Journal of Heredity Advance Access published online on January 5, 2007
Journal of Heredity, doi:10.1093/jhered/esl061
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Evolution of Duplicate Gene Expression in Polyploid and Hybrid Plants
From the UBC Botanical Garden & Centre for Plant Research and Department of Botany, University of British Columbia, 6270 University Blvd, Vancouver, BC V6T 1Z4, Canada
Address correspondence to K. L. Adams at the address above, or e-mail: keitha{at}interchange.ubc.ca.
Allopolyploidy is a prominent mode of speciation in flowering plants. On allopolyploidy, genomic changes can take place, including chromosomal rearrangement and changes in gene expression; these processes continue over evolutionary time. Recent studies of gene expression in polyploid and hybrid plants, reviewed here, have examined expression in natural polyploids and synthetic neopolyploids as well as in diploid and F1 hybrids. Considerable changes in gene expression have been observed in allopolyploids, including up- or downregulation of expression in the polyploids compared with their parents, unequal expression of duplicated genes, and silencing of one copy. Genes in a variety of functional categories show altered expression, and the patterns vary considerably by gene. Some changes seem to be stochastic, whereas others are repeatable. Gene expression changes can be organ specific. Reciprocal silencing of duplicates in different organs has been observed, suggesting subfunctionalization and long-term retention of duplicates. It has become clear that hybridization has a much greater effect than chromosome doubling on gene expression in allopolyploids. Diploid and triploid F1 hybrids can show alterations of expression levels compared with their parents. Parent-of-origin effects on gene expression have been examined, and loss of gene imprinting has been shown. Some gene expression changes in polyploids and hybrids can be correlated with phenotypic effects. Demonstrated mechanisms of gene expression changes include DNA methylation, histone modifications, and antisense RNA. Several hypotheses have been proposed for why gene expression is altered in allopolyploids and hybrids.
Polyploidy has been a recurrent process during flowering plant evolution that has made a considerable impact on plant species diversity (reviewed in Wendel and Doyle 2005). Polyploids can show novel phenotypes, ecological diversification, and new niche invasion, and polyploidy is a prominent mechanism of speciation (reviewed in Otto and Whitton 2000). There can be effects on reproductive systems, including asexuality and selfing. Polyploids have a state of fixed heterozygosity that provides a vast reservoir of new alleles for selection, mutation, and gene evolution. A large number of the duplicated genes found in genomes, especially plant genomes, are derived from polyploidy. Numerous episodes of polyploidy have occurred during the evolution of flowering plants, including ancient events as well as many recent events in various plant groups (e.g., Blanc and Wolfe 2004).
The consequences of polyploidy on gene and genome evolution and gene expression have been investigated extensively in plants in recent years. Polyploidy can result in chromosomal rearrangements and gene loss (reviewed in Song et al. 1995; Levy and Feldman 2004; Pires et al. 2004; Pontes et al. 2004; Udall and Wendel 2006), interlocus concerted evolution of ribosomal DNA repeats (e.g., Wendel et al. 1995), unequal rates of sequences evolution of duplicated genes (Small et al. 1999), and changes in DNA methylation (Salmon et al. 2005; Madlung et al. 2005; Lukens et al. 2006). There can be considerable consequences on the expression of genes duplicated by polyploidy, termed "homeologs." The consequences of evolutionarily recent allopolyploidy events on gene expression have been investigated in several plant groups, including wheat, cotton, Arabidopsis suecica, soybean, Senecio, and Tragopogon. In this minireview I summarize and discuss recent literature on the evolution of homeologous gene expression in allopolyploid plants and the effects of hybridization on gene expression to provide a gateway to the most recent literature in this very active area of research.
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Patterns of Duplicate Gene Expression in Allopolyploid Plants |
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Patterns of Duplicate Gene...
