large extent, historical biogeography biotas to disparate reaches of the Earth on owes its renewed vitality to the molecular gen- drifting continents and that identifies di- etics revolution in systematics and population vergence between lineages as a function genetics that began with the proposition of passive separation via Earth events such that neutral molecular markers evolved in a as mountain-building. A basic premise is clock-like fashion (Zuckerkandl and Pauling, that, under a vicariance model, a suite of 1965). The molecular revolution in bio- species or other taxa sharing a common geography received an enormous infusion geographical distribution (hereafter, ‘co- in the 1990s when phylogenetic systematics distributed species/taxa’) would demonstrate

Downloaded from http://ppg.sagepub.com at DUKE UNIV on February 11, 2009 Brett R. Riddle et al.: Molecular genetics in the future of integrative biogeography 175 congruent spatial patterns of isolation 2003; Ree et al., 2005; Wojcicki and and divergence. Vicariance biogeography Brooks, 2005; Ree and Smith, 2008); and, was conceived as a plausible alternative on the other hand, within the increasingly to dispersalist biogeography, the approach sophisticated realm of single-taxon or com- that prevailed prior to the 1970s (Brundin, parative phylogeography (eg, Knowles, 2004; 1966). The vicariance biogeographers sought Templeton, 2004; Lapointe and Rissler, to rid historical biogeography of the non- 2005; Hickerson et al., 2006; 2007; Kidd and testable ‘just-so stories’ of the dispersalists Ritchie, 2006; Carstens and Richards, 2007). by grounding the discipline conceptually Both directions are fuelled by increasing focus within a framework that fused Croizat’s on dating palaeoenvironmental events and by (1964) goals of searching for general patterns major advances in acquisition and analysis of of distribution with Hennig’s (1966) method molecular genetic data. that emphasized the critical importance Our goal in this paper is to explore the cur- of monophyletic groups in phylogenetic rent and expanding role of molecular genetic systematics and biogeography (Croizat information and molecular approaches to et al., 1974). Thus, the state of biogeography biogeography. We begin with a brief review prior to molecular genetics involved a ten- of its historical underpinnings, follow with sion between dispersal and vicariance as an overview of advances in key theoretical hypotheses behind the distribution of di- and analytical issues, and then present a versity, often with the dating of geological series of ‘case studies’ from both marine and events feeding, rather than solving, the terrestrial biospheres. We aim to illustrate debates (for an early example, see Darlington, how a molecular-based biogeography is 1965; Brundin, 1966). providing a framework for resolving long- Yet, as we have entered the twenty- standing and unresolved questions in bio- first century, a rapidly expanding set of geography by integrating across time and molecular phylogenies is providing historical space, by motivating novel questions and biogeographers with compelling reasons to approaches, and, perhaps most importantly, believe that dispersal has played a role at by giving insight into probable future changes least equivalent to vicariance in the history in biodiversity on our planet. of life on Earth – even across those iconic taxa and biotas inhabiting Gondwanan land- II The molecular revolution in masses that have for several decades been biogeography considered exemplars of a vicariance-driven system (Sanmartín and Ronquist, 2004; de 1 From albumin to phylogenomics Queiroz, 2005; McGlone, 2005; Yoder and The molecular revolution in biogeography Nowak, 2006; Barker et al., 2007). Thus, began rather humbly with the advent of we have entered yet another stage in the an immunological approach to estimating evolution of historical biogeography, fuelled the underlying genetic variation coding for by a new generation of goals and methods amino acid differences in a single protein, motivating progress in the discipline, but with albumin (Sibley, 1970). Early studies using much of the same rancor (eg, Brooks et al., this method addressed island biogeography 2004; Siddall, 2005). Unlike the upheaval of in Galapagos iguanas (Higgins, 1977), inva- the 1970s, however, these conceptual and sion versus speciation models in western analytical developments are emerging in Australian heleioporid frogs (Maxson and parallel along two tracks: on the one hand, Roberts, 1984), Tertiary versus Quaternary within a more traditional area and taxon- speciation models in several Australian based historical biogeography (eg, Ronquist, anuran species (Roberts and Maxson, 1985),

Downloaded from http://ppg.sagepub.com at DUKE UNIV on February 11, 2009 176 Progress in Physical Geography 32(2) and biogeographical histories in a wide range efficiently, further revolutionizing mole- of vertebrates (Gill, 1976; Everaarts et al., cular biogeography. With the availability 1983; Schill and Dorazio, 1990). of ‘universal’ oligonucleotide primers that Protein electrophoresis (ie, allozymes) were useful across a broad range of animal improved on albumin immunology by pro- (Kocher et al. 1989) and plant (Taberlet viding a cost-effective approach to surveying et al., 1991; Demesure et al., 1995) taxa, the genetic variation across multiple nuclear mitochondrial cytochrome b gene in animals markers (Avise, 2004), and resulted in ad- and chloroplast introns in plants became vances in population genetic theory because among the most extensively sequenced allozyme data assay Mendelian markers molecular markers. The range of sub- (Avise, 2004). Many allozyme studies have stitution rates across mitochondrial genes employed phylogenetic and population gen- in animals and chloroplast introns in plants etic analyses to infer both intra and inter- enables their use over a broad range of time- specific evolutionary and biogeographical frames (Demesure et al., 1995; Johns and histories in animals, plants, and fungi (eg, Avise, 1998). A variety of PCR-based tech- Spieth, 1975; Patton and Yang, 1977; Sites niques now provide ways to assay variation and Greenbaum, 1983; Turner, 1983; across the nuclear genome, including micro- Hofman et al., 2007; Izawa et al., 2007; satellites, amplified fragment length poly- Pauly et al., 2007). morphisms (AFLPs), short interspersed The transformation from indirect to elements (SINEs), and single nucleotide direct assay of genetic changes along a polymorphisms (SNPs) (reviewed in Avise, DNA sequence came with the discovery of 2004). restriction enzymes (Nathans and Smith, A molecular-based biogeography is now 1975) that digest DNA at 4, 5, or 6 base-pair poised to enter a new era with the increasing ‘recognition sites’. Hundreds of enzymes numbers of whole genomes available for are now available to digest DNA, and com- analysis, although few have yet been used binations of them can be used to create DNA for this purpose. The emerging field of fragments that vary in length according to phylogenomics is a result of this explosive presence or absence of different restriction data boom, representing the study of com- sites. Multi-enzyme restriction proﬁ les can be plete genomes from many closely related generated quickly, producing large amounts species using an evolutionary perspective of data assaying whole genome base-pair (Delsuc et al., 2005). For example, Macey mutation differences between individuals, (2005) explored the origin of plethodontid populations, species, and higher taxa. Fol- salamanders in North America with 27 com- lowing the pioneering study of a species plete mitochondrial genomes. The potential of pocket gopher (Geomys) by Avise et al. for a phylogenomics approach to disentangle (1979), biogeographers were quick to adopt stubborn phylogenetic and biogeographical this approach for testing biogeographical relationships can be illustrated with two hypotheses (eg, Kessler and Avise, 1984; recent studies that have provided support for Bermingham and Avise, 1986; Honeycutt a Gondwanan clade of placental mammals et al., 1987; Riddle and Honeycutt, 1990; (Atlantogenata) distinct from a northern Bernatchez and Dodson, 1991; Lovette et al., clade (Boreoeutheria) – consistent with 1999; Kuchta, 2007). the tectonic split of Pangea into southern The advent of the polymerase chain (Gondwana) and northern (Laurasia) con- reaction (PCR; Mullis et al., 1986), coupled tinents about 175 million years ago (Ma). with the development of chain-terminating In order to resurrect robust support for DNA sequencing (Sanger et al., 1977), led Atlantogenata, Hallström et al. (2007) aligned to the ability to sequence DNA quickly and 2,168,859 nucleotides from about 2,840

