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Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. DNA and Genetic Markers
  5. Genetic Frontiers within Biogeography
  6. Frontiers Spanning Disciplinary Lines
  7. Acknowledgements
  8. Short biographies
  9. References

The last decade has seen tremendous increases in the variety and cost-efficiency of markers available to investigate genetic questions. Molecular markers have been used in a number of biogeographic studies; however, most of this work has been done by scholars in fields other than geography, despite the inherently spatial nature of questions many authors have addressed. This article calls for greater contribution by geographers to this body of work. We begin with a primer that reviews several of the most commonly used molecular markers available today. Next, we illustrate the use of those markers with biogeographic studies in two areas that have a long-standing tradition within geography: paleoenvironmental reconstruction and human-biota interactions. Finally, we identify areas where genetic approaches can greatly expand our biogeographic horizons, including collaborative work with geographers in other subdisciplines, as well as with scholars in other fields.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. DNA and Genetic Markers
  5. Genetic Frontiers within Biogeography
  6. Frontiers Spanning Disciplinary Lines
  7. Acknowledgements
  8. Short biographies
  9. References

Since the mid-1990s, the forensic capabilities of DNA have captured the attention of the media and the public. DNA has been entered as evidence in sensational, as well as relatively mundane criminal trials; it has also established the identity or paternity of individuals, including identification of Nazi physician Josef Mengele, whose body was found buried under an alias in Brazil (Jeffreys et al. 1992). DNA has also been used to unravel mysteries pertaining to the realm of biogeography and evolutionary biology, such as determining the time of divergence of modern elephants from woolly mammoths based on ca.12,000-year-old DNA found in Siberia (Krause 2006), or identifying the diet of an iceman recently found in the Alps, 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 address many biogeographic questions; however, the majority of this research has been done by scholars in other disciplines, with only minimal input from geographers. Nonetheless, many questions addressed by geneticists, ecologists, plant scientists, and zoologists using molecular methods are inherently spatial in nature; furthermore, they often call on an understanding of paleoenvironments and human-biota interactions – two long-standing traditions 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 research among geographers (Parker and Jorgensen 2003; Rigg 2003; Young 2003). This article furthers that call by providing background for the use of molecular analysis, and identifying areas of biogeography that are particularly ripe for the incorporation of genetic methods and perspectives. Our specific goals are to (i) review some of the key markers that are used to inform 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 diversity of fields; and (iii) identify fertile liaisons between biogeographers and scholars in other areas of geography, as well as in other disciplines, whose collaboration could be richly informed by the incorporation of genetic analyses. Our intent is not to provide a comprehensive treatment of the wide array of molecular markers available, or the breadth of questions addressable with molecular approaches; in-depth reviews of the use of molecular markers are available elsewhere (Cruzan 1998; DeYoung and Honeycutt 2005; Ouborg et al. 1999; Parker et al. 1998; Schaal et al. 1998; Shaw et al. 2005, forthcoming; Sunnucks 2000). Instead, our intent is to introduce basic concepts concerning molecular markers that are relevant to biogeography and to discuss selected questions that are made possible by the use of molecular tools. In many cases molecular approaches, expand the horizons of biogeographic research questions that are based on more traditional methodologies.

