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Efficient mitigation of founder effects
during the establishment of a leadingedge oak population
rspb.royalsocietypublishing.org
Arndt Hampe1,2, Marie-Hélène Pemonge3 and Rémy J. Petit1,2
1
INRA, UMR 1202 BIOGECO, 69, Route d’Arcachon, F-33610 Cestas, France
Univ. Bordeaux, UMR 1202 BIOGECO, Av. des Facultés, F-33405 Talence, France
3
Univ. Bordeaux, UMR 5199 PACEA, Av. des Facultés, F-33405 Talence, France
2
Research
Cite this article: Hampe A, Pemonge M-H,
Petit RJ. 2013 Efficient mitigation of founder
effects during the establishment of a leadingedge oak population. Proc R Soc B 280:
20131070.
http://dx.doi.org/10.1098/rspb.2013.1070
Received: 27 April 2013
Accepted: 3 June 2013
Subject Areas:
ecology, evolution
Keywords:
founder event, genetic rescue, inbreeding
depression, long-distance gene flow, Quercus
ilex, range expansion
Author for correspondence:
Arndt Hampe
e-mail: [email protected]
Electronic supplementary material is available
at http://dx.doi.org/10.1098/rspb.2013.1070 or
via http://rspb.royalsocietypublishing.org.
Numerous plant species are shifting their range polewards in response to
ongoing climate change. Range shifts typically involve the repeated establishment and growth of leading-edge populations well ahead of the main
species range. How these populations recover from founder events and
associated diversity loss remains poorly understood. To help fill this gap,
we exhaustively investigated a newly established population of holm oak
(Quercus ilex) growing more than 30 km ahead of the nearest larger stands.
Pedigree reconstructions showed that plants belong to two non-overlapping
generations and that the whole population originates from only two founder
trees. The four first-generation trees that have reached maturity showed disparate mating patterns despite being full-sibs. Long-distance pollen
immigration was notable despite the strong isolation of the stand: 6 per
cent gene flow events in acorns collected on the trees (n ¼ 255), and as
much as 27 per cent among their established offspring (n ¼ 33). Our results
show that isolated leading-edge populations of wind-pollinated forest trees
can rapidly restore their genetic diversity through the interacting effects of
efficient long-distance pollen flow and purging of inbred individuals
during recruitment. They imply that range expansions of these species are
primarily constrained by initial propagule arrival rather than by
subsequent gene flow.
1. Introduction
Modern climate change is driving the expansion of numerous plant and animal
populations worldwide towards higher elevations and latitudes [1]. Climate
envelope models predict extensive redistributions of many species, but it is
unclear whether they will be able to colonize new territories in pace with a
rapidly changing climate. Such uncertainty is particularly worrying in longlived sessile organisms such as forest trees [2,3]. Assessing the capacity of
trees to respond to modern climate change is crucial, because they play a prominent role in many ecosystems and provide vital habitat for a great diversity of
other organisms. However, direct empirical evidence for contemporaneous
poleward range expansions of forest trees following a changing climate remains
scant and the corresponding evolutionary processes poorly understood [4].
Those populations that form the leading edge of an expanding species range
are predicted to experience profound evolutionary changes [5–7]. In many
organisms, including trees, range expansions are typically promoted by rare
events of long-distance dispersal that enable small pioneer populations to establish far ahead of the continuous range and to fill the empty area with their
progeny [5,8]. The associated successive founder events represent a spatial analogue of genetic drift, reducing genetic diversity and increasing differentiation
of populations near the leading edge [9]. This intense drift can result in allele
surfing (i.e. the increase in frequency of formerly rare alleles) [6]. On the
other hand, leading-edge populations are disproportionally susceptible to
Allee effects; that is, a lower per capita growth rate at low densities, caused in
particular by reduced mating opportunities and inbreeding [10]. Allee effects
& 2013 The Author(s) Published by the Royal Society. All rights reserved.
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(a)
(a) Study organism
Figure 1. (a) Present distribution range of Quercus ilex in France and
(b) modelled potential distribution by 2100. Black circles indicate the study
site. The modelled climatic suitability of areas increases from cold to warm colours, while grey indicates 100% suitability. Illustration adapted from [16].
can significantly delay or even impede the establishment of
leading-edge populations unless there is some gene immigration from other parts of the range. Hence, the performance
and evolution of such populations should ultimately
depend on the interplay between gene immigration and
local reproductive success [3].
These evolutionary mechanisms have been well established in theory and through simulations, yet empirical
evidence for their role during the initial establishment of
leading-edge populations remains scant (but see [11] for a
bird, [12] for insects and [13] for a mammal). Hence, we are
lacking a sound understanding of the processes that accompany the establishment of tree populations at the leading
edge. In particular, it remains unclear how such populations
recover from the strong loss of genetic diversity experienced
during the founder event. Levels of diversity can have important consequences for plant fecundity, mating patterns and
offspring performance, which in turn exert a strong influence
on population growth, and ultimately on the capacity for
rapid range expansion [14,15].
Here, we report on the genetic composition of an exhaustively sampled small pioneer population of holm oak
Holm oak is one of the most widespread and abundant trees
of the Mediterranean Basin, and a keystone species of many
forest ecosystems in the area. This evergreen species is considered
to have expanded from Iberia into southern France after the last
ice age [17]. It is common along the Mediterranean coast and
more sparsely distributed along the Atlantic coast (figure 1a).
Today, it is increasingly planted in parks and gardens of southern
and central France, as well as in Britain, where it has been listed as
a potential invader [18]. Projections based on bioclimatic envelope
modelling indicate that the species should encounter suitable
climatic conditions for establishment throughout the southern
half of France by 2100 (figure 1b).
Holm oak is largely self-incompatible and pollinated by
wind. Pollen has been shown to remain viable for more than a
month [19]. Holm oak acorns are regularly dispersed by different
vertebrates. In particular, the Eurasian jay (Garrulus glandarius)
can regularly transport them up to several kilometres [20].
(b) Study area and field sampling
The study was conducted in 2004 and 2005 in Cestas, some
25 km southwest of Bordeaux in southwestern France (448450 N
08380 W; figure 1a). Only four reproductive trees grow at the
site, which is located about 32 km away from the nearest
larger, natural holm oak populations growing along the Atlantic
coast. An extensive survey was conducted to locate potential
parent trees in the surroundings of the study population. All
tree-bearing areas within a radius of 5 km around the study
site were searched during the winter months (i.e. when the evergreen holm oak trees are most conspicuous) without spotting a
single adult-size individual. Searching an area of roughly 2 ha
around the four reproductive trees, we located, tagged and
mapped all established recruits. Although we do not know
under which circumstances the first holm oak individuals
arrived at our study site, the spatial distribution of the existing
plants (figure 2) and the characteristics of their growing sites
suggest that their offspring have established by natural means.
All plants were measured (total height and stem diameter) and
leaf tissue was collected for molecular analyses. In addition, a
total of 255 ripe acorns were collected from the two trees that
Proc R Soc B 280: 20131070
2. Material and methods
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(b)
(Quercus ilex L.) that has established and reproduces more
than 30 km ahead of the species’s nearest larger stands.
Holm oak reaches the northern distribution limit of its natural
range in southwestern and western France (figure 1a), and
projections indicate that the range and local abundance of
the species could strongly increase during the coming decades (figure 1b). The capacity of leading-edge populations
to recover from founder events could thus have important
impacts on population structure, diