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Spontaneous hybridization among crops and their wild relatives may promote the rapid evolution of weeds (Ellstrand et al., 1999). As recent advances in genetic engineering and breeding have introduced novel, transgenic traits into crops, ecologists have asked whether subsequent gene flow could lead to the introgression of dominant, single-gene traits into populations of wild relatives that occur near crops (e.g. in rice, Gealy et al., 2003; sunflower, Snow et al., 2003; squash, Fuchs et al., 2004). Transgenic traits such as resistance to diseases, herbivores, and insects could enhance fitness in some cases and might allow weedy relatives to become more abundant (Snow et al., 2003). Meanwhile, little is known about the potential for complex, quantitative crop traits to enhance the fecundity of wild relatives. Although hybridization with some cultivated plants may reduce the fitness of weeds in natural environments (Stewart et al., 2003), possible benefits of crop–wild hybridization for weeds suggest this phenomenon should not be overlooked (Boudry et al., 1993; Miura & Terauchi, 2005; Campbell et al., 2006). Studies of advanced-generation hybrids find that some interspecific hybrid genotypes persist for multiple generations under certain environmental conditions and therefore long-term gene introgression is possible (Lexer et al., 2003). Introgression may lead to trait combinations that enhance fecundity, competitiveness, and/or pest resistance, and these advantageous genotypes may be able to invade new habitats because of their superior weediness (Rhymer & Simberloff, 1996; Ellstrand & Schierenbeck, 2000; Hauser et al., 2003; Whitney et al., 2006).
Performance measures of late-generation hybrids under ‘realistic’ environmental conditions are fundamental to understanding how crop–wild hybridization may alter the phenotype and fecundity of weeds (Lexer et al., 2003). Superior performance of crop–wild hybrids has been detected in a few cases where fecundity, number of flowers, or above-ground biomass were used as estimates of lifetime fitness (Klinger & Ellstrand, 1994; Pertl et al., 2002; Vacher et al., 2004). Although examples of superior performance of hybrids are rare, a growing number of studies show that hybrid fitness depends on genotype, generation, and environment (Campbell et al., 1998; Hauser et al., 2003; Lexer et al., 2003). However, most studies involve only early generation hybrids that may display either heterosis, a transient condition that may overestimate the probability of persistence of crop genes within weed populations (reviewed in Arnold & Hodges, 1995; Arnold, 1997), or outbreeding depression, a transient condition that may underestimate the probability of persistence of crop genes within weed populations (Ellstrand, 1992).
The fecundity and resulting evolutionary impact of crop–wild hybrids may depend on their ability to compete with wild relatives, given that crop allele introgression will inevitably lead to populations composed of both wild and crop–wild hybrid plants (Vacher et al., 2004). Predicting the probability of crop allele introgression and the population dynamics of weeds may be accomplished by modeling plant competition with individual performance values derived from plant competition studies (Pascual & Kareiva, 1996; Damgaard, 1998). Many studies have attempted to estimate hybrid success under competitive conditions (Halfhill et al., 2005; Mercer, 2005; for more examples, see the Discussion) and often conclude that, based on the relative number of seeds produced per plant, hybrids are less competitive or equally as competitive as wild taxa (but see Hauser et al., 2003). Alternatively, the effect of competition on the population growth rates of crop–wild hybrids and wild plants may be predicted using mathematical models to provide insights into the long-term evolutionary impact of introgressed alleles (Volterra, 1926; Damgaard, 1998; Hauser et al., 2003).
Many studies of plant competitive ability, fecundity, and invasiveness have attempted to detect the life-history strategies that contribute to successful competitors and invaders (Rejmánek & Richardson, 1996; Gerlach & Rice, 2003). One approach involves comparative studies of weedy and nonweedy species (Baker, 1965; Crawley et al., 1996; Williamson & Fitter, 1996; Sutherland, 2004). However, it may be more meaningful to examine the life-history traits of a group of closely related species to determine which traits contribute to weediness (Mack, 1996; Grotkopp et al., 2002). Specifically, identification of successful weed life-history strategies may depend on the complex interactions between the weed phenotype and environment. Small differences in the life-history traits of a plant, such as the timing of germination or reproduction, may interact with the competitive environment to influence at a small scale, plant fecundity, and at a larger scale, plant distributions and abundance (Sans et al., 2004).
In this study, we used plants from experimental populations of the weedy annual Raphanus raphanistrum and its crop–wild hybrid offspring (R. raphanistrum × Raphanus sativus) to investigate both the effects of competition on hybrid fitness and how fitness differences between wild and hybrid plants may be altered by variation in the competitive environment. Raphanus raphanistrum is a well-established model system in studies of plant evolution and ecology that has been used to evaluate the ecological consequences of crop-to-wild gene flow (Klinger et al., 1991; Snow et al., 2001; Hegde et al., 2006). We estimated the competitive ability of two ‘biotypes’, wild R. raphanistrum and advanced-generation crop–wild hybrids, using a response surface competition experiment. We also explored how life-history traits and fecundity were affected by varying density and biotype frequency. We used a path analytic approach to test a model of causal interactions among life-history traits and fecundity (Shipley, 2000), derived from a combination of previous path analytical studies of Raphanus (Scheiner et al., 2002) and our own experience with this system. We discuss the potential implications of these processes for the introgression of crop alleles into weed populations.
