doi: 10.1111/j.1420-9101.2009.01908.

Genetic variation in flowering phenology and avoidance of seed

predation in native populations of Ulex europaeus

A. ATLAN, M. BARAT, A. S. LEGIONNET, L. PARIZE & M. TARAYRE

Laboratoire ‘‘ECOBIO’’ – UMR 6553, Université de Rennes 1, Rennes, France

Keywords: Abstract
The genetic variation in flowering phenology may be an important component
flowering phenology;
of a species’ capacity to colonize new environments. In native populations of
invasive plants;
the invasive species Ulex europaeus, flowering phenology has been shown to be
life-history traits;
bimodal and related to seed predation. The aim of the present study was to
seed predation;
determine if this bimodality has a genetic basis, and to investigate whether the
Ulex europaeus.
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.

generally maintained in experimental gardens, demon-

Introduction
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 availabil-
ity 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
Correspondence: Anne Atlan, UMR 6553 ECOBIO, Université de Rennes 1,
Campus de Beaulieu, Bâtiment 14A, 35042 Rennes Cedex, France.
Tel.: +33 223 236 172; fax: +33 223 235 047;
e-mail: anne.atlan@univ-rennes1.fr
strating genetic differentiation (Tarasjev, 1997; Quinn &
Wetherinton, 2002; Leger & Rice, 2007). Within popu-
lations, 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.

ª 2009 THE AUTHORS. J. EVOL. BIOL. 23 (2010) 362–371

362 JOURNAL COMPILATION ª 2009 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY

English-Loeb & Karban, 1992). However, synchroniza-
tion 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 combina-
tions 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 aggres-
sive 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 satia-
tion. This polymorphism in strategy may provide this
species with high genetic variance for flowering phenol-
ogy, 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
ª 2009 THE AUTHORS. J. EVOL. BIOL. 23 (2010) 362–371
JOURNAL COMPILATION ª 2009 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY
Genetic variation in Ulex europaeus 363
traits. Based on mixed analyses of variance, we demon-
strated genetic differences between the two main flow-
ering 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 evolution-
ary potential may be particularly expressed in situations
where seed predators are absent, as is often the case in
newly invaded areas.
Materials and methods
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
364 A. ATLAN ET AL.
Long-flowering Short-flowering
Population Habitat plants (%) mothers sampled
Château de Vaux Fallow 42 3 2
La Réauté Hedge 29 2 3
Pointe du Grouin Seaside 7 3
Pointe du Meinga Seaside 10 2 3
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.
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
JOURNAL COMPILATION ª 2009 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY
Table 1 Populations of Ulex europaeus
Long-flowering
sampled in Brittany (France).
mothers sampled
2
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 syn-
chronously. This measurement corresponds to the infes-
tation rate of pods that were all exposed to the same pool
of seed predators.
Statistical analyses
All analyses were performed using S A S software (SAS
Institute, 2005). The significance of the effects was tested
independently for each of the 12 life-history variables,
using a mixed-model A N O V A (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
ª 2009 THE AUTHORS. J. EVOL. BIOL. 23 (2010) 362–371

rates arcsine-transformed to meet assumptions of nor-
mality. 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
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 popula-
tions, 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
50
Short flowering mother
45
Long flowering mother
40
Number of individuals
35
30
25
20
15
10
5 highly significant effect on plant growth and infestation
0 rate in late June, and a lower effect on flowering and
Sep Oct Nov Dec Jan Feb
Fig. 1 Distribution of flowering onset (by month) of 190 Ulex
europaeus plants grown in a common garden, according to maternal
flowering type.
ª 2009 THE AUTHORS. J. EVOL. BIOL. 23 (2010) 362–371
JOURNAL COMPILATION ª 2009 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY
Genetic variation in Ulex europaeus 365
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 popula-
tions. 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.
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 respec-
tively).
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).
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.
Results of the statistical analysis on all 12 life-history
traits are provided in Table 3. Population of origin had a
Mar Apr May
fruiting phenology and annual pod production per shoot.
Within populations, the maternal family had a strong
influence on all variables except pod and seed produc-
tion. The flowering type of the mother had a significant
366 A. ATLAN ET AL.