Table 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 the maternal and paternal chromosome contributions.
Allopatric speciation– when a physical barrier prevents two parts of a population from interbreeding, eventually leading to intrinsic reproductive isolation and the development of separate species.
Allozymes– enzymes that differ in their sequence of amino acid building blocks but that have the same function. Allozymes are a co-dominant marker; they can be analyzed by gel electrophoresis, with inferred genetic differences based on the differential protein migration patterns.
Amplified fragment length polymorphism (AFLP)– a modification of RFLP that uses PCR to amplify DNA fragments. AFLP analysis screens widely across the genome to detect variation in DNA fragments. AFLPs are dominant markers that are highly variable.
Chloroplast DNA (cpDNA)– the DNA contained in the chloroplast organelles of a plant's cells (Figure 2). cpDNA is haploid and is maternally inherited in most angiosperms and paternally inherited in most gymnosperms.
Co-dominant marker– when the pattern of variation exhibited by the marker permits the distinction of heterozygotes (individuals that possess different alleles for a locus) from homozygotes (with two identical alleles).
Diploid– having two copies of each chromosome, typically one inherited maternally and the other paternally.
DNA (deoxyribonucleic acid)– the molecules that contain an organism's genetic material. DNA molecules form a double helix made of two DNA strands weakly held together by bonds between nucleotide bases. It includes functional units that carry information 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 the analysis of genetic variation, this is done with PCR.
DNA sequencing– method used to determine the specific arrangement of nucleotides in a fragment of DNA.
Dominant marker– when homozygotes are indistinguishable from heterozygotes because one allele (the dominant allele) expresses over the other (recessive) allele.
Expected heterozygosity (He)– the probability, based on allele frequencies within a population, that an individual will be heterozygous at a particular gene locus. He is often summarized over a number of loci to provide a measure of genetic diversity for a population.
Gel electrophoresis– a method used to separate DNA fragments by their size (in direct DNA analysis), or proteins by their electrical charge (in allozyme analysis). An electrical current passed through a gel containing tissue or DNA extracted from individuals 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 protein synthesis.
Gene flow– the movement of genes from one population to another.
Genetic drift– random variation in the genes that happen to be passed along from generation to generation, causing a statistical shift in allele frequencies within a population. Genetic drift is most pronounced in small populations and may arise when a few individuals disperse to a new area, creating a new population (founder effect), or when a population crashes, then re-expands (bottleneck).
Genome– broadly defined as the total DNA that is contained in the cells of an organism. It can also be applied specifically to DNA of the nucleus (nDNA), or DNA in 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 array of loci, with each unique array of alleles constituting a separate genotype.
Glacial refugia– ice-free locations where many species were able to exist, when glacial advances and associated climatic change made their original ranges uninhabitable. Many species 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 are typically passed on from just one parent to the offspring; therefore both are inherited as unified haplotypes.
Heterozygote– an individual that has different alleles at a particular gene locus on corresponding (i.e. homologous) chromosomes.
Homozygote– an individual that has identical alleles at a particular gene locus on corresponding (i.e. homologous) chromosomes.
Inbreeding depression– loss of fitness that results from mating between closely related individuals, which often increases homozygosity and the expression of deleterious recessive 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 is repeated many times in a row (Figure 3). Because they have a relatively high mutation rate relative to other neutral markers, they are highly variable and provide detailed information about intraspecific genetic variation. They are a codominant marker.
Mitochondrial DNA (mtDNA)– the DNA contained in the mitochondrial organelles of an organism's cells (Figure 2). mtDNA is haploid and is typically passed on from the mother to her offspring.
Molecular clock– a tool used to estimate the timing of splits in species or genetic lineages. Some genetic markers show a remarkably consistent mutation rate over time; these are calibrated with dating techniques (e.g. isotope analysis) to define the time spanned by each mutation.
Molecular marker– heritable character with different states, or alleles, that can be used to discern genetic differences among individuals, populations, or taxa.
Natural selection– when individuals that possess certain heritable traits produce more offspring 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 at least one phosphate group. The four different nucleotides found in DNA are designated by the letters A, T, G, and C (A and T pair in complementary DNA strands, and G and C also pair) (Figure 4).
Polymerase chain reaction (PCR)– a method used to amplify, or replicate, certain regions of a DNA molecule, generating more than several billion replicates of a DNA fragment in less than a day. PCR has revolutionized genetic analysis, making the direct analysis of variation in fragments of DNA far easier than with previous methods.
Primer– a nucleic acid strand involved in the replication of DNA in PCR. The primer determines the particular DNA fragment to be replicated.
Restriction fragment length polymorphism (RFLP)– a method for determining genetic variation among samples based on the length of DNA fragments cut by enzymes that 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 to DNA insertions or deletions (certain types of mutations), or the destruction of the restriction site by nucleotide base mutation. Gel electrophoresis and radioactive probes are 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 of genetic variation.

DNA and Genetic Markers

  1. Top of page
  2. Abstract
  3. Introduction
  4. DNA and Genetic Markers
  5. Genetic Frontiers within Biogeography
  6. Frontiers Spanning Disciplinary Lines
  7. Acknowledgements
  8. Short biographies
  9. References

Genetic markers are used in biogeographic studies to characterize genetic variation that exists within populations, among populations, or among closely related species (or other taxonomic levels; e.g. Figure 1). Expressed characteristics in individuals, such as feather color, leaf shape, and tail length, are largely controlled by genetic encoding. Mutations, or changes in the sequence of nucleotides in DNA that are passed from parents to their 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 with mating, may act to filter that variation and further contribute to spatial genetic variation (i.e. variation in allele frequencies; for excellent basic instruction on evolutionary processes, see Holsinger [2006]; University of California Museum of Paleontology [2006]). Different types of genetic markers reflect genetic changes accumulating at different rates, and they differ in the temporal resolution they lend to biogeographic analysis. Markers that evolve relatively quickly are appropriate for addressing short-term processes, such as population differentiation or modern gene flow; in contrast, slowly evolving markers are more suitable for examining processes operating at longer-time scales, like speciation. Due to the role that chance, mutation rates, and other evolutionary processes can play in shaping genealogical histories, Avise (2000) offered guidelines for separating genealogical noise from significant phylogeographic patterns using several alternative approaches. These include statistical testing, as well as more qualitative comparison of phylogeographic patterns with other independently derived lines of evidence. More confidence is given to patterns showing genealogical concordance, or correlation of genetic patterns among independent genes, genomes, co-distributed species, and other biogeographic data. Genetic markers must be carefully selected so that the evolution rate, or temporal resolution, of the marker matches the timescale of the processes and patterns examined by a specific research question.