Downloaded from http://ppg.sagepub.com at DUKE UNIV on February 11, 2009 Brett R. Riddle et al.: Molecular genetics in the future of integrative biogeography 177 genes, and Wildman et al. (2007) aligned and geographically structured evolutionary 1,443,825 nucleotides from 1,698 genes! lineages – often suggesting presence of For many, the ability to explore these data several distinct species – are embedded with the current phylogenetic reconstruction within a single phenotypically conservative methods (eg, computer algorithms and species. Furthermore, discovery of ‘cryptic’ resources) may be a limiting factor (Delsuc gene tree structure, frequently accompanied et al., 2005), and the development of by crude molecular clocks to estimate diver- innovative analytical approaches will be re- gence times, allows for postulation of plaus- quired in order to take maximum advantage ible geological and palaeoclimatic events in of these enormous data sets (eg, Edwards Neogene Earth history as causal agents of et al., 2007; Li et al., 2007). distribution and divergence patterns within species and among closely related species. 2 The phylogeographical expansion of From its inception, the strength of phylo- biogeography geography (Avise, 2000) has been its cap- While classic biogeography rooted in plate acity to provide a connection between con- tectonics has been reconstructing the over- ceptually and analytically separate views of arching assembly and disassembly of con- history – lying at the junction between the tinental biotas, phylogeography has been population genetics of microevolutionary building up the history of species from the processes (eg, historical population size and ground fl oor. Indeed, the focus of phylogeo- structure, migration rates, gene tree coales- graphy on lineages within species and be- cence times [the point in time when two tween closely related species serves to estab- allelic lineages diverged from an ancestral lish a temporal context for phylogeographical lineage]) and the phylogenetics of macro- studies, which are almost completely con- evolution (eg, the geography of speciation strained within the Neogene, and with the and assembly of biotas). This ‘micro versus majority focused on the Quaternary (Riddle macro’ duality is refl ected in the incorporation and Hafner, 2006a). Putatively neutral of population genetic, phylogenetic, or some genetic markers such as mitochondrial DNA combination of both approaches, which (mtDNA) in animals and chloroplast DNA results in a challenge to phylogeographers in (cpDNA) in plants have frequently been choosing from the broad spectrum of methods used to estimate the timing of events within available (see, for example, Kidd and Ritchie, lineages and provide an independent assess- 2006). However, the expansive nature of ment of the age of the event relative to geo- phylogeography positions it as a bridge be- graphical and geological history. Although tween what have become two essentially much of phylogeography has been orientated separate foci in biogeography that occupy toward the discovery of the geographical often disparate spatial and temporal regimes. distributions of single gene lineages, many On the one hand, a biogeography of the studies now are also incorporating data from Late Neogene has emerged to address ques- multiple nuclear loci in attempts to resolve tions such as locations of and expansion of the problem of ‘gene tree versus species populations, species, and biotas from re- tree’ discordance (Edwards and Beerli, 2000; fugia following climate change, often while Carstens and Knowles, 2007). invoking explicit ecological influences (eg, Whereas phylogeography is often con- palaeoclimatically induced range shifts). sidered to be strictly a study of intraspecifi c Biogeography of the latest Holocene now pattern and process, one of the important extends into the temporal realm of the insights from two decades of phylo- past few decades with the emergence of geographical research has been the high fre- landscape genetics (Manel et al., 2003; quency at which ‘cryptic’ temporally deep Storfer et al., 2007). On the other hand,

Downloaded from http://ppg.sagepub.com at DUKE UNIV on February 11, 2009 178 Progress in Physical Geography 32(2) the more time-honoured realm of historical environmental history, and thus we have biogeography frequently references pre- only limited empirical evidence of genetic Neogene geological processes such as drift- response of populations to perturbations ing continents, emerging islands, and land such as climatic change (Hoffman and Blows, bridges. Here, the questions have been more 1993; Bradshaw and Holzapfel, 2008), the focused on biogeographical phenomena such signifi cance of which is heightened with on- as the locations, originations, composition, and going global warming. A means to decipher relationships between areas of endemism, the relative roles of environmental change, the locations of and expansion of lineages and vicariance, and dispersal is to use a com- biotas away from ancestral areas, and the parative multispecies phylogeographical ap- relative importance of dispersal versus vicari- proach (ie, Schneider and Moritz, 1999; ance in shaping Earth’s biotas (Riddle and Hewitt, 2004; Kirchman and Franklin, 2007) Hafner, 2006a). Much progress is needed to harking back to the fundamental premise of merge these two arenas into a more unifi ed, vicariance biogeography. When many species molecular-based historical biogeography show similar geographical and temporal dis- (Riddle and Hafner, 2006a; 2006b). continuities in the genetic diversity of populations, an environmental event, dispersal, 3 Phylochronology: integration of ancient or emergence of a barrier can be inferred genetic data with modern genetic variation (Avise et al., 1987; Riddle, 1995; Arbogast Detailed evidence of species evolutionary and Kenagy, 2001). responses to particular environmental events An alternative, but powerful, approach is lacking and controversial (Vrba, 1993; Alroy is one that uses serial genetic data such as et al., 2000; Barnosky, 2001), yet import- historic or ancient DNA within a single species. ant for reconstructing the biogeographical By using serial sets of fossil genetic data history of lineages, communities, and within a locality it is possible to reconstruct biomes. Phylogeographical reconstructions the history of a population through time (eg, of Neogene events have done much to Hadly et al., 2004; Shepherd et al., 2005). inform biologists about the age of species The advantage of this approach is that we yet, surprisingly, have revealed how rarely glimpse the dynamics of populations as they modern species divergences are tied to pro- evolved. We can measure how population found recent global environmental events bottlenecks (Paxinos et al., 2003; Shapiro such as Pleistocene glaciation (eg, Hewitt, et al., 2004; Chan et al., 2005), population 2000). One limitation of contemporary expansions (Barnes et al., 2006), gene fl ow single-species phylogeography is that modern between populations (Hadly et al., 1998; genetic data alone do not permit an investi- Belle et al., 2006), and isolation (Hadly et al., gation of the individuals that inhabited that 1998; Leonard et al., 2000) infl uenced the sig- location through time, which would provide a natures of genetic diversity within species on dynamic between environmental events and a landscape. However, ancient genetic data the evolutionary potential of species. Very are not easy to collect (Handt et al., 1994), different historic demographic events, such and this type of approach is often limited to as dispersal or population growth, can yield non-recombining parts of the genome such identical population genetic signatures. Con- as mtDNA. Enzymes that degrade DNA sequently, we cannot always determine begin working immediately upon death of if the pattern of diversity we detect is a an organism, cutting up lengths of DNA result of intra- or interspecific population and decreasing the copy number rapidly processes (McCaughley, 1991; Templeton (Kelman and Moran, 1996; Hebsgaard et al., et al., 1995). In addition, we cannot reliably tie 2005). Only under particular conditions (low the inferred population history to the local humidity, low temperature, and low acidity)