(a) 100 Moth June and plant height; the tallest plants were the most
90 Weevil + moth heavily infested. There was a negative correlation
80 Weevil between plant height and flowering onset; the tallest
Infested pods (%)

89
70 plants began to flower earlier. There was a positive
60 correlation between flowering onset and annual pod
50 production, but this correlation was only significant
161
40 among maternal family means: families that began to
84
30 flower the latest had the highest annual pod production.
20 A similar result was observed where flowering onset was
10 17 23 correlated with pod density in June (n = 20, R = +0.71,
0 P < 0.01).
April May Early June Late June July
The most significant correlation was the one observed
between flowering onset and infestation rate in late
(b)
100 June. The later the flowering onset, the lower its
90 Long-flowering plants 16
infestation rate in late June. When the two species of
Infested pods (%)

80 Short-flowering plants seed predators were analysed separately, the correlation

70
45 73 among maternal family means between infestation rate
60
in late June and flowering onset was significant for
50
40
weevils (n = 20, R = )0.87, P < 10)4, Fig. 3a), but not for
30
48 116 moths (n = 20, R = )0.41, P = 0.07). To test the influ-
36 ence of predator satiation, we also tested the correlation
20
10 17 0 23 0
between infestation rate in late June and pod density in
0 June. This correlation was significant for infestation by
April May Early June Late June July weevils (n = 20, R = )0.60, P < 0.01, Fig. 3b), but not by
moths (n = 20, R = )0.24, P > 0.10).
(c) 25
Long-flowering plants When infestations rates were considered over the
Short-flowering plants entire fruiting season, neither annual infestation rate
20 by weevils, nor annual infestation rate by moths was
Pod production

significantly correlated with flowering onset (n = 20,

15 R = )0.18 and R = +0.19 respectively, P > 0.10). How-
ever, the relationship between infestation rate by weevils
10 over the entire fruiting season and flowering onset could
be fitted to a second-order polynomial regression (Fig. 4,
5 n = 20, R = 0.51, F2,17 = 8.88, P < 0.01*****). The moth
infestation rate could not be fitted to this type of
0 regression.
April May Early June Late June July

Fig. 2 Temporal changes in pod infestation and pod production in Discussion

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.
influence on flowering and fruiting phenologies, but not
on any of the other variables studied.
Correlations between traits
The correlation coefficients between plant height, flow-
ering 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
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

ª 2009 THE AUTHORS. J. EVOL. BIOL. 23 (2010) 362–371

JOURNAL COMPILATION ª 2009 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY
 Genetic variation in Ulex europaeus 367

Table 2 Descriptive statistics of four life-history traits of Ulex europaeus plants grown in a common garden from seeds collected in Brittany
(France).

Populations n = 4 Maternal families n = 20 Individuals n = 190

Variance Variance Residual

Traits Mean ± SD* Min.–max. explained (%) Min.–max. explained (%) Min.–max. variance (%)

Flowering duration (days) 81 ± 55 67–101 5 34–135 36 19–252 59

Plant height (cm) 150 ± 51 119–191 41 66–210 24 32–252 35
Infested pods (% in late June) 32 ± 27 19–54 30 2–80 21 0–100 49
Pods per shoot (annual production) 45 ± 24 33–53 10 18–67 14 14–131 76

All traits were measured in four-year-old plants.

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

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 dif-
ferences 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 correla-
tion 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

Table 3 Results from mixed-model A N O V A

for 12 life-history traits of Ulex europaeus Effects
plants grown in a common garden from Traits Population (v2) Maternal family (v2) Mother’s type (F1,16)
seeds collected in Brittany (France).
Phenology
Flowering onset 1.4 23.2**** 13.53**
Flowering duration 0.1 17.4**** 12.71**
Fruiting onset 4.0* 16.4**** 5.15*
Fruiting duration 1.2 11.1*** 2.64
Architecture
Plant height 9.6** 45.8**** 1.66
Branch length 13.4*** 16.8**** 4.22
Branch angle 4.8* 56.8**** 0.45
Infestation rate
Late June 8.1** 12.9*** 4.31
Entire fruiting season 0.4 17.0**** 0.01
Annual production
Pods per shoot 4.3* 2.1 0.08
Seeds per pod 1.7 1.2 0.68
Seeds per shoot 1.4 1.3 0.56

All traits were measured in 4-year-old plants, except branch length and branch angle that
were measured in 3-year-old plants.
*P < 5%, **P < 1%, ***P < 10)3, ****P < 10)4.