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

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nuclear versus non-nuclear genomes

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

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

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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. In plants, this is the fastest of the three genomes to evolve (Wolfe et al. 1987); therefore, it provides information about evolutionary processes occurring at a relatively short timescale, and is relevant to biogeographic questions pertaining to populations. Some sections of nuclear DNA molecules contain the genetic code for specific functions, like protein synthesis, while others have no known purpose (Queller et al. 1993) and are considered ‘junk DNA’. Both types of DNA units are valuable as genetic markers.

Mitochondrial DNA (mtDNA), which occurs outside the nucleus in the mitochondria, was among the earliest genetic markers used for biogeographic studies (Hewitt 2001). Most analyses using this genome have involved animals, thanks to several characteristics that make it particularly useful for zoogeographic studies. In animals, mtDNA is the most 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 offspring from only one parent – in this case, the mother. Because offspring receive mtDNA from only one parent, mtDNA is haploid rather than diploid. In plants, mtDNA evolves more slowly than the other two genomes (Zhang and Hewitt 2003); as a result, temporal resolution of this genome is too coarse for most biogeographic questions (Schaal et al. 1998).

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

genetic markers

In addition to differing in their mutation rates, some nuclear markers permit the distinction of homozygotes from heterozygotes (co-dominant markers), while others do not (dominant markers). Co-dominant markers allow straightforward estimation of allele frequencies, which constitute the basis 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)-based markers that rely on amplification of DNA, allozymes were the marker used most frequently to infer genetic relationships (Avise 1994). Allozyme analysis detects variation among individuals based on differences in proteins whose synthesis is encoded by nuclear DNA. Even though methods that examine DNA directly (i.e. most other markers) have become widespread in the last decade or so, allozyme analysis remains a straightforward and cost-effective way to determine levels of genetic diversity and the distribution of genetic variation within and among populations (Avise 1994; Cruzan 1998). Allozymes are co-dominant markers; their chief disadvantage is that they may underestimate genetic variability, because they reveal only mutations that are involved in synthesis of the proteins examined (DeYoung and Honeycutt 2005).

Microsatellites are tandem repeats of a single DNA unit that is 1–4 base pairs long (Figure 3). They occur within each of the three genomes, and, like allozymes, are co-dominant markers in the nuclear genome. They experience high mutation rates relative to the other markers (Levinson and Gutman 1987); errors during DNA replication show up primarily as changes in the number of repeat units, hence the length of the repeat string (Selkoe and Toonen 2006). Gel electrophoresis is used to determine differences among individuals in the length of the repeat string (see Figure 1 for an example of gel electrophoresis). The high mutation rate leads to a high diversity of alleles at individual loci, as well as high variability from individual to individual (Hewitt 2001). With improved laboratory protocols for their use, their cost-efficiency has increased; and they have become one of the most widely used genetic markers (DeYoung and Honeycutt 2005). The high level of variability characteristic of microsatellites makes them ideal for analysis of biogeographic processes operating over relatively localized spatial scales and short temporal scales, like estimating current gene flow among populations. For questions involving longer timescales, their high variability may make elucidation of genetic relationships between populations or lineages impossible (Ouborg et al. 1999).

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Figure 3. A nuclear DNA sequence of a variable tandem-repeat region, with nonvariable flanking sequences, from shoals spider lily (Hymenocallis coronaria). The bottom sequence has one additional tandem repeat compared to the top sequence, which is an example of microsatellite marker variation, or polymorphism.

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Analysis of restriction fragment length polymorphisms (RFLP) uses restriction enzymes that recognize certain base combinations along the DNA molecule, or restriction sites, to cut DNA into fragments. Gel electrophoresis 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 individuals in fragment length: (i) nucleotide changes that destroy an existing restriction site or create a new one, and (ii) insertions or deletions of nucleotides within a 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 straightforward estimation of allele frequencies.

Amplified fragment length polymorphisms (AFLP) have joined microsatellites as a highly variable marker that has become widely used, particularly in studies of plants (Koch and Keifer 2006). AFLP analysis screens widely across different regions of the genome to produce a large number of DNA fragments (Vos et al. 1995). The presence or absence of individual fragments within different individuals constitutes the basis for estimating genetic variation. AFLPs resolve small genetic differences among individuals, making them a useful marker for analyzing genetic variation within and among populations and closely related species (Parker and Jorgensen 2003). Unlike the markers discussed previously, however, ALFPs are dominant, not co-dominant, markers; hence, allele frequencies cannot be inferred without making certain assumptions about evolutionary processes (Enright et al. 2003), and they must be analyzed using statistical methods particular to dominant markers.

Although scientists have been able to sequence DNA for over 30 years, the process was painfully slow and prohibitively expensive until the early 1990s, when the development of PCR revolutionized the sequencing of DNA. In the last few years, direct sequencing of DNA fragments for biogeographic analysis has become more common, with increased cost-efficiency and improvements in automated DNA-sequencing techniques (DeYoung and Honeycutt 2005). Direct sequencing involves determining the specific arrangement of nucleotides within a fragment of DNA (Figure 4). Different portions of the genome, each with its characteristic mutation rate, can be sequenced; therefore, this approach is versatile in terms of the temporal resolution of analysis it permits (DeYoung and Honeycutt 2005).