Specifically, we asked the following questions:
What is the lifetime fecundity of crop–wild hybrids compared to their wild relatives, and under which competitive conditions is the relative fecundity of advanced-generation hybrids maximized?;
Is crop–wild hybrid radish as competitive as its weedy progenitor, as measured by competition coefficients?;
Does competition affect the relative fecundity of wild and hybrid plants by altering their size or age at reproduction?.
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Our study shows that competitive conditions may increase the evolutionary impact of advanced-generation crop–wild hybrids through indirect effects on life history traits. These traits include age and size at flowering, and seeds per fruit (i.e. clutch size). Based on lifetime fecundity, hybrids had less competitive impact on wild plants than the competitive effect of wild plants on hybrids (Table 1, Fig. 3). As expected, increased density reduced the fecundity of wild and hybrid plants (Table 1), a result consistent with previous competition studies of Raphanus (Uthus, 2001; Wolfe & Mazer, 2005). However, increasingly competitive conditions had a greater negative effect on the lifetime fecundity of wild plants than on hybrid plants (Table 1: Biotype × Density × Hybrid freq. Interaction). Therefore, relative hybrid fecundity was maximized under more intense competitive conditions (Fig. 3).
A common purpose of competition experiments is to anticipate the dynamics of natural plant communities. The probability of species coexistence is estimated using a competition model under a range of simplified environments and is encapsulated by the competition coefficient parameter (Damgaard, 1998; Inouye, 2001). Estimating competition coefficients may improve predictions of persistence of crop alleles within weedy populations across generations and the success of hybrids within weedy populations over a growing season. Yet, despite the abundance of empirical studies on the effect of competition on crop–wild hybrid fecundity (Table 3), only one other study has expressed hybrid competitive ability in terms of competition coefficients (Hauser et al., 2003). Hauser et al. (2003), in contrast to our study, found that the competitive ability of F1 hybrids (Brassica rapa × Brassica napus) was greater than that of the wild parents (cwild,hybrid = 5.80, chybrid,wild = 0.12). High competitive ability of early generation hybrids will be important to the early stages of crop gene introgression; however, the persistence of crop genes within weed populations also depends on the competitive ability of advanced-generation hybrids when growing near its wild relative as well as with other weed species (Vacher et al., 2004). Further, the accuracy of competition models in predicting community dynamics will be limited by the ability of experimental designs to represent the complexity of field conditions, including differential herbivory, seed longevity, emergence dates, and multispecies communities.
Table 3. Summary of 12 competition studies of fecundity of crop-wild hybrids relative to their wild parent
|Family||Cultivated spp.||Wild relative||Gen.||Experiment type||Traits measured||Hybrid fitness relative to wild with no/low competition||Hybrid fitness under varying density||Hybrid fitness highest under which type of competition?|
|Asteraceae|| Helianthus annuus 1a || H. annuus ||F1||A||F||Reduced||Higher with competition|| |
| H. annuus 2b || H. annuus||F1||RP||S||No data|| ||Same|
| H. annuus 2b || H. petiolaris ||F1||RP||S||No data|| ||Same|
| H. annuus 3 || H. annuus ||F1||A||S||Reduced||Higher with competition|| |
| Echinacea purpurea 4 || E. purpurea ||F1||A||B, F||Similar||Highest at medium density||Inter|
|Brassicaceae|| Brassica napus 5 || Raphanus raphanistrum ||BC6napus||A||S||Reduced||Higher with competition|| |
| B. napus 5 || R. raphanistrum ||BC6raph||A||S||Similar||Highest at low density|| |
| B. napus 6 || B. rapa ||F1||RS||S, PA||Condition-dependent, Reduced||Frequency-dependent, Higher under low density||See belowe|
| B. napus 7 || R. raphanistrum ||F1||A||B||Reduced||Higher without competition|| |
| B. napus 7 || R. raphanistrum ||F1||A||B||Reduced||Highest at low density|| |
| B. napus 8 || B. rapa ||F1g||RS||S||Condition-dependent||Highest at high density||Inter|
| B. napus 8 || B. rapa ||BC1rapa||RS||S||Density-dependent||Highest at low density||Intra|
| B. napus 8 || B. rapa ||BC1napus||RS||S||Reduced||Highest at low density|| |
| B. napus 8 || B. rapa ||F2||RS||S||Density-dependent||Highest at low density|| |
| B. napus 8 || B. rapa ||BC2rapa||RS||S||Reduced||Highest at intermediate density|| |
| B. napus 9 || B. rapa ||F1||A||B||Greater||Highest at high density|| |
| B. napus 10c || B. rapa ||BC2F2||A||B||Reduced||Higher with competition|| |
| B. napus 11 || B. rapa ||F2||RP||S||Reduced|| ||Inter|
| B. napus 11 || B. rapa ||F2BC1||RP||S||Reduced|| ||Inter|
| B. napus 11d || B. rapa ||F2||RP||S||Reduced|| ||Inter|
| B. napus 11d || B. rapa ||F2BC1||RP||S||Reduced|| ||Inter|
| R. sativus 12 || R. raphanistrum ||F1||A||S||Reduced||Higher with competition|| |
| R. sativus 12 || R. raphanistrum ||BC1||A||S||Reduced||Higher with competition|| |
| R. sativus 13 || R. raphanistrum ||F3h||RS||S||Reduced||Higher with competition||Same|
Highly competitive conditions, such as those one might find in a natural weed population, may facilitate the introgression of crop alleles into weedy populations by increasing the relative fecundity of hybrids (Fig. 3). In the literature, this is a common but under-appreciated result (Table 3). When crop–wild hybrid performance is compared with wild taxa under increasingly competitive conditions, the difference between hybrid and wild genotypes is often reduced by competition (Snow et al., 1998; Uthus, 2001; Guéritaine et al., 2002; Halfhill et al., 2005; Mercer, 2005). However, in this collection of studies, imposing competition on hybrid plants rarely, if ever, reversed the relative performance of hybrids compared with their wild relative (Table 3). That is, hybrids that possessed reduced relative fitness without competition do not exhibit superior fitness under competitive conditions. These results suggests that hybrid success in natural populations is unlikely to be limited by density alone but that hybrid relative fitness may be promoted by increased density.
