Introgression of Crop Alleles into Wild or Weedy Populations

The evolutionary significance of introgression has been discussed for decades. Questions about potential impacts of transgene flow into wild and weedy populations brought renewed attention to the introgression of crop alleles into those populations. In the past two decades, the field has advanced with considerable descriptive, experimental, and theoretical activity on the dynamics of crop gene introgression and its consequences. As illustrated by five case studies employing an array of different approaches, introgression of crop alleles has occurred for a wide array of species, sometimes without significant consequence, but on occasion leading to the evolution of increased weediness. A new theoretical context has emerged for analyzing empirical data, identifying factors that influence introgression, and predicting introgression’s progress.With emerging molecular techniques and analyses, research on crop allele introgression into wild and weedy populations is positioned to make contributions to both transgene risk assessment and reticulate evolution. HISTORICAL PERSPECTIVE Most crops were domesticated from wild plants centuries or even millennia ago (Warwick & Stewart 2005). Early evolution under anthropogenic selection produced domesticated plants that were locally adapted and more productive. With the advent of formal plant breeding, progress in plant improvement depended on selection from (a) pre-existing variation in the evolving crop and (b) alleles obtained by intentional hybridization with the crop progenitor and other wild or weedy (henceforth, WW) relatives. Recently, techniques available to breeders have expanded to include methods such as human-mediated intertaxon crosses, hybrid embryo rescue, protoplast fusion, induced mutations, and transgenesis. Still, spontaneous and intentional hybridization betweenWWpopulations and locally adapted landraces continue to be sources of variation for crop improvement both in formal breeding and in traditionally managed agroecosystems (Hajjar & Hodgkin 2007, Jarvis & Hodgkin 1999). Conversely, spontaneous hybridization can be the first step for the flow of novel crop alleles in the other direction, i.e., into WW relatives (Ellstrand 2003). Subsequent establishment of those alleles is known as introgression, “the permanent incorporation of genes from one set of differentiated populations (species, subspecies, race, and so on) into another” (Stewart et al. 2003, p. 806). The process of introgression begins when a fertile or semifertile hybrid (or even an F2 or later segregant) successfully backcrosses with one of the parental species. Unless opposed by selection or drift, further introgression proceeds under repeated backcrossing or selfing. The importance of crop allele introgression in the evolution of WW populations has been controversial. In the late twentieth century, deWet & Harlan (1975) recognized peripatric and sympatric wild-weed-crop complexes as zones of significant gene exchange across reproductive isolating barriers of varying permeability. They argued that two of the three avenues of exchange would be significant: (a) Such evolutionary hotbeds would favor the flow of beneficial alleles from the wild to the crop, providing farmers with a constant source of genetic variation useful for plant improvement, and (b) gene flow from crops into weedy populations could stimulate the evolution of crop mimics. But their view was that “selection almost completely prevents gene flow in the 326 Ellstrand et al. A nn u. R ev . E co l. E vo l. Sy st . 2 01 3. 44 :3 25 -3 45 . D ow nl oa de d fr om w w w .a nn ua lr ev ie w s. or g by U ni ve rs ity o f T en ne ss ee K no xv ill e H od ge s L ib ra ry o n 03 /1 7/ 14 . F or p er so na l u se o nl y. ES44CH16-Ellstrand ARI 29 October 2013 11:1 direction of the wild race” (deWet & Harlan 1975, p. 106). Others had a contrasting view, e.g., “. . . gene flow, if it exists, is apparently more effective in the direction from the cultivated to the wild populations” (Ladizinsky 1985, p. 191). At a time when gene flow and hybridization were often inferred frommorphology alone, rather than genetically based markers, conclusive evidence for intertaxon gene flow was often lacking. The flow of crop alleles intoWWpopulations might have remained solely a topic for academic discussion; but applied evolutionists subsequently recognize that intertaxon gene flow can lead to evolutionary changes that impact human affairs. Hybridization can sometimes stimulate the evolution of new weeds or invasives (Schierenbeck & Ellstrand 2009) or contribute to the risk of extinction (Ellstrand & Elam 1993, Levin et al. 1996). Given these potential problems, the advent of genetically engineered crops and subsequent questions about possible consequences of transgene flow brought renewed attention to the flow of crop alleles into WW populations. Stimulated by questions regarding transgene dispersal, dozens of evolutionary geneticists and ecologists took to the field in the 1990s to conduct experimental or descriptive studies addressing the likelihood of such