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Figure 4. DNA replication. The original DNA double helix unwinds, exposing bases of the nucleotides. 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 two identical DNA double helices, each made of one old and one new strand.

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analysis of genetic variation and genetic relationships

Regardless of the marker used, the ultimate goal of molecular analysis is to determine the genetic profile of each sample (i.e. each individual, population, or species, depending on the level of analysis) in terms of the alleles present at each of the genetic loci examined. For the study of processes that structure genetic variation within populations, genetic profiles of individuals typically constitute the basis for analysis. The distribution of alleles at this scale in plants may reflect such processes as seed dispersal, pollen movement, or competitive interactions and resulting spatial patterns of mortality. These high-resolution data may also be used to estimate the amount of genetic divergence or similarity among populations to determine their evolutionary relationships to one another, to examine effects of historical land use on spatial patterns of genetic variation, or to trace pathways of gene flow across the landscape – a particularly useful tool in anthropogenically modified landscapes. Some broader-scale analyses rely on summarization of allele frequencies as population-level indices of genetic diversity, such as the number of alleles per locus, the percentage of loci that are variable, or expected heterozygosity (a standard measure of genetic diversity; DeYoung and Honeycutt 2005). Many analytical approaches are available to apply these types of data to biogeographic questions; each with its own theoretical underpinnings and computer programs available for conducting computations. Rather than providing a comprehensive discussion of these approaches, our intent is to illustrate several different analytical approaches with the examples we discuss below. Some excellent resources that discuss specific procedures and software used in biogeographic analyses are available for consultation (Felsenstein 2006; Louisiana State University Department of Biological Sciences 2006).

Genetic Frontiers within Biogeography

  1. Top of page
  2. Abstract
  3. Introduction
  4. DNA and Genetic Markers
  5. Genetic Frontiers within Biogeography
  6. Frontiers Spanning Disciplinary Lines
  7. Acknowledgements
  8. Short biographies
  9. References

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

phylogeography

The development of phylogeography in the late 1980s served to bridge the diverse disciplines of historical biogeography, which reconstructs paleo-environments based on biogeographic data; phylogenetic systematics, which reconstructs evolutionary lineages; and population genetics, which examines micro-evolutionary (short-term) processes within and among populations (Avise et al. 1987; Koch and Keifer 2006; Young 2003). Avise first coined the term phylogeography in 1987 to mean the ‘field of study concerned with the principles and processes governing the geographic distributions of genealogical lineages, especially those within and among closely related species’ (Avise 2000, 3). As various species spread through space and time, mutations and other evolutionary processes occur; and analysis of selected genetic markers, which record those processes, allows us 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 analytical tools available at the time only permitted a relatively coarse temporal resolution. The new generation of markers made possible by the development of PCR, however, gave scientists a higher-powered lens through which to examine evolutionary relationships. Suddenly, genetic variation within species could be readily resolved, and the field of phylogeography was born (Avise 1998; Taberlet et al. 1998). The pioneering phylogeographic studies used RFLP analysis of mtDNA to focus on animals; but after development of appropriate markers, phylogeographic studies of plants have become more numerous (but are still greatly overshadowed by analyses of 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 work together to interpret geographic distributions of lineages. Particularly in view of the tradition of paleoenvironmental analysis within geography, we see phylogeography as a fertile field for involvement by geographers; indeed, a number of biogeographers have already contributed to the phylogeographic literature (e.g. Enright et al. 2003; Markwith and Parker forthcoming; Parker and Hamrick 1996; Parker and Jorgensen 2003; Parker et al. 1997; Premoli et al. 2000). In this section, we explore two phylogeographic themes that incorporate perspectives or foci that have long been within the purview of geography.

First, a number of phylogeographic studies have relied on paleoenvironmental reconstructions to estimate the timing of divisions in evolutionary lineages. Using fairly conservative (i.e. slowly evolving) cpDNA markers, Givnish et al. (1995) examined adaptive radiation in the Cyanea-Rollandia genera, a diverse group of trees and shrubs, with a candelabra-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 often encounter unoccupied niches, and diversification follows rapidly. The sequential formation of islands in a chain (like the Hawaiian Islands) as a lithospheric plate moves over a hot spot has prompted many scholars to hypothesize a sequential pattern of colonization and diversification from oldest to youngest islands throughout such chains. Givnish et al. (1995) tested this pattern by using a molecular clock to estimate the timing of evolutionary splits in the Cyanea-Rollandia complex. They calculated the average mutation rate within each lineage subsequent to a divergence, then combined that information with the geographic distributions of the lineages and the known geologic ages of the various islands, in order to assign approximate times to key radiation events. They found that splits in the lineage and dispersal to different islands generally proceeded from the oldest islands toward younger islands, with only one case of a reverse dispersal against the prevailing time gradient (Figure 5).

