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1 Department of Biology, Tufts University, Medford, Massachusetts 02155 USA
Received for publication February 4, 2000. Accepted for publication June 6, 2000.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONHYBRIDIZATION AND CHEMICAL...PATTERNS OF CHEMICAL VARIATIONIMPLICATIONS FOR PLANT-HERBIVORE...CONCLUSIONLITERATURE CITED |
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Key Words: genetics • hybridization • inheritance • introgression • novelty • plant–herbivore interactions • secondary chemistry
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONHYBRIDIZATION AND CHEMICAL...PATTERNS OF CHEMICAL VARIATIONIMPLICATIONS FOR PLANT-HERBIVORE...CONCLUSIONLITERATURE CITED |
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). More recently Anderson (1949)
proposed that hybridization facilitates the transfer of traits between species, a process known as introgressive hybridization, and Stebbins (1959)
and Lewontin and Birch (1966)
suggested that hybridization and introgression could promote adaptive evolutionary change. Hybridization and introgression are widespread features of many natural plant populations (e.g., Levin, 1966
; Harborne and Turner, 1984
; McArthur, Welch, and Sanderson, 1988
; Keim et al., 1989
; Smith and Sytsma, 1990
; Soltis and Soltis, 1991
; Rieseberg and Wendel, 1993
; Arnold, 1994
; Fritz, Nichols-Orians, and Brunsfeld, 1994
; Rieseberg, 1995
; Ellstrand, Whitkus, and Rieseberg, 1996
; Arnold, 1997
; Rieseberg and Carney, 1998
), and 
70% of all flowering plant species are believed to have originated via hybridization (Whitham, Morrow, and Potts, 1991
; Arnold, 1994
). So what determines the ecological performance and evolutionary fates of hybrids? Historically, most research has focused on gametic barriers and viability, specifically, the ability of hybrids to survive the abiotic conditions present in parental or nearby nonparental habitats (Arnold and Hodges, 1995
; Rieseberg, 1995
; Rieseberg and Carney, 1998
). Relatively little attention has been paid to their resistance to herbivores and pathogens, yet recent reviews suggest that resistance is an important component of hybrid survival (Whitham, 1989
; Strauss, 1994
; Fritz, Nichols-Orians, and Brunsfeld, 1994
; Fritz, 1999
; Fritz, Moulia, and Newcombe, 1999
).
The production of secondary chemicals mediates plant resistance to herbivores and pathogens (e.g., Rosenthal and Janzen, 1979
). Not surprisingly several studies have shown that plant secondary chemistry alters the resistance of hybrid plants (Huesing et al., 1989
; Ben-Hammouda et al., 1995
; Orians et al., 1997
; Fritz and Orians, unpublished data). Although plant breeders use hybridization to obtain or introgress desired chemical traits (e.g., Maxwell and Jennings, 1980
; Huesing et al., 1989
; Altman, Stipanovic, and Bell, 1990
; Gómez and Ledbetter, 1993
), surprisingly little attention has been paid to the effects of hybridization on secondary chemistry and the survival of hybrids in natural populations. In one study, Rodman (1980)
suggested that selection against hybrid glucosinolate phenotypes (Cakile, Brassicaceae) maintains a narrow hybrid zone and minimizes gene flow. Clearly, secondary chemistry may be an important component of hybrid fitness and influence speciation, introgression, and plant–herbivore interactions.