gene flow, usually using nontransgenic plants as model systems. Their initial focus was to determine whether spontaneous hybridization between crops and WW relatives occurred under field conditions. Secondary questions included whether gene flow occurred at distances and rates large enough to permit crop genes (and by extension, transgenes) to enterWW populations and, if so, what consequences were expected to ensue. Subsequent introgression was often assumed, yet introgression-related data, such as the fitness of advanced hybrid generations and the effects of specific crop traits, were largely neglected. Themost frequent relevant data from that early research were measurements of the relative fitness of the F1s versus that of the WW parents (Ellstrand 2003). Ellstrand (2003) reviewed these and earlier relevant hybridization studies. He examined data for the world’s 25 most important domesticated plants in terms of area planted; for 22 of these plants, he found substantial empirical evidence for some spontaneous hybridization with WW relatives somewhere in the world. Hybridization patterns were idiosyncratic for the crops. For some, such as coffee, hybridization apparently occurs rarely and in a few locations. For others, low levels of hybridization typically occur over much of the globe; in the case of wheat and its weedyAegilops relatives, hybridization occurs whenever the species co-occur in temperate regions. For a few, such as cultivated sunflower, hybridization can occur at relatively high rates. Several years later, a book by Andersson & de Vicente (2010) re-evaluated and updated what is known regarding opportunities for crop gene flow to WW relatives for a similar list of 20 important food crops. With rich detail describing the crops’ reproductive and dispersal biology, compatible relatives, and hybrid fitness, each case study is presented as a crop-specific guide for transgene flow assessment. Both books (Andersson & de Vicente 2010, Ellstrand 2003) mention introgression when they found supporting data. Both books focus strongly on hybridization, and hybridization is not introgression. If significant evolutionary or ecological impacts occur, they typically occur through introgression (Arnold 2006). As the significance of introgression became clear, the research focus of the twenty-first century changed considerably, and the research emphasis shifted from “Does hybridization occur?” to the next step of “How and when does introgression occur and at what levels?” The context broadened from focusing on the transgene escape to the introgression of any domesticated alleles (den Nijs et al. 2004). The question of “When and how will introgression have any significant impact?” has also become paramount. Although the introgression of domesticated plant genes has received attention from publications in the context of transgene flow (den Nijs et al. 2004, Kwit et al. 2011, Stewart et al. 2003), the wider burst of research activity that started this century awaits a thorough review. www.annualreviews.org • Crop-to-Wild/Weed Introgression 327 A nn u. R ev . E co l. E vo l. Sy st . 2 01 3. 44 :3 25 -3 45 . D ow nl oa de d fr om w w w .a nn ua lr ev ie w s. or g by U ni ve rs ity o f T en ne ss ee K no xv ill e H od ge s L ib ra ry o n 03 /1 7/ 14 . F or p er so na l u se o nl y. ES44CH16-Ellstrand ARI 29 October 2013 11:1 Thus, we address introgression from domesticated plants to theirWW relatives. As mentioned above, such gene flow provides examples of contemporary microevolution that may have important implications. Below we ask, “What do we know about crop gene introgression into WW populations?” including when evolution by introgression creates a negative impact (Natl. Res. Counc. 2002, Organ. Econ. Co-op. Dev. 1993). Our specific focus is the establishment of alleles from domesticated plants inWWpopulations. How alleles are naturally introgressed may follow a variety of pathways. The pollen parent in the initial hybridization event (or events) could involve a plant in cultivation, a volunteer left from a previous planting or from seed spillage into a natural population, or a recent escape from cultivation. An alternate evolutionary pathway could start with an uncultivated plant as pollen parent hybridizing with a plant in cultivation. If the hybrid seed from the maternal plant naturally disperses or is harvested and sown in the same location, it can variously self-pollinate, cross with other hybrids, or spontaneously backcross with its parental parent (depending, in part, on the breeding system of each of the parental taxa). We define wild plants as those capable of growing and reproducing in ecosystems that are largely undisturbed by humans. Weeds are those whose populations persist only under anthropogenic disturbance. Of course, intermediate cases exist; also, some taxa may include both wild and weedy populations. First, we present a brief overview of hybridization and introgression in plants.Next, we examine various molecular approaches for identifying and studying crop allele introgression. Some case studies of introgression of domesticated alleles into WW populations