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Figure 5. Adaptive radiation within Cyanea-Rollandia, two genera of unbranched or sparsely branched shrubs and trees that are endemic to the Hawaiian Islands (redrawn from Givnish et al. 1995). (A) Tree, or cladogram, showing phylogenetic relationships among species. Species are grouped together on the basis of traits (in this case cpDNA restriction site variation) that members of the group, or clade, share that were derived from a common ancestor. The primary island of occurrence of each species is indicated by the color of the vertical line; the shared 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 the dispersal 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-Rollandia indicated by the phylogenetic analysis, with the width of the arrows proportional to the number of dispersal events between islands pairs. Note the singular back-dispersal from Maui Nui to Oahu, a rare dispersal event from a younger to an older island.

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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 had examined radiations in different species complexes in the natural laboratory made famous by Charles Darwin nearly two centuries ago; collectively, however, they cast an inconsistent picture of evolutionary diversification relative to the history of island formation. The emergence of islands and recent volcanic eruptions have been a bit more complicated in the Galápagos than the relatively straightforward linear model presented by the Hawaiian Islands; Beheregaray et al. (2004) used molecular methods to 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 (the timing of the emergence of the island of Isabela) as the anchor points to calibrate their molecular clock. As expected, they found sequential colonization of the island chain from the oldest islands in the east to the youngest islands in the west. They also found that populations inhabiting newly colonized terrain were not as thoroughly differentiated genetically as the long-established populations in the east, thanks to more recent gene flow among populations. Interestingly, they also found that the largest tortoise population (∼4000 tortoises) in the island chain, which inhabits Volcano Alcedo on Isabela, had a surprisingly low genetic diversity, with over 90% of the population descendent from the same maternal lineage. In an insightful integration of evolutionary biology and historical physical geography, they attributed this to a severe bottleneck, likely dating from an unusually explosive eruption of Volcano Alcedo 100,000 years ago – in an island chain where most eruptions are nonexplosive basaltic lava flows (Beheregaray et al. 2004).

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Figure 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 the foreground).

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A second theme that is particularly relevant to geographers involves comparative phylogeography. Several regions of the world have been the focus of comparative phylogeographic studies; these have identified close correspondence among many independent lineages of plants and animals in their geographic distributions, often with strong regional patterns that seem indicative of major biogeographic barriers. Such phylogeographic patterns have been used to infer processes that have shaped these distributions (Soltis et al. 2006), such as isolating mechanisms fostering allopatric speciation, the location of Pleistocene refugia, and postglacial dispersal corridors and barriers. These components of paleo-environments have traditionally been of interest to biogeographers (e.g. Cwynar and MacDonald 1987), although more frequently in contexts other than their genetic significance. Two regions that have received comparative phylogeographic analysis are Europe (Hewitt 2000; Taberlet et al. 1998) and the southeastern United States (Avise 1992, 2000).

Taberlet et al. (1998) and Hewitt (2000) reviewed studies of a diverse group of European plant and animal species based on allozymes, cpDNA, and mtDNA, looking for phylogeographic similarities that might reflect common historical influences. Even though they found no uniform phylogeographic 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 often coincide with physical barriers that limit dispersal, allowing populations migrating from different glacial refugia (where they previously diverged genetically) 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 lineages migrating from refugia located to the north and west of the Alps, (ii) central Scandinavia, which may represent a zone of contact between lineages from the south and lineages migrating from farther east, by way of northern Scandinavia, and (iii) a complex pair of zones near the border of France and Germany and in the Pyrenees, both corresponding to a junction between lineages migrating from the Iberian Peninsula and from refugia farther east. Despite these common patterns, Taberlet et al. (1998) emphasized that many phylogeographic questions about this region remain; and to solve them, we need the combined efforts of molecular geneticists and scholars in other fields that can contribute paleoenvironmental perspectives (e.g. geographers).

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Figure 7. Hypothesized patterns of postglacial migration and colonization from Pleistocene refugia 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 from Taberlet et al. 1998). (B–D) Specific pathways of migration and colonization for the common meadow grasshopper (Chorthippus parallelus, B), European hedgehog (Erinaceus europeus/concolor, C), and the brown bear (Ursus arctos, D) that are representative of common patterns exhibited by many European species of plants and animals (Adapted with permission from MacMillan Publishers Ltd: /Science/405: 907–913, G. Hewitt, ‘The genetic legacy of the Quaternary ice ages’, copyright 2000).

