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Population Biology |
2Plant Research Department, Risø National Laboratory, P.O. Box 49, DK-4000 Roskilde, Denmark; 3National Environmental Research Institute, Vejlsøvej 25, 8600 Silkeborg, Denmark
Received for publication August 22, 2002. Accepted for publication November 8, 2002.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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x B. rapa) produced many more seeds per plant in pure plots than in mixtures and more seeds in plots when each was present at high frequency. The opposite was true for F1 plants that produced many more seeds than B. rapa in mixtures, but fewer in pure stands. Both vegetative and reproductive interactions may be responsible for these effects. Our results show that the fitness of both parents and hybrids is strongly frequency-dependent and that the likelihood of introgression of genes between the species thus may depend on the numbers and densities of parents and their various hybrid offspring in the population.
Key Words: backcross plants • Brassicaceae • density • fitness • frequency • interspecific hybrids • seed production
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). Genes may be transferred between the species by introgression (transfer of novel genes or alleles from one species to the other via a hybrid), possibly influencing the evolution of the parental species. Complexes of crops, weeds, and wild plants have been studied for a relatively long time, with the earlier studies focusing mainly on the evolutionary relationship of crops and weeds (Harlan, 1965
; De Wet and Harlan, 1975
). Recently, the hybridization between crops and wild plants has received renewed interest, spurred by two important concerns: the environmental effects of growing genetically modified crops (Snow and Palma, 1997
) and the extinction of rare plant species (Ellstrand, 1992
; Levin et al., 1996
; Ellstrand et al., 1999
). If genes inserted by genetic modification (transgenes) are transferred to weedy and wild populations by natural hybridization and introgression, the novel genes and traits may perhaps enable the plants to expand and invade new habitats. Alternatively, the novel traits may lead to maladaptedness and decreased plant fitness.
These single-gene effects are just a subset of the effects that are thought sometimes to accrue by hybridization between crops (transgenic or non-transgenic) and wild species. Locally, rare wild species may be affected by outbreeding depression or hybrid dysfunction and become extinct, or be swamped by cultivar genes to an extent that their specific characteristics disappear (Rhymer and Simberloff, 1996
). Hybrids may, on the other hand, sometimes combine beneficial traits from their parents (Rhymer and Simberloff, 1996
; Arnold et al., 1999
), which may trigger, e.g., the evolution of new invasive genotypes (Ellstrand and Schierenbeck, 2000
).
Fitness of first and advanced generation hybrids is a crucial parameter for predicting the likelihood and dynamics of gene introgression. Contrary to conventional wisdom, an increasing number of studies show that hybrids may sometimes be as fit, or more fit, than their parents (Arnold and Hodges, 1995
; Arnold, 1997
). It is also evident that the fitness of hybrids often depends on the environment in which they occur, especially if the two different species or subspecies are adapted to different conditions. Thus, even in cases where hybridization seems unlikely, because of a strong crossing barrier, special local or temporal conditions may allow occasional hybridization and introgression.
Oilseed rape (Brassica napus L.) and weedy B. rapa are able to hybridize and backcross spontaneously in both experimental plots and cultivated fields (Jørgensen and Andersen, 1994
; Jørgensen et al., 1996
; Mikkelsen et al., 1996
; but see Wilkinson et al., 2000
for different results). A recent study has detected introgression of oilseed rape genes (as opposed to only F1 hybridization) into a weedy Danish B. rapa population (Hansen et al., 2001
). F1 hybrids between the species are sometimes more fit than their wild parents (Hauser et al., 1998b
), whereas second generation hybrids (backcrosses and F2) are somewhat depressed in fitness (Hauser et al., 1998a
). However, different fitness studies have yielded contradictory results (Hauser et al., 1998b
): the seed production per F1 plant in two of our studies was lower than that of B. rapa (Jørgensen et al., 1996
; Mikkelsen, 1996
), but much higher in a third (Hauser et al., 1998b
). In the latter article, we suggested that differences in planting density or composition of the pollen cloud could explain the variation in hybrid fitness. Because the results came from experiments in different years and under different conditions, we could not confidently explain these differences.
