Expanding Biogeographic Horizons with Genetic Approaches

© 2007 The AuthorsJournal Compilation © 2007 Blackwell Publishing Ltd

Geography Compass

1/3 (2007): 246–274, 10.1111/j.1749-8198.2007.00018.x

Expanding Biogeographic Horizons with Genetic Approaches

Kathleen

Parker

* and

Scott

Markwith

University of Georgia

Abstract

The last decade has seen tremendous increases in the variety and cost-efficiencyof markers available to investigate genetic questions. Molecular markers have beenused in a number of biogeographic studies; however, most of this work has beendone by scholars in fields other than geography, despite the inherently spatialnature of questions many authors have addressed. This article calls for greatercontribution by geographers to this body of work. We begin with a primer thatreviews several of the most commonly used molecular markers available today.Next, we illustrate the use of those markers with biogeographic studies in twoareas that have a long-standing tradition within geography: paleoenvironmentalreconstruction and human-biota interactions. Finally, we identify areas wheregenetic approaches can greatly expand our biogeographic horizons, includingcollaborative work with geographers in other subdisciplines, as well as with

scholars in other fields.

Introduction

Since the mid-1990s, the forensic capabilities of DNA have captured theattention of the media and the public. DNA has been entered as evidencein sensational, as well as relatively mundane criminal trials; it has alsoestablished the identity or paternity of individuals, including identificationof Nazi physician Josef Mengele, whose body was found buried under analias in Brazil ( Jeffreys et al. 1992). DNA has also been used to unravelmysteries pertaining to the realm of biogeography and evolutionary biology,such as determining the time of divergence of modern elephants fromwoolly mammoths based on ca.12,000-year-old DNA found in Siberia(Krause 2006), or identifying the diet of an iceman recently found in theAlps, based on the 5000-year-old frozen remains of his intestinal contents(Rollo et al. 2002).

DNA sequencing (see Box 1 for a definition of basic genetic terms)and older genetic techniques have been used for several decades to addressmany biogeographic questions; however, the majority of this research hasbeen done by scholars in other disciplines, with only minimal input from

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1/3 (2007): 246–274, 10.1111/j.1749-8198.2007.00018.xJournal Compilation © 2007 Blackwell Publishing Ltd

Expanding biogeographic horizons with genetic approaches 247

Box 1.

Glossary of terms.

Adaptive radiation

– the evolution of a variety of new species from an ancestral form.Adaptive radiation typically occurs when previously unoccupied niches become available,and species diverge to fill those niches.

Allele

– alternative states of a gene found at corresponding locations (or loci) on thematernal and paternal chromosome contributions.

Allopatric speciation

– when a physical barrier prevents two parts of a populationfrom interbreeding, eventually leading to intrinsic reproductive isolation and thedevelopment of separate species.

Allozymes

– enzymes that differ in their sequence of amino acid building blocks butthat have the same function. Allozymes are a co-dominant marker; they can be analyzedby gel electrophoresis, with inferred genetic differences based on the differential proteinmigration patterns.

Amplified fragment length polymorphism (AFLP)

– a modification of RFLPthat uses PCR to amplify DNA fragments. AFLP analysis screens widely across thegenome to detect variation in DNA fragments. AFLPs are dominant markers that arehighly variable.

Chloroplast DNA (cpDNA)

– the DNA contained in the chloroplast organellesof a plant’s cells (Figure 2). cpDNA is haploid and is maternally inherited in mostangiosperms and paternally inherited in most gymnosperms.

Co-dominant marker

– when the pattern of variation exhibited by the markerpermits the distinction of heterozygotes (individuals that possess different alleles for alocus) from homozygotes (with two identical alleles).

Diploid

– having two copies of each chromosome, typically one inherited maternallyand the other paternally.

DNA (deoxyribonucleic acid)

– the molecules that contain an organism’s geneticmaterial. DNA molecules form a double helix made of two DNA strands weakly heldtogether by bonds between nucleotide bases. It includes functional units that carryinformation about protein synthesis, as well as units that serve no known function(Figure 4).

DNA amplification

– production of multiple copies of a DNA sequence. In theanalysis of genetic variation, this is done with PCR.

DNA sequencing

– method used to determine the specific arrangement of nucleotidesin a fragment of DNA.

Dominant marker

– when homozygotes are indistinguishable from heterozygotesbecause one allele (the dominant allele) expresses over the other (recessive) allele.

Expected heterozygosity (H

e

)

– the probability, based on allele frequencies within apopulation, that an individual will be heterozygous at a particular gene locus. H

e

is oftensummarized over a number of loci to provide a measure of genetic diversity for apopulation.

Gel electrophoresis

– a method used to separate DNA fragments by their size (indirect DNA analysis), or proteins by their electrical charge (in allozyme analysis). Anelectrical current passed through a gel containing tissue or DNA extracted fromindividuals causes differential migration of proteins or DNA fragments, respectively,thereby permitting analysis of the genetic variation among samples (Figure 1).

Gene

– a unit of DNA that contains instructions for an amino acid sequence in proteinsynthesis.

Gene flow

– the movement of genes from one population to another.

248 Expanding biogeographic horizons with genetic approaches

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Genetic drift

– random variation in the genes that happen to be passed along fromgeneration to generation, causing a statistical shift in allele frequencies within apopulation. Genetic drift is most pronounced in small populations and may arise whena few individuals disperse to a new area, creating a new population (

founder effect

), orwhen a population crashes, then re-expands (

bottleneck

).

Genome

– broadly defined as the total DNA that is contained in the cells of anorganism. It can also be applied specifically to DNA of the nucleus (nDNA), or DNAin the mitochondrial (mtDNA) and chloroplast (cpDNA) organelles.

Genotype

– the genetic identity of an individual based on the total genetic information,or a few specific loci. Genotypes can be summarized for a single locus or for an arrayof loci, with each unique array of alleles constituting a separate genotype.

Glacial refugia

– ice-free locations where many species were able to exist, when glacialadvances and associated climatic change made their original ranges uninhabitable. Manyspecies re-expanded their ranges from refugia when post-glacial conditions improved.

Haploid

– having only one copy of each chromosome.

Haplotype

– the genetic makeup of a single chromosome. cpDNA and mtDNA aretypically passed on from just one parent to the offspring; therefore both are inheritedas unified haplotypes.

Heterozygote

– an individual that has different alleles at a particular gene locus oncorresponding (i.e. homologous) chromosomes.

Homozygote

– an individual that has identical alleles at a particular gene locus oncorresponding (i.e. homologous) chromosomes.

Inbreeding depression

– loss of fitness that results from mating between closely relatedindividuals, which often increases homozygosity and the expression of deleteriousrecessive alleles.

Locus

– the location of an individual gene on a chromosome.

Microsatellite

– a short segment of DNA (only 1–4 base pairs in length) that isrepeated many times in a row (Figure 3). Because they have a relatively high mutationrate relative to other neutral markers, they are highly variable and provide detailedinformation about intraspecific genetic variation. They are a codominant marker.

Mitochondrial DNA (mtDNA)

– the DNA contained in the mitochondrialorganelles of an organism’s cells (Figure 2). mtDNA is haploid and is typically passed onfrom the mother to her offspring.

Molecular clock

– a tool used to estimate the timing of splits in species or geneticlineages. Some genetic markers show a remarkably consistent mutation rate over time;these are calibrated with dating techniques (e.g. isotope analysis) to define the timespanned by each mutation.

Molecular marker

– heritable character with different states, or alleles, that can beused to discern genetic differences among individuals, populations, or taxa.

Natural selection

– when individuals that possess certain heritable traits produce moreoffspring than individuals with other traits (because of greater survival or fecundity),those favorable heritable traits become more common in subsequent generations.

Nucleotide

– the building blocks of DNA. Nucleotides contain a base, a sugar, and atleast one phosphate group. The four different nucleotides found in DNA are designatedby the letters A, T, G, and C (A and T pair in complementary DNA strands, and Gand C also pair) (Figure 4).

Polymerase chain reaction (PCR)

– a method used to amplify, or replicate, certainregions of a DNA molecule, generating more than several billion replicates of a DNAfragment in less than a day. PCR has revolutionized genetic analysis, making the directanalysis of variation in fragments of DNA far easier than with previous methods.

Box 1.

Continued.

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Primer

– a nucleic acid strand involved in the replication of DNA in PCR. The primerdetermines the particular DNA fragment to be replicated.

Restriction fragment length polymorphism (RFLP)

– a method for determininggenetic variation among samples based on the length of DNA fragments cut by enzymesthat recognize specific base nucleotide combinations along the DNA, or restriction sites.The length of the segment between cuts can differ from individual to individual due toDNA insertions or deletions (certain types of mutations), or the destruction of therestriction site by nucleotide base mutation. Gel electrophoresis and radioactive probesare used to determine the length of the fragments. Not all mutations (hence variation)are recognizable by this process; therefore RFLP’s provide a conservative estimate ofgenetic variation.

Box 1.

Continued.

geographers. Nonetheless, many questions addressed by geneticists, ecologists,plant scientists, and zoologists using molecular methods are inherentlyspatial in nature; furthermore, they often call on an understanding ofpaleoenvironments and human-biota interactions – two long-standingtraditions within biogeography (Veblen 1989; Young 2003; Young et al.2003). Several authors contributing to a special issue of

Physical Geography

focusing on genetics called for increased participation in genetic researchamong geographers (Parker and Jorgensen 2003; Rigg 2003; Young2003). This article furthers that call by providing background for the useof molecular analysis, and identifying areas of biogeography that areparticularly ripe for the incorporation of genetic methods and perspectives.Our specific goals are to (i) review some of the key markers that are used toinform biogeographic analyses (including their advantages and limitations);(ii) illustrate their application to inherently biogeographic questions,with examples drawn from studies conducted by scientists in a diversityof fields; and (iii) identify fertile liaisons between biogeographers andscholars in other areas of geography, as well as in other disciplines, whosecollaboration could be richly informed by the incorporation of geneticanalyses. Our intent is not to provide a comprehensive treatment of thewide array of molecular markers available, or the breadth of questionsaddressable with molecular approaches; in-depth reviews of the use ofmolecular markers are available elsewhere (Cruzan 1998; DeYoung andHoneycutt 2005; Ouborg et al. 1999; Parker et al. 1998; Schaal et al.1998; Shaw et al. 2005, forthcoming; Sunnucks 2000). Instead, our intentis to introduce basic concepts concerning molecular markers that arerelevant to biogeography and to discuss selected questions that are madepossible by the use of molecular tools. In many cases molecularapproaches, expand the horizons of biogeographic research questions thatare based on more traditional methodologies.


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DNA and Genetic Markers

Genetic markers are used in biogeographic studies to characterize geneticvariation that exists within populations, among populations, or amongclosely related species (or other taxonomic levels; e.g. Figure 1). Expressedcharacteristics in individuals, such as feather color, leaf shape, and taillength, are largely controlled by genetic encoding. Mutations, or changesin the sequence of nucleotides in DNA that are passed from parents totheir offspring, are the ultimate source of this variation (Hedrick 2000),and result in the existence of different alleles. Other evolutionary processes,such as natural selection, genetic drift, gene flow, and recombination withmating, may act to filter that variation and further contribute to spatialgenetic variation (i.e. variation in allele frequencies; for excellent basicinstruction on evolutionary processes, see Holsinger [2006]; University ofCalifornia Museum of Paleontology [2006]). Different types of geneticmarkers reflect genetic changes accumulating at different rates, and theydiffer in the temporal resolution they lend to biogeographic analysis.Markers that evolve relatively quickly are appropriate for addressing

Fig. 1. Agarose gel electrophoresis of shoals spider lily (Hymenocallis coronaria) cpDNA variation.Individuals from three different populations showing variation among populations are repre-sented: populations A (lane 1), B (lane 2), and C (lanes 3–7). Lane 8 contains a 100-base-pairsize standard, and the ladder sizes are indicated to the right.

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short-term processes, such as population differentiation or modern geneflow; in contrast, slowly evolving markers are more suitable for examiningprocesses operating at longer-time scales, like speciation. Due to the rolethat chance, mutation rates, and other evolutionary processes can play inshaping genealogical histories, Avise (2000) offered guidelines for separatinggenealogical noise from significant phylogeographic patterns using severalalternative approaches. These include statistical testing, as well as morequalitative comparison of phylogeographic patterns with other independentlyderived lines of evidence. More confidence is given to patterns showinggenealogical concordance, or correlation of genetic patterns amongindependent genes, genomes, co-distributed species, and other biogeographicdata. Genetic markers must be carefully selected so that the evolution rate,or temporal resolution, of the marker matches the timescale of the processesand patterns examined by a specific research question.

nuclear versus non-nuclear genomes

DNA exists within the nucleus, as well as two organelles occurring outsidethe nucleus of the cell – the mitochondria and the chloroplasts (Figure 2).The three genomes differ in their mutation rates, as well as their patternsof inheritance.

Nuclear DNA is the largest of the three genomes (Parker et al. 1998).It is biparentally inherited, or passed from both parents to their offspring. Inplants, this is the fastest of the three genomes to evolve (Wolfe et al.1987); therefore, it provides information about evolutionary processesoccurring at a relatively short timescale, and is relevant to biogeographicquestions pertaining to populations. Some sections of nuclear DNAmolecules contain the genetic code for specific functions, like protein

Fig. 2. The structure of a generalized plant cell, showing the organelles that contain DNA.


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synthesis, while others have no known purpose (Queller et al. 1993) andare considered ‘junk DNA’. Both types of DNA units are valuable asgenetic markers.

Mitochondrial DNA (mtDNA), which occurs outside the nucleus inthe mitochondria, was among the earliest genetic markers used forbiogeographic studies (Hewitt 2001). Most analyses using this genomehave involved animals, thanks to several characteristics that make itparticularly useful for zoogeographic studies. In animals, mtDNA is themost rapidly evolving of the three genomes (Wilson et al. 1985); hence,the mtDNA of most animals shows appreciable variation (Avise 1992).Inheritance is uniparental, which means that mtDNA is passed to offspringfrom only one parent – in this case, the mother. Because offspring receivemtDNA from only one parent, mtDNA is haploid rather than diploid. Inplants, mtDNA evolves more slowly than the other two genomes (Zhangand Hewitt 2003); as a result, temporal resolution of this genome is toocoarse for most biogeographic questions (Schaal et al. 1998).

The chloroplast genome, which is restricted to plants, generally exhibitsless variation than mtDNA of animals; nevertheless, development ofchloroplast DNA (cpDNA) markers has greatly advanced our understandingof plant geography in the last two decades (Koch and Keifer 2006). LikemtDNA, inheritance in cpDNA is uniparental in most plant species, butthe details of this pattern are more complex. cpDNA is maternally inheritedin most angiosperms and paternally inherited in most gymnosperms,although there are exceptions (Schaal et al. 1998). This makes it a usefulmarker, when used together with nuclear markers, for disentangling geneflow due to seed dispersal versus pollen movement. Although initiallyviewed as a genome with too low a mutation rate for analysis of intraspecificvariation (Wolfe et al. 1987), recent work has detected more cpDNAvariation within species (e.g. Figure 1), refining the temporal window ofanalysis possible with cpDNA markers (Shaw et al. 2005, forthcoming).

genetic markers

In addition to differing in their mutation rates, some nuclear markerspermit the distinction of homozygotes from heterozygotes (co-dominantmarkers), while others do not (dominant markers). Co-dominant markersallow straightforward estimation of allele frequencies, which constitute thebasis for many genetic analyses used in biogeography (see next section);with dominant markers, estimation of allele frequencies is more difficult(Ouborg et al. 1999).

Before the development of polymerase chain reaction (PCR)-basedmarkers that rely on amplification of DNA, allozymes were the markerused most frequently to infer genetic relationships (Avise 1994). Allozymeanalysis detects variation among individuals based on differences inproteins whose synthesis is encoded by nuclear DNA. Even though methods

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that examine DNA directly (i.e. most other markers) have become wide-spread in the last decade or so, allozyme analysis remains a straightforwardand cost-effective way to determine levels of genetic diversity and thedistribution of genetic variation within and among populations (Avise1994; Cruzan 1998). Allozymes are co-dominant markers; their chiefdisadvantage is that they may underestimate genetic variability, becausethey reveal only mutations that are involved in synthesis of the proteinsexamined (DeYoung and Honeycutt 2005).

Microsatellites are tandem repeats of a single DNA unit that is 1–4 basepairs long (Figure 3). They occur within each of the three genomes, and,like allozymes, are co-dominant markers in the nuclear genome. Theyexperience high mutation rates relative to the other markers (Levinsonand Gutman 1987); errors during DNA replication show up primarily aschanges in the number of repeat units, hence the length of the repeatstring (Selkoe and Toonen 2006). Gel electrophoresis is used to determinedifferences among individuals in the length of the repeat string (seeFigure 1 for an example of gel electrophoresis). The high mutation rateleads to a high diversity of alleles at individual loci, as well as highvariability from individual to individual (Hewitt 2001). With improvedlaboratory protocols for their use, their cost-efficiency has increased; andthey have become one of the most widely used genetic markers (DeYoungand Honeycutt 2005). The high level of variability characteristic ofmicrosatellites makes them ideal for analysis of biogeographic processesoperating over relatively localized spatial scales and short temporal scales,like estimating current gene flow among populations. For questionsinvolving longer timescales, their high variability may make elucidation

Fig. 3. A nuclear DNA sequence of a variable tandem-repeat region, with nonvariable flankingsequences, from shoals spider lily (Hymenocallis coronaria). The bottom sequence has oneadditional tandem repeat compared to the top sequence, which is an example of microsatellitemarker variation, or polymorphism.


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of genetic relationships between populations or lineages impossible(Ouborg et al. 1999).

Analysis of restriction fragment length polymorphisms (RFLP) usesrestriction enzymes that recognize certain base combinations along theDNA molecule, or restriction sites, to cut DNA into fragments. Gelelectrophoresis is used to determine differences in DNA fragment length;this constitutes the basis for estimating genetic variation among individuals.RFLPs reveal two types of mutations that cause variation among individualsin fragment length: (i) nucleotide changes that destroy an existing restrictionsite or create a new one, and (ii) insertions or deletions of nucleotides withina fragment (Figure 3). Because other types of mutations are not detected,RFLPs provide a relatively conservative estimate of genetic variation(DeYoung and Honeycutt 2005). Like allozymes and microsatellites,they are co-dominant markers, thereby permitting the straightforwardestimation of allele frequencies.

Amplified fragment length polymorphisms (AFLP) have joinedmicrosatellites as a highly variable marker that has become widely used,particularly in studies of plants (Koch and Keifer 2006). AFLP analysisscreens widely across different regions of the genome to produce a largenumber of DNA fragments (Vos et al. 1995). The presence or absence ofindividual fragments within different individuals constitutes the basisfor estimating genetic variation. AFLPs resolve small genetic differencesamong individuals, making them a useful marker for analyzing geneticvariation within and among populations and closely related species (Parkerand Jorgensen 2003). Unlike the markers discussed previously, however,ALFPs are dominant, not co-dominant, markers; hence, allele frequenciescannot be inferred without making certain assumptions about evolutionaryprocesses (Enright et al. 2003), and they must be analyzed using statisticalmethods particular to dominant markers.

Although scientists have been able to sequence DNA for over 30 years, theprocess was painfully slow and prohibitively expensive until the early 1990s,when the development of PCR revolutionized the sequencing of DNA. Inthe last few years, direct sequencing of DNA fragments for biogeographicanalysis has become more common, with increased cost-efficiency andimprovements in automated DNA-sequencing techniques (DeYoung andHoneycutt 2005). Direct sequencing involves determining the specificarrangement of nucleotides within a fragment of DNA (Figure 4). Differentportions of the genome, each with its characteristic mutation rate, can besequenced; therefore, this approach is versatile in terms of the temporalresolution of analysis it permits (DeYoung and Honeycutt 2005).

analysis of genetic variation and genetic relationships

Regardless of the marker used, the ultimate goal of molecular analysis isto determine the genetic profile of each sample (i.e. each individual,

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population, or species, depending on the level of analysis) in terms of thealleles present at each of the genetic loci examined. For the study ofprocesses that structure genetic variation

within

populations, genetic profilesof individuals typically constitute the basis for analysis. The distribution ofalleles at this scale in plants may reflect such processes as seed dispersal,pollen movement, or competitive interactions and resulting spatialpatterns of mortality. These high-resolution data may also be used toestimate the amount of genetic divergence or similarity

among

populationsto determine their evolutionary relationships to one another, to examine

Fig. 4. DNA replication. The original DNA double helix unwinds, exposing bases of the nucle-otides. A new strand is formed from free nucleotides as a complement to each original strand,with A and T pairing, and C and G pairing. Each pair of strands then retwists, forming twoidentical DNA double helices, each made of one old and one new strand.


© 2007 The Authors Geography Compass 1/3 (2007): 246–274, 10.1111/j.1749-8198.2007.00018.xJournal Compilation © 2007 Blackwell Publishing Ltd

effects of historical land use on spatial patterns of genetic variation, or totrace pathways of gene flow across the landscape – a particularly usefultool in anthropogenically modified landscapes. Some broader-scale analysesrely on summarization of allele frequencies as population-level indices ofgenetic diversity, such as the number of alleles per locus, the percentageof loci that are variable, or expected heterozygosity (a standard measureof genetic diversity; DeYoung and Honeycutt 2005). Many analyticalapproaches are available to apply these types of data to biogeographicquestions; each with its own theoretical underpinnings and computerprograms available for conducting computations. Rather than providing acomprehensive discussion of these approaches, our intent is to illustrateseveral different analytical approaches with the examples we discuss below.Some excellent resources that discuss specific procedures and software usedin biogeographic analyses are available for consultation (Felsenstein 2006;Louisiana State University Department of Biological Sciences 2006).

Genetic Frontiers within Biogeography

We draw primarily from two broad realms of biogeography in ourillustration of markers and research questions: phylogeography andhuman-biota interactions. We selected these areas for two reasons. First,with modification, they constitute two areas of biogeographic researchwithin geography that have long-standing traditions (Veblen 1989; Younget al. 2003); use of molecular markers allows us to push our research inthese areas to new frontiers. Second, together they encompass biogeographicprocesses (evolution, dispersal, and extinction) operating at a broad rangeof temporal and spatial scales, thus exemplifying the utility of variousmarkers for questions pertaining to different scales.

phylogeography

The development of phylogeography in the late 1980s served to bridgethe diverse disciplines of historical biogeography, which reconstructspaleo-environments based on biogeographic data; phylogenetic systematics,which reconstructs evolutionary lineages; and population genetics, whichexamines micro-evolutionary (short-term) processes within and amongpopulations (Avise et al. 1987; Koch and Keifer 2006; Young 2003). Avisefirst coined the term phylogeography in 1987 to mean the ‘field of studyconcerned with the principles and processes governing the geographicdistributions of genealogical lineages, especially those within and amongclosely related species’ (Avise 2000, 3). As various species spread throughspace and time, mutations and other evolutionary processes occur; andanalysis of selected genetic markers, which record those processes, allowsus to reconstruct the migration and colonization history of those lineages(Koch and Keifer 2006). Phylogenetic analysis had previously focused on



evolutionary relationships above the species level, because the analyticaltools available at the time only permitted a relatively coarse temporalresolution. The new generation of markers made possible by the developmentof PCR, however, gave scientists a higher-powered lens through whichto examine evolutionary relationships. Suddenly, genetic variation withinspecies could be readily resolved, and the field of phylogeography wasborn (Avise 1998; Taberlet et al. 1998). The pioneering phylogeographicstudies used RFLP analysis of mtDNA to focus on animals; but afterdevelopment of appropriate markers, phylogeographic studies of plantshave become more numerous (but are still greatly overshadowed by analysesof animals; Soltis et al. 2006).

Avise (2000) emphasized the interdisciplinary nature of phylogeography,and called on molecular and population geneticists, demographers,ethologists, phylogeneticists, and historical biogeographers to worktogether to interpret geographic distributions of lineages. Particularly inview of the tradition of paleoenvironmental analysis within geography, wesee phylogeography as a fertile field for involvement by geographers;indeed, a number of biogeographers have already contributed to thephylogeographic literature (e.g. Enright et al. 2003; Markwith and Parkerforthcoming; Parker and Hamrick 1996; Parker and Jorgensen 2003;Parker et al. 1997; Premoli et al. 2000). In this section, we explore twophylogeographic themes that incorporate perspectives or foci that havelong been within the purview of geography.

First, a number of phylogeographic studies have relied on paleo-environmental reconstructions to estimate the timing of divisions inevolutionary lineages. Using fairly conservative (i.e. slowly evolving)cpDNA markers, Givnish et al. (1995) examined adaptive radiation in theCyanea-Rollandia genera, a diverse group of trees and shrubs, with acandelabra-like growth form, that is endemic to the Hawaiian Islands.Such spectacular adaptive radiations are common in oceanic island chains:isolation frequently occurs after dispersal to a new island, colonists oftenencounter unoccupied niches, and diversification follows rapidly. Thesequential formation of islands in a chain (like the Hawaiian Islands) as alithospheric plate moves over a hot spot has prompted many scholars tohypothesize a sequential pattern of colonization and diversification fromoldest to youngest islands throughout such chains. Givnish et al. (1995)tested this pattern by using a molecular clock to estimate the timing ofevolutionary splits in the Cyanea-Rollandia complex. They calculated theaverage mutation rate within each lineage subsequent to a divergence,then combined that information with the geographic distributions of thelineages and the known geologic ages of the various islands, in order toassign approximate times to key radiation events. They found that splits inthe lineage and dispersal to different islands generally proceeded from theoldest islands toward younger islands, with only one case of a reversedispersal against the prevailing time gradient (Figure 5).



Beheregaray et al. (2004) used a similar approach, based on mtDNA,to examine rapid diversification among giant tortoises (Geochelone nigra)in the Galápagos Islands (Figure 6). Many evolutionary biologists hadexamined radiations in different species complexes in the natural laboratorymade famous by Charles Darwin nearly two centuries ago; collectively,however, they cast an inconsistent picture of evolutionary diversificationrelative to the history of island formation. The emergence of islands andrecent volcanic eruptions have been a bit more complicated in theGalápagos than the relatively straightforward linear model presented bythe Hawaiian Islands; Beheregaray et al. (2004) used molecular methodsto tease apart the details of the giant tortoise’s complex diversification.They used 3.3 million years (the age of the oldest island) and 700,000

Fig. 5. Adaptive radiation within Cyanea-Rollandia, two genera of unbranched or sparselybranched shrubs and trees that are endemic to the Hawaiian Islands (redrawn from Givnishet al. 1995). (A) Tree, or cladogram, showing phylogenetic relationships among species. Speciesare grouped together on the basis of traits (in this case cpDNA restriction site variation) thatmembers of the group, or clade, share that were derived from a common ancestor. Theprimary island of occurrence of each species is indicated by the color of the vertical line; theshared derived cpDNA restriction site gains or losses are shown by the horizontal bars;and the clade membership is indicated by the different symbols. Each clade evolved by thedispersal of the ancestral species to a certain island, followed by speciation, and in some cases,subsequent dispersal to other islands. (B) Reconstructed dispersal history of Cyanea-Rollandiaindicated by the phylogenetic analysis, with the width of the arrows proportional to thenumber of dispersal events between islands pairs. Note the singular back-dispersal from MauiNui to Oahu, a rare dispersal event from a younger to an older island.



(the timing of the emergence of the island of Isabela) as the anchor pointsto calibrate their molecular clock. As expected, they found sequentialcolonization of the island chain from the oldest islands in the east to theyoungest islands in the west. They also found that populations inhabitingnewly colonized terrain were not as thoroughly differentiated geneticallyas the long-established populations in the east, thanks to more recent geneflow among populations. Interestingly, they also found that the largesttortoise population (∼4000 tortoises) in the island chain, which inhabitsVolcano Alcedo on Isabela, had a surprisingly low genetic diversity, withover 90% of the population descendent from the same maternal lineage.In an insightful integration of evolutionary biology and historical physicalgeography, they attributed this to a severe bottleneck, likely dating froman unusually explosive eruption of Volcano Alcedo 100,000 years ago – inan island chain where most eruptions are nonexplosive basaltic lava flows(Beheregaray et al. 2004).

A second theme that is particularly relevant to geographers involvescomparative phylogeography. Several regions of the world have been thefocus of comparative phylogeographic studies; these have identified closecorrespondence among many independent lineages of plants and animalsin their geographic distributions, often with strong regional patterns thatseem indicative of major biogeographic barriers. Such phylogeographicpatterns have been used to infer processes that have shaped thesedistributions (Soltis et al. 2006), such as isolating mechanisms fosteringallopatric speciation, the location of Pleistocene refugia, and postglacialdispersal corridors and barriers. These components of paleo-environmentshave traditionally been of interest to biogeographers (e.g. Cwynar andMacDonald 1987), although more frequently in contexts other than theirgenetic significance. Two regions that have received comparative phylo-geographic analysis are Europe (Hewitt 2000; Taberlet et al. 1998) and thesoutheastern United States (Avise 1992, 2000).

Fig. 6. (A) Giant tortoise (Geochelone nigra) on the island of Isabela in the Galápagos Islands.(B) Volcanic peak supporting tortoises on Isabela (with the island of Fernandina in theforeground).



Taberlet et al. (1998) and Hewitt (2000) reviewed studies of a diversegroup of European plant and animal species based on allozymes, cpDNA,and mtDNA, looking for phylogeographic similarities that might reflectcommon historical influences. Even though they found no uniform phylo-geographic pattern evident across the different species they examined,both studies reported several consistent zones of hybridization (termed‘suture zones’) that resulted from secondary contact between sister species(or subspecies) during postglacial migration (Figure 7). Such zones oftencoincide with physical barriers that limit dispersal, allowing populationsmigrating from different glacial refugia (where they previously divergedgenetically) to intermingle in a narrow zone and hybridize. Taberlet et al.(1998) and Hewitt (2000) identified three suture zones: (i) the Alps,which separated lineages expanding their ranges from refugia in Italy and

Fig. 7. Hypothesized patterns of postglacial migration and colonization from Pleistocene refu-gia in Europe. (A) General locations of migration routes (arrows) and suture zones (bars), i.e.physical barriers to migration that constitute areas of widespread hybridization (redrawn fromTaberlet et al. 1998). (B–D) Specific pathways of migration and colonization for the commonmeadow grasshopper (Chorthippus parallelus, B), European hedgehog (Erinaceus europeus/concolor, C), and the brown bear (Ursus arctos, D) that are representative of common patternsexhibited by many European species of plants and animals (Adapted with permission fromMacMillan Publishers Ltd: /Science/405: 907–913, G. Hewitt, ‘The genetic legacy of theQuaternary ice ages’, copyright 2000).



lineages migrating from refugia located to the north and west of the Alps,(ii) central Scandinavia, which may represent a zone of contact betweenlineages from the south and lineages migrating from farther east, by wayof northern Scandinavia, and (iii) a complex pair of zones near the borderof France and Germany and in the Pyrenees, both corresponding to ajunction between lineages migrating from the Iberian Peninsula and fromrefugia farther east. Despite these common patterns, Taberlet et al. (1998)emphasized that many phylogeographic questions about this regionremain; and to solve them, we need the combined efforts of moleculargeneticists and scholars in other fields that can contribute paleoenvironmentalperspectives (e.g. geographers).

The southeastern United States is another area where a multitude ofstudies have reported concordant phylogeographic divisions, in this casebetween the Atlantic and Gulf coastal regions (Soltis et al. 2006). Aviseand his colleagues (Avise 1992; Avise and Nelson 1989; Bermingham andAvise 1986) were among the first to report deep genetic divergencebetween these two regions within a number of freshwater aquatic andmarine animal species. In the wake of their pioneering work, broadlysimilar phylogeographic patterns have been reported for a number ofother animal and plant species occurring in southeastern freshwater andterrestrial environments based on a wide array of markers (includingmtDNA RFLPs and sequencing, cpDNA RFLPs and sequencing, alloz-ymes, AFLPs, and microsatellites; Figure 8). Such concordances have beenattributed to Pliocene and Pleistocene changes in sea level that causedrepeated fragmentation and isolation of populations (Ellsworth et al. 1994;Hayes and Harrison 1992) and/or the postglacial expansion of speciesnorthward from separate refugia on opposites sides of the AppalachianMountains (Church et al. 2003; Soltis et al. 2006). In a review of manystudies reporting these patterns, Soltis et al. (2006) noted that the specificlocation of the genetic division within lineages varies among species andquestioned whether the same historical processes could have been responsiblefor the slightly different locations of genetic divides in the diverse arrayof species examined. They called for more work that pins down thetiming and specific nature of environmental changes that affected keyevolutionary processes.

In the brief period of time since the first phylogeographic analyses, awealth of research has greatly improved our knowledge about the evolu-tionary history of specific regions. Phylogeographic work has increasedthe resolution of our models of speciation, highlighting divergenceswithin species lineages (e.g. the giant tortoise in the Galápagos Islands);it has also identified likely Pleistocene refugia and barriers to subsequentmigration as ranges have undergone postglacial expansion. Use of molecularmarkers has allowed us to see the genetic consequences of isolation inrefugia, recent dispersal out from refugia, hybridization, and evolutionresulting from environmental change, whereas previous techniques limited



our knowledge to patterns of distribution and the timing of dispersal. Insome cases, phylogeographic research has even altered our thinking aboutthe timing of speciation events, pushing back the timing of splits previouslythought to date from the Pleistocene (Bermingham and Moritz 1998;Hewitt 2000; Klincka and Zink 1997). Despite these tremendousadvances, there is much yet to accomplish in the realm of phylogeography.Comparative phylogeographic studies done to date fail to provide uniformcoverage; certain areas have been the focus of many investigations, whileothers have received much less attention (Hewitt 2000). Although molecularclocks have been used to estimate the timing of divergence within lineages,nucleotide substitution (i.e. mutation) rates are often assumed to be constantamong species, among markers, and throughout time. Too few studieshave tested calibrations of molecular clocks with independent informationon dates, such as well dated fossils, radiometric dating, or other datingtechniques; more work is needed in this area (Bermingham and Moritz

Fig. 8. Biogeographic discontinuities of the southeastern United States (redrawn from Soltiset al. 2006 and additional sources where indicated). (A) Hypothesized migration pathwaysfrom coastal refugia. (B) Unweighted pair group clustering based on arithmetic mean (UPGMA)dendrogram showing separation of Gulf and Atlantic populations of seaside sparrow populationsbased on mtDNA sequence divergence (redrawn from Avise and Nelson 1989). (C) UPGMAdendrogram showing separation of Gulf and Atlantic populations of Atlantic white cedar basedon allozyme analysis. (D) Drainages flowing into the Atlantic Ocean (dashed black line) andthe Gulf of Mexico (solid red line). The Tombigbee and Apalachicola Rivers act as importantbiogeographic lines separating Gulf from Atlantic populations of many freshwater aquaticspecies. (E) UPGMA dendrogram showing separation of spotted sunfish populations inhabitingstreams west of the Apalachicola River and those to the east (redrawn from Avise 1992).



1998; Soltis et al. 2006). With recent developments in the analysis ofancient DNA, we are now able to retrieve DNA from well-preservedfossil material up to 100,000 years old (Parducci and Petit 2004). Thesetechnological advances provide new tools for assessing the evolutionaryhistory of plant and animal populations (Gugerli et al. 2005). Work in thisarea will benefit greatly from the integration of molecular phylogeo-graphic information with independent evidence about landscape history– an arena where geographers can make an important contributionthrough their expertise in paleo-environments.

3.2 human-environment interactions

Cultural biogeography has a strong tradition within geography, initiallyfocusing on human alterations of rural landscapes (e.g. Sauer 1972), andmore recently evolving to include broader anthropogenic effects on thebiosphere. These encompass air pollution and environmental contamination,biotic invasions, and habitat loss and fragmentation; cultural biogeographersalso study the sustainability of land-use systems causing these environmentalchanges (Young 2003; Young et al. 2003). Although geographers havemade some use of genetic perspectives to extend our understanding inthis area (e.g. Blumler 1992, 2003; Brush et al. 1995; Zimmerer andDouches 1991), there is potential for greater involvement.

One area that is ripe for geographic contribution is biodiversity andconservation genetics. Conservation genetics is the field concerned withpreserving genetic diversity when populations have been reduced in size,or their habitat has been fragmented or otherwise adversely affected byhuman activity (DeYoung and Honeycutt 2005). Surprisingly, this area hasseen very little involvement by geographers to date. Before the developmentof molecular markers, conservation recommendations often ignored existinggenetic variation among populations and the underlying evolutionaryprocesses ( Jelinski 1997). Molecular markers have made it possible todetermine the spatial distribution of different genetic lineages within speciesand their historical roots, enabling resource managers to incorporategenetic processes among the criteria used to identify target populations forconservation (Avise 1998). For example, Markwith and Parker (forthcoming)used nuclear DNA (nDNA) and cpDNA markers to examine geneticvariation in a rare aquatic plant, shoals spider lily (Hymenocallis coronaria;Figure 9), which has a disjunct range in the southeastern United States.The species is restricted to a highly localized habitat in streams (rockyshoals), which makes populations especially vulnerable to anthropogenicdisturbances, such as damming and flow manipulation. They examinedrecent land use changes and geologic characteristics of drainage basins andfound that the range disjunction has potentially persisted from prehistoricorigins, and that the populations on either side of the range gap haveundergone substantial allopatric divergence. The majority of nDNA



variation was found within populations, and much of the cpDNA variationwas distributed among drainage basins. They proposed a three-tieredconservation plan based on spatial genetic patterns that targets conservationof the genetic varieties on either side of the range gap, the cpDNAhaplotypes at the drainage-basin scale, and the most diverse populations.Avise (1992) also used molecular markers to examine lineage divergencesin the southeastern United States and formulate management guidelines,particularly with respect to subspecific taxonomic recognition and advisabilityof reintroduction.