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The southeastern United States is another area where a multitude of studies have reported concordant phylogeographic divisions, in this case between the Atlantic and Gulf coastal regions (Soltis et al. 2006). Avise and his colleagues (Avise 1992; Avise and Nelson 1989; Bermingham and Avise 1986) were among the first to report deep genetic divergence between these two regions within a number of freshwater aquatic and marine animal species. In the wake of their pioneering work, broadly similar phylogeographic patterns have been reported for a number of other animal and plant species occurring in southeastern freshwater and terrestrial environments based on a wide array of markers (including mtDNA RFLPs and sequencing, cpDNA RFLPs and sequencing, allozymes, AFLPs, and microsatellites; Figure 8). Such concordances have been attributed to Pliocene and Pleistocene changes in sea level that caused repeated fragmentation and isolation of populations (Ellsworth et al. 1994; Hayes and Harrison 1992) and/or the postglacial expansion of species northward from separate refugia on opposites sides of the Appalachian Mountains (Church et al. 2003; Soltis et al. 2006). In a review of many studies reporting these patterns, Soltis et al. (2006) noted that the specific location of the genetic division within lineages varies among species and questioned whether the same historical processes could have been responsible for the slightly different locations of genetic divides in the diverse array of species examined. They called for more work that pins down the timing and specific nature of environmental changes that affected key evolutionary processes.

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

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In the brief period of time since the first phylogeographic analyses, a wealth of research has greatly improved our knowledge about the evolutionary history of specific regions. Phylogeographic work has increased the resolution of our models of speciation, highlighting divergences within species lineages (e.g. the giant tortoise in the Galápagos Islands); it has also identified likely Pleistocene refugia and barriers to subsequent migration as ranges have undergone postglacial expansion. Use of molecular markers has allowed us to see the genetic consequences of isolation in refugia, recent dispersal out from refugia, hybridization, and evolution resulting from environmental change, whereas previous techniques limited our knowledge to patterns of distribution and the timing of dispersal. In some cases, phylogeographic research has even altered our thinking about the timing of speciation events, pushing back the timing of splits previously thought to date from the Pleistocene (Bermingham and Moritz 1998; Hewitt 2000; Klincka and Zink 1997). Despite these tremendous advances, there is much yet to accomplish in the realm of phylogeography. Comparative phylogeographic studies done to date fail to provide uniform coverage; certain areas have been the focus of many investigations, while others have received much less attention (Hewitt 2000). Although molecular clocks have been used to estimate the timing of divergence within lineages, nucleotide substitution (i.e. mutation) rates are often assumed to be constant among species, among markers, and throughout time. Too few studies have tested calibrations of molecular clocks with independent information on dates, such as well dated fossils, radiometric dating, or other dating techniques; more work is needed in this area (Bermingham and Moritz 1998; Soltis et al. 2006). With recent developments in the analysis of ancient DNA, we are now able to retrieve DNA from well-preserved fossil material up to 100,000 years old (Parducci and Petit 2004). These technological advances provide new tools for assessing the evolutionary history of plant and animal populations (Gugerli et al. 2005). Work in this area will benefit greatly from the integration of molecular phylogeographic information with independent evidence about landscape history – an arena where geographers can make an important contribution through their expertise in paleo-environments.

3.2 human-environment interactions

Cultural biogeography has a strong tradition within geography, initially focusing on human alterations of rural landscapes (e.g. Sauer 1972), and more recently evolving to include broader anthropogenic effects on the biosphere. These encompass air pollution and environmental contamination, biotic invasions, and habitat loss and fragmentation; cultural biogeographers also study the sustainability of land-use systems causing these environmental changes (Young 2003; Young et al. 2003). Although geographers have made some use of genetic perspectives to extend our understanding in this area (e.g. Blumler 1992, 2003; Brush et al. 1995; Zimmerer and Douches 1991), there is potential for greater involvement.

One area that is ripe for geographic contribution is biodiversity and conservation genetics. Conservation genetics is the field concerned with preserving genetic diversity when populations have been reduced in size, or their habitat has been fragmented or otherwise adversely affected by human activity (DeYoung and Honeycutt 2005). Surprisingly, this area has seen very little involvement by geographers to date. Before the development of molecular markers, conservation recommendations often ignored existing genetic variation among populations and the underlying evolutionary processes (Jelinski 1997). Molecular markers have made it possible to determine the spatial distribution of different genetic lineages within species and their historical roots, enabling resource managers to incorporate genetic processes among the criteria used to identify target populations for conservation (Avise 1998). For example, Markwith and Parker (forthcoming) used nuclear DNA (nDNA) and cpDNA markers to examine genetic variation 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 (rocky shoals), which makes populations especially vulnerable to anthropogenic disturbances, such as damming and flow manipulation. They examined recent land use changes and geologic characteristics of drainage basins and found that the range disjunction has potentially persisted from prehistoric origins, and that the populations on either side of the range gap have undergone substantial allopatric divergence. The majority of nDNA variation was found within populations, and much of the cpDNA variation was distributed among drainage basins. They proposed a three-tiered conservation plan based on spatial genetic patterns that targets conservation of the genetic varieties on either side of the range gap, the cpDNA haplotypes at the drainage-basin scale, and the most diverse populations. Avise (1992) also used molecular markers to examine lineage divergences in the southeastern United States and formulate management guidelines, particularly with respect to subspecific taxonomic recognition and advisability of reintroduction.