Downloaded from http://ppg.sagepub.com at DUKE UNIV on February 11, 2009 Brett R. Riddle et al.: Molecular genetics in the future of integrative biogeography 179 will the DNA be preserved (Hofreiter et al., dates can be incorporated within its meth- 2001; Smith et al., 2003). Eventually DNA odological framework. Precise estimates will degrade even under optimal conditions, of clade ages permit ecological and evolu- so that few fossils preserve DNA older than tionary investigation on a scale not allowed 100,000 years (Lindahl, 2000; Willerslev and by relative (ie, hierarchical) age estimates. For Cooper, 2005). example, only absolute dates of divergence Recent interest in historic genetic data among lineages allow investigators to draw preserved in museum specimens, usually fi rm conclusions about the historical effects confi ned to the past century, has facilitated of climatological and geological conditions on focus on species responses to environmental patterns of speciation and dispersal among change (Villablanca, 1994; Bouzat et al., organisms. Absolute age estimates can also 1998; Austin and Melville, 2006; van Tuinen permit more subtle measures such as the et al., 2008). When ancient data describing estimation of rates of morphological and thousands of generations are acquired and molecular evolution and their fi t to the pre- analysed using powerful new modelling dictions of ecological and evolutionary theory. tools such as the serial coalescent (Rodrigo Accordingly, these measures are essential for and Felsenstein, 1999; Drummond et al., critically testing models of speciation within a 2005), remarkable insights into the history of historical biogeographical framework. When populations can emerge (van Tuinen et al., an investigator observes that the estimated 2004). For example, using Bayesian serial times of divergence for a given clade (or better coalescent modelling and 10,000 years of yet, multiple clades) correlate with known genetic data, Chan et al. (2006) reconstructed climatological or geological events, that in- the most likely timing and magnitude of an vestigator has reason to postulate causality. extreme bottleneck in tuco-tucos of South Correlation does not mean causation, how- America as coincident with a massive Andean ever. Therefore, correlations between diver- volcanic eruption and ashfall (Villarosa et al., gence age and geological conditions should 2006), providing a possible cause for this be interpreted as tentative hypotheses to be vicariant event and population bottleneck subjected to further external testing with that determined the evolution of this species. additional data or taxa. The major limitation for phylochronology is Although methods for estimating time availability of temporal data (Ramakrishnan are still in their infancy, tremendous strides et al., 2005). Well-dated localities preserving have been made within the past decade. serially stacked fossils are uncommon and Bayesian (Thorne et al., 1998; Kishino et al., their specimens are few. These rare palae- 2001; Thorne and Kishino, 2002; Yang and ontological sites that preserve the past 100 Rannala, 2006) and likelihood (Yang and to 100,000 years are therefore extremely Yoder, 2003; Yang, 2004) methods have valuable snapshots of evolutionary history for been developed and modifi ed such that they many species. can account for violations of the molecular clock and for uncertainties of the fossil record III Estimating taxon divergence times by incorporating multiple calibration points and inferring biotic responses to Earth within a single analysis. Most recently, these history methods have been refi ned to incorporate data partition heterogeneity in genetic para- 1 Estimating times of organismal divergence meters (Thorne and Kishino, 2002; Yang and Historical biogeography will be most Yoder, 2003), an innovation allowing the effective as a means both for generating and investigator to combine different gene loci in testing hypotheses if methods that allow for a single analysis while accounting for their accurate calculation of organismal divergence idiosyncratic patterns of evolutionary change.

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In brief, methods for estimating divergence 2002). However, this undertaking is an time are evolving and improving at an ac- analytical challenge because biogeographical celerated rate (Drummond et al., 2006; systems involve a large number of variables Rutschmann, 2006; Rutschmann et al., 2007; and a wide array of hypotheses and models Cutter, 2008). We predict the coming years that conform to no generality with regard to will witness an explosion of empirical studies model complexity, parameterization, and that utilize an explicit temporal framework sampling. Tackling these analytical challenges for investigating biogeographical phenomena, will require a computationally powerful and much as the refi nement and improved under- fl exible interpretive framework that can infer standing of phylogenetic methods (Hillis large-scale patterns of spatial and temporal et al., 1994) did for evolutionary and other congruence across co-distributed taxa, while biological studies. incorporating the expected idiosyncratic within-taxon variation in historical demo- 2 Testing for spatial and temporal congruence graphic parameters (eg, migration, population Testing for spatial and temporal congruence sizes, and divergence times) – unfortunately, across different co-distributed taxa is of empirically relevant demographic data central importance to biogeography (Lessios, are scarce. In special cases, using phylo- 1998; Wen, 1999; Avise, 2000; Barraclough chronological data to validate processes in- and Nee, 2001). Under the comparative phylo- ferred from only modern data may improve geographical approach, practitioners aim to simulation techniques, or at least better use population genetic and phylogenetic data circumscribe their limitations. sampled across the ranges of co-distributed species in order to extract the causal processes a Temporal congruence: Estimating lineage behind species diversifi cation, distribution, divergence times with an appropriate statis- and community assembly (Bermingham and tical model derived from coalescent theory Moritz, 1998; Avise, 2000; Arbogast and (Tajima, 1983; Knowles and Maddison, 2002) Kenagy, 2001). However, the most detailed can be accomplished using a variety of well- and rigorous tests of alternative models of established approaches (Rannala and Yang, speciation rely on estimates of population 2003; Yoder and Yang, 2004; Edwards et al., divergence times across sister-taxon pairs. 2007; Hey and Nielsen, 2007). Analysing Most recently, these models are beginning to data from multiple co-occurring species be integrated with georeferenced ecological pairs that vary with respect to demographic and morphological information to test alter- parameters and pairwise coalescent times is native spatial models of climate-driven and currently less straightforward. One approach ecologically deterministic community diversi- would be to conduct an independent analysis fi cation and distribution (Hugall et al., 2002; on every population-pair and test the hy- Graham et al., 2004; Carstens et al., 2005; pothesis of temporal congruence based on Galindo et al., 2006; Kidd and Ritchie, 2006; a resulting set of independent parameter Carstens and Richards, 2007; Kozak and estimates of divergence time. Alternatively, Wiens, 2007; Richards et al., 2007; Waltari large-scale comparative phylogeographical et al., 2007; Kozak et al., 2008). studies can employ a hierarchical model such Given the importance of divergence time as an ‘approximate Bayesian computation estimates in comparative phylogeographical algorithm’ (ABC; Hickerson et al., 2006) that studies, rigorous methods using modelling can estimate ‘hyperparameters’ – representing approaches that incorporate the coalescent amalgamations of ‘subparameters’ such as variation among and within lineages are divergence time, migration, and current, needed to prevent misleading inferences ancestral, and founding effective population about community history (Arbogast et al., sizes – that characterize processes across the