ª 2009 THE AUTHORS. J. EVOL. BIOL. 23 (2010) 362–371

JOURNAL COMPILATION ª 2009 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY
368 A. ATLAN ET AL.

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 height Infestation* rate Pods  per shoot Plant height Infestation* rate Pods  per shoot

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)

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.
*Proportion of infested pods in late June.
 Annual production.

(a) 90 (b) 90
80 80
Pods infested by weevils

70 70
(% in late June)

60 60
50 50
40 40
30 30
Fig. 3 Pod infestation by weevils in late
20 20 June. Proportion of ripe pods infested in late
10
R 2 = 0.79
10 R 2 = 0.36 June according to flowering onset (a) and
0 0 pod density in June (mean number of pods
Oct Nov Dec Jan Feb Mar Apr 0 10 20 30 40 50 60 70 80 per shoot) (b). Each point represents a
Flowering onset Pod density maternal family; n = 20.

closely connected to fitness are generally those with study shows that short- and long-flowering mothers
the lowest genetic variability (Houle, 1992; Merilä & produced offspring with distinct distributions of flower-
Sheldon, 1999). ing onset. Short-flowering mothers mainly produced
short-flowering offspring, while long-flowering mothers
produced all flowering phenotypes. This confirms that
Flowering strategies and seed predation
the genetic constitution of the two flowering types is
Observations in natural populations have shown that different. The determination of flowering is often simple
flowering onset is clearly bimodal, leading us to define and coded by a small number of genes (Putterill et al.,
two main phenotypes (Tarayre et al., 2007). The present 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
50 main ecotypes of Arabidopsis thaliana (Mitchell-Olds &
Schmitt, 2006), or between the two flowering types of
(% entire fruiting season)
Pods infested by weevils

40 Poa annua (Johnson & White, 1998). Our results would

be in agreement which such determinism, and suggest
30 that the long- and short-flowering phenotypes are under
the control of a major gene, while minor genes could be
20 involved to explain the variability observed.
The two flowering types underwent contrasting pre-
10 dation pressures, because the infestation rates increased
R 2 = 0.51 throughout the fruiting season, both in our common
0 garden (Fig. 2a) and in natural populations (Barat et al.,
Oct Nov Dec Jan Feb Mar Apr
2007; Tarayre et al., 2007). Long-flowering plants pro-
Flowering onset
duced most of their pods before the peak of seed
Fig. 4 Pod infestation by weevils over the entire fruiting season.
predation, when infestation rate was nil or low (Fig. 2b).
Relationship between flowering onset and the proportion of ripe They thus escaped seed predation in time. Short-flower-
pods infested by weevils over the entire fruiting season, fitted to a ing plants produced most of their pods when infestation
second-order polynomial regression. Each point represents a rate was high, but during the peak of seed predation,
maternal family; n = 20. they suffered fewer attacks by weevils than long-flowering

ª 2009 THE AUTHORS. J. EVOL. BIOL. 23 (2010) 362–371

JOURNAL COMPILATION ª 2009 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY

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 mecha-
nisms 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 pred-
ator 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 effec-
tive 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 compo-
nent 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 pre-
dation may thus lead to the loss of flowering dimor-
phism, the weakening of genetic correlations between
ª 2009 THE AUTHORS. J. EVOL. BIOL. 23 (2010) 362–371
JOURNAL COMPILATION ª 2009 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY
Genetic variation in Ulex europaeus 369
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 intro-
ductions 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
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 anon-
ymous referees for their helpful comments.
References
Astles, P.A., Moore, A.J. & Preziosi, R.F. 2006. A comparison
to methods to estimate cross-environment genetic correlations.
J. Evol. Biol. 19: 114–122.
Barat, M., Tarayre, M. & Atlan, A. 2007. Plant phenology and
seed predation: interactions between gorse (Fabaceae) and
weevils (Curculionoidea) in Brittany. Ent. Exp. Appl. 124: 167–
176.
Bossdorf, O., Auge, H., Lafuma, L., Rogers, W.E., Siemann, E. &
Prati, D. 2005. Phenotypic and genetic differentiation between
native and introduced plant populations. Oecologia 144: 1–11.
Botto, J. & Coluccio, M.P. 2007. Seasonal and plant-density
dependency for quantitative trait loci affecting flowering time
in multiple populations of Arabidopsis thaliana. Plant Cell
Environ. 30: 1465–1479.
Bowman, G., Tarayre, M. & Atlan, A. 2008. How is the invasive
gorse Ulex europaeus pollinated during winter? A lesson from
its native range Plant Ecol. 197: 197–206.
Brody, A.K. 1997. Effects of pollinators, herbivores, and seed
predators on flowering phenology. Ecology 78: 1624–1631.
Chao, C.T. & Parfitt, D.E. 2003. Genetic analyses of phenological
traits of pistachio (Pistacia vera L.). Euphytica 129: 345–349.
Crawley, M.J. & Long, C.R. 1995. Alternate bearing, predator
satiation and seedling recruitment in Quercus robur L. J. Ecol.
83: 683–696.
370 A. ATLAN ET AL.
Davies, W.M. 1928. The bionomics of Apion ulicis Forst
(gorse weevil) with special reference to its role in the
control of Ulex europaeus in New Zealand. Ann. Appl. Biol.
15: 263–386.
Dudley, L.S., Mazer, S.J. & Galusky, P. 2007. The joint evolution
of mating system, floral traits and life history in Clarkia
(Onagraceae): genetic constraints vs. independent evolution.
J. Evol. Biol. 20: 2200–2218.
Elzinga, J.A., Atlan, A., Biere, A., Gigord, L., Weis, A.E. &
Bernasconi, G. 2007. Time after time: flowering phenology
and biotic interactions. TREE 22: 432–439.
English-Loeb, G.M. & Karban, R. 1992. Consequences of
variation in flowering phenology for seed head herbivory
and reproductive success in Erigeron glaucus (Compositae).
Oecologia 89: 588–595.
Falconer, D.S. & Mackay, T.F.C. 1996. Introduction to Quantitative
Genetics, Longmans Green, Harlow, Essex, UK.
Franks, S.J., Sim, S. & Weis, A.E. 2007. Rapid evolution of
flowering time by an annual plant in response to a climate
fluctuation. Proc. Natl. Acad. Sci. 104: 1278–1282.
Freeman, R.S., Brody, A.K. & Neefus, C.D. 2003. Flowering
phenology and compensation for herbivory in Ipomopsis
aggregata. Oecologia 136: 394–401.
Gardner, K.M. & Latta, R.G. 2008. Heritable variation and
genetic correlation of quantitative traits within and between
ecotypes of Avena barbata. J. Evol. Biol. 21: 737–748.
Genton, B.J., Shykoff, J.A. & Giraud, T. 2005. High genetic
diversity in French invasive populations of common ragweed,
Ambrosia artemisiifolia, as a result of multiple sources of
introduction. Mol. Ecol. 14: 4275–4285.
Gomez, J.M. 1993. Phenotypic selection on flowering synchrony
in a high-mountain plant, Hormathophylla spinosa (Cruciferae).
J. Ecol. 81: 605–613.
Grafen, A. & Hails, R. 2002. Modern Statistics for the Life Sciences.
Oxford University Press, Oxford.
Herrera, J. 1999. Fecundity above the species level: ovule
number and brood size in the Genisteae (Fabaceae: Papilio-
noideae). Int. J. Plant Sci. 160: 887–896.
Hilker, M. & Meiners, T. 2002. Induction of plant responses
towards oviposition and feeding of herbivorous arthropods: a
comparison. Ent. Exp. Appl. 104: 181–192.
Hill, R.L., Gourlay, A.H. & Martin, L. 1991. Seasonal and