SubfunctionalizationRecent studies of allopolyploid plants indicate that changes have occurred in gene expression compared with the progenitors and that the copies of genes duplicated by polyploidy can have different expression patterns and fates. Studies have been done using allopolyploids formed on 4 different time scales: Plants that have a polyploidy event greater than about 10 million years ago in the evolutionary history of their lineage, even though the plants in question may be diploids, are useful for studying the long-term evolutionary effects on duplicate gene expression. Studies of genes that were duplicated by polyploidy roughly 25–40 million years ago during the evolutionary history of the Arabidopsis lineage have been especially fruitful in this regard (Blanc and Wolfe 2004). Allopolyploids that formed from several thousand to a few million years ago, such as cotton, wheat, A. suecica, and soybean, are useful for examination of the short-term evolutionary effects on duplicate gene expression. Allopolyploids that formed within the last 100 years, including Senecio cambrensis, Tragopogon miscellus and Tragopogon mirus, and Spartina anglica, provide the opportunity to study the short-term consequences of duplicate gene expression after polyploidy in natural populations. Lastly, studies of man-made neopolyploids, often created with parental genome combinations that are the same as or close to those thought to have given rise to natural polyploid species, provide insights into what kinds of changes in gene expression can occur immediately on allopolyploidy and within a few generations. Research on allopolyploids of each type gives complementary information about how homeologous gene expression patterns are altered and evolve in polyploids.
Two types of expression changes have been reported, using different approaches. Some studies have measured the ratio of transcripts derived from each homeolog. Silencing of one homeolog or a considerable expression bias toward one homeolog has been shown using experimental approaches that distinguish between the homeologous sequences (such as amplified fragment length polymorphisms-cDNA, single strand conformation polymorphisms, and a new homeologous microarray approach developed by Udall et al. [2006]). Such studies of the evolution of duplicate gene expression in natural allopolyploid cotton, A. suecica, and wheat have identified numerous genes that show silencing of one copy, or a strong expression bias toward one copy, in the allopolyploid (Lee and Chen 2001; Adams et al. 2003; Bottley et al. 2006; Tate et al. 2006; Udall et al. 2006). These results indicate that homeologous genes need not contribute equally to the transcript pool. Differences in expression patterns between homeologous genes seen in natural allopolyploids may have arisen during the evolutionary history of these plants. It would be interesting in the future to examine the evolution of homeologous gene expression in multiple species derived from the same polyploidy event to observe how expression variation has evolved; the 5 polyploid Gossypium species would be ideal for such a study. Alternatively, many of the differences in expression levels between homeologous gene pairs in natural polyploids may have arisen on or within a few generations after polyploidy. Indeed, unequal expression of homeologs and silencing of one copy have been observed in neopolyploids, as shown by several studies of allotetraploid Gossypium, Triticum, and Arabidopsis (Comai et al. 2000; Kashkush et al. 2002; He et al. 2003; Adams et al. 2004; Wang et al. 2004). Sometimes, parallel expression and silencing patterns are observed in natural and neopolyploids that are of similar genomic constitution (Adams et al. 2003; He et al. 2003; Wang et al. 2004), whereas expression patterns for other genes appear to be more stochastic. (For a discussion of the issue of stochastic and nonstochastic expression changes, see Adams et al. [2004], Wang et al. [2004], and Adams and Wendel [2005b]). Homeologous gene expression patterns can vary by generation in neopolyploids (Wang et al. 2004), suggesting a sorting out process of expression regulation immediately after allopolyploidy that lasts for a few generations.
