SEARCH

SEARCH BY CITATION

Keywords:

  • flowering phenology;
  • invasive plants;
  • life-history traits;
  • seed predation;
  • Ulex europaeus

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgments
  8. References

The genetic variation in flowering phenology may be an important component of a species’ capacity to colonize new environments. In native populations of the invasive species Ulex europaeus, flowering phenology has been shown to be bimodal and related to seed predation. The aim of the present study was to determine if this bimodality has a genetic basis, and to investigate whether the polymorphism in flowering phenology is genetically linked to seed predation, pod production and growth patterns. We set up an experiment raising maternal families in a common garden. Based on mixed analyses of variance and correlations among maternal family means, we found genetic differences between the two main flowering types and confirmed that they reduced seed predation in two different ways: escape in time or predator satiation. We suggest that this polymorphism in strategy may facilitate maintain high genetic diversity for flowering phenology and related life-history traits in native populations of this species, hence providing high evolutionary potential for these traits in invaded areas.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgments
  8. References

The onset and duration of flowering have a dramatic influence on reproductive success of plants. Flowering phenology leading to successful seed production depends on factors that may vary in space and time, such as pollination efficiency, seed predation, resource availability and climatic conditions (Rathcke & Lacey, 1985; Brody, 1997). When a plant species is introduced into a new area, its capacity to reproduce sexually is thus tightly linked to its ability to adapt its flowering time to the new environmental conditions. As the evolutionary potential of a trait is directly related to its genetic variance (Falconer & Mackay, 1996; Lynch & Walsh, 1998), the genetic variation in flowering phenology may be an important component of a species’ capacity to colonize new environments.

Variation in flowering phenology has often been studied along altitudinal or latitudinal gradients. The phenotypic variation observed in natural populations is generally maintained in experimental gardens, demonstrating genetic differentiation (Tarasjev, 1997; Quinn & Wetherinton, 2002; Leger & Rice, 2007). Within populations, plants under seasonal environments usually flower synchronously, because of constraints such as winter frost or summer drought (Ims, 1990; Franks et al., 2007). Despite these climatic constraints, genetic variation for flowering time has been demonstrated within natural populations of several species (e.g. Chao & Parfitt, 2003; Johnson, 2007; Botto & Coluccio, 2007). This genetic variation may be maintained by the heterogeneity of biotic interactions (Elzinga et al., 2007). In particular, the avoidance of seed predation is often in conflict with other selective pressures exerted on flowering times.

Two types of flowering phenology can minimize predispersal seed predation. One strategy is the ‘escape in time’, i.e. producing fruit before (e.g. Mahoro, 2003) or after (e.g. Freeman et al., 2003) the seed predation peak. However, escaping in time can lead to flowering under non-ideal biotic conditions (e.g. fewer pollinators or seed dispersers) or abiotic conditions (e.g. frost or drought). The other strategy is ‘predator satiation’ (Janzen, 1971). In this case, fruits are produced in massive quantities over a short period of time so that the seed predator cannot manage to attack all of them (e.g. English-Loeb & Karban, 1992). However, synchronization of flower and fruit productions can have negative repercussions on pollination or dispersion efficiency (Gomez, 1993). These conflicting selection pressures may lead to the maintenance of genetic variation in timing of flowering and fruiting if all traits cannot be simultaneously optimized, or if different trait combinations lead to similar reproductive success (Rose, 1982; Houle, 1998).