In the following experiment, we studied the seed production per plant of B. napus, B. rapa, F1, F2, and various backcrosses grown at three different densities and in several defined mixtures and pure stands. We can thus address if the seed production of F1 and other hybrid classes is indeed as variable as found before and whether plant densities or frequencies of parents and hybrids are responsible for this fitness variation.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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) and is insect and wind pollinated. Brassica rapa (= B. campestris; 2n = 20, AA) is a common weed in Denmark, occurring in oilseed rape fields, along roadsides, and in other disturbed habitats. The species is self-incompatible and pollinated by insects and to some extent by wind (Downey et al., 1980
).
The following plant types were included in the experiment: pure B. napus (abbreviated Bn), pure B. rapa (Br), F1, backcrosses to B. rapa (B1r), F2, backcrosses to B. napus (B1n), and second generation backcrosses to B. rapa (B2r). All hybrid types originated from the B. napus cultivar Drakkar and from three weedy Danish B. rapa populations (Br25, Br45, and Br54 in Hauser et al., 1998a
, b
), and they were all produced by controlled pollinations (see Table 1 for more details). To avoid the inclusion of occasional hybrids among the original B. rapa parents, all plants were checked by morphology and had a pollen viability >90% (see Jørgensen and Andersen, 1994
).
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). After approximately a month (April 1998), when the seedlings were about 5–10 cm tall, they were transplanted into cleared plots within a barley field at Risø National Laboratory. The experimental design is shown in Table 2. All plant types were planted in pure stands at three different densities, ranging from a commonly used field density of oilseed rape (90 plants/m2) to a rather low density (20 plants/m2). Brassica napus, B. rapa, F1, and B1r were also planted in six different mixtures (B1r only in two; Table 2), chosen partly systematically (1 : 1 : 1 : 1, 3 : 1 : 1 : 0, 1 : 3 : 1 : 0, and 1 : 1 : 3 : 0) and partly to present ecologically realistic mixtures, such as in an oilseed rape field (10 : 5 : 1 : 0) and a set-aside field (2 : 4 : 1 : 1). Each mixture was planted at the same three densities as the pure stands. Plants were randomized within mixtures, with the same randomization pattern for each density. The different pure stands and mixtures were grown at least 9 m apart and separated at flowering by a dense barley field; the three densities for each plot type were placed 1 m apart in the same clearing. For logistical reasons, the seven pure stands, six mixtures, and their three densities were only represented once in the experiment (i.e., there was no replication of treatments; see Discussion).
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When pods were ripe, but before they shattered, approximately 20 individual plants per plant type were harvested from each pure stand, mixture, and density. After drying, the pods were threshed and the number of fully developed, round seeds counted per plant. A total of 1440 harvested plants and 3 790 158 seeds were included in the data. Unfortunately, some of the seed bags were lost during harvesting, and data for B. napus and F1 are missing in mixture 1 : 1 : 1 : 1.
Data analysis
Seed production per plant of the various plant types was analyzed by ANOVA (SAS, 1990
) after square-root transformation of the data to improve variance structure and normality. First, we tested for a difference in the average number of seeds produced per plant between the pure plots and the mixtures (including only plant types present in both). A model including effects of plant type (Bn, Br, F1, and B1r), density (continuous), plot type (pure or mixture), and their interactions was used for this test. Next, we tested if average seed production was different in the various mixed plots (i.e., excluding pure plots), using a model including effects of plant type, density (continuous), mixture, and their interactions. We also tested if the seed production per plant of a given plant type varied according to its frequency in the mixtures (continuous; single regressions for each plant type) and if seed production was additionally influenced by the frequency of other plant types present (multiple regressions). Finally, we tested if the plant types in the pure plots differed in seed production, using a model with effects of plant type, density, and their interactions.