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

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Equally crucial to conservation genetics is determining recent patterns of gene flow within target species. The exchange of genes among populations in the modern landscape reflects a number of factors, including pollination and dispersal agents (for plants), home range size and social structure (for animals), breeding system, and the landscape matrix (Schaal et al. 1998). Maintaining gene flow among existing populations is often a concern in fragmented landscapes; gene flow helps prevent inbreeding depression and counters the loss of genetic diversity through genetic drift, helping populations maintain sufficient variation to adapt to future environmental changes (Ellstrand 1992). In some cases, however, introgression or hybridization may occur, diluting the gene pool of a population and potentially reducing its fitness (Ellstrand 1992). A classical example of deleterious gene flow is the near-extinction of the red wolf (Canis niger) due to hybridization with the much more common coyote (Canis latrans; Wayne 1996). Therefore, a critical component of conservation genetics is determining not only existing levels of gene flow, but also whether those levels are conducive to long-term conservation of species of concern.

With introduced species becoming increasingly common (Vitousek et al. 1997), gene flow and potential introgression raise additional concerns in the realm of conservation genetics that extend beyond individual species. Ellstrand and Schierenbeck (2000) reviewed invasiveness in plants and found that many species became invasive after hybridization between closely related species, or even populations of the same species that had previously been isolated from each other. Often an introduced species goes through an initial period of slow expansion, then begins dramatically accelerated spread, in some cases becoming so successful that the parental species all but disappear (Ayres et al. 1999). Success of hybrids may result from several factors: increased genetic variation, particularly in cases of polyploidy; enhanced fitness of novel combinations of genes, thanks to recombination between parental species; and fixed heterozygosity of many (or key) loci, which may confer an advantage upon individuals that have two different forms of a gene (Arnold 1997; Ellstrand and Schierenbeck 2000).

An introduced species that has become invasive in coastal environments of the British Isles is a case in point. Spartina alterniflora is a cordgrass species that is native to North America (Figure 10), where it forms monotypic stands in lower intertidal zones along the east coast. In the 1800s, S. alterniflora was accidentally introduced in southern England with the discharge 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 the chromosome number doubled, and a new, fertile species (S. anglica) formed (Ferris et al. 1997). Then, it started to spread rapidly across low salt marsh habitats. Allozyme analyses and cpDNA sequencing have been used to study the species’ hybrid origin, its spread, and reasons for its success. The temporal resolution of allozymes is well suited to reveal genetic changes that have occurred in the few generations of S. anglica's existence, and the maternal inheritance of cpDNA in cord-grasses permits identification 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. anglica alters the structure and processes characteristic of its invaded ecosystem – in this case, by trapping more tidal sediment than native species, leading to an elevation of the marsh surface (Thompson 1991). As introduced species become more problematic, in some cases dramatically altering ecosystem function, it is imperative that we understand the genetic and ecological foundations for the success of invasive species.

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

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

A related area where geographers can play a significant role is in the use of molecular markers to study anthropogenic influences on the biodiversity of both domesticated and wild species. Despite the long tradition in geography of studying domestication (e.g. Sauer 1972), geographic involvement in this area of research largely represents untapped potential (but see Blumler 1992; Brush et al. 1995; Zimmerer and Douches 1991 for exceptions). In a rare glimpse at the genetic diversity maintained by pre-Columbian farmers, Parker et al. (forthcoming) studied the effects of cultivation 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. Contrary to previous speculation that all plants were descended from a single clone likely introduced from Mexico, they found appreciable genetic diversity, similar to levels reported for modern traditional agricultural systems. They also used patterns of genetic variation to make inferences about prehistoric cultural practices. Studying modern agricultural systems, Brush et al. (1995) found that potatoes grown by Andean farmers for subsistence use were an important storehouse of genetic diversity, significantly supplementing the diversity of landraces grown for a market economy. As anthropogenic modification of the environment increasingly threatens biodiversity of both cultivated and wild species, basic biodiversity (including genetic) surveys, and studies of cultural modification of the landscape and the effects on biodiversity become increasingly urgent. Particularly with our long-standing involvement in cultural biogeography, geographers have an important contribution to make in this area.

Frontiers Spanning Disciplinary Lines

  1. Top of page
  2. Abstract
  3. Introduction
  4. DNA and Genetic Markers
  5. Genetic Frontiers within Biogeography
  6. Frontiers Spanning Disciplinary Lines
  7. Acknowledgements
  8. Short biographies
  9. References

We think some of the more exciting opportunities to expand biogeographic horizons come from interdisciplinary collaboration between biogeographers and either geographers in other subdisciplines or scholars in other fields, such as archaeology, ecology, evolutionary biology, or geology. In an era characterized by our increased appreciation of the complexity of environmental and biological systems (especially when altered by human activity), narrowly focused scientists with highly specialized training have difficulty grasping the dimensions of the systems they are examining, making cross-disciplinary collaboration increasingly necessary. Exposure to other disciplines’ 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 genetic variation, we find it surprising that there have not been more studies combining GIS and genetic analyses. Geneticists often use statistical analyses to examine gene flow over distance, without explicitly modeling the nature of the landscape. GIS could improve our models of gene flow by integrating real land-use patterns and other spatially explicit landscape characteristics into gene flow models.