Ulex europaeus L. (Genisteae, Fabaceae) is a good model for studying the diversity of flowering phenology in relation to seed predation. It is native of the Atlantic coast of Europe (Portugal, Spain, France and UK). When introduced to other continents, it has become an aggressive invader that has successfully colonized very different climatic areas, from the mountains of Hawaii to the coasts of Tasmania (Holm et al., 1997; Lowe et al., 2000). Populations in the invaded areas were initially free of any seed predators. Their flowering peak may occur in autumn, winter or spring depending on their altitude and latitude (Hill et al., 1991; Markin & Yoshioka, 1996). Within the native area, variation of flowering time has been studied in natural populations of Brittany (Western France). These populations appeared to be characterized by the coexistence of two main flowering types – a short massive flowering period in spring and an extended flowering period from autumn to spring (Tarayre et al., 2007). We hypothesize that these two main phenotypes correspond to two different strategies that reduce seed predation. Indeed, the main seed predator of this species, the weevil Exapion ulicis, may attack up to 95% of seed pods (Davies, 1928), but lays eggs only in spring (Hill et al., 1991; Barat et al., 2007). The long-flowering plants may partly escape their seed predators in time, while the short-flowering plants may benefit from predator satiation. This polymorphism in strategy may provide this species with high genetic variance for flowering phenology, and facilitate to explain why U. europaeus had the capacity to adapt its flowering period to a vast range of climatic and ecological conditions.

To confirm this hypothesis, it is essential to ensure that the diversity observed in natural populations of the native range is genetically determined, because flowering phenology responds to various environmental stimuli such as solar irradiance and temperature (Rathcke & Lacey, 1985; Nakagawa et al., 2005). We thus set up an experimental study by raising maternal families in a common garden. The aims of this study were (i) to determine if the variability of flowering time, and in particular the bimodality of flowering onset, has a genetic basis and (ii) to check whether this polymorphism is involved in the avoidance of seed predation. This second goal was achieved by (i) exploring the genetic variation of the life-history traits potentially involved in the escape of seed predation, i.e. fruiting phenology, pod density, pod infestation rate, plant height and architecture and (ii) testing genetic correlations among these life-history traits. Based on mixed analyses of variance, we demonstrated genetic differences between the two main flowering types and showed that variation in phenology, seed predation and plant height architecture have a genetic basis. We also found strong genetic correlations among these life-history traits, and confirmed that the two main flowering types avoid seed predation through different strategies. We suggest that these variations provide the species with high evolutionary potential for flowering phenology and related life-history traits. This evolutionary potential may be particularly expressed in situations where seed predators are absent, as is often the case in newly invaded areas.

Materials and methods

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgments
  8. References

Study species

Ulex europaeus (Fabaceae), also known as common gorse, is a spiny hexaploid shrub. It lives for up to 30 years, and its adult height usually varies from 1 to 4 m. Flowers are hermaphroditic and ovaries may bear up to 12 ovules. Pollination depends on large insects such as honeybees or bumblebees (Herrera, 1999; Bowman et al., 2008).

Pods start to form on the previous years’ shoots immediately after flowers have been fertilized. Young pods are green and soft, but grow, harden and turn brown at maturation. They are infested by a specific weevil, Exapion ulicis (Apionidae), and by the larvae of the moth Cydia succedana (Tortricidae), that may eat several seeds per pod and infest up to 90% of a plant’s pods. The life history of E. ulicis has been described by Davies (1928), Hoddle (1991) and Barat et al. (2007). Females lay eggs in early spring within green pods that are 10–35 days old. Larvae develop within the maturing pods, and adults emerge from the ripe pods at dehiscence, about 2 months later. The life history of C. succedana has been described by Sixtus et al. (2007). The larvae can escape before pod dehiscence, but the droppings they leave and the hole they bore are reliable signs of their presence.

Experimental design

The stock of seeds used to create the maternal families was collected from four populations occurring in a radius of 100 km around the city of Rennes (Brittany, France). These populations were regularly monitored from 2000 to 2005, and the flowering type of the plants was well known. We collected seeds in late June 2001 from five mother-plants per population, and chose the mothers to sample both short- and long-flowering plants in all populations (Table 1). This gave us 20 families: 10 families derived from short-flowering mothers and 10 families derived from long-flowering mothers. Seeds were produced by open pollination, and a maternal family consisted of individuals derived from seeds collected from the same mother-plant. Self-fertilization is rare in this species, and we collected only one seed per pod. These maternal families are thus mainly composed of half-sibs, but seeds from selfing or full-sibs may also be present.