We know that hybridization results in progeny that differ qualitatively and quantitatively from the parents in the expression of secondary chemicals (Harborne and Turner, 1984
). It is often incorrectly assumed that traits of hybrids will be intermediate to the two parental taxa (Rieseberg, 1995
). In fact, patterns of inheritance are quite complex. In first-generation (F1) hybrids, the suite of chemicals may be: (1) similar to that in one of the two parental taxa (Fahselt and Ownbey, 1968
), (2) intermediate between those of the two parental taxa (McMillan, Chavez, and Mabry, 1975
; Orians et al., 2000
), (3) overexpressed or present in higher concentrations than in either parent (Spring and Schilling, 1990
), (4) underexpressed or present in lower concentrations than either parent (Court et al., 1992
), (5) deficient, in that hybrids lack chemicals that both parents produce (Fahselt and Ownbey, 1968
), or (6) novel, in that hybrids may contain chemicals lacking in both parental taxa (Levy and Levin, 1974
; Rieseberg and Ellstrand, 1993
; Buschmann and Spring, 1995
). Later-generation hybrids generate even more variability (Connor and Purdie, 1976
; Rieseberg and Ellstrand, 1993
). Another important feature of hybridization is that individuals may differ qualitatively and quantitatively from each other even within a hybrid class (e.g., F1, F2, and backcross hybrids) (Connor and Purdie, 1976
; Crins, Bohm, and Carr, 1988
; Orians et al., 2000
).
It is my goal to review what is known about the secondary chemistry of hybrid plants and to discuss the importance of variation in hybrid chemistry to resistance. Although morphological traits are also highly variable and may contribute to patterns of resistance, this review focuses solely on secondary chemistry. I address the following questions. First, is hybridization more common between closely related but chemically similar parental taxa compared to closely related chemically dissimilar taxa? Second, what are the patterns of qualitative and quantitative variation in hybrid chemistry and what do we know about the genetic mechanisms underlying the patterns? Third, how might chemical variation among hybrids influence the ecology and evolution of plant-herbivore interactions?
For the purposes of this paper, I adopt Arnold's (1997)
definition of hybridization: "the successful mating in nature between individuals from two populations or groups of populations which are distinguished on the basis of one or more heritable characters." I use this definition because it avoids the pitfalls associated with delineating species and directs attention to which populations are being compared, and how they differ. Nevertheless, this review uses data from hybrids between taxa considered to be different biological species because most studies of the secondary chemistry of hybrids have focused at this level. The chemistry of alloploid, polyploid, F1, F2, backcross, and later generation hybrids are reviewed. In addition, I discuss the chemistry of hybrid-derived species—species that are recognized as independent but have been shown, using molecular data, to have originated via hybridization between two other species.
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HYBRIDIZATION AND CHEMICAL SIMILARITY OF PARENTAL TAXA |
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TOPABSTRACTINTRODUCTIONHYBRIDIZATION AND CHEMICAL...PATTERNS OF CHEMICAL VARIATIONIMPLICATIONS FOR PLANT-HERBIVORE...CONCLUSIONLITERATURE CITED |
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suggest that chemical similarity between parental taxa does not appear to be a prerequisite to successful hybridization. In fact, there are a number of excellent examples of hybridization between species that differ dramatically in secondary chemistry (Alston and Simmons, 1962
; Connor and Purdie, 1976
; Crins, Bohm, and Carr, 1988
; Huesing et al., 1989
; Spring and Schilling, 1990
; Buschmann and Spring, 1995
; Orians and Fritz, 1995
). For example, hybridization is common between two chemically distinct willow (Salicaceae: Salix) species: one that produces phenolic glycosides in its leaves and one that produces condensed tannins in its leaves (Fritz, Nichols-Orians, and Brunsfeld, 1994
; Orians and Fritz, 1995
). Also, Helianthus annuus (Asteraceae), a sunflower species that has foliar glandular trichomes that contain sesquiterpene lactones (STLs), hybridizes naturally with H. petiolaris, a species that lacks foliar glandular trichomes (Spring and Schilling, 1989
; Rieseberg, 1991
). Although both these species produce STLs in their flowers, the major STLs belong to different groups (the niveusin and argophyllin types in H. annuus and the budlein type in H. petiolaris). These two species of sunflowers have apparently hybridized naturally for thousands of years and resulted in the evolution of three hybrid-derived species (Rieseberg, 1991
; Rieseberg et al., 1996
).
Although chemical similarity does not appear to dictate patterns of hybridization, hybridization is nonrandom. Hybrids are more common in some plant groups than others (Ellstrand, Whitkus, and Rieseberg, 1996
). For example, hybrids are frequently found in Asteraceae, Poaceae, Rosaceae, Salicaceae, and Scrophulariaceae, but rare in Brassicaceae and Solanaceae (Ellstrand, Whitkus, and Rieseberg, 1996
). In general, stabilized hybrids are most common in outcrossing perennials that exhibit vegetative spread and are insect pollinated. Nevertheless, many annuals hybridize.
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PATTERNS OF CHEMICAL VARIATION |
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TOPABSTRACTINTRODUCTIONHYBRIDIZATION AND CHEMICAL...PATTERNS OF CHEMICAL VARIATIONIMPLICATIONS FOR PLANT-HERBIVORE...CONCLUSIONLITERATURE CITED |
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; Harborne and Turner, 1984
; Rieseberg and Ellstrand, 1993
). Chemosystematics began in earnest in the 1950s, and the number of studies peaked in the 1960s and 1970s, but systematists today rely more on molecular sequences and less on secondary chemistry. Because most of the data have been collected by systematists, there are limits to the database from which I have drawn. First, most researchers focused on the expression of flavonoids, largely because they are stable and variable. However, many flavonoids are pigments and UV screens and generally not considered highly bioactive. Only a few studies have looked at other phenolics, terpenes, alkaloids, and isothiocyanates. Second, most studies report only whether a given chemical is present or absent. This is because researchers typically look at spots on a chromatography plate or peaks from gas chromatography or high-performance liquid chromatography outputs. Therefore, we know more about qualitative than about quantitative chemical variation in hybrids. Third, very few studies have attempted to determine the mechanisms behind the patterns of chemical variation. These limitations reduce our ability to predict which hybrids will be more or less variable, or how hybrids would differ in susceptibility to herbivores. Nonetheless, patterns that have emerged show a fascinating array of chemical variation that is likely ecologically and evolutionarily important.
Qualitative variation
Qualitatively, the chemistry of hybrids is quite variable, even among F1 hybrids. A partial review of the literature indicates that hybrids typically express parental chemicals, but, in a number of hybrids, parental compounds were missing or novel compounds were present (Table 1). Of the 80 hybrid crosses that were examined for both parental and novel chemicals, at least one specific compound was missing in 60% and at least one novel chemical was found in 40% of the crosses (Table 1). Rieseberg and Ellstrand (1993)
calculated the frequency for all chemicals identified. They show that of the chemicals produced by parents and their F1 hybrids, the majority of chemicals in the hybrids are of parental origin (68%), 27% of parental chemicals are lost, and 5% of the chemicals in hybrids are novel. Interestingly, the frequency of novelty was 8% in later generation hybrids and even higher (18%) in hybrid-derived species.
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; Chew and Rodman, 1979
; Seaman and Mabry, 1979
; McKey, 1980
; Berenbaum, 1983
; Crins, Bohm, and Carr, 1988
; Stipanovic et al., 1994
; Buschmann and Spring, 1995
). Finally, disruption of regulatory genes following hybridization can cause a shift in where the chemical is produced (Levy and Levin, 1974
). For example, Alston and Simmons (1962)
showed that chemicals specific to the flower of one parental species (Baptisia viridis) were absent in hybrid flowers, but were expressed in hybrid leaves. Preliminary evidence from Helianthus (Asteraceae) also indicates that one sesquiterpene lactone (STL C) produced only in flowers of H. petiolaris is present as the major peak in the leaves of H. petiolaris x H. annuus hybrids (Table 2; Orians, unpublished data). Overall, I found evidence of intermediacy, dominance, novelty (new to the system and shifts in location), and loss in this hybrid system (Table 2).