follow, including the few described examples of spontaneous transgene introgression.We concludewith a look to the future. HYBRIDIZATION AND INTROGRESSION IN PLANTS Hybridization is an important component of plant evolution, occurring in roughly 25% of plant species (Baack & Rieseberg 2007). Nonetheless, hybridization occurs unevenly among plant taxa; a higher propensity occurs in certain genera, families, and orders (Whitney et al. 2010). In a few families, natural intergeneric hybridization occasionally occurs (Stace 2010). Even for readily hybridizing species, hybridization and introgression rarely occur at high enough rates to jeopardize the integrity of a species (Levin et al. 1996). Thus, although hybrids are produced,most of them have no further evolutionary impact. However, sometimes a little hybridization has considerable evolutionarily significance (Arnold 2006). Mechanisms such as alloploidyor apomixis canfixhybridity, leading to the evolutionof newhybridderived species from one or just a few founders (Arnold 2006). Likewise, homoploid hybrid speciation can yield new species without a change in ploidy level or mating system (Buerkle et al. 2000). More frequently, the evolutionary impact of hybridization is mediated through introgression. Edgar Anderson’s 1949 book Introgressive Hybridization championed introgression as a potentially important process for introducing adaptive variation into a population. At that early date, hybrids and hybrid derivatives were largely assigned bymorphology.Nowadays,multilocusmolecular markers have greatly enhanced the ability to detect introgression (Rieseberg&Wendel 1993). The last major review, twenty years ago, examined hundreds of putative cases of introgression, identifying about three dozen cases (almost all bolstered bymolecular data) of probable natural introgression in plants (Rieseberg&Wendel 1993). Today, that numbermight be larger by an order of magnitude (examples below and in Table 1). By definition, introgression cannot be as common as hybridization. Determining how common introgression in plants is and its real evolutionary significance remains challenging and generally requires molecular marker-based methods. 328 Ellstrand et al. A nn u. R ev . E co l. E vo l. Sy st . 2 01 3. 44 :3 25 -3 45 . D ow nl oa de d fr om w w w .a nn ua lr ev ie w s. or g by U ni ve rs ity o f T en ne ss ee K no xv ill e H od ge s L ib ra ry o n 03 /1 7/ 14 . F or p er so na l u se o nl y. ES44CH16-Ellstrand ARI 29 October 2013 11:1 Table 1 Examples of introgressed crop alleles in wild or weedy populations with strong support Cultivated ancestor Example of wild or weedy (WW) taxon with one or more populations with introgressed crop alleles Reference Beta vulgaris vulgaris, beet Europe’s weed beet (descendant of beet × B. v. maritima) Case study in this review Brassica napus, oilseed rape B. rapa Andersson & de Vicente 2010 Cichorium intybus, chicory WW C. intybus Kiaer et al. 2007 Cynara cardunculus var. scolymus, artichoke Some populations of California’s artichoke thistle (descendant of artichoke × C. c. cardunculus) Leak-Garcia et al. 2013 Glycine max, soybean G. soja Andersson & de Vicente 2010 Gossypium hirsutum, cotton G. barbadense Andersson & de Vicente 2010 Helianthus annuus, sunflower H. petiolaris Case study in this review Lactuca sativa, lettuce L. serriola Case study in this review Oryza glaberrima, African domesticated rice O. barthii Andersson & de Vicente 2010 Oryza sativa, Asian domesticated rice O. rufipogon Case study in this review Phaseolus vulgaris, common bean P. vulgaris Andersson & de Vicente 2010 Raphanus sativus, radish R. raphanistrum Case study in this review Solanum tuberosum, potato S. edinense (a stabilized clonal hybrid of potato × S. demissum) Ellstrand 2003 Sorghum bicolor, sorghum S. halepense Andersson & de Vicente 2010 Triticum turgidum, wheat Aegilops peregrina Kwit et al. 2011 Ulmus pumila, Siberian elm U. minor Ellstrand 2003 Zea mays mays, maize Z. m. mexicana Andersson & de Vicente 2010 IDENTIFYING HYBRIDS AND INTROGRESSANTS Determining whether an individual is a hybrid or has hybrid ancestry is not straightforward in the absence of genetic markers. Phenotypic intermediacy might indicate an early-generation hybrid, a segregant, or a later generation backcross retaining some characters from both parental species. Also, phenotypic response to environmental variation or developmental instability may create unexpected morphologies that mimic hybrid ancestry. Furthermore, experimental research has revealed that, more often than not, for any given morphological or otherwise quantitative trait, F1s are not necessarily intermediate compared to their parents (Rieseberg & Ellstrand 1993). For detecting introgression, the problem becomes worse. In his seminal book, Edgar Anderson, believing introgression became increasingly important as the number of introgressed alleles decreased, bemoaned: How important is introgressive hybridization? I do not know. One point seems fairly certain; its importance is paradoxical. The more imperceptible introgression becomes, the greater is its biological significance. It may be of the greatest fundamental importance when by our crude methods we can do no more than demonstrate its existence (Anderson 1949). Co-dominant genetic-based markers can provide more certainty than phenotypic measurements. For hybridizing taxa fixed for the alternate alleles, a1 and a2, if an individual is heterozygous for both alleles, the individual can be assigned hybrid ancestry. But information from a single locus is insufficient to distinguish an introgressant from a first generation hybrid. www.annualreviews.org • Crop-to-Wild/Weed Introgression 329 A nn u. R ev . E co l. E vo l. Sy st . 