Downloaded from http://ppg.sagepub.com at DUKE UNIV on February 11, 2009 Brett R. Riddle et al.: Molecular genetics in the future of integrative biogeography 181 co-distributed taxa, such as the variance in simply those being developed as described divergence times. An advantage to the latter in the phylogeography section above, the approach is that it can explicitly incorporate novelty of this approach comes from the uncertainty and variation in the sub- increasing capabilities to build ecological parameters that independently describe the niche (also called spatial distribution or demographic history of each population pair bioclimatic) models of taxon responses to (Hickerson et al., 2006; 2007). Such hier- past (eg, glacial maximum) and predicted archical models can account for both sto- future climatic changes. Although the chastic coalescent and mutational variance, methods for this integrative approach are in as well as being ﬂ exible enough to incorporate their infancy, a growing number of studies and parameterize with uncertainty the bio- have recently emerged (above citations). logical differences among taxa. Although such One of the remaining challenges will be to a model can involve an enormous number of develop spatially explicit population genetic parameters, a hierarchical model that utilizes models (Irwin, 2002; Novembre et al., 2005; an ABC approach can test for temporal Wegmann et al., 2006) so that georefer- congruence without the prohibitive compu- enced specimen data can be fully integrated tational burden of explicitly expressing with the genetic information. and calculating the likelihood of the model (Beaumont et al., 2002; Chan et al., 2006). c Future directions: testing for congruence in Studies that have used hyperparameter ‘whole ecosystems’: Using genetic markers estimates to test for temporal congruence to resolve deep-seated questions about how include Hickerson et al. (2006), Leaché et al. climate change drives community assembly (2007), and Topp and Winker (2008). and evolution of whole biotas was one of the original objectives of phylogeography gen- b Spatial congruence: One of the remaining erally (Avise et al., 1987) and comparative analytical challenges is the interpretation of phylogeography in particular (Bermingham genetic breaks within species and whether and Moritz, 1998; Avise, 2000; Arbogast such breaks arise from geographical breaks. and Kenagy, 2001). However, this grand Although genetic breaks within species are objective has so far been unrealized because often found to span putative geographical comparative phylogeographical studies rarely barriers, computer simulations have demon- involve more than a handful of co-distributed strated that such breaks can emerge as sto- species. Although continuing development chastic byproducts of the spatial coalescent of methods based on coalescent theory process (Irwin, 2002; Kuo and Avise, 2005). (Beaumont, 2004; Anderson et al., 2005; Such patterns should be interpreted with Beerli, 2006; Carstens and Richards, 2007; caution, and causal associations between Edwards et al., 2007; Hey and Nielsen, 2007; geographical barriers and genetic breaks Hickerson et al., 2007; Knowles and should be verified by spatial concordance Carstens, 2007) and niche-modelling (above across loci within species (Kuo and Avise, citations) are reinvigorating phylogeography, 2005) and across co-distributed species (Avise nothing yet in comparative phylogeography et al., 1987). A rapidly expanding approach has reached the scale of other broad and to testing for spatial congruence across co- ambitious initiatives that grew from the distributed taxa involves the integration of 1990s PCR revolution such as assembling population genetic data with georeferenced the Tree of Life, the Barcode of Life and ecological information collected from both CIPRES (Cyberinfrastructure for Phylo- the genetically sampled individuals as well as genetic Research). However, the ﬁ eld of com- all georeferenced specimens available for parative phylogeography is about to explode the taxon. While the genetic methods are as collecting DNA sequence data across a

Downloaded from http://ppg.sagepub.com at DUKE UNIV on February 11, 2009 182 Progress in Physical Geography 32(2) wide diversity of co-distributed taxa scales only revealing previously unknown patterns up to the level of comprehensive ecosystem or demonstrating contested hypotheses in sampling. Such community-scale compara- the structure of biotas at a variety of spatial tive phylogeographical, or community and temporal scales, but is also establishing a genetics, data sets could potentially test robust basis for inferring historical processes. classic biogeographical hypotheses (eg, Frequently, the strength of inference from vicariance versus dispersal) at the com- molecular results has suggested new ques- munity level (Carlquist, 1966; Rosen, 1978; tions for biogeographers and their allies in Yoder and Nowak, 2006), as well as test con- related disciplines. troversial and fundamental hypotheses in community ecology such as Hubbell’s 1 Vicariance and dispersal in the Neutral Theory (Hubbell, 2001), Tilma’s sto- biogeographical history of Madagascar chastic competitive assembly model (Tilma, To have an interest in the historical bio- 2004), and Diamond’s niche assembly rules geography of Madagascar necessitates a (Diamond, 1975; Gotelli and McCabe, 2002). thorough understanding of the origins and Given this exciting prospect, there is a need gradual sundering of Gondwana. When the for developing and deploying coalescent- supercontinent Pangea began to divide based models that are ﬂ exible enough to be into the southern continental landmasses used across a broad array of idiosyncratic (Gondwana) and northern continental land- biogeographical contexts. These models masses (Laurasia), approximately 175 Ma, should also be capable of estimating hyper- Madagascar was tucked away, deep within parameters of interest such as multi-species Gondwana (Rakotosolofo et al., 1999; Reeves patterns in range expansion, colonization, and et al., 2002). Shortly thereafter, Madagascar divergence while also being able to incorp- began the long journey to its current state of orate uncertainty and variance in within- remote isolation in the Indian Ocean. Pre- species demographic parameters. Finally, sently, Madagascar is surrounded by a vast these models should be capable of testing oceanic barrier on all sides. It is closest to highly parameterized hypotheses without continental Africa, approximately 400 km prohibitive computational burden given data to the west, but lies 4000 km from India, sets of 50–500 co-distributed species or 5000 km from Antarctica, and 6000 km populations. Hierarchical ABC models can from Australia. It is therefore remarkable to satisfy these features and thereby potentially consider that each of these landmasses was allow researchers to address computation- at one time contiguous with Madagascar. ally challenging biogeographical questions. Initially, Gondwana was a single contiguous supercontinent comprised of what would IV Illustrating the value of molecular become Africa, South America, Antarctica, genetics in biogeography Australia, India, and Madagascar. Shortly In this section, we chose three separate after separating from Laurasia, rifting be- systems – a large oceanic island known for tween western Gondwana (Africa plus its wonderfully unique endemic animals and South America) and eastern Gondwana plants, a continental biota that has diversiﬁ ed (Madagascar plus India, Antarctica, and in a geologically dynamic theatre, and the Australia) commenced (Briggs, 2003) as oceans of the world – to provide a range of evidenced by the vast outpourings of the examples illustrating the often novel results Karoo volcanics (182±1 Ma; de Wit, 2003). and added clarity that have given molecular From that point, Madagascar and the rest of genetics a pre-eminent place within a eastern Gondwana began to drift southward modern, integrative historical biogeography. relative to Africa, sliding along the strike-slip In each case, the molecular perspective is not fault known as the Davie Ridge (Bassias,