Secondly, the effects of allopolyploidy on gene expression have been examined by detecting how expression levels in the allopolyploid deviate from the midpoint value of the 2 parents. These studies have been done primarily by hybridization-based approaches, such as microarrays, that assay the total expression level of both homeologs simultaneously. Studies of gene expression in flower buds of allohexaploid S. cambrensis, using cDNA microarrays, showed extensive expression variation between the allohexaploid and its progenitors (Hegarty et al. 2005, 2006). Nonadditive gene expression can be an immediate consequence of allopolyploidy, as shown by 2 recent microarray studies of neopolyploids (Hegarty et al. 2006; Wang, Tian, Lee, Wei, et al. 2006). Newly created allohexaploid Senecio lines showed considerable differences in expression relative to their parents. Interestingly, many of the same genes were affected in both the neopolyploids and natural allopolyploid, suggesting a directed process of expression alteration of these genes. A comprehensive and impressive microarray study of Arabidopsis neopolyploids provided a genome-wide survey of gene expression in the allopolyploids compared with their parents (Wang, Tian, Lee, Wei, et al. 2006). About 5–6% of the genes showed alterations in expression levels in the allopolyploids compared with their parents, with a majority showing downregulation. Most of the repressed genes were those that are expressed at a higher level in the Arabidopsis thaliana parent compared with the Arabidopsis arenosa parent. Although most studies of gene expression changes in allopolyploids have been done at the transcriptional level, a pioneering proteomics study of Brassica neopolyploids showed that protein abundance can also be altered by allopolyploidy (Albertin et al. 2006). A relatively high number of proteins showed quantitative differences in the polyploids as compared with their parents, but few proteins disappeared or appeared. It would be interesting to examine RNA expression levels for the genes corresponding to the proteins with nonadditive expression to look at the correspondence (or lack thereof) between transcripts and proteins.
Nonadditive expression in allopolyploids can have consequences on phenotypic characters. A recent and clever study of genes involved in regulating flowering time, flowering locus C (FLC; negatively regulates flowering) and FRI (positively regulates FLC), in neopolyploids of Arabidopsis showed that expression levels of FLC derived from the A. thaliana parent in the allopolyploid were considerably upregulated, whereas expression levels of FLC from the A. arenosa parent were downregulated (Wang, Tian, Lee, and Chen 2006). Upregulation of the A. thaliana copy was achieved by activation of the A. arenosa copy of FRI. Flowering time in the neopolyploids was later than in either parent. The results show a correlation between altered expression levels of FLC (caused by FRI) and novel flowering time in the neopolyploids.
One of the surprising findings of recent studies of gene expression in allopolyploids is that homeologous genes can be expressed at different levels and can respond differently to allopolyploidy in various organs of the plant. Adams et al. (2003) documented considerable variation in the expression and silencing patterns of homeologous genes in different organs of allopolyploid Gossypium hirsutum. A dramatic variation was observed in floral organs, where certain genes showed a gradient of expression levels of the homeologs when comparing different organs. Wheat allohexaploids also show organ-specific silencing of homeologs as evidenced from a study that compared expression in leaves versus roots (Bottley et al. 2006). Organ-specific variation in homeologous gene expression can be an immediate response to allopolyploidy, as observed in neopolyploids of Gossypium and Arabidopsis. Considerable variation was seen in the expression levels of homeologous gene pairs in different floral organs of a Gossypium neopolyploid (Adams et al. 2004). Allopolyploidy can result in gene expression changes relative to the diploid parents that are organ specific, observed at both the transcript and protein levels (Albertin et al. 2006; Wang, Tian, Lee, Wei, et al. 2006). Organ-specific expression changes have relevance for the fate of duplicated genes. When one homeolog has been silenced in some organs and the other homeolog has been silenced in other organs, subfunctionalization has occurred, as discussed below.