2 01 3. 44 :3 25 -3 45 . D ow nl oa de d fr om w w w .a nn ua lr ev ie w s. or g by U ni ve rs ity o f T en ne ss ee K no xv ill e H od ge s L ib ra ry o n 03 /1 7/ 14 . F or p er so na l u se o nl y. ES44CH16-Ellstrand ARI 29 October 2013 11:1 When few individuals are surveyed, it is often uncertain whether both parental taxa are actually fully fixed for alternate alleles. If not, an allele might be wrongly assigned as introgressed. To illustrate, imagine both putative parents are not fixed for alternative alleles but have retained alleles from a common ancestor (symplesiomorphy or incomplete lineage sorting). One species has the a1 allele at 97% frequency and the a2 allele at 3%; the other has a1 at 1% and a2 at 99%. If an individual is found that is heterozygous at that locus, does it have hybrid ancestry or is it just one of the rare heterozygotes within either species? Thus, thorough sampling of putative parental taxa is crucial, especially when few loci are assayed. Populations that have never been in reproductive contact with crops are particularly useful but are difficult to identify for widespread ancient crops whose distributions have changed. The accuracy of assigning hybrid ancestry and introgression increases for each additional independent marker assayed and as more data are available from other sources of information. Alternatively, transgenes, the result of genetic engineering, are evolutionarily unique to crops. If we find an engineered gene in a WW plant, we can be certain that it has hybrid ancestry. At the moment, evidence for transgene introgression is known from only a few cases (Warwick et al. 2008, Wegier et al. 2011). In most cases, the ideal tool kit is a set of genetically based markers for large numbers of loci dispersed throughout the whole genome that can be easily and unambiguously scored. The most useful markers are codominant, allowing for homozygous loci to be distinguished from heterozygous loci. Furthermore, access to a set of anonymous loci with no a priori expectations of selection history can provide a baseline expectation of patterns of introgression to compare with a locus of interest. However, fully dominant molecular markers and/or markers whose genetic basis is unclear have limited value in elucidating ancestry (Whitkus et al. 1994). Allozymes were the first widely used biochemical marker system, an improvement over morphological markers, but they were constrained by the low number of loci sampled. For a given taxon, polymorphic allozyme loci rarely number more than a dozen, each with two or a few more alleles. DNA-based markers are much more powerful. For example, polymorphic microsatellite loci may have several to dozens of alleles per locus. Their primary limitation is their relatively high back-mutation rate, resulting in alleles with different histories appearing to be identical (homoplasy). Microsatellite mutation rate should be less problematic for crop allele introgression research when such introgression has occurred recently in evolutionary time, in many cases, less than a century (Ellstrand et al. 2010). Single nucleotide polymorphisms (SNPs) are emerging as highly informative markers for characterizing introgression. SNPs can be confidently scored and provide high throughput analysis; SNP microarrays can survey polymorphism at up to tens of thousands of sites across a plant’s genome and are now available at relatively affordable prices. Alternative methods using reduced genomic libraries include RADtag sequencing, which might also be useful for larger genomes (Baird et al. 2008). Also, the genotyping-by-sequencing approach allows direct evaluation of large, complex (e.g., polyploid) genomes without prior development of other molecular tools (Elshire et al. 2011). Although such an approach is feasible for any species, currently genome assembly remains labor-intensive and costly for many nonmodel species, especially those with large genomes. Direct SNP genotyping as well as single molecule sequencing are advancing rapidly, and cheaper flexible genotyping methods are becoming available (Maughan et al. 2011). Even sequencing of polyploid plants is within reach because of single molecule sequencing (Kovalic et al. 2012), yielding allele dosage and haplotype information. With access to a large number of loci of known genome location, variation in introgression rates throughout the genome can be estimated. Genome-level approaches have already revealed that introgression occurs unevenly across the genome of the species involved 330 Ellstrand et al. A nn u. R ev . E co l. E vo l. Sy st . 