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1992; Reeves and de Wit, 2000). There is a considerably more ancient than many of the general consensus among geologists that this extant subclades in Madagascar (eg, feliform occurred sometime between 165 and 155 Ma carnivorans). Thus, the present-day biota of (Rabinowitz et al., 1983; Agrawal et al., 1992; Madagascar must of necessity be composed Reeves and de Wit, 2000; Scotese, 2000; of groups whose presence is best explained Reeves et al., 2002; Briggs, 2003). By 140 by a mix of ancient vicariant events and trans- Ma (Seward et al., 2004), marine conditions oceanic dispersal. The challenge for bio- are clearly prevalent along the entirety of geographers is to distinguish between these Madagascar’s west coast. Thus, although two possibilities. separation from Africa began as early as 165 A recent analysis of dated phylogenies Ma, there was a subsequent period of per- across multiple lineages (plants, vertebrates, haps 20 million years wherein biotic exchange invertebrates; Yoder and Nowak, 2006) would have been likely between western and points to two generalities: (1) that there are eastern Gondwana. Madagascar reached numerous endemic clades of Malagasy taxa its current position with respect to Africa whose closest sister group relationships are by 130–118 Ma (Rabinowitz et al., 1983; to African taxa; and (2) that there appears to Harland et al., 1990; Seward et al., 2004). be an overwhelming signal of Cenozoic dis- Although shifts in latitude and relationships persal. The consideration of outgroup nodes to other landmasses remained dynamic for suggests that the majority of lineages ances- many millions of years subsequent to this tral to Malagasy endemics had their origins in positioning, it is certain that Madagascar’s Africa. For those groups in which divergence present geographical isolation relative to ages have been estimated, the vast majority Africa has been stable for at least 118 million of both crown and stem ages fall within the years, and probably considerably longer. Cenozoic. The inescapable inference, al- Moreover, the Mozambique Channel, ap- though the number of studies relative to the proximately 400 km wide and separating number of endemic taxa is paltry, appears Madagascar and Africa, is quite deep (3000 m, to be that the living biota is predominantly at the deepest point) and would not have comprised of ‘neo-endemics’ that have been notably affected by changing sea levels evolved from transoceanic dispersers. after the ﬁ nal separation of Madagascar and This strains credulity for some (eg, Africa (Krause et al., 1997). Stankiewicz et al., 2006), especially given our The dynamic sundering of Gondwana knowledge of Madagascar’s extreme and over the past 165 million years or so has been long-standing isolation. However, it is not a marked by temporal windows wherein biotic novel observation to view the living Malagasy exchange would have been facilitated by biota as ‘immigrants’ (Simpson, 1952; Krause contact with other landmasses, followed by a et al., 1997; 2003). Simpson (1952) disputed long period of progressive geographical hypotheses of landbridge connections be- isolation. The timing and sequence of frag- tween Madagascar and other landmasses, mentation and isolation may at times have pointing out that the very limited represen- been slowly progressive (eg, Madagascar’s tation of mammalian taxa in Madagascar is long slide south, relative to Africa), or relatively deﬁ nitive indication that the probability of abrupt (eg, the hypothesized severing of colonization must have been ‘exceedingly southern connections via Antarctica). The low’. Platnick (1981) even considered trans- most recent conceivable connection to other oceanic dispersal hypotheses to border on the landmasses via the Kerguelen Plateau at 80 ‘miraculous’. Yet landbridge hypotheses have Ma was approximately contemporaneous continued to be invoked (eg, McCall, 1997), with the temporal origins of major extant despite no empirical support (eg, Yoder et al., clades (eg, placental mammals), but 2003; Poux et al., 2005) because there is

Downloaded from http://ppg.sagepub.com at DUKE UNIV on February 11, 2009 184 Progress in Physical Geography 32(2) compelling evidence that there may once four endemic lineages of Malagasy mammals have been two small subaerial exposures (lemurs, carnivores, tenrecs, and nesomyine in the Mozambique Channel for a limited rodents) are now focused on reconstructing geological period during the Miocene that their in situ diversification. Intensive field could have broken the trip from Africa into survey and systematic revision have already three north to south stages of 295, 210, and revealed an enormous amount of cryptic 125 km, and in the direction of the prevailing variation: of the 56 currently recognized spe- currents (Malod et al., 1991; Bassias, 1992; cies of tenrecs and nesomyines, a quarter of Krause et al., 1997). these have been described since 1992. Con- A more useful model of dispersal may sequently, phylogeographical studies of en- be drawn from present-day phenomena. demic Malagasy lineages show great promise Krause et al. (1997) review contemporary in revealing geographical patterns important reports of floating ‘islands’ of vegetation, for conservation planning, which is now a often with standing trees and mammalian process proceeding independently using habi- inhabitants, observed in remote oceanic tat and species distribution data (Kremen locations, tens and hundreds of kilometres et al., 2008). from land (Millot, 1953; King, 1962; Carlquist, Initially, the foundation of geological 1965). Certainly, there have been numerous knowledge as the basis for phylogeographical empirical reports of transoceanic dispersal in studies of the North American aridlands ap- lizards during recent history (Censky et al., peared to be equally fi rm. Four major regional 1998; Carranza et al., 2000; Calsbeek and deserts have been recognized since their initial Smith, 2003). Add to this evidence the likeli- description by Shreve (1942): a colder Great hood that the ancestors of today’s Malagasy Basin, transitional Mojave, and two warmer mammals either were hibernators or had southern deserts, Sonoran and Chihuahuan. other physiological capacities for reduced The distribution and diversifi cation of these metabolic demands (Kappeler, 2000), and the regional deserts resulted from a complicated ‘miraculous’ becomes slightly more routine. and dynamic geological and climatological his- Credulity is even less strained by hypotheses tory during the Cenozoic (fi rst appreciated of long-distance dispersal in plants and and described by Axelrod, 1958; 1983). Their invertebrates given their less stringent life- origin followed a major period of mountain- history attributes (Monaghan et al., 2005; building during the early Eocene, including Thiel and Gutow, 2005; Barnes et al., 2006; uplift of the Rocky Mountains and Sierra Cowie and Holland, 2006). Given the data Madre Oriental and volcanic origin of the on hand, and the remarkable consistency Sierra Madre Occidental (Ortega-Gutiérrez of the signal across evolutionary lineages, and Guerrero-Garcia, 1982; Swanson and we must consider the following to be the McDowell, 1984; Ferrusquía-Villafranca most credible hypothesis for the time being: et al., 2005). Putative causal events invoked Madagascar is an island primarily composed in the subsequent diversifi cation of aridlands of ‘neo-endemics’ that are the descendants taxa include major climatic shifts, mountain- of Cenozoic waif dispersers. building, and plate movement. Global cooling of the early Oligocene and middle Miocene 2 Neogene origins of deserts and desert biotas marked an abrupt and extreme shift from in western North America mesic to drought-tolerant plant species and The case study of Malagasy biota (above) began the cooling and drying trend that has indicates how a fi rm foundation of geological led to the current glacial episodes (Prothero, studies permitted explicit testing of dispersal 1998; Woodburne, 2004; Hafner et al. 2007; versus vicariance hypotheses to account for Hafner and Riddle, 2008). Following collision the origin of that fauna. Current studies of of North America with the East Pacifi c Rise