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Subfunctionalization |
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Subfunctionalization of duplicated genes refers to the partitioning of function and/or expression patterns between duplicated copies such that both copies continue to be needed (Lynch and Force 2000b). Evolutionarily recent cases of subfunctionalization in plants where expression patterns have been partitioned between duplicated genes include the maize genes ZMM1 and ZAG1 (Mena et al. 1996), as well as duplicated germin genes in barley (Federico et al. 2006). Subfunctionalization can be a fate of genes duplicated by polyploidy. Adams et al. (2003) showed reciprocal, organ-specific silencing of homeologs of the alcohol dehydrogenase gene AdhA in various floral organs of G. hirsutum, such that one homeolog has been silenced in some organs and the other homeolog has been silenced in other organs. Thus, AdhA expression has been partitioned such that both homeologs are now necessary to maintain the original expression pattern. The expression changes could have occurred sometime during the
1.5 million years of evolution since polyploidy or immediately on or soon after polyploidy. To determine if reciprocal, organ-specific silencing can occur soon after allopolyploidy, or if it is a long-term evolutionary effect, AdhA expression was examined in 2 independently created neopolyploids of similar genomic constitution to the natural allopolyploids. Remarkably, the same pattern of organ-specific silencing in floral organs was observed as in the natural allopolyploid G. hirsutum (Adams et al. 2003; Adams K, unpublished data), showing that partitioning of expression in an organ-specific manner can occur within a few generations after allopolyploidy and that the phenomenon is repeatable after different allopolyploidy events. Subfunctionalization of homeologous genes has considerable implications for speciation. If duplicated genes are subfunctionalized or reciprocally lost in geographically isolated populations, uniting of individuals from each population can lead to hybrids that lack both copies of a duplicated gene pair, resulting in hybrid inviability, reproductive isolation, and speciation (Werth and Windham 1991; Lynch and Force 2000a; Taylor et al. 2001). Even loss of one duplicated gene copy might result in speciation by divergent resolution if the gene product from one copy is insufficient for normal function. A recent study of homeologous gene losses after an ancient polyploidy in yeasts provided remarkable evidence for reciprocal gene loss being associated with speciation (Scannell et al. 2006).
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Hybridization Has Greater Effects on Gene Expression than Chromosome Doubling |
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Allopolyploids are often derived from a 2-step process: hybridization between 2 species and then doubling of all the chromosomes by the union of unreduced gametes (or by other mechanisms). Either process could have effects on gene expression. An alternative mode of allopolyploid formation is hybridization between 2 species that are already polyploid. In contrast, autopolyploids are usually formed by chromosome doubling within a species. Recent studies indicate that interspecific hybridization has a much greater effect than chromosome doubling on gene expression and that a majority, if not most, of changes in gene expression observed in newly formed allopolyploids were caused by hybridization. In addition, it has become clear that homoploid hybrids can show considerable changes in gene expression compared with their parents.
The effects of interspecific hybridization and chromosome doubling on gene expression were cleverly separated and analyzed in a study of Senecio. Hegarty et al. (2006) observed that triploid F1 hybrids (Senecio x baxteri) displayed considerably more changes in gene expression (including up- and downregulation) than resynthesized lines of the allohexaploid derived by doubling the chromosomes of the F1 hybrid. They concluded that most changes associated with allopolyploidy in Senecio were caused by interspecific hybridization and that polyploidy even had a calming effect on expression. Also indicating the greater effects of hybridization than chromosome doubling on gene expression were results from a proteomics study that compared newly created allopolyploid and amphihaploid hybrid Brassica lines with their parents. Albertin et al. (2006) observed that most (89%) of the expression changes were due to hybridization, and chromosome doubling had a very minor effect. The effects of hybridization between 2 tetraploid species have been examined in newly created allopolyploids of Arabidopsis and compared with autotetraploids of A. thaliana (Wang, Tian, Lee, Wei, et al. 2006). The allopolyploids showed considerable alternations in gene expression levels compared with their parents, but the autotetraploids showed few changes compared with their parents.