Most of the models had significant interactions when analyzed. In all cases, additional analyses of subsets of the data were performed (using the same model, but excluding the effect used for subsetting). At the most detailed level, differences in seed production between plant types were tested for all combinations of plot type and density. Tukey's test was used for tests of significant mean effects.
In order to summarize interactions between the plant types present in both mixtures and pure stands, we estimated their "competition coefficients" from a hyperbolic competition model (using data from both pure plots and mixtures). The model of Damgaard (1998)
was generalized to four different interacting plant types:
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Despite large variation, the seed production of all hybrid classes was relatively high compared to their weedy parent, B. rapa. In the pure plots, only F1 hybrids produced fewer seeds than B. rapa (significantly different for all densities combined) whereas the other hybrid types were not significantly different from B. rapa. In the mixed plots, F1 hybrids produced significantly more seeds than B. rapa, whereas B1r produced fewer seeds (Fig. 1).
The competition coefficients of B. napus, B. rapa, F1, and B1r are shown in Table 6. The seed production per B. napus plant was depressed more by F1 than by other B. napus plants, whereas the presence of B. rapa to some nonsignificant degree benefited the seed set of B. napus. The seed production per B. rapa plant was depressed when growing together with B. napus and F1, whereas the seed production per F1 plant increased when growing together with B. napus and B. rapa. The effects of B1r plants on the seed production of the other plant types was not strong and not significantly different from unity.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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): seed production by B. rapa was strongly suppressed by growing in mixtures, and seed production by the F1, in all but two of the mixed plots, was higher than B. rapa.
Previous studies by our group have shown that seed production by F1 hybrids may change from being higher than B. rapa, to being lower (discussed by Hauser et al., 1998b
). We suggested (Hauser et al., 1998b
) that different planting densities or compositions of the pollen cloud could be responsible for this. We can now clearly refute that planting density by itself is responsible for the change in relative seed production. In the present experiment, seed production of F1 in a given mixture did not change much relative to B. rapa over the three densities used (including the densities of the former experiments).
Composition of the pollen cloud is more likely to cause the observed variation in seed production. In the pure plots, B. napus and B. rapa receive only pollen from conspecific individuals (although pollen from other plant types sometimes may have flown in from other plots; see later), have a high fertilization success, and produce zygotes with a high rate of survival to mature seeds (Hauser et al., 1997
, 1998a
). In the mixed plots, some of the ovules on B. napus and B. rapa are fertilized by heterospecific pollen or by pollen from F1 and backcross plants. The resulting F1 or backcross zygotes have a lower probability of survival, especially when competing against conspecific zygotes. For example, in pods containing both conspecific and heterospecific zygotes, the survival of B. rapa () x B. napus zygotes is about 50% compared to pure B. rapa, and the survival of B. napus () x B. rapa zygotes is about 15% compared to B. napus zygotes (Hauser et al., 1997
). Reproductive interactions can thus explain why the various parental plants produce fewer seeds in mixed plots and in mixtures with low proportions of themselves.
In contrast, F1 plants growing in pure stands produce F2 zygotes with a rather low survival to mature seed (58%, Hauser et al., 1998a
). In the mixed plots, some of the zygotes produced in F1 pods will result from backcrosses and have a higher survival (F1 x B. rapa, 75%; but F1 x B. napus, 55%; Hauser et al., 1998b
; however, these survival estimates come from single donor crosses and may be different in pods of mixed parentage). Reproductive interactions may thus also explain (to some extent) why the seed production of the F1 is greater in mixed than in pure plots and in plots with low frequencies of themselves.
An alternative explanation for the different frequency responses is vegetative competition. F1 plants, and to a lesser degree B. napus, are very plastic and able to grow very large and branch profusely (T. P. Hauser, unpublished observations). When growing in mixtures, they may suppress the vegetative growth of other plant types, while increasing in size themselves. Because larger plants produce more seeds, seed production by F1 would increase in mixtures, while seed production of other types would decrease. Supporting the hypothesis of vegetative competition, F1 plants produced more flowers than B. napus and B. rapa in a parallel experiment with plant mixtures (Pertl et al., 2002
), indicating their larger size and competitive ability. The effects of vegetative and reproductive interactions are not mutually exclusive and may operate at the same time. If F1 plants grow larger in mixtures, they produce more flowers that can produce more seeds. At the same time, more pollen is produced that can fertilize other plant types and depress their seed production.