Table 1.   Populations of Ulex europaeus sampled in Brittany (France).
PopulationHabitatLong-flowering plants (%)Short-flowering mothers sampledLong-flowering mothers sampled
Château de VauxFallow4232
La RéautéHedge2923
Pointe du GrouinSeaside732
Pointe du MeingaSeaside1023

The seeds were stored at 4 °C until October 2002 to break dormancy, then scarified using a scalpel. The seedlings were grown in pots for 1 year. In November 2003, 10 seedlings per mother-plant were planted in a randomized pattern in a common garden of 700 m2, situated on the University of Rennes campus, with a minimum spacing of 1.20 m between each plant. Ulex europaeus reaches full reproductive maturity at 4 years of age, when the plant can be more than 2 m tall and wide. We obtained between eight and 10 adult plants per maternal family, i.e. a total of 190 individuals.

Flowering and fruiting phenologies, growth

The plants started to flower in 2004–2005. Architectural measurements were taken in June 2005. The three longest branches of each plant were chosen, their length and the angle they formed with a horizontal plane were measured, and the mean values of the three branches were calculated. Flowering and fruiting phenologies were monitored in 2005–2006. The plants were observed every month from September 2005 to May 2006, then every 2 weeks in June and July 2006. The date of flowering onset corresponded with the appearance of the first flowers, associated with the presence of large-sized flower buds. The date of fruiting onset corresponded with the appearance of the first ripe pods associated with the presence of browning pods. Plant height was measured in June 2006; but the plants were too bushy to repeat the architectural measurements taken the previous year.

Pod production

To estimate annual pod production per shoot, several visits were necessary, because the latest pods were initiated after the dehiscence of the earliest pods. At each visit, six shoots per plant were chosen at random. The number of pods they produced was counted as in Tarayre et al. (2007), and the plant mean of these six measurements was calculated. To avoid counting the same pods twice, only the browning or ripe pods were counted. When all the counted pods of the previous visit had fallen off, the same operation was conducted again. This process was repeated up to five times, until the end of fruiting.

To estimate pod density, i.e. the total number of pods per shoot at a given point in time, we had to include both green and brown pods. Pod density in June was thus obtained by adding the values of pods that became mature in mid-June and early July.

Seed predation

To estimate pod content, 30 ripe pods were opened at each visit, when available. We estimated the proportion of infested pods and recorded the number of seeds and seed predators. Flat, rotten or chewed seeds were excluded from the counts.

At each visit, seed predation was estimated by the infestation rate of ripe pods. There were two estimates. The annual infestation rate corresponds to the proportion of infested ripe pods over the entire fruiting season. It was obtained by calculating the mean number of infested pods at each visit, weighted by the number of pods per shoot. We also compared the infestation rate at the same date for all plants. We chose to do it in late June, when the highest proportion of individuals was fruiting synchronously. This measurement corresponds to the infestation rate of pods that were all exposed to the same pool of seed predators.

Statistical analyses

All analyses were performed using sas software (SAS Institute, 2005). The significance of the effects was tested independently for each of the 12 life-history variables, using a mixed-model anova (proc MIXED), in which maternal families were nested within their population of origin, and flowering type of the mother was crossed with the population of origin. Families and populations were treated as random effects. Flowering type was treated as a fixed because it was suspected to be a source of heterogeneity, and both types were sampled in all populations (Table 1). The significance of random effects was determined by comparing the likelihood of the models with and without the random effect, using the chi-square distribution with 1 df (Pinhero & Bates, 2000; Grafen & Hails, 2002). The significance of the fixed effect was determined using type III F-statistics. Infestation rates arcsine-transformed to meet assumptions of normality. The proportion of variance explained by maternal family and population of origin was calculated with proc GLM, using a simplified model where only the random effects were declared.

The correlations were tested with proc CORR, using Spearman’s rank-order correlation coefficient. Genetic correlations were estimated by correlations between family means. Although it has been criticized by Lynch & Walsh (1998), this method appears to be reliable for experiments performed in a common garden (Gardner & Latta, 2008), and is relevant when the goal is to establish the genetic basis of the correlation observed (Astles et al., 2006).