2 01 3. 44 :3 25 -3 45 . D ow nl oa de d fr om w w w .a nn ua lr ev ie w s. or g by U ni ve rs ity o f T en ne ss ee K no xv ill e H od ge s L ib ra ry o n 03 /1 7/ 14 . F or p er so na l u se o nl y. ES44CH16-Ellstrand ARI 29 October 2013 11:1 (Baack &Rieseberg 2007, Hooftman et al. 2011, Twyford&Ennos 2012). Information on linkage disequilibrium (LD) between markers can aid in making inferences about introgression because, in cases of recent introgression, tightly linked taxon-specific markers would still be in LD. LD should decrease in later generation hybrids and is expected to be very low if similarity between taxa resulted from a common but ancient ancestry—unless selection acting on allele combinations is extremely strong (e.g., Linder et al. 1998). Linkage information can be obtained by crossing the taxa being studied and analyzing segregation in the F2 or BC1 generation. Because most important crops have been already extensively genetically mapped, new markers can easily be placed on that map and tested for LD. In particular, haplotype data are ideal for reconstruction of introgression as they provide information about linkage relationships, that is, whether genes are in coupling or repulsion phase, which in turn gives information on the ancestral genotypes. The most detailed genetic information regarding loci and linkage is obtained via genome sequencing. One example of detection of introgression through sequencing is the discovery of Neanderthal DNA inmodern humans (Green et al. 2010) revealed by next-generation sequencing techniques combined with what is known regarding the migration patterns of modern humans. MEASURING INTROGRESSION Once introgression has been identified, more questions follow: What fraction of the recipient population is introgressed? Are introgression rates roughly equivalent across the genome or are some loci or genomic regions significantly more or less introgressed relative to neutral expectations; that is, does selection appear to be involved in which loci have passed from one taxon to the next? As the number of marker loci increases, so too will the ability to answer these questions, especially if the genomic location of those loci is known. Another important factor is the timescale over which introgression has occurred. How many years or generations of introgression have occurred? For example, for transgenes the timescale of introgression into unmanaged populations is necessarily recent, no longer than since the first field release of the transgenic crop, obtainable from public regulatory records. However, the detectionmethodology depends on publicly available transgenic sequences.Other kinds of historic information may be useful for establishing time since contact between potentially hybridizing data—ranging from newspaper accounts to archeological artifacts (e.g., Leak-Garcia et al. 2013). The combination of historic information and genetic data can be used to infer the amount of gene exchange between populations. Traditional population genetics methods for estimating genetic differentiation, such as F statistics (Wright 1931) and their analogs, have often been used to estimate levels of gene flow. These methods measure genetic differentiation, which can be used to estimate historic gene flow (average number of successful immigrants per generation) but make some potentially biologically unrealistic assumptions (Whitlock & McCauley 1999). Recently, methods have been developed for assigning individuals into groups based on patterns of linkage equilibrium or genetic differentiation (e.g., Corander et al. 2004, Pritchard et al. 2000). Suchmethods can identify admixed individuals (those whose genetic content is derived frommore than one of the inferred groups). Such admixture implies recent introgression. Another method, BAYESASS (Wilson & Rannala 2003), explicitly estimates population-level introgression rates rather than individualmigrant ancestries and does not assumeHardy-Weinberg equilibrium (often the case with other methods). BAYESASS and related approaches are appropriate for detecting introgression that has occurred relatively recently (<20 generations ago). The relatively new (at least to population genetics) method of Approximate Bayesian Computation (Beaumont 2010) has been successfully applied in crop-wild introgression during domestication (e.g., Ross-Ibarra et al. 2009) andhas potential regardingmore recent crop-WWquestions.Thismethod is versatile, given www.annualreviews.org • Crop-to-Wild/Weed Introgression 331 A nn u. R ev . E co l. E vo l. Sy st . 2 01 3. 