Although a few geographers have examined the effect that local political and economic systems have on spatial patterns of genetic variation in crop plants, such questions could be richly informed by collaborative efforts between 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 Mexican state control of those two agricultural systems (Colunga-GarcíaMarín et 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 management systems to grow a cactus species, and each maintained a different level of genetic diversity (Figure 12). Although it is well appreciated that the nature of agricultural and political systems greatly influences crop biodiversity (including genetic diversity), there are many details of this general relationship that are yet to be examined and that would benefit from collaborative work involving human and physical geographers.

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

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

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Cooperative efforts among scholars in different disciplines would enable us to further our biogeographic understanding on many frontiers. A number of questions posed in the social sciences could benefit from the added dimension provided by genetic analyses. Parker et al. (forthcoming) suggested a relationship between prehistoric human migration and spatial patterns of genetic variation in two species of agave that were cultivated in pre-Columbian times in central Arizona; they are currently examining those relationships in more detail with an interdisciplinary team involving geographers, ethnobotanists, geneticists, ecologists, archaeologists, and plant biologists. The phylogeographic examples explored above all benefited from interdisciplinary collaboration involving evolutionary biologists, geologists, paleo-environmentalists, and others. In many cases, collaboration provided a richer understanding of paleo-environmental processes than would have been possible without such cooperation.

Recent technological advancements for working with fossil DNA open up a whole new realm of inquiry. Ancient DNA has been extracted from ice cores, soil samples, and even fossilized fecal material, and used to infer animal diets or the composition of plant communities existing several millennia ago (Gugerli et al. 2005; Parducci and Petit 2004). Fossil DNA can also be used to analyze genetic changes in populations at different points in the past directly, rather than inferring historical changes from modern genetic relationships among populations. Such an advance could fine-tune our calibration of molecular clocks, thus helping scholars pinpoint the timing of paleo-environmental and evolutionary events. Molecular methods have been used to study human phylogeography; the wealth of markers now available, each with a different temporal resolution, enables us to examine a wide array of questions about human migration from the recent to more distant past.

The opportunities for geographic participation in the genetic revolution are both numerous and diverse. Young scholars currently receiving their training in geography have the opportunity to become well grounded in both evolutionary theory and the associated laboratory methods to explore the kinds of questions discussed above. Established scholars who were not trained in these specific areas can either gain exposure to evolutionary theory and methods through sabbatical programs or summer workshops, or they can collaborate with scholars in genetics or related biological fields in a larger interdisciplinary effort. The recent advances in molecular genetics have provided many new and powerful technologies for not only geographers but scholars of many other disciplines as well; together we can expand the horizons of biogeography in exciting new directions.

Acknowledgements

  1. Top of page
  2. Abstract
  3. Introduction
  4. DNA and Genetic Markers
  5. Genetic Frontiers within Biogeography
  6. Frontiers Spanning Disciplinary Lines
  7. Acknowledgements
  8. Short biographies
  9. References

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

Short biographies

  1. Top of page
  2. Abstract
  3. Introduction
  4. DNA and Genetic Markers
  5. Genetic Frontiers within Biogeography
  6. Frontiers Spanning Disciplinary Lines
  7. Acknowledgements
  8. Short biographies
  9. References

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 research focuses on plants of arid regions of North America and Mexico, where she has studied vegetation-environment relationships, plant population dynamics, biogeomorphic relationships, and genetic structure of long-lived succulent species. She is currently examining relationships between human land use and genetic variation in several species of agave that were grown in pre-Columbian times in the Sonoran Desert, as well as a columnar cactus species currently grown by traditional farmers in the Tehuacán Valley, Mexico. Papers reporting results of her work have been published in Annals of the Association of American Geographers, Professional Geographer, American Journal of Botany, Heredity, Journal of Biogeography, Vegetatio, Conservation Genetics, and Journal of Arid Environments. She received her BS from Michigan State University and her MS and PhD from the University of 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 diversity and genetic diversity, as well as anthropogenic disturbances in these systems. Current projects examine interaction of aquatic plants with the stream environment, and the influence of water flow on seed movement, genetic structure, and diversity. Articles resulting from his research have been published in the American Journal of Botany, Conservation Genetics, Southeastern Geographer, and Molecular Ecology Notes. He received a BA from the University of Mary Washington and MS and PhD from the University of Georgia.

Note
  • *

     Correspondence address: Kathleen Parker, Department of Geography, University of Georgia, 204 Geography/Geology Building, Athens, GA, USA. E-mail: kcparker@uga.edu.

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  6. Frontiers Spanning Disciplinary Lines
  7. Acknowledgements
  8. Short biographies
  9. References
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