geographic variation in the predation of gorse seed, Ulex
europeaus L., by seed weevil Apion ulicis Forst. N. Z. J. Zool. 18:
37–43.
Hjältén, J., Ericson, L. & Roininen, H. 2000. Resistance of Salix
caprea, S. phylicifolia, and their Fk1 hybrids to herbivores and
pathogens. Ecoscience 7: 51–56.
Hoddle, M.S. 1991. Gorse pod susceptibility and oviposition
preference to the gorse seed weevil, Apion ulicis (Forster)
(Coleoptera: Apionidae). N. Z. J. Zool. 18: 31–35.
Holm, L.G., Doll, J., Holm, E., Pancho, J.V. & Herberger, J.P.
1997. World Weeds: Natural Histories and Distribution, pp. 880–
888. Wiley, J. & Sons, New York.
Houle, D. 1992. Comparing evolvability and variability of
quantitative traits. Genetics 130: 195–204.
Houle, D. 1998. How should we explain variation in the genetic
variance of traits? Genetica 102 ⁄ 103: 241–253.
Housman, D.C., Price, M.V. & Redak, R.A. 2002. Architecture of
coastal and desert Encelia farinosa (Asteraceae): consequences
of plastic and heritable variation in leaf characters. Am. J. Bot.
89: 203–208.
JOURNAL COMPILATION ª 2009 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY
Ims, R.A. 1990. The ecology and evolution of reproductive
synchrony. TREE 5: 135.
Janzen, D.H. 1971. Seed predation by animals. Ann. Rev. Ecol.
Syst. 2: 465–492.
Johnson, M.T.J. 2007. Genotype-by-environment interactions
lead to variable selection on life-history strategy in Evening
Primrose (Oenothera biennis). J. Evol. Biol. 20: 190–200.
Johnson, P.G. & White, D.B. 1998. Inheritance of flowering
pattern among four annual bluegrass (Poa annua L.) geno-
types. Crop Sci. 38: 163–168.
Lavergne, S. & Molofsky, J. 2007. Increased genetic variation
and evolutionary potential drive the success of an invasive
grass. Proc. Natl Acad. Sci. USA 104: 3883–3888.
Lee, C.E. & Gelembiuk, G.W. 2008. Evolutionary origin of
invasive populations. Evol. Appl. 1: 427–448.
Leger, E.A. & Rice, K.J. 2007. Assessing the speed and predict-
ability of local adaptation in invasive California poppies
(Eschscholzia californica). J. Evol. Biol. 20: 1090–1103.
Leimu, R. & Syrjänen, K. 2002. Effects of population size, seed
predation and plant size on male and female reproductive
success in Vincetoxicum hirundinaria (Asclepiadaceae). Oikos 98:
229–238.
Lowe, S., Browne, M., Boudjelas, S. & De Poorter, M. 2000.
100 of the World’s Worst Invasive Alien Species. A Selection
from the Global Invasive Species Database. Published by the
IUCN ⁄ SSC Invasive Species Specialist Group (ISSG), Auck-
land, New Zealand.
Lynch, M. & Walsh, B. 1998. Genetics and Analysis of Quantitative
Traits. Sinauer, Sunderland, MA.
Mahoro, S. 2003. Effects of flower and seed predators on fruit
production in two sequentially flowering congeners. Plant
Ecol. 166: 37–48.
Markin, G.P. & Yoshioka, E. 1996. The phenology and growth
rates of the weed gorse (Ulex europaeus) in Hawaii. New. Haw.
Bot. Soc. 35: 45–50.
Misset, M.-T. 1992. Meiotic abnormalities during microsporo-
genesis and low fertility in prostrate ecotypes of Ulex species
(Papilionoideae, Genisteae). Can. J. Bot. 70: 1223–1227.
Merilä, J. & Sheldon, B. 1999. Genetic architecture of fitness and
non-fitness traits – empirical patterns and development of
ideas. Heredity 83: 103–109.
Mitchell-Olds, T. & Schmitt, J. 2006. Genetic mechanisms and
evolutionary significance of natural variation in Arabidopsis.
Nature 441: 947–952.
Nakagawa, H., Yamagishi, J., Miyamoto, N., Motoyama, M.,
Yano, M. & Nemoto, K. 2005. Flowering response of rice to
photoperiod and temperature: a QTL analysis using a pheno-
logical model. TAG 110: 778–786.
Newton, A.C., Watt, A.D., Lopez, F., Cornelius, J.P., Mesén, J.F.
& Corea, E.A. 1999. Genetic variation in host susceptibility to
attack by the mahogany shoot borer, Hypsipyla grandella
(Zeller). Agric. For. Entomol. 1: 11–18.
Novak, S.J. 2007. The role of evolution in the invasion process.
Proc. Natl Acad. Sci. USA 104: 3671–3672.
Ollerton, J. & Lack, A. 1998. Relationships between flowering
phenology, plant size and reproductive success in Lotus
corniculatus (Fabaceae). Plant Ecol. 139: 35–47.
Pinhero, J.C. & Bates, D.M. 2000. Mixed-effects Models in S and
S-PLUS J. Springer-Verlag, New York.
Prentis, P.J., Wilson, J.R.U., Dormont, E.E., Richardson, D.M. &
Lowe, A.J. 2008. Adaptive evolution in invasive species.
Trends Plant Sci. 6: 288–294.
ª 2009 THE AUTHORS. J. EVOL. BIOL. 23 (2010) 362–371