Equally crucial to conservation genetics is determining recent patternsof gene flow within target species. The exchange of genes amongpopulations in the modern landscape reflects a number of factors, includingpollination and dispersal agents (for plants), home range size and socialstructure (for animals), breeding system, and the landscape matrix (Schaalet al. 1998). Maintaining gene flow among existing populations is often aconcern in fragmented landscapes; gene flow helps prevent inbreedingdepression and counters the loss of genetic diversity through genetic drift,helping populations maintain sufficient variation to adapt to future envi-ronmental changes (Ellstrand 1992). In some cases, however, introgressionor hybridization may occur, diluting the gene pool of a population andpotentially reducing its fitness (Ellstrand 1992). A classical example ofdeleterious gene flow is the near-extinction of the red wolf (Canis niger)

Fig. 9. Shoals spider lily (Hymenocallis coronaria), a rare aquatic species that shows substantialgenetic divergence across its disjunct distribution in the southeastern United States.



due to hybridization with the much more common coyote (Canis latrans;Wayne 1996). Therefore, a critical component of conservation genetics isdetermining not only existing levels of gene flow, but also whether thoselevels are conducive to long-term conservation of species of concern.

With introduced species becoming increasingly common (Vitouseket al. 1997), gene flow and potential introgression raise additional con-cerns in the realm of conservation genetics that extend beyond individualspecies. Ellstrand and Schierenbeck (2000) reviewed invasiveness in plantsand found that many species became invasive after hybridization betweenclosely related species, or even populations of the same species that hadpreviously been isolated from each other. Often an introduced speciesgoes through an initial period of slow expansion, then begins dramaticallyaccelerated spread, in some cases becoming so successful that the parentalspecies all but disappear (Ayres et al. 1999). Success of hybrids may resultfrom several factors: increased genetic variation, particularly in cases ofpolyploidy; enhanced fitness of novel combinations of genes, thanks torecombination between parental species; and fixed heterozygosity of many(or key) loci, which may confer an advantage upon individuals that havetwo different forms of a gene (Arnold 1997; Ellstrand and Schierenbeck2000).

An introduced species that has become invasive in coastal environmentsof the British Isles is a case in point. Spartina alterniflora is a cordgrassspecies that is native to North America (Figure 10), where it forms monotypicstands in lower intertidal zones along the east coast. In the 1800s,

Fig. 10. A saltmarsh dominated by Spartina alterniflora, one of the parental species of theinvasive hybrid S. anglica, which formed after S. alterniflora was inadvertently introduced insouthern England with the discharge of ballast water in the early 1800s.



S. alterniflora was accidentally introduced in southern England with thedischarge of ballast water from an ocean-going vessel (Thompson 1991).There it crossed with the native S. maritima to form a sterile hybrid.Initially, the hybrid persisted clonally, only expanding slowly, until thechromosome number doubled, and a new, fertile species (S. anglica)formed (Ferris et al. 1997). Then, it started to spread rapidly across lowsalt marsh habitats. Allozyme analyses and cpDNA sequencing have beenused to study the species’ hybrid origin, its spread, and reasons for itssuccess. The temporal resolution of allozymes is well suited to revealgenetic changes that have occurred in the few generations of S. anglica’sexistence, and the maternal inheritance of cpDNA in cord-grasses permitsidentification of the maternal species in the hybridization (Ferris et al.1997). These analyses have revealed a great deal of phenotypic plasticity,as well as novel properties in the hybrid not evident in either parent(Thompson 1991). Like many other introduced invasive species, S. anglicaalters the structure and processes characteristic of its invaded ecosystem –in this case, by trapping more tidal sediment than native species, leadingto an elevation of the marsh surface (Thompson 1991). As introducedspecies become more problematic, in some cases dramatically alteringecosystem function, it is imperative that we understand the genetic andecological foundations for the success of invasive species.

Particularly with the proliferation of genetically modified organisms(GMO), use of appropriate molecular markers to measure current levelsof gene flow and introgression between crops and nearby relatives iscritical. Ellstrand (1992) stressed the importance of examining gene flowbetween crops (either conventional or GMOs) and their wild relatives inthe context of their specific landscape (e.g. Elliott et al. 2004) – a facetof conservation genetics to which geographers could make a tremendouscontribution with geographic information science (GIS) and the analysisof landscape dynamics. Blumler (2003) commented that introgressionis an inherently spatial process and called for greater participation bygeographers in its study.

A related area where geographers can play a significant role is in theuse of molecular markers to study anthropogenic influences on the bio-diversity of both domesticated and wild species. Despite the long traditionin geography of studying domestication (e.g. Sauer 1972), geographicinvolvement in this area of research largely represents untapped potential(but see Blumler 1992; Brush et al. 1995; Zimmerer and Douches 1991for exceptions). In a rare glimpse at the genetic diversity maintained bypre-Columbian farmers, Parker et al. (forthcoming) studied the effects ofcultivation on two species of agave (Agave murpheyi and A. delamateri)grown in pre-Columbian times in central Arizona, the United States –species that remain in the landscape today near prehistoric ruins. Contraryto previous speculation that all plants were descended from a single clonelikely introduced from Mexico, they found appreciable genetic diversity,



similar to levels reported for modern traditional agricultural systems. Theyalso used patterns of genetic variation to make inferences about prehistoriccultural practices. Studying modern agricultural systems, Brush et al.(1995) found that potatoes grown by Andean farmers for subsistence usewere an important storehouse of genetic diversity, significantly supple-menting the diversity of landraces grown for a market economy. Asanthropogenic modification of the environment increasingly threatensbiodiversity of both cultivated and wild species, basic biodiversity (includinggenetic) surveys, and studies of cultural modification of the landscape andthe effects on biodiversity become increasingly urgent. Particularly withour long-standing involvement in cultural biogeography, geographers havean important contribution to make in this area.

Frontiers Spanning Disciplinary Lines

We think some of the more exciting opportunities to expand biogeographichorizons come from interdisciplinary collaboration between biogeographersand either geographers in other subdisciplines or scholars in other fields,such as archaeology, ecology, evolutionary biology, or geology. In an eracharacterized by our increased appreciation of the complexity of environ-mental and biological systems (especially when altered by human activity),narrowly focused scientists with highly specialized training have difficultygrasping the dimensions of the systems they are examining, makingcross-disciplinary collaboration increasingly necessary. Exposure to otherdisciplines’ theories and methodologies helps us to think ‘outside the box’and develop creative new approaches to geographic problems.