Although hybrids were generally poor competitors, as indicated by their competition coefficient, their relative performance was enhanced when grown in mixed pots of wild and hybrid plants rather than purely hybrid pots. This, too, is a common result of competition studies (Table 3). Typically, hybrids of several crop–wild complexes, under at least some densities, tend to be more successful, although not superior, under interbiotype vs intrabiotype competition conditions (van Gaal et al., 1998; Pertl et al., 2002; Hauser et al., 2003; Al-Ahmad & Gressel, 2006). Although our analysis of variance was limited to two frequencies (50% and 100%), the path analysis confirmed this trend continues when hybrids are grown under other hybrid frequencies (33% and 66%). Under interbiotype competition, the hybrids initiated reproduction at a smaller size and assumed a more ‘wild-like’ appearance than under intrabiotype competition. These findings suggest that the rate of introgression in wild populations will be highest when hybrids grow in mixed populations. This finding supports previous hypotheses about the evolution of weedy R. sativus in California. Panetsos & Baker (1967) speculated that hybridization with R. raphanistrum allowed cultivated radish to evolve into ‘a highly successful weed’. Recently, Hegde et al. (2006) used field observations, morphological data, and allozyme frequencies to conclude that hybrid populations of crop–wild genotypes have displaced ancestral populations of weedy R. raphanistrum in California. This suggests that the relative fitness of crop–wild hybrids within wild radish populations was sufficiently high so as to promote coexistence of biotypes and crop allele persistence.
Although the effect of competition on the relative fecundity of our crop–wild hybrids was apparent from an analysis of variance, the results of the path analysis contributed several novel insights into the indirect, but causal, consequences of competition on relative hybrid performance via its effects on life history (Fig. 2). While the phenotypic correlations of wild and hybrid plants often responded similarly to density, we were able to detect key differences that may ultimately have led to differences in the response of fecundity to density treatments. Age at flowering in wild plants was more sensitive to changes in density than hybrid plants. The delay in flowering induced by high density in wild plants resulted in a significant decrease in the number of seeds per fruit in wild plants and ultimately a reduction in lifetime fecundity of wild plants. At the same time, size at flowering in hybrids was more sensitive to changes in density than wild plants and was significantly reduced at high densities, suggesting that hybrids tended to advance flowering and increase seeds per fruit and flower production at high density. Therefore, increasing density altered life history, resulting in wild plants that more closely resembled hybrid plants and vice versa. In future studies, it will be important to incorporate more life-history traits, including timing of germination and seedling growth, in order to fully understand the competitive dynamics between wild and hybrid plants within a population (Guéritaine et al., 2003; Hooftman et al., 2005).
Competition had a dramatic effect on the life history of both wild and hybrid plants. Although hybrids began as bigger seedlings they had less competitive impact on neighbors than wild plants. This suggests that competitive dominance may result from different patterns of resource allocation, further reinforcing the idea that changes in life-history are likely to change performance. Another intriguing result, emerging from both path analyses and anova, was that greater density significantly delayed flowering in wild plants but not in hybrids, and that increased density decreases size at flowering more in hybrid plants than wild ones. These results suggest that hybridization may alter both the average phenotype of weeds and the plasticity of those traits (Pigliucci & Kolodynska, 2006).
In summary, we demonstrate through both experimental manipulations and literature review that competition may indirectly impact the relative performance of hybrids and their wild relatives, via its effect on life history, potentially enhancing hybrid fitness in weed populations. We suggest that subsequent competition experiments evaluate those life-history traits most affected by competition and the consequences of plant–plant interactions for the introgression of crop traits into wild populations. Studies that consider the effect of competition on both absolute and relative hybrid fecundity will provide more comprehensive predictions of the ecological consequences of crop gene introgression into wild populations (Damgaard, 1998; Lexer et al., 2003).