Given the possibility of homogamy, the bimodality of the mothers, the hexaploidy of the species and that the fathers were unknown, it was impossible to calculate reliable estimates of heritabilities.

Results

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgments
  8. References

Flowering and fruiting phenologies, growth

The dates of flowering onset of the 190 adult plants grown from 20 maternal families ranged from September to May, with a peak in April (Fig. 1). The dates when flowering ended were much less variable and ranged from May to June, with an almost perfect negative correlation between the date of flowering onset and flowering duration (n = 190, R = −0.94, P < 10−4): the earlier a plant flowered, the longer it flowered. According to the bimodal distribution observed in natural populations, the 55 plants that began to flower before the end of January will be considered as long-flowering plants, and the 135 plants that began to flower after January will be considered as short-flowering plants. The two types of mother-plants produced different offspring distributions, with short-flowering mothers producing almost only short-flowering offspring, and long-flowering mother producing all flowering types. The distribution observed in the common garden (Fig. 1) does not show the peak of autumn-flowering plants observed in natural populations. This is probably because of a bias in seed sampling: all seeds were collected in late June, and seeds resulting from autumn or winter pollination were not represented.

image

Figure 1.  Distribution of flowering onset (by month) of 190 Ulex europaeus plants grown in a common garden, according to maternal flowering type.

Download figure to PowerPoint

Mature pods were produced between March and July for the long-flowering plants, and between May and July for the short-flowering plants. The onset and duration of the fruiting period were correlated with the onset and duration of flowering (n = 190, R = +0.75, P < 10−4 and R = +0.32, P < 10−4 respectively).

Plant architecture at 3 years of age was very variable: branch angle varied from 0 to 90°, branch length varied from 52 to 165 cm, and these two variables were positively correlated (n = 190, R = +0.64, P < 10−4). Plant height at 4 years of age was highly correlated both with branch length and branch angle at 3 years (n = 190, R = +0.81, P < 10−4 and R = +0.76, P < 10−4 respectively).

Proportion of infested pods

Ripe pods produced before June had no seed predators. Subsequently, the proportion of infested pods increased continuously, both for weevils and moths, with weevils always being more common (Fig. 2a). When seed predators were present, long-flowering plants had a higher infestation rate than short-flowering plants (Fig. 2b). However, short-flowering plants produced pods only during the peak of pod infestation, while long-flowering plants had produced most of their pods before the peak of pod infestation (Fig. 2c). As a consequence, the total infestation rate over the whole fruiting season was similar for the two types of plant (29% for long-flowering plants and 30% for short-flowering plants).

image

Figure 2.  Temporal changes in pod infestation and pod production in Ulex europaeus plants grown in a common garden. (a) Per cent of infested ripe pods (±SE) according to insect species. (b) Per cent of infested ripe pods (±SE) according to flowering type. Numbers above the bars indicate the number of plants that produced ripe pods at a given sampling event. (c) Pod production (mean number of ripe pods per shoot ±SE) estimated from all long-flowering plants (n = 55) and all short-flowering plants (n = 135). No pods were produced after July.

Download figure to PowerPoint

Family and population effects

As the phenotypic correlations among phenological variables and among growth variables were high and significant, we reduced the set of 12 variables to four main variables to describe the distribution of variance among maternal families and populations (Table 2). Differences between populations explained the highest per cent of variance for plant height and infestation in late June, while the maternal family effect explained the highest per cent of variance for flowering duration and pods per shoot.

Table 2.   Descriptive statistics of four life-history traits of Ulex europaeus plants grown in a common garden from seeds collected in Brittany (France).
TraitsMean ± SD*Populations n = 4Maternal families n = 20Individuals n = 190
Min.–max.Variance explained (%) Min.–max.Variance explained (%) Min.–max.Residual variance (%)
  1. All traits were measured in four-year-old plants.

  2. *Standard deviation of the whole sample (n = 190).

Flowering duration (days)81 ± 5567–101534–1353619–25259
Plant height (cm)150 ± 51119–1914166–2102432–25235
Infested pods (% in late June)32 ± 27 19–5430 2–80210–10049
Pods per shoot (annual production)45 ± 24 33–531018–671414–13176

Results of the statistical analysis on all 12 life-history traits are provided in Table 3. Population of origin had a highly significant effect on plant growth and infestation rate in late June, and a lower effect on flowering and fruiting phenology and annual pod production per shoot. Within populations, the maternal family had a strong influence on all variables except pod and seed production. The flowering type of the mother had a significant influence on flowering and fruiting phenologies, but not on any of the other variables studied.

Table 3.   Results from mixed-model anova for 12 life-history traits of Ulex europaeus plants grown in a common garden from seeds collected in Brittany (France).
TraitsEffects
Population (χ²)Maternal family (χ²)Mother’s type (F1,16)
  1. All traits were measured in 4-year-old plants, except branch length and branch angle that were measured in 3-year-old plants.

  2. *P < 5%, **P < 1%, ***P < 10−3, ****P < 10−4.

Phenology
 Flowering onset1.423.2****13.53**
 Flowering duration0.117.4****12.71**
 Fruiting onset4.0*16.4****5.15*
 Fruiting duration1.211.1***2.64
Architecture
 Plant height9.6**45.8****1.66
 Branch length13.4***16.8****4.22
 Branch angle4.8*56.8****0.45
Infestation rate
 Late June8.1**12.9***4.31
 Entire fruiting season0.417.0****0.01
Annual production
 Pods per shoot4.3*2.10.08
 Seeds per pod1.71.20.68
 Seeds per shoot1.41.30.56

Correlations between traits

The correlation coefficients between plant height, flowering onset, annual pod production and infestation rate in late June were always stronger among maternal family means than among individual values (Table 4). There was a positive correlation between infestation rate in late June and plant height; the tallest plants were the most heavily infested. There was a negative correlation between plant height and flowering onset; the tallest plants began to flower earlier. There was a positive correlation between flowering onset and annual pod production, but this correlation was only significant among maternal family means: families that began to flower the latest had the highest annual pod production. A similar result was observed where flowering onset was correlated with pod density in June (n = 20, R = +0.71, P < 0.01).

Table 4.   Phenotypic and among maternal family correlations between four life-history traits of Ulex europaeus plants grown in a common garden from seeds collected in Brittany (France).
 Among individuals (n = 190)Among maternal family means (n = 20)
Plant heightInfestation* ratePods† per shootPlant heightInfestation* ratePods† per shoot
  1. Spearman correlation coefficients and P-values (in parentheses) are provided. Significant correlations are in bold. Correlations between other relevant life-history traits are provided in the text.

  2. *Proportion of infested pods in late June.

  3. †Annual production.

Flowering onset−0.27 (<10−3)−0.48 (<10−4)+0.10 (0.17)−0.42 (0.06)−0.88 (<10−4)+0.55 (0.01)
Pods† per shoot+0.01 (0.99)−0.08 (0.30) −0.08 (0.72)−0.36 (0.11) 
Infestation* rate+0.35 (10−4)  +0.68 (<10−3)  

The most significant correlation was the one observed between flowering onset and infestation rate in late June. The later the flowering onset, the lower its infestation rate in late June. When the two species of seed predators were analysed separately, the correlation among maternal family means between infestation rate in late June and flowering onset was significant for weevils (n = 20, R = −0.87, P < 10−4, Fig. 3a), but not for moths (n = 20, R = −0.41, P = 0.07). To test the influence of predator satiation, we also tested the correlation between infestation rate in late June and pod density in June. This correlation was significant for infestation by weevils (n = 20, R = −0.60, P < 0.01, Fig. 3b), but not by moths (n = 20, R = −0.24, P > 0.10).

image

Figure 3.  Pod infestation by weevils in late June. Proportion of ripe pods infested in late June according to flowering onset (a) and pod density in June (mean number of pods per shoot) (b). Each point represents a maternal family; n = 20.