Downloaded from http://ppg.sagepub.com at DUKE UNIV on February 11, 2009 Brett R. Riddle et al.: Molecular genetics in the future of integrative biogeography 185 in the Miocene, the relatively fl at landscape of based on panbiogeographical methods western North America was reshaped with (Arriaga et al., 1997; Morrone, 2001a; 2001b; the block-fault origin of parallel mountain 2004; 2005). In even greater contrast to the ranges that created massive rainshadows, prevailing view of the Baja California Peninsula intensifi ed plate movement that opened the as a somewhat depauperate extension of Gulf of California, and volcanic eruptions the Sonoran desert, these studies revealed along the plate boundary that created the a deep-history divergence of the peninsular Baja California Peninsula (Norris and Webb, and Sonoran-mainland biota, prompting 1976; Coney, 1983; Gastil et al., 1983; consideration of earlier vicariance, rather Lonsdale, 1989; Spencer and Normark, 1989; than more recent dispersal, as the source of Stock and Hodges, 1989). The Cape Region much of the peninsular fl ora and fauna. Sub- at the southern tip of the peninsula was ori- sequent molecular phylogeographical studies ginally part of the continental mainland that of additional taxa (eg, Sinclair et al., 2004; was transferred to the Pacifi c plate across the Lindell et al., 2005; Patton and Álvarez- East Pacifi c Rise about 10 Ma, and was later Castañeda, 2005; Crews and Hedin, 2006; joined to the California mainland as volcanic Devitt, 2006; Lindell et al., 2006; Wood et al., eruptions and uplift coalesced to form the 2008) have underscored this deep historical peninsula. Sea levels fluctuated and eco- separation, as well as indicating a far more logical zones shifted (in latitude and elevation) complicated history of vicariance and dis- in response to repeated waxing and waning persal on the peninsula itself. Consequently, of the late Pleistocene glacial-interglacial there is increasing support for recognition cycles, which became markedly longer and of the peninsular desert as the most distinct more extreme about 700,000 Ka (Webb and North American regional desert, as initially Bartlein, 1992). proposed by Hafner and Riddle (1997) and Comparative phylogeographical studies supported by panbiogeographical studies of the southern regional deserts were based of Morrone and his colleagues (see above initially on a cadre of arid-adapted rodents citations). (Riddle et al., 2000a; 2000b) and later were At this point, biotic patterns resulting from expanded to include 22 clades of mammals, comparative molecular phylogeographical birds, reptiles, amphibians, and plants (Riddle studies of Baja California species have et al., 2000c; Riddle and Hafner, 2006b). In advanced far ahead of geological evidence: contrast to previous biogeographical models instead of testing phylogeographical hypoth- that emphasized late Pleistocene events, eses based on firm geological evidence, these molecular phylogeographical studies geological hypotheses based on phylogeo- recovered relatively deep divergence be- graphical patterns await further geological tween the Sonoran and Chihuahuan regional field study (Hafner and Riddle, 2008). It deserts (putatively correlated with the uplift is unknown when terrestrial contact was of the Sierra Madre and Mexican Plateau) as severed between the peninsula and either well as more recent dispersal and vicariance the eastern mainland (across the central Gulf putatively correlated with late Pleistocene of California) or the northern mainland (at glacial cycles. Phylogeographical patterns the head of the Gulf). While it is generally generally supported the distinction of accepted that a proto-Gulf of California Sonoran and Chihuahuan regions, revealing opened as early as 12 Ma, Ledesma-Vázquez idiosyncratic species sensitivity to different (2002) maintains that a mid-peninsular land fi lter-barriers and supporting an inclusion of connection persisted until the proto-Gulf a unique desert plant community (Sinaloan and current Gulf opening were connected thornscrub) in a southern extension of the as recently as 3 Ma; whereas Murphy and Sonoran desert, in agreement with studies Aguirre-León (2002) indicate complete

Downloaded from http://ppg.sagepub.com at DUKE UNIV on February 11, 2009 186 Progress in Physical Geography 32(2) separation from the mainland much earlier in Ledesma-Vázquez, 2002). Murphy and the process. Two temporary aquatic barriers Aguirre-León (2002) cite geological evidence (marine inundations and perhaps a chain (Ochoa-Landin, 1998) that dates the seaway of freshwater to estuarine lakes) appear to at 3 Ma. Circumstantial evidence in the have limited or completely severed terrestrial form of topography, elevation, limited strati- communication between the peninsula and graphic data, and recent volcanic eruptions the mainland at its northern end (Lucchitta, suggest that limestone in the region may have 1979; Boehm 1984; Buizing, 1990; Faulds been deposited by shallow, warm seas some- et al., 2001; Spencer and Pearthree, 2001; time during the last million years (Minch and Murphy and Aguirre-León, 2002; Spencer Leslie, 1991). A series of low-elevation salt and Perthree, 2005), and remnants of each fl ats connect the two marine lagoons that barrier or fi lter-barrier are being revealed in penetrate the flat Vizcaíno lowlands, and a growing number of terrestrial taxa (Riddle intense eruptions of the Tres Virgenes vol- and Hafner, 2006b). canic complex that began 1.2 Ma may have Repeated phylogeographical patterns triggered uplift and expulsion of marine among diverse vertebrate (terrestrial and waters (Hafner and Riddle, 2008). marine), invertebrate, and plant taxa indicate Lindell et al. (2006: 1329) argued that a past fragmentation of the peninsula itself. As single ‘vicariant event affecting all species the number and diversity of co-distributed similarly’ (ie, a single temporary seaway) is the lineages has grown, with each showing a most parsimonious explanation for the large molecular divergence in the vicinity of the number of co-distributed lineages (nearly 20 central-peninsula Vizcaíno Desert, argument terrestrial and 10 marine) in the mid-peninsular has focused on whether this divergence is due region. The wide range of molecular sequence to abrupt ecological and climatic change (eg, divergence (from extensive to subtle) that has Grismer, 2002) or on a past mid-peninsular been observed among a variety of terrestrial seaway. Upton and Murphy (1997) initially and marine lineages in the area might argue hypothesized a temporary mid-peninsular instead for multiple seaways of disparate seaway at about 1 Ma as the causal vicariant age in the central peninsula, as suggested event for a lizard lineage, and subsequent independently by Lindell et al. (2005), Crews studies of rodent lineages appeared to sup- and Hedin (2006), Leaché et al. (2007; based port this recent date (Riddle et al., 2000a; on hierarchical Bayesian analysis) and Hafner 2000b; 2000c). Riginos (2005) presented and Riddle (2008). Until and unless detailed evidence from near-shore reef fishes that geological or palaeontological evidence is strongly supported the past existence of a found of multiple seaways in the central seaway, but argued that the extensive mole- peninsula, the hypothesis of abrupt ecological cular sequence divergence observed among a change in concert with Pleistocene climatic variety of terrestrial and marine lineages in the shifts cannot be rejected as the source of area support a much earlier date (eg, reptiles, vicariance of terrestrial lineages, particularly Rodriguez-Robles and De Jesus-Escobar, of taxa separated by more subtle molecular 2000; Lindell et al., 2005; spiders, Crews and divergence. Hedin, 2006; near-shore reef fi shes, Riginos, Similarly, elements of the Cape Region 2005). Geological and palaeontological evi- flora and fauna may include relicts of its dence indicate a late Miocene (7 Ma) or Miocene-age Mexican mainland connection early Pliocene submergence of the central (eg, a number of reptilian lineages listed by peninsula, associated with the opening of Murphy and Aguirre-León, 2002), may retain the initial proto-Gulf (Smith, 1984; 1991; records of temporary Pliocene-age seaways Ortlieb, 1991; Helenes and Carreño, 1999; in that region (McCloy, 1984; Riddle et al., Holt et al., 2000; Carreño and Helenes, 2002; 2000c), or may represent recent immigrants

Downloaded from http://ppg.sagepub.com at DUKE UNIV on February 11, 2009 Brett R. Riddle et al.: Molecular genetics in the future of integrative biogeography 187 via Pleistocene glacial-maximum dispersal et al., 2001; Williams and Reid, 2004; Barber corridors. A broader reconnaissance of pos- et al., 2006). Thus, the gradualist allo- sible Pliocene and Pleistocene marine deposits patric evolutionary mechanisms predom- coupled with a more exact understanding of inant in evolutionary theory for over 50 years the history of uplift, subsidence, and fault dy- (Mayr, 1942; 1954; Palumbi and Lessios, namics in this region will be required to better 2005) and explicit in the phylogeographical evaluate patterns of genetic divergence ob- hypotheses (Avise et al., 1987) have garnered served in Cape Region lineages. considerable support even in an environment Both the Malagasy and North American as fl uid as the oceans. aridlands case studies have demonstrated In each classical example of process, how- that molecular phylogeographical studies ever, there also is an undercurrent of dispersal. based on hypotheses derived from geological For instance, divergence times of geminate evidence can eventually lead heuristically to species pairs across the Isthmus of Panama hypotheses that await testing with new geo- vary depending on, among other things, logical, palaeontological, or climatological species’ proclivities to disperse across shallow evidence. For Madagascar, diversification water (Knowlton and Weigt, 1998; see also of endemic mammalian lineages almost cer- Marko, 2002). Dozens of taxa have dispersed tainly predated the late Quaternary, for which across the 5000 km wide East Pacifi c Barrier the earliest palaeoclimatic data are avail- (Leis, 1984; Scheltema, 1988; Briggs, 1995; able. For the North American deserts, phylo- Lessios and Robertson, 2006), the Indo- geographical studies have indicated specifi c West Pacifi c is traversed by numerous spe- areas on the Baja California Peninsula and the cies (Williams and Reid, 2004), and the surrounding mainland that are deserving of Floridian fauna includes taxa with little or heightened geological and palaeontological no population subdivision (eg, Avise et al., survey. 1987; Avise, 1992). Such remarkable feats of dispersal have come to epitomize marine 3 Vicariance, dispersal, and connectivity in biogeography, particularly as a counterpoint the seas to terrestrial systems, for example in the long- Classical examples of marine biogeography standing focus on relationships between include regional faunas separated vicariantly pelagic larval duration and gene flow (eg, east versus west of the Isthmus of Panama, Crisp, 1978; Doherty et al., 1995; Bohonak, across the East Pacifi c Barrier, and among 1999; Lester et al., 2007). the many basins of the Indo-West Pacific That marine taxa, like terrestrial and fresh- (eg, Briggs, 1974; 1995; Santini and Winter- water taxa, should show varying degrees bottom, 2002) among others (eg, Dartnall, of geographical isolation and of dispersal is 1974; Wilson and Allen, 1987). Concomi- not unexpected considering the complexity tantly, the classic phylogeographical studies of biological and environmental systems described reciprocally monophyletic, geo- (Rosenblatt, 1963; Dawson and Hamner, graphically discrete, mitochondrial clades 2008). Efforts to understand how physical in co-distributed maritime taxa of south- environmental and organismal traits interact eastern USA (Avise 1992), a pattern that to determine community and population also characterizes intraspecifi c variation in genetic structure have received renewed at- a number of other regional biotas, including tention in studies of connectivity (eg, Kinlan southwestern North America (Burton, 1998; and Gaines, 2003; O’Connor et al., 2007; Dawson et al., 2006), southeastern Australia Ramon et al., 2008). (eg, Waters and Roy, 2003; Waters et al., Studies of connectivity originated in the 2005), and the aforementioned exemplars early to mid-1990s, when the term was fi rst of vicariance (eg, Benzie, 1998; Lessios used in organizational and prepublication

Downloaded from http://ppg.sagepub.com at DUKE UNIV on February 11, 2009 188 Progress in Physical Geography 32(2) settings, but rarely in journals, in contexts study of marine microbial phylogeography such as fl uxes across the landscape or be- because the underexplored ‘rare biosphere’ tween ecosystems, or dispersal and gene (Sogin et al., 2006) must harbour many flow among marine populations (http:// microbes diffi cult to culture ex situ (Kaeberlein aims.gov.au/pages/research/trp/pages/ et al., 2002), and in situ methods bias the com- trp2-43.html; J.A.H. Benzie, R.K. Cowen, munity sampled (Yasumoto-Hirose et al., personal communication; see also DeFreese, 2006). Thus, only environmental genomic 1995; Doherty et al., 1995; Ray, 1996). The methods, typically DNA fingerprinting term appeared in mainstream marine science such as automated rRNA intergenic spacer at the turn of the century, when it was used analysis (ARISA) and terminal restriction to describe dispersal between geographically fragment length polymorphism (TRFLP), distinct populations in terms of larval can adequately attempt to describe natural advection, diffusion, and mortality (Cowen microbial diversity. The results are intriguing, et al., 2000). Connectivity is now the key ranging from extreme local heterogeneity, concept in coastal resources management through ‘moderate endemicity’ or regional- (Mora and Sale, 2002; Steneck, 2006) and ization within broad climatic bands or eco- an umbrella term for processes ‘pivotal to our logically relevant depth strata, to global understanding of the population dynamics, dispersal (Baldwin et al., 2005; Bell et al., genetic structure, and biogeography of many 2005; Noguez et al., 2005; Pommier et al., coastal species’ (Cowen et al., 2006: 522). 2005; van der Gast et al., 2005; Bass et al., It has attained this degree of success in part 2007; Darling et al., 2007; Medlin, 2007; by encapsulating in a single word the plural- Yutin et al., 2007; Zwirglmaier et al., 2008). istic framework in which molecular genetics, The currently rudimentary knowledge of satellite oceanography, individual dispersal, how microbial ribotype diversity is infl uenced and selection may be integrated empirically via phenotype by the environment, however, with mathematical oceanography and com- precludes an important perspective on the putational simulation (eg, Dawson et al., major thesis in microbial biogeography: that 2005; Cowen et al., 2006; Galindo et al., ‘everything is everywhere, the environment 2006; Follows et al., 2007), largely separate selects’ (eg, see Green and Bohannan, 2006). from long-standing, sometimes polar- Experimental environmental manipulations, izing, debates in biogeographical theory. inclusion of functional genotypes in mole- It represents a milieu in which studies at cular analyses, and selective in situ sampling the extremes of biogeography, from global of community composition (eg, Battin et al., microbial biogeography to island evolution, 2003; Hewson and Fuhrman, 2006; can co-exist and, moreover, be synthesized. Yasumoto-Hirose et al., 2006) are addressing We specifi cally mention these two areas of this issue and undoubtedly will in time ex- research because, in addition to representing plain why, seemingly against the odds, the the apparent extremes of biogeographical distributions of some microbes with poten- patterns, microbial biogeography and island tially massive dispersal ability appear to evolution also mirror historical debates in show island biogeographical patterns on local marine biogeography – the perceived pre- scales (Bell et al., 2005; Noguez et al., 2005; eminence of dispersal (see above) and con- van der Gast et al., 2005). sequent absence of closed marine systems High β-diversity (a measure of taxonomic (Hatcher, 1997) – and will play a large role turnover) across short spatial scales in marine in advancing our understanding of marine taxa with potential for long-distance dis- biogeography. persal has typically been explained as the The study of marine microbial bio- result of environmental heterogeneity, or geography is currently, and unavoidably, the ‘patchiness’ (eg, Smith and Witman, 1999;