Putterill, J., Laurie, R. & Macknight, R. 2004. It’s time to flower:
the genetic control of flowering time. BioEssays 26: 363–373.
Quinn, J.A. & Wetherington, J.D. 2002. Genetic variability and
phenotypic plasticity in flowering phenology in populations of
two grasses. J. Torrey. Bot. Soc. 129: 96–106.
Rathcke, B. & Lacey, E.P. 1985. Phenological patterns of
terrestrial plants. Ann. Rev. Ecol. Syst. 16: 179–214.
Roach, D.A. & Wulff, R.D. 1987. Maternal effects in plants. Ann.
Rev. Ecol. Syst. 18: 209–235.
Roff, D.A. & Fairbairn, D.J. 2007. The evolution of trade-offs:
where are we? J. Evol. Biol. 20: 433–447.
Rose, M.R. 1982. Antagonistic pleiotropy, dominance, and
genetic variation. Heredity 48: 63–78.
SAS Institute 2005. Version 9.1. SAS institute, Cary, NC.
Shen, C. & Bach, C. 1997. Genetic variation in resistance and
tolerance to insect herbivory in Salix cordata. Ecol. Entomol. 22:
335–342.
Sinervo, B. & Svensson, E. 2002. Correlation selection and
the evolution of genomic architecture. Heredity 89: 329–
338.
ª 2009 THE AUTHORS. J. EVOL. BIOL. 23 (2010) 362–371
JOURNAL COMPILATION ª 2009 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY
Genetic variation in Ulex europaeus 371
Sixtus, C.R., Scott, R.R. & Hill, G.D. 2007. The phenology of
Cydia succedana on gorse in Canterbury. N. Z. Plant Protection
60: 146–151.
Tarasjev, A. 1997. Flowering phenology in natural populations
of Iris pumila. Ecography 20: 48–54.
Tarayre, M., Vergnerie, G., Schermann-Legionnet, A., Barat, M.
& Atlan, A. 2007. Flowering phenology of Ulex europaeus:
ecological consequences of variation within and among
populations. Evol. Ecol. 21: 395–409.
Weis, A.E. & Kossler, T.M. 2004. Genetic variation in flowering
time induces phenological assortative mating: quantitative
genetic methods applied to Brassica rapa. Am. J. Bot. 91: 825–
836.
Widén, B. 1991. Environmental and genetic influences of
phenology and plant size in a perennial herb, Senecio integrifo-
lius. Can. J. Bot. 69: 209–217.
Received 3 July 2008; accepted 3 November 2009