Download figure to PowerPoint

When infestations rates were considered over the entire fruiting season, neither annual infestation rate by weevils, nor annual infestation rate by moths was significantly correlated with flowering onset (n = 20, R = −0.18 and R = +0.19 respectively, P > 0.10). However, the relationship between infestation rate by weevils over the entire fruiting season and flowering onset could be fitted to a second-order polynomial regression (Fig. 4, n = 20, R = 0.51, F2,17 = 8.88, P < 0.01*****). The moth infestation rate could not be fitted to this type of regression.

image

Figure 4.  Pod infestation by weevils over the entire fruiting season. Relationship between flowering onset and the proportion of ripe pods infested by weevils over the entire fruiting season, fitted to a second-order polynomial regression. Each point represents a maternal family; n = 20.

Download figure to PowerPoint

Discussion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgments
  8. References

Variability of the traits studied

The results obtained in the common garden show that the variability previously observed in natural populations of U. europaeus for flowering and fruiting phenologies, plant height and seed predation, has a genetic basis. Highly significant maternal family effects were found for all of these life-history traits. These family effects could not be explained only by maternal effects, as maternal effects are known to particularly influence annual plants and juvenile stages in perennial plants (Roach & Wulff, 1987), while our study involved 4-year-old adult plants.

Flowering onset and flowering duration were perfectly correlated, and can be considered as two attributes of the same trait. The range of variation observed in the experimental garden was similar to the range observed in natural populations (Tarayre et al., 2007): flowering onset varied from September to May, and flowering duration varied from 1 to 8 months. This variation is much larger than what is generally found in studies conducted in common gardens (e.g. Widén, 1991;Quinn & Wetherington, 2002;Weis & Kossler, 2004; Dudley et al., 2007). Maternal family explained a higher per cent of variance than population of origin, reflecting the fact that extreme flowering phenotypes coexist within all natural populations (Tarayre et al., 2007).

Genetic variation in plant height is common (see review in Housman et al., 2002), but U. europaeus is especially remarkable for the range of variation observed. Plant height varied eight-fold among individuals and three-fold among families. Although the family effect was significant, most of the variance could be attributed to the population of origin, in accordance with previous observations showing ecological differences for plant size and architecture (Misset, 1992). Among-population differences were more pronounced for plant height than for flowering phenology. However, the two traits were genetically correlated (Table 4). As in many species, the plants that began to flower the latest were also the smallest (e.g. Widén, 1991; Ollerton & Lack, 1998; Leger & Rice, 2007).

Finally, we showed genetic variability for sensitivity to seed predation. Indeed, the infestation rate in late June, among pods that were exposed to the same pool of seed predators, varied from 2% to 80%, depending on the families. Genetic variation for resistance of plants to insects has been demonstrated in many species (e.g. Shen & Bach, 1997; Newton et al., 1999; Hjältén et al., 2000), but such a high level of variability is unusual. In U. europaeus, variation was continuous, and strongly correlated with flowering onset (Table 4). This correlation was mainly because of infestation by the most abundant seed predator, the weevil E. ulicis.

The annual numbers of pods per shoots and the numbers of seeds per pod did not vary with maternal family, perhaps because the characters that are the most closely connected to fitness are generally those with the lowest genetic variability (Houle, 1992; Merilä & Sheldon, 1999).

Flowering strategies and seed predation

Observations in natural populations have shown that flowering onset is clearly bimodal, leading us to define two main phenotypes (Tarayre et al., 2007). The present study shows that short- and long-flowering mothers produced offspring with distinct distributions of flowering onset. Short-flowering mothers mainly produced short-flowering offspring, while long-flowering mothers produced all flowering phenotypes. This confirms that the genetic constitution of the two flowering types is different. The determination of flowering is often simple and coded by a small number of genes (Putterill et al., 2004) and a polymorphism conferred by one major flowering time locus modulated by additional minor loci has been found in many species, e.g. between the two main ecotypes of Arabidopsis thaliana (Mitchell-Olds & Schmitt, 2006), or between the two flowering types of Poa annua (Johnson & White, 1998). Our results would be in agreement which such determinism, and suggest that the long- and short-flowering phenotypes are under the control of a major gene, while minor genes could be involved to explain the variability observed.