Given the inherently spatial nature of many processes that shape geneticvariation, we find it surprising that there have not been more studiescombining GIS and genetic analyses. Geneticists often use statisticalanalyses to examine gene flow over distance, without explicitly modelingthe nature of the landscape. GIS could improve our models of gene flowby integrating real land-use patterns and other spatially explicit landscapecharacteristics into gene flow models.

Although a few geographers have examined the effect that local politicaland economic systems have on spatial patterns of genetic variation in cropplants, such questions could be richly informed by collaborative effortsbetween geneticists (or genetic biogeographers) and human geographers.Several scholars have reported a loss of genetic diversity in both henequen(Agave fourcroydes; an important fiber plant; Figure 11) and blue agave (A.tequilana var. Azul; grown for tequila distillation) with increased Mexicanstate control of those two agricultural systems (Colunga-GarcíaMarínet al. 1999; Colunga-GarcíaMarín and Zizumbo-Villarreal forthcoming;Gil Vega et al. 2001). In the Tehuacán Valley of Mexico, Casas et al. (1997,1999, 2006) found that traditional farmers used three different managementsystems to grow a cactus species, and each maintained a different level of



genetic diversity (Figure 12). Although it is well appreciated that thenature of agricultural and political systems greatly influences crop bio-diversity (including genetic diversity), there are many details of this generalrelationship that are yet to be examined and that would benefit fromcollaborative work involving human and physical geographers.

Cooperative efforts among scholars in different disciplines would enableus to further our biogeographic understanding on many frontiers. Anumber of questions posed in the social sciences could benefit from theadded dimension provided by genetic analyses. Parker et al. (forthcoming)suggested a relationship between prehistoric human migration and spatialpatterns of genetic variation in two species of agave that were cultivatedin pre-Columbian times in central Arizona; they are currently examiningthose relationships in more detail with an interdisciplinary team involvinggeographers, ethnobotanists, geneticists, ecologists, archaeologists, andplant biologists. The phylogeographic examples explored above all bene-fited from interdisciplinary collaboration involving evolutionary biologists,

Fig. 11. One of several agave species (Agave spp.) grown for food or fiber in Mexico.



geologists, paleo-environmentalists, and others. In many cases, collabora-tion provided a richer understanding of paleo-environmental processesthan would have been possible without such cooperation.

Recent technological advancements for working with fossil DNA openup a whole new realm of inquiry. Ancient DNA has been extracted fromice cores, soil samples, and even fossilized fecal material, and used to inferanimal diets or the composition of plant communities existing severalmillennia ago (Gugerli et al. 2005; Parducci and Petit 2004). Fossil DNAcan also be used to analyze genetic changes in populations at differentpoints in the past directly, rather than inferring historical changes frommodern genetic relationships among populations. Such an advance couldfine-tune our calibration of molecular clocks, thus helping scholarspinpoint the timing of paleo-environmental and evolutionary events.Molecular methods have been used to study human phylogeography; thewealth of markers now available, each with a different temporal resolution,enables us to examine a wide array of questions about human migrationfrom the recent to more distant past.

The opportunities for geographic participation in the genetic revolutionare both numerous and diverse. Young scholars currently receiving their

Fig. 12. Xoconochtli (Stenocereus stellatus), a columnar cactus that is endemic to the TehuacánValley in Mexico, where it is grown by traditional farmers under three management schemes:(A) wild populations, where fruits are collected; (B) managed populations, where desirablenaturally occurring individuals are encouraged and undesirable competitors are removed; and(C and D) cultivated populations, where desirable phenotypes are planted from seeds or stemcuttings, along with other cultivated plants.



training in geography have the opportunity to become well grounded inboth evolutionary theory and the associated laboratory methods toexplore the kinds of questions discussed above. Established scholars whowere not trained in these specific areas can either gain exposure toevolutionary theory and methods through sabbatical programs or summerworkshops, or they can collaborate with scholars in genetics or relatedbiological fields in a larger interdisciplinary effort. The recent advances inmolecular genetics have provided many new and powerful technologiesfor not only geographers but scholars of many other disciplines as well;together we can expand the horizons of biogeography in exciting newdirections.

Acknowledgements

We thank the National Science Foundation, which funded part of the workreported herein (awards BCS-0216832, BCS-0401799, DEB-0519553,DEB-0519546); Wendy Gimiski of Research Media at the University ofGeorgia for graphic assistance; and Albert J. Parker, Glen M. MacDonald,and two anonymous reviewers for comments on the manuscript.

Short biographies

Kathleen C. Parker is Professor of Geography at the University of Georgia,Athens, GA, USA, where she teaches Introductory Physical Geography,Biogeography, and Human-Environment Relationships. Her researchfocuses on plants of arid regions of North America and Mexico, whereshe has studied vegetation-environment relationships, plant populationdynamics, biogeomorphic relationships, and genetic structure of long-livedsucculent species. She is currently examining relationships betweenhuman land use and genetic variation in several species of agave that weregrown in pre-Columbian times in the Sonoran Desert, as well as a columnarcactus species currently grown by traditional farmers in the TehuacánValley, Mexico. Papers reporting results of her work have been publishedin Annals of the Association of American Geographers, Professional Geographer,American Journal of Botany, Heredity, Journal of Biogeography, Vegetatio, Con-servation Genetics, and Journal of Arid Environments. She received her BSfrom Michigan State University and her MS and PhD from the Universityof Wisconsin-Madison.

Scott H. Markwith is a PhD candidate at the University of Georgia,Athens, GA, USA, where he has taught Introduction to Landforms,Resources and the Environment, and labs for physical geography courses.His research investigates natural processes that influence species diversityand genetic diversity, as well as anthropogenic disturbances in these systems.Current projects examine interaction of aquatic plants with the streamenvironment, and the influence of water flow on seed movement, genetic



structure, and diversity. Articles resulting from his research have beenpublished in the American Journal of Botany, Conservation Genetics, South-eastern Geographer, and Molecular Ecology Notes. He received a BA from theUniversity of Mary Washington and MS and PhD from the University ofGeorgia.

Note

* Correspondence address: Kathleen Parker, Department of Geography, University of Georgia,204 Geography/Geology Building, Athens, GA, USA. E-mail: [email protected].

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Expanding Biogeographic Horizons with Genetic Approaches