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; Smith and Levin, 1963
; Levin, 1967a, b
; Belzer and Ownbey, 1971
; King, 1977
; Buschmann and Sprint, 1995
; Veit et al., 1995). For example, Belzer and Ownbey (1971)
looked at the expression of >100 flavonoids in hybrids of several species of Tragopogon (Asteraceae) and found no novel chemicals in the F1 hybrids. Veit et al. (1995) found only one novel phenolic (of 62) in five different hybrid lines of Equisetum (Equisetaceae). Novel phenolics are also very rare in alloploid Phlox (Polemoniaceae, flavonoids) and Asplenium (Aspleniaceae, flavonoids) and only slightly more common in Dicentra (Fumariaceae, flavonoids), Dubautia (Asteraceae, flavonoids), and Phaseolus (Fabaceae, flavonoids) (Schwarze, 1959
; Smith and Levin, 1963
; Levin, 1966
; Fahselt and Ownbey, 1968
; Belzer and Ownbey, 1971
; Crins, Bohm, and Carr, 1988
). In contrast, novel chemicals are common in polyploid hybrids of Phlox and hybrids of Helianthus (Asteraceae, sesquiterpene lactones, STLs) (Levy and Levin, 1974
; Altman, Stipanovic, and Bell, 1991; Stipanovic et al., 1994
; Buschmann and Spring, 1995
; Table 2). In tetraploid hybrid Phlox, at least five novel compounds have been identified (Levy and Levin, 1974
), and in sunflowers a total of 16 STLs were found in Helianthus annuus, H. debilis, and their F1 hybrids, and three of those (19%) were novel (Buschmann and Spring, 1995
).
Three conditions may favor the generation of novel compounds. First, pathway elaboration (leading to novelty) may be more common if one or both parental taxa produce enzymes capable of modifying the basic skeleton of the other parent (sensu McKey, 1980
). If true, novelty might be more common if the parental taxa have chemical similarities. Second, novelty may be more common for plants that produce chemicals in specialized cells, such as glandular trichomes or flowers. Disruption of the regulatory pathway upon hybridization could alter gene expression and result in the displacement of these cells to a different part of the plant. Both these conditions exist in sunflowers. Parental sunflowers usually contain multiple types of STLs, all of which are produced in glandular trichomes and/or flowers (Table 2). Further studies are needed to determine the robustness of this relationship. Third, there is some evidence that novelty is more common in polyploids than alloploids (Geissman and Matsueda, 1968
; Levy and Levin, 1974
; King, 1977
; Seaman and Mabry, 1979
; Harborne and Turner, 1984
; Rieseberg and Ellstrand, 1993
). For example, novel flavonoids are common in Phlox tetraploid hybrids but rare in diploid hybrids. This may represent complex genetic rearrangement during the formation of polyploids (Levy and Levin, 1974
). Further comparisons of polyploid and diploid hybrids are needed to determine whether this pattern holds true.
As described earlier, novelty is less common in first-generation hybrids than later generation hybrids (Harney and Grant, 1963
; Belzer and Ownbey, 1971
; Crins, Bohm, and Carr, 1988
; but see King, 1977
; reviewed by Rieseberg and Ellstrand, 1993
). For example, none of the Tragopogon balanicus x T. pterodes F1 hybrids contained novel flavonoids, but four of 16 flavonoids (25%) were novel in the F2 generation (Belzer and Ownbey, 1971
). Crins, Bohm, and Carr (1988)
found that six of 20 flavonoids (30%) were novel in later generation hybrids of Dubautia (Asteraceae), while only one flavonoid (5%) was novel in the F1 generation. The greater frequency of novelty in these later generation hybrids could be due to further segregation of alleles at multiple loci.
Although relatively few data are available, novelty is frequent in hybrid-derived species (27% of hybrid chemicals) (Levin, 1966
; Wolf and Denford, 1984
; Spring and Schilling, 1989
; reviewed by Rieseberg and Ellstrand, 1993
). For example, H. anomalus and H. deserticola, both hybrid-derived species of H. annuus and H. petiolaris, produce novel STLs (Spring and Schilling, 1989
). Specifically 26 different STLs have been found in the four species and eight of the STLs (31%) are unique to the two hybrid-derived species. (However, a third hybrid-derived species, H. paradoxus, does not produce any STLs whatsoever.) Levin (1966)
also found novel phenolics in hybrid-derived species of Phlox, even though F1 hybrids do not have any. The presence of novel compounds in hybrid-derived species could reflect higher survival of the early generation hybrids that contain novel chemicals. Alternatively, the novel chemicals could have arisen after the hybridization event due to the gradual accumulation of mutations.
Quantitative variation
Although few studies have quantified chemical variation, patterns are emerging. When parental chemicals are expressed in hybrids, most are either expressed at concentrations similar to one of the parents or at intermediate concentrations (33 and 29%, respectively) (Table 3). Some are overexpressed (19%), while others are underexpressed (14%) (Table 3). However, the relative concentrations of chemicals in hybrids may vary among crosses (Levy and Levin, 1974
; Orians et al., 2000
). For example, Orians et al. (2000)
found that the concentrations of condensed tannin and two phenolic glycosides are more variable in F1 hybrids of S. sericea x S. eriocephala than in either parental taxon. As would be expected, the chemistry of F2 recombinant hybrids is even more variable (Connor and Purdie, 1976
; Hochwender, Fritz, and Orians, in press).
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), and when only one parent produces a chemical, the hybrids usually produce it as well (Parks and Kondo, 1974
; van Brederode, van Wielink-Hillebrands, and van Nigtevecht, 1974
; McMillan, Chavez, and Mabry, 1975
; Crawford and Giannasi, 1982
; Harborne and Turner, 1984
; Gupta, 1994
). For example, Connor and Purdie (1976)
crossed Cortaderia araucana (Poaceae), which produces two triterpene methyl ethers, with C. selloana, which does not, and showed that all F1 hybrids produce both triterpene methyl ethers. They obtained similar results with other crosses and argued that triterpene methyl ether production is either inherited as a single dominant or as a linked dominant. (Note: dominance here is qualitative and does not necessarily mean hybrids have the same concentration as found in one parent. Quantitative analysis would have been required to determine this.) Though less common, some chemicals show Mendelian inheritance and recessive expression. This typically results in the loss of production in the F1 generation, but recovery in the F2 generation (Belzer and Ownbey, 1968). Because these chemicals are not expressed when crossed with nonproducing genotypes, introgression of these resistance traits would be highly unlikely. Quantitatively, many chemicals (29%) are under additive control, i.e., are present at intermediate concentrations (Table 3). Therefore, we would expect, in the absence of chromosomal rearrangement, concentrations of these chemicals to decline with each successive backcross. Introgression of these chemicals also would be unlikely.
Numerous studies have shown that expression in later generation hybrids and backcrosses often segregates according to Mendelian ratios (van Brederode, van Wielink-Hillebrands, and van Nigtevecht, 1974
; Connor and Purdie, 1976
; King, 1977
). For chemicals under dominant control, Connor and Purdie's (1976)
work serves as a nice illustration. As mentioned above, all F1s of C. araucana and C. selloana produced the two triterpenes of C. araucana. As expected, 75% of the F2s, 100% of F1 backcrosses to C. araucana, and 50% of the F1 backcrosses to C. selloana contained triterpene methyl ethers.
Although parental chemicals often show similar patterns of inheritance in a given cross, this cannot be assumed (reviewed by Harborne and Turner, 1984
; Orians et al., 2000
; Table 2). Some chemicals are negatively correlated, especially when derived from different parental taxa. For example, when Torenia fournieri, which produces carotenoids but not flavonoids, is crossed with T. baillonii, which produces flavonoids but not carotenoids, the F1 hybrids produce only flavonoids (Hess, 1971, as cited in Harborne and Turner, 1984
). Harborne and Turner (1984)
refer to this as block expression. In Helianthus hybrids, I have found that those that express STL F lack STL C in their leaves (Orians, unpublished data). This suggests there is a switch or branch point in the biosynthetic pathway with two mutually exclusive alternative end products. The relationship need not be all or none. Salix sericea x S. eriocephala hybrids produce both condensed tannins (produced at high concentrations in S. eriocephala) and phenolic glycosides (produced by S. sericea). In hybrids, increases in one class of compounds result in decreases in the other (Orians and Fritz, 1995
; Orians et al., 2000
), perhaps because they compete for some limiting substrate.
Maternal effects also can be important in determining hybrid chemistry (Harney and Grant, 1963
; Belzer and Ownbey, 1971
; Spring and Schilling, 1990
; Buschmann and Spring, 1995
; Orians, unpublished data). Buschmann and Spring (1995)
found that some STLs were absent in Helianthus debilis x H. annuus hybrids but present in H. annuus x H. debilis crosses, with each hybrid more similar to the maternal taxon. Belzer and Ownbey (1971)
found similar patterns for flavonoids in 20 different hybrid lines. In addition, Spring and Schilling (1990)
found that the amount of novel STLs produced in F1 sunflower hybrids varied as a function of the direction of cross, and Harney and Grant (1963)
found that a novel flavonoid was only present in one of the two reciprocal crosses. Two mechanisms, genetic and nongenetic, could generate these maternal effects. If maternally inherited organelles regulate gene expression, the effect is genetic. However, the maternal environment can affect the cytoplasm, and this in turn can regulate gene expression. This is a nongenetic effect. Few studies have performed reciprocal crosses, and the mechanism of these maternal effects remains unknown. Nonetheless, it is clear that marked differences can occur, and this creates extensive variation among F1 hybrids that may be ecologically and evolutionarily important.
In conclusion, although hybrid chemistry is highly variable, several patterns emerge. First, the chemistry of F1, F2, and later generation hybrids are both qualitatively and quantitatively different. Qualitatively, the occurrence of novel chemicals appears to be more likely in polyploid, F2, and later generation hybrids. Quantitatively, the concentration of chemicals in F1 hybrids may be similar, intermediate, less than or greater than one or both of the parental taxa. In addition, F2 hybrids are quantitatively more variable than F1 hybrids. Consequently, hybrid swarms consisting of multiple hybrid classes would be expected to exhibit the greatest variability. Second, the type and location of chemical produced by the parental taxa appear to have an effect on the occurrence of novel chemicals. Novelty seems to be especially common in hybrids of taxa that produce sesquiterpenes in trichomes, but whether similar patterns emerge with other chemical types needs to be tested. Finally, patterns of inheritance (e.g., dominance, recessive, additive) affect the expression of chemicals in hybrids, and maternal effects modify patterns of expression. Generally, the potential for introgression of chemicals under dominant control would be much higher than for chemicals under recessive or additive control.
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IMPLICATIONS FOR PLANT–HERBIVORE INTERACTIONS |
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TOPABSTRACTINTRODUCTIONHYBRIDIZATION AND CHEMICAL...PATTERNS OF CHEMICAL VARIATIONIMPLICATIONS FOR PLANT-HERBIVORE...CONCLUSIONLITERATURE CITED |
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; Fritz, Nichols-Orians, and Brunsfeld, 1994
; Hanhimäki, Senn, and Haukioja, 1994
; Strauss, 1994
; Messina, Richards, and McArthur, 1996
; Orians et al., 1997
; Fritz, 1999
; Fritz, Moulia, and Newcombe, 1999
; Pilson, 1999
; Whitham et al., 1999
). The patterns of susceptibility are quite variable (Strauss, 1994
; Fritz, Moulia, and Newcombe, 1999
; Table 4). What contributes to such variability? Unfortunately, there have been few mechanistic studies. I suggest that differences in secondary chemistry may mediate hybrid resistance. For example, sesquiterpene lactones are both toxic and show extensive variation among hybrids (Rogers et al., 1987
; Stipanovic et al., 1990
; Buschmann and Spring, 1995
). Below is a brief review of how qualitative and quantitative differences in secondary chemistry could alter the resistance of hybrids to herbivores.
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argue that if the abundance of a host plant producing a novel chemical is highly variable over time, herbivores will be unable to track the plant and adapt to that chemical. Shifts in the location of production may be important as well. Since few herbivores feed on both flowers and leaves, an herbivore is unlikely to be pre-adapted to feed on leaves containing flower-derived chemicals or vice versa. Could novel chemicals decrease resistance? The lack of previous exposure to novel chemicals makes it unlikely that novel chemicals would stimulate feeding by insects. However, if the novel chemical is produced at the expense of a toxic chemical, resistance could be reduced. Thus, to predict the effects of novel chemicals knowledge of their relative toxicity must be examined. How would the loss of parental chemicals affect resistance? The loss of a chemical critical to resistance may increase susceptibility. In contrast, the loss of a chemical important to host selection may result in instantaneous escape. To date, studies examining the effects of novelty and loss have not been examined in any hybrid system. Quantitative differences also may influence which hybrid progeny survive. Overall higher concentrations are likely to be associated with enhanced resistance, especially if parental compounds show codominant inheritance. However, resistance would not be higher if the chemicals increase herbivore resistance to their natural enemies or if the chemicals stimulate attack by their natural enemies.
Plant chemistry can affect herbivores indirectly via affecting their natural enemies (Keating, Yendol, and Schultz, 1988
; Keating, Hunter, and Schultz, 1990
; Turlings and Tumlinson, 1992
). Keating and colleagues showed that high tannin content is associated with increased resistance of gypsy moths to their pathogens. Although, this has not been examined in hybrid systems, it is possible that the abundance of herbivores on hybrid plants also may involve the effects of secondary chemistry on the interactions between herbivores and their natural enemies.
We know that herbivores respond differently to the same secondary compound. A single chemical can, depending on the herbivore, stimulate feeding, deter feeding, or have no effect. For example, Orians et al. (1997)
examined the susceptibility of hybrid and parental willows that differed in chemistry. Salix sericea contains phenolic glycosides in its leaves and S. eriocephala contains tannin but no phenolic glycosides. The hybrids contain both types of chemicals but at intermediate concentrations (Orians and Fritz, 1995
). Orians et al. (1997)
found that willow specialists were stimulated to feed on S. sericea and its hybrid, the generalist was deterred by the phenolic glycosides and only fed on S. eriocephala, and a few herbivores were unresponsive to changes in phenolic chemistry. Messina, Richards, and McArthur (1996)
also showed that species of herbivores differ in their response to sagebrush hybrids, but the role of chemistry was not examined.
Clearly differences in secondary chemistry, whether or not of parental origin, have the potential to affect patterns of hybrid resistance. Therefore, I argue that the secondary chemistry of hybrids is an important force governing the ecological and evolutionary dynamics of plants and their associated herbivores. Four hypotheses are described below with a brief description of the potential role of secondary chemistry.
Chemical diversification hypothesis
Hybridization may be an important evolutionary mechanism for generating novel secondary chemicals. We know that novel chemicals are found in F1 hybrids, and frequently in later generation hybrids. The fact that hybrid-derived species do contain many novel chemicals suggests that selection may favor hybrids expressing novel chemicals.
Can we expect novel chemicals to be more common in some plant groups than others? McKey (1980)
argues that new chemicals commonly form when two separate biosynthetic pathways merge. Although McKey was not referring to hybridization, hybridization causes such mergers. Perhaps, novelty is greater if the parental taxa possess similar pathways. Also there is some evidence that novel chemicals are more common in polyploid than diploid hybrids. Ploidy-level tests could be used to test this. Finally, novel chemicals might be more common in plants that vary in abundance over time because herbivores would be unable to track these plants and adapt to the novel chemicals. If true, the frequency of novel chemicals might be higher in annual than in perennial hybrid-derived species. Comparative research on the chemistry and survival of both hybrid-derived species and early-generation hybrids could be used to test these ideas.
Chemical introgression hypothesis
Introgression of traits between species may depend upon secondary chemistry. If hybrids containing higher concentrations of secondary chemicals are more resistant to herbivores, nonrandom survivorship would lead to a disproportionate expression of these chemicals, and traits genetically linked to them, in future generations. There are a couple of studies that indicate chemical introgression has occurred (excellently reviewed by Harborne and Turner, 1984
).
As discussed earlier, most chemicals segregate in subsequent generations. Introgression is more likely for traits that are under dominant control or are overexpressed than are traits under recessive control (unless linked to traits under dominant control). For example, as predicted for traits under dominant control, only 50% of the (C. araucana x C. selloana) x C. selloana backcrosses produce triterpene methyl ethers. If mortality were complete for those plants lacking the triterpenes, then 50% of each subsequent backcross generation would initially contain the triterpenes and introgression could occur.
If hybrid traits are additive (intermediate) or show incomplete dominance (lower than the midpoint), a gradual decline in each backcross generation would be expected, and introgression would be unlikely. However, despite a general pattern of reduced expression of phenolic glycosides in Salix (Orians et al., 2000)
, Hardig et al. (2000)
present preliminary evidence in support of introgression of a resistance trait (the phenolic glycoside 2'-cinnamoylsalicortin) from Salix sericea to S. eriocephala. How could such a trait have been introgressed? Perhaps variation in the genetics of expression is responsible. Orians et al. (2000)
found that the concentration of 2'-cinnamoylsalicortin in one F1 family (cross) was similar to that of S. sericea. If this were coupled with strong selection favoring the survival of high phenolic glycoside producing crosses, introgression of these defensive chemicals could occur.
Even if later generation hybrids lose the ability to produce a secondary chemical, nonrandom survival early in the process of hybridization could result in the transfer of traits that were genetically linked to those chemicals.
Hybrids-as-bridges hypothesis
Floate and Whitham (1993)
hypothesized that hybrids may facilitate host shifts by herbivores. Are there conditions that would favor host shifts? Since herbivores, especially specialists, use secondary chemistry to locate suitable hosts (Bell and Cardé, 1984
), host shifts might be more common if hybrids express these chemicals. For example, Orians et al. (1997)
showed that specialist willow beetles were stimulated to feed by the phenolic glycosides present in S. sericea and its hybrid. Whether this is facilitating a host shift from S. sericea to S. eriocephala is unknown. In general, host shifts should be more common if the chemical traits are under dominant or additive control and unlikely if the traits are under recessive control. Moreover, the rate of host shift would be rapid if herbivores evolve to use chemicals of the other parental species during host selection.
What conditions might reduce the likelihood of host shifts? Host shifts might be slow, or not occur at all, for herbivores that do not use secondary chemicals in host selection. Also the loss of chemical stimulants or the presence of novel toxic chemicals could delay or prevent host shifts.
Hybrids-as-sinks hypothesis
If hybrids are more susceptible than either parent to herbivores, their presence may slow the evolution of virulence on the parental taxa (Whitham, 1989
). Whitham (1989)
argues that if hybrid plants support higher populations of herbivores they act as an ecological sink for herbivores. They could also act as an evolutionary source if herbivores migrate away from the hybrid zone and mate with individuals that developed on the parental species. In support of this hypothesis, hybrids are often more susceptible than either parent. However, chemical variation among hybrids could determine which hybrids act as ecological sinks.
I suggest that hybrids that have lost an important resistant trait or are chemically intermediate would be more likely to serve as ecological sinks. In contrast, if novel compounds are produced or if resistant chemicals show dominance, hybrids might be less likely to act as sinks for herbivores.
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CONCLUSION |
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TOPABSTRACTINTRODUCTIONHYBRIDIZATION AND CHEMICAL...PATTERNS OF CHEMICAL VARIATIONIMPLICATIONS FOR PLANT-HERBIVORE...CONCLUSIONLITERATURE CITED |
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; Bell and Cardé, 1984
; Bernays and Chapman, 1994
), but a task that is likely to help elucidate the role of plant chemistry in the ecology and evolution of plants and of plant-herbivore interactions. Hybrids are by their nature immensely variable, and we must embrace and study that variability. In this review I have outlined a few factors that are likely to increase the patterns of variability (i.e., ploidy level, hybrid class, the presence of hybrid swarms, and plant taxon) and examined how this variability could lead to nonrandom survival of hybrids and affect their interactions with herbivores.
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FOOTNOTES |
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2 Reprint requests: FAX: 617-627-3805; e-mail: colin.orians{at}tufts.edu
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONHYBRIDIZATION AND CHEMICAL...PATTERNS OF CHEMICAL VARIATIONIMPLICATIONS FOR PLANT-HERBIVORE...CONCLUSIONLITERATURE CITED |
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