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Effects of Hybridization on Gene Expression in Diploid Hybrids |
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Several recent studies have explored the effects of hybridization, both intraspecific and interspecific, on gene expression in F1 diploid hybrids. Results indicate that F1 hybrids can show nonadditive gene expression relative to their parents, indicating that up- or downregulation of the expression of some genes is a response to hybridization. Nonadditive expression in intraspecific crosses of maize was examined using microarrays in 2 recent studies; these studies built on a previous analysis of 30 genes (Auger et al. 2005). Both microarray studies documented numerous genes that were nonadditively expressed in the hybrids compared with their parents, although most of these genes were expressed at levels within the parental range (Stupar and Springer 2006; Swanson-Wagner et al. 2006). A small percentage of genes (
44 of 14 000) were inferred to display underdominance or overdominance because of their expression levels that exceeded those of either parent (Swanson-Wagner 2006). It has been speculated that gene expression changes in hybrids, such as overdominant gene action, might play a role in heterosis (e.g., Birchler et al. 2005; Swanson-Wagner 2006). Another observed phenomenon regarding gene expression in hybrids is unequal allelic expression. Diploid hybrids can show unequal expression of genes derived from each parent, which is somewhat analogous to the phenomenon of unequal expression of homeologous genes in polyploids. This phenomenon was first explored in plants by a study of allelic variation of gene expression in maize intraspecific hybrids. Several genes of the 15 genes examined showed unequal expression, and one gene showed monoallelic expression (Guo et al. 2004). Allelic expression was also examined in maize hybrids by Stupar and Springer (2006), who found that much of the allelic expression variation appeared to be due to cis-regulation, with some genes showing both cis- and trans-regulation. To determine if the parent-of-origin affects gene expression in a hybrid, Stupar and Springer (2006) used reciprocal crosses between 2 different maize lines. They found that few genes showed expression differences in the reciprocal crosses and thus exhibit parental effects on gene expression. Similar results were obtained by Guo et al. (2004) in their study of allelic expression in maize hybrids. Somewhat more genes were shown to have parent-of-origin effects on expression in a study of Arabidopsis hybrids that were created by reciprocally hybridizing 2 ecotypes of A. thaliana (Vuylsteke et al. 2005). Although the authors of all 3 studies concluded that the effects of maternal or paternal transmission were minimal, further study of those genes that did show parent-of-origin effects could be informative.
A surprising phenomenon regarding allelic expression that can occur in F1 diploid hybrids is organ-specific silencing of alleles. Adams and Wendel (2005a) showed reciprocal silencing of AdhA homeologs in different organs of a diploid F1 hybrid formed by crossing 2 species of Gossypium. If such differential expression is stably inherited in at least a portion of the F2 and later offspring, it would be suggestive of instant subfunctionalization on hybridization.
The evolutionary effects on hybridization on gene expression were analyzed in the homoploid (diploid) hybrid species Helianthus deserticola, using cDNA microarrays. A set of 58 genes showed up- or downregulation, with about equal numbers of each, in the hybrid species compared with its diploid progenitors (Lai et al. 2006). This study also explored the effects of gene expression changes on fitness. Five genes that were differentially expressed between the hybrid and its progenitors map to quantitative trait locis (QTLs) that control morphological and physiological traits and represent candidate genes for adaptive differentiation (Lai et al. 2006). One of the genes maps to QTLs for traits related to fitness and rapid flowering that may be of adaptive significance in the arid environment where H. deserticola is found.
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Loss of Imprinting on Hybridization and Its Phenotypic Effects |
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Josefsson et al. (2006) recently showed loss of imprinting of 2 genes on hybridization between tetraploid A. thaliana and diploid A. arenosa. Maternal imprinting of PHE1 and paternal imprinting of MEDEA appeared to be lost in the hybrid. Both genes are important for seed development. PHE1 is overexpressed in the hybrids, but, surprisingly, most expression is from the maternal allele. A phe1 mutant line had significantly improved seed set, showing that PHE1 overexpression in the hybrids contributes to seed death. The results establish a causal link between breakdown of imprinting and seed lethality in the hybrids and show how gene expression changes on hybridization can have major phenotypic effects.
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Types of Genes with Altered Expression Patterns in Polyploids and Hybrids |
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One of the major benefits of microarray studies is that they allow expression of thousands of genes to be assayed simultaneously, and thus, inferences can be made about the types and categories of genes whose expression is affected by allopolyploidy and hybridization. A microarray study of Senecio allopolyploid and hybrid species found that expression of no particular functional category of genes was overly affected, although genes involved in floral or pollen development were slightly overrepresented (Hegarty et al. 2006). Similarly, a microarray study of the homoploid hybrid species H. deserticola showed differential regulation of genes in various functional categories in the hybrid (Lai et al. 2006). Interestingly, transport-related proteins were particularly susceptible to transgressive expression. A comprehensive microarray study of Arabidopsis neopolyploids showed differential expression of genes in a variety of functional categories, but genes involved in hormonal regulation, in particular the ethylene biosynthesis pathway and cell defense and aging categories such as the heat shock proteins, were highly represented (Wang, Tian, Lee, Wei, et al. 2006). Overall, it appears that expression of a variety of types and categories of genes is altered in allopolyploids and hybrids, but certain species or organ types may show biases for certain types of genes.