The two flowering types underwent contrasting predation pressures, because the infestation rates increased throughout the fruiting season, both in our common garden (Fig. 2a) and in natural populations (Barat et al., 2007; Tarayre et al., 2007). Long-flowering plants produced most of their pods before the peak of seed predation, when infestation rate was nil or low (Fig. 2b). They thus escaped seed predation in time. Short-flowering plants produced most of their pods when infestation rate was high, but during the peak of seed predation, they suffered fewer attacks by weevils than long-flowering plants (Fig. 2c). They thus had another way to reduce seed predation.

As short-flowering plants produced most of their pods during the peak of seed predation, they may have reduced the incidence of seed predation through predator satiation. The negative correlation between pod density and seed predation in late June illustrates that predator satiation may reduce seed predation. However, this predator satiation effect was not sufficient to explain the strong negative correlation between flowering onset and seed predation in late June (Fig. 3). Other mechanisms must be involved. These may include physical or chemical defences (Hilker & Meiners, 2002), or lower attractiveness to weevils because of architectural patterns (Leimu & Syrjänen, 2002).

The two flowering types exhibited different strategies: the long-flowering plants escaped predation in time but were more vulnerable during the infestation peak, while the short-flowering plants fruited during the peak of predation pressure, but reduced the incidence of seed predation through other mechanisms that include predator satiation. The efficiency of these strategies can be estimated by comparing the infestation rate over the entire fruiting season: this comparison revealed that the families with the two extreme phenotypes were the least infested, while the families with intermediate flowering onset were the most heavily infested (Fig. 4). Each strategy was thus the attribute of a given flowering phenotype, and intermediate strategies were less effective in reducing seed predation. These two predation-escape strategies have been described in other species [e.g. escaping in time in Vaccinium hirtum (Mahoro, 2003), or predator satiation in Quercus robur (Crawley & Long, 1995)]. However, the situation in U. europaeus is unusual, as both strategies can be observed in the same species, expressed by different flowering phenotypes.

Selection acting on trait combinations rather than on a single trait favours the maintenance of genetic variation (Sinervo & Svensson, 2002; Roff & Fairbairn, 2007). The coexistence of two strategies to avoid seed predation by weevils may thus play an important role in shaping not only flowering phenology, but also the traits that are genetically associated with flowering onset, such as pod density and growth pattern.

Implication for invasive areas

The capacity for flowering phenology and growth pattern to respond to natural selection is an important component of a plant’s adaptation to a novel environment: flowering phenology is a key feature of reproductive success, and plant growth is related to abiotic constraints and competitive ability. In U. europaeus, the genetic variability observed for these traits appeared to be associated with seed predation. Release from seed predation may thus lead to the loss of flowering dimorphism, the weakening of genetic correlations between flowering phenology, pod density and growth pattern, and thus leaving more latitude for these traits to evolve in response to a new environment.

The condition for this kind of evolutionary response to occur in invaded areas is that the genetic variability of the native range be imported. Similar genetic variation in invasive and native areas resulting from multiple introductions has been observed in many species (Genton et al., 2005; Bossdorf et al., 2005; Novak, 2007). Genetic variability in non-native U. europaeus populations is also likely to be high (M. Tarayre & V. Roussel, unpublished) because its presence in invaded areas results from multiple voluntary introductions.

Genetic variation in the native area is increasingly considered as a key feature in the invasive success of a species (Lavergne & Molofsky, 2007; Lee & Gelembiuk, 2008; Prentis et al., 2008). Although many aspects need to be explored to understand why U. europaeus is one of the most invasive species in several parts of the world, it is likely that the high evolutionary potential revealed by this study for flowering phenology and growth pattern has facilitated the adaptation of U. europaeus to a wide range of environmental conditions.

Acknowledgments

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgments
  8. References

This work was supported by a CNRS (ATIP) grant. The authors thank Thierry Fontaine for technical assistance, Alan Scaife and Carolyn Engel-Gautier for English translation and editing. The authors are grateful to Luc Gigord, Jacques van Alphen, the Editor and the anonymous referees for their helpful comments.

References

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgments
  8. References