Backcross plants (B1r) strongly reduced their seed production in mixed plots. This reduction may be due to an inferior ability of the plants to compete vegetatively against B. napus and F1, perhaps caused by their aneuploid chromosomal constitution (20 A + 0–9 C). Aneuploid individuals are known to be less vigorous and are thus elected against (Fantes and Mackay, 1978
; Metz et al., 1997
; Lu and Kato, 2001
). It may also be partly caused by abortion of zygotes pollinated by B. napus and F1 plants in the mixtures, but no data are available on this.
Seed production as a fitness measure
In our experiment, seed production per plant was used as a fitness measure. The importance of seed production for overall fitness is indicated by the experiments of Hauser et al. (1998a
, b
), where seed production per plant explained 93% of the variation in estimated fitness among plant types (Bn, Br, F1, F2, B1r, and B1n; this fitness estimate included, in addition to the seed production parameters, zygote survival to mature seeds and plant survival in the field). However, experimental procedures and different environmental conditions may have affected seed production in the present experiment, and fitness components other than seed production may have an important influence on the fitness realized under natural conditions.
Because of limits on resources, our design did not include replication, i.e., pure plots, mixtures, and their densities were only represented once. We judged that it was more important to have a range of different mixtures and plots large enough to allow the reproductive interactions to develop realistically than to have fewer mixtures and several smaller replicate plots that would probably be too small to develop the differences in pollen composition that affect seed production. Also, unintended pollen flow between mixtures and pure stands (across the barley field that separated the plots) would have a larger influence on reproduction within plots, if these were smaller. Without replicates, however, environmental changes over the field and among plots could lead to biased results on the effects of density and frequency. The field was chosen because of its homogeneity with respect to soil, slope, and agronomic properties (according to the farm manager at the Risø experimental farm). And our main results, that the plant types respond very differently to growing in mixtures and to their frequencies in the mixtures, are very unlikely to result from environmental variation. As all plant types were present in all sections of the field (in either pure plots or mixtures), we would only get these results if the different plant types responded very differently to the environment. In our experience, they do not do so.
Pollen may to some extent have flown among mixtures and pure stands, across the separating barley field. However, the incoming pollen would most likely only change the composition of the fertilizing pollen to a minor degree. Even if pollen may be transported over large open distances to male sterile bait plants, its contribution to seed production within male fertile stands is rather low (Simpson et al., 1999
), as pollen production is so high and competition therefore so strong locally.
We planted seedlings at about the same developmental stages and replaced dead plants during the first month. Seed processes and early plant survival are thus not influencing our results. As discussed by Landbo and Jørgensen (1997)
, F1 offspring may be killed by weeding in well-managed fields because of their low seed dormancy. But we do not know how their low dormancy affects fitness in less intensively managed fields and outside fields. Plant survival after emergence was not measured in this experiment, but it is often fairly high under field conditions (Hauser et al., 1998a
, b
).
In spite of their high seed production, hybrid Brassicas produce pollen with rather depressed viability (e.g., F1, ca. 46%; B1r, 43%; F2, 48%; Hauser et al., 1998a
, b
), and there is strong selection against heterospecific pollen and zygotes (Hauser et al., 1997
). In a parallel experiment to determine the paternity (B. napus, B. rapa, or F1) of seeds produced by B. rapa (Pertl et al., 2002
), only very few seeds were sired by F1 and almost only if B. rapa were growing completely surrounded by F1 plants. F1 would most likely have a very low paternity among seeds produced by B. napus, too, but this situation has never been studied. Even if F1 hybrids are very fit with respect to seed production, especially in mixtures, their male fitness (paternity) is probably very low.