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Causes and Mechanisms of Gene Silencing and Upregulation in Polyploids |
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What molecular mechanisms are responsible for gene silencing and reactivation in polyploids and hybrids? Hypermethylation of DNA cytosines has been shown to silence homeologs in Arabidopsis neopolyploids and in A. suecica (Lee and Chen 2001; Wang et al. 2004). These experiments were done by using a methyltransferase inhibitor or by silencing a methyltransferase gene using RNA interference, causing reactivation of silenced genes. Activation of retrotransposons on allopolyploidy in wheat was shown to cause gene silencing by readout transcription into adjacent genes that were in the opposite orientation (Kashkush et al. 2003). In the same study, retrotransposon activation was also shown to cause gene activation by readout transcription into an inactive downstream gene that was in the same orientation as the transposon. Another mechanism for gene activation on allopolyploidy was shown for the FLC gene in neopolyploids of Arabidopsis. Activation of the A. thaliana copy of FLC was associated with changes in histone modifications including demethylation and acetylation (Wang, Tian, Lee, and Chen 2006). Other possible mechanisms for novel expression patterns of duplicated genes in polyploids were discussed in recent reviews (Liu and Wendel 2003; Osborn et al. 2003; Madlung and Comai 2004; Rapp and Wendel 2005; Chen and Ni 2006).
Why are some genes silenced, downregulated, or upregulated in polyploids? Several hypotheses have been proposed relating to gene dosage, altered regulatory networks, epigenetic remodeling, interactions of parental copies with each other, as well as side effects of other molecular processes; these hypotheses have been discussed in several recent articles (Osborn et al. 2003; Riddle and Birchler 2003; Adams and Wendel 2005c; Birchler et al. 2005; Comai 2005; Veitia 2005). Gene dosage factors include preservation of the appropriate level of gene expression despite the increased dosage caused by chromosome doubling, as well as increased variation in dosage-regulated gene expression. Altered regulatory networks include the consequences of reuniting diverged regulatory factors and their target genes (see Riddle and Birchler 2003, for a nice diagram). It is likely that multiple factors cause gene expression changes in polyploids and that the causes vary by gene and perhaps by organism.
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Concluding Remarks |
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Recent studies have considerably added to our knowledge of the complex effects of allopolyploidy and hybridization on gene expression and the evolution of genes duplicated by allopolyploidy. Major advances have been made in separating the effects of hybridization versus chromosome doubling on gene expression, defining organ-specific patterns of duplicate gene expression and silencing, determining what types and categories of genes are affected by hybridization and allopolyploidy, and examining gene expression changes at the protein level. Future studies in this active area of research will undoubtedly provide new insights into gene expression patterns and regulation, causes and underlying mechanisms, and the evolution of duplicate gene expression. In particular, it will be interesting to explore the effects of gene expression changes in polyploids and hybrids on phenotypic characters, the molecular mechanisms causing homeologous gene silencing, the effects of stress conditions on homeologous gene expression patterns, and the evolution of expression patterns in multiple species derived from the same polyploidy event. Research using plants from multiple plant families will be important to determine what phenomena are general consequences of hybridization and allopolyploidy and what phenomena are specific to a particular species or family.
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Acknowledgments |
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The author thanks an anonymous reviewer for helpful comments on the manuscript. Research in the laboratory of K.A. is supported by a grant from the National Science and Engineering Research Council of Canada. This paper is based on a presentation given at the 2006 Annual Meeting of the American Genetic Association, "Genetics of Speciation," University of British Columbia, Vancouver, Canada, July 21–24, 2006.
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Footnotes |
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Corresponding Editor: Loren Rieseberg
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