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Reed et al., 2000). Although a flourish of potential for long-overdue integration of studies in the 1970s found some evidence the biogeography of marine and terrestrial in marine systems of island biogeographical systems suggested a half-century ago (Mayr, patterns (eg, Schoener, 1974a; 1974b; Dauer 1954; Dawson and Hamner, 2008), and the and Simon, 1976; Molles, 1978) the impli- more recently compared micro- and macro- cations, such as limits on migration, were not biota (eg, Horner-Devine et al., 2007). widely adopted – note the absence of island theory from texts by Nybakken (1997) and V Predicting the future of biodiversity Castro and Huber (2003), in contrast to its using genetic approaches and data representation in Ricklefs and Miller (1999), Use of molecular genetics will fi gure prom- Krebs (2001), Krohne (2001), and Whittaker inently in discourse about the effect of near- and Fernández-Palacios (2007). In part, this term environmental change on local, was due to experimental design confounded regional, continental, and global biodiversity. by scale (Schoener, 1974a; 1974b), a growing Undeniably, extinction will play an import- emphasis on dispersal (Crisp, 1978), and evi- ant role in changing the structure of the future dence that endemism was lower in marine biota of the earth. Thus, to best preserve taxa than in terrestrial taxa on the same Earth’s biota, we must anticipate and con- oceanic islands (eg, Sterrer, 1998; Randall, struct an early warning system that identifi es 1998; Wagner and Funk, 1995; Drew and species vulnerable to extinction. Further, Roderick, 2005; see also Paulay and Meyer, this warning system must be made more 2002). However, the commonplace appli- robust by knowledge of how species handle cation of molecular tools to marine taxa has environmental change in natural settings over demonstrated that many supposed wide- centuries to millennia to millions of years – spread ecological generalists are complexes knowledge that does not presently exist. of cryptic species (eg, Knowlton, 1993; 2000), While we would expect a number of species often occurring as archipelagic endemics (eg, to go extinct under the combined infl uences Paulay and Meyer, 2002; Williams and Reid, of global climate change, habitat modifi cation 2004), or in marine lake ‘islands’ (Dawson and and destruction, and invasive species, we Hamner, 2005). It is not surprising, there- need to understand further the ways in fore (when one looks) to also fi nd evidence which species have, alternatively, shifted of other aspects of island evolution in marine ranges – possibly in combination with rapid biotas (eg, McClain et al., 2006; see also morphological evolution (Hellberg et al., Knowlton, 2001; Robertson, 2001). 2001) – or shifted phenotypes in situ (Smith Connectivity is a new term, but its gestalt et al., 1995; Chiba, 1998; Hadly et al., 1998) bears the synthetic hallmarks of evolutionary under previous episodes of climate change. and biogeographical classics (eg, Mayr, 1942; Integrative biogeography can provide us with 1963; Carlquist, 1965), island biogeography a global perspective on the unique set of theory (MacArthur and Wilson, 1967), phylo- events that structure species, communities, geography (Avise, 2000), and population and biomes yielding insights relevant to con- genetics (eg, Conner and Hartl, 2004). Its servation not otherwise possible (Barnosky purview includes synthesis of colonization- et al., 2001). This new biogeography, aided extirpation dynamics; mutation, migration, by advancements in population genetics, gen- and selection; and micro- and macro- omics, and phylogeography, as well as more evolution. Its novelty, particularly in terms of sophisticated Earth history reconstructions, associated technological advances – including provides a powerful toolkit because early molecular genetics – and a readjustment warning signs such as population subdivision, of research focus, also offers renewed local extinction (extirpation), and loss of

Downloaded from http://ppg.sagepub.com at DUKE UNIV on February 11, 2009 190 Progress in Physical Geography 32(2) connectivity leave indelible genetic marks, population sizes and, hence, genetic diversity often over the variable timescales most rele- of many species (eg, Kohlmann et al., 1988; vant for future global change. Debinski and Holt, 2000; Root et al., 2003). Not only do genomes of species harbour Thus, understanding the contribution of past evidence of events past (excluding direct mea- environmental change, vicariance and dis- sures of extinction events, which remains persal on the connectivity and genetic diver- the purview of palaeontology), but genomes sity of populations and species is paramount are species’ futures as well (Lacy, 1987). All the to making predictions about the future of spe- tools available to populations, species, and cies persistence, and ultimately their evolu- communities are stored in their genetic codes. tion (Waits et al., 1998; Allendorf and Luikart, In fact, the evolutionary potential of species 2006). Genetic diversity and its distribution, and populations has been questioned in light in fact, may be a valuable harbinger of things of human-accelerated climate change (Myers to come. and Knoll, 2001; Thomas et al., 2006) and In March, 2007, a group of 25 biogeo- habitat degradation (Novacek and Cleland, graphers, ecologists, and palaeontologists 2001). The genetic diversity of any given convened a workshop to consider the future population through time is a result of the of a new Integrative Biogeography. One of addition of novelty through recombination, the themes that emerged from that exercise mutation or gene fl ow, and the relative change was the need to develop a ‘Map of Life’ pro- in gene frequency (including loss of unique ject (Kidd, personal communication) – that alleles) through selection or drift. Because will be equivalent and complementary to the mutation is a relatively slow process, its con- ongoing Tree of Life (aTOL: http://atol.sdsc. tribution to the addition of genetic novelty edu/) and Barcode of Life (CBOL: http:// and shaping genetic diversity is likely to be less barcoding.si.edu/) projects. While such an signifi cant over the temporal scales of current endeavour will require synthesis across a environmental change (100 to 1000 years), broad range of disciplines and approaches, predicted by the IPCC (2007) to increase in the rapid growth in our understanding of the the future, than are genetic drift, gene fl ow, diversifi cation and distributional histories of and selection. Thus the population processes populations, species, higher taxa, and biotas most important for shaping genetic diversity is directly related to the acceleration in ap- are genetic drift, gene fl ow, and, potentially, proaches to estimating molecular genetic selection (Hoffman and Blows, 1993). Over similarities and differences across taxa. The time, the degree of isolation of a population need for such an initiative is both timely, will determine whether genetic diversity is due to its direct connections to the aTOL primarily the product of within-population and CBOL projects, and critical, in that processes or the result of interactions be- the diversity that we wish to map is rapidly tween populations. Ongoing and future disappearing due to human agency. climatic change and habitat fragmentation is already decreasing the potential for inter- Acknowledgements actions between populations, resulting in We thank the National Science Foundation indirect effects on the genetic diversity of for their support of a March 2007 workshop species (Bradshaw and Holzapfel, 2008). (DEB-0639022) in which several of the Relevant empirical data are scarce, however, themes reviewed in this paper emerged. leaving uncertain the effects that physical perturbations may have on genetic diversity References Agrawal, P.K., Pandey, O.P. and Negi, J.G. 1992: and connectivity of populations. Human Madagascar – a continental fragment of the Paleo- activities also are likely to further infl uence Super Dharwar Craton of India. Geology 20, 543–46.

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