44 :3 25 -3 45 . D ow nl oa de d fr om w w w .a nn ua lr ev ie w s. or g by U ni ve rs ity o f T en ne ss ee K no xv ill e H od ge s L ib ra ry o n 03 /1 7/ 14 . F or p er so na l u se o nl y. ES44CH16-Ellstrand ARI 29 October 2013 11:1 the range of evolutionary simulation programs now available (partially reviewed by Hoban et al. 2012), with relatively few limitations for demographic scenarios that can be accommodated (e.g., some cases of asymmetrical gene flow). However, it requires large amounts of data, especially for complex scenarios. Just how far into the past these methods are informative needs to be addressed with additional simulation or controlled experimental work. The foregoing methods are often applied to microsatellite data. As discussed above, the high mutability of microsatellites can result in homoplasy, a problem for estimating long-term introgression. Questions of long-term introgression measurement are better addressed with slowly evolving markers such as SNPs or longer sequenced regions. Therefore, for longer-term introgression estimates, coalescent-based methods (Kuhner 2009) may be appropriate. Two widely used programs implementing these methods are MIGRATE (Beerli 2006) and the isolation with migration (IM) suite of programs (Hey 2010). These methods explicitly take into account genealogical relationships between alleles, enabling estimates of both directional introgression rates and other demographic parameters such as divergence time and population size (Kuhner 2009). MIGRATE assumes an equilibrium scenario in which population sizes and migration rates have been stable for a long time relative to initial divergence. In contrast, the IM programs explicitly model a nonequilibrium scenario in which divergence occurred in the relatively recent past, allowing for the disentangling of genetic similarity due to gene flow versus shared retention of ancestral polymorphisms. Consequently, IM is likely more appropriate for many crop-WW systems. However, the current methods do not efficiently estimate the timing of introgression (Strasburg & Rieseberg 2011); additional relevant research would be valuable. A “genomic clines”method for examining genomic patterns of introgression for both shortand long-term timescales has recently been described (Gompert & Buerkle 2009, 2011). This method compares introgression patterns at individual loci relative to the genomic background for detecting selection that affects introgression rates. Simulations suggest that this method can be informative on timescales as short as five generations, making it applicable to many crop-WW systems. CROP ALLELE INTROGRESSION INTO WW POPULATIONS Crops and theirWW relatives present both disadvantages and advantages for detecting introgression. Most crops began their evolutionary journey hundreds to thousands of years ago, leaving little time for substantial genome divergence. However, the plant improvement process may have fixed alleles that are nearly absent inWWpopulations because they are detrimental under natural conditions. Undesirable traits eliminated from crops include seed dormancy, seed shattering in seed crops, and early bolting in vegetable crops (e.g., Hartman et al. 2013a,Weeden 2007). Bottlenecks from strong selection under domestication vary widely in both intensity and duration (Gross & Olsen 2010); stronger bottlenecks generally promote higher levels of differentiation between domesticates and their wild ancestors. Furthermore, plant breeders have occasionally introgressed wild germplasm into a crop, resulting in decreased genetic differentiation between the taxa. Such deliberate wild-to-crop introgression might be difficult to distinguish from introgression in the opposite direction, but methods exist for detecting asymmetric patterns of gene flow (Beerli 2006, Hey 2010). In contrast, transgenesis and mutation breeding create evolutionarily unique single locus (for transgenics) and multiple locus (for mutation breeding) crop-specific markers. Crops, as part of the study system, provide numerous benefits because of their economic importance. They are well studied; for example, at the moment, substantial genome sequence data are available for 49 plant species, 35 of which are crops. (Michael & Jackson 2013). Dozens of crop species not yet sequenced have been extensively geneticallymappedwithmuch transcriptome data available (e.g., Bowers et al. 2012). Crops have the advantage that historical and geographic 332 Ellstrand et al. A nn u. R ev . E co l. E vo l. Sy st . 2 01 3. 44 :3 25 -3 45 . D ow nl oa de d fr om w w w .a nn ua lr ev ie w s. or g by U ni ve rs ity o f T en ne ss ee K no xv ill e H od ge s L ib ra ry o n 03 /1 7/ 14 . F or p er so na l u se o nl y. ES44CH16-Ellstrand ARI 29 October 2013 11:1 information are often available—e.g., cultivars and the duration of cultivation in a given location. Crop genetic resources are readily available, and pure material of specific crop cultivars involved in hybridization can be obtained for screening. Moreover, extensive germplasm collections of old landraces and wild accessions are available for many crops. Consequently, reports of domesticated allele introgression into WW populations have gradually accumulated. Table 1 features a nonexhaustive list of crop species for which introgression is known to have occurred or is occurring on the basis of substantial data. We provide some case studies below as examples. These represent an array of crops from different plant families with different uses, breeding systems, and life histories. None of the following crops, except for beet, have genetically engineered cultivars that are commercially available.