Using seed production per plant as a fitness measure ignores that the seeds could be inviable. Only round, fully developed seeds were counted in our experiment, and our data thus excludes those that are aborted early in development. Results from Landbo and Jørgensen (1997)
show that F1 seeds from controlled pollinations with similar plant material and seeds from F1 hybrids that grew together with B. rapa (i.e., backcross and F2 seeds) are mostly viable (tetrazolium tests) and as viable as seeds collected on wild B. rapa.
Hybrid fitness
Our findings have important implications for the understanding of hybridization and introgression. First of all, they contradict the common notion that interspecific hybrids are generally less fit than their parents (Arnold and Hodges, 1995
; Rieseberg, 1995
; Arnold, 1997
). Female fitness of the F1 hybrids, as estimated by their seed production, was higher than their weedy parent over a large range of mixtures and densities; it was even higher than their cultivar parent at high density. All other hybrid classes (F2 and backcrosses) were as fit, or almost as fit, as B. rapa. Our study adds to the increasing list of species complexes in which hybrids seem to be doing fine and where gene exchange across species seems to be relatively common (Arnold and Hodges, 1995
; Arriola and Ellstrand, 1997
; Emms and Arnold, 1997
; Burke et al., 1998
; Vila and D'Antonio, 1998
; Parris, 1999
; Fritsche and Kaltz, 2000
).
In contrast to female fitness, male fitness of F1 hybrids was very low, as found in a simultaneous paternity experiment using similar design and plant material (Pertl et al., 2002
). Female and male fitness of F1 hybrids, and probably of other hybrid classes, may thus be very different, even in hermaphrodites. A male gamete has to pass through many more selective barriers from gamete formation to fertilization than a female gamete (pollen germination on the stigma, pollen tube growth, competition with other pollen, micropyle penetration, etc.). Our guess is that male fitness of plant hybrids often is depressed even when female fitness is relatively high.
Another important implication of our study is that the fitness of hybrids may be strongly frequency dependent. It is well documented that environmental conditions may affect hybrid fitness (Anderson, 1948
; Arnold, 1997
; Rieseberg and Carney, 1998
; Campbell and Waser, 2001
), but we were surprised that fitness was so strongly influenced by the composition of the population. The relative fitnesses of B. rapa and F1 in our experiment changed completely between the pure and mixed plots. The frequency response of various hybrid classes may even be very different, as shown by the F1 and B1r in our experiment. Another example of frequency-dependent hybrid fitness has been reported by Parris (1999)
. Arnold and Hodges (1995)
pointed out that pooling different hybrid classes may lead to erroneous conclusions on hybrid fitness. Our results verify and extend this by showing that hybrid classes not only have different fitnesses, but they also have different frequency responses in mixed populations.
It is important to note that the fitness of parental plants is also frequency dependent. The parents in our study were significantly less fit in the mixed plots and in the plots where they only occurred at low frequencies. Thus, hybrids may be more or less fit than their parents, but the parent's fitness also changes in contact with hybrids. Arnold (1997)
emphasized that hybridization sometimes occurs even between species with strong barriers to reproduction. Our results suggest that special mixtures of parents and hybrids may be responsible for some of these rare events.
Our initiative for this study came from consideration of the possibility for introgression of transgenes from oilseed rape to weedy B. rapa. The high female fitness of F1 and advanced generation hybrids suggests that genes are likely to introgress from the cultivar to the weed. But our results also show that the likelihood of hybridization and introgression is strongly dependent on local frequencies of the parents and different hybrid classes. Knowing these processes, we can point to the most likely introgression routes: F1 plants are most likely to transfer genes to the next generation via seeds if they grow at low frequencies among B. rapa plants, probably a common situation in Danish fields. In contrast, transmission of genes from F1 plants to B. rapa via pollen is biologically much more difficult and only likely if F1 plants occur in much higher frequencies than B. rapa, a rather unusual situation.
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FOOTNOTES |
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4 Author for reprint requests (thure.hauser{at}risoe.dk
)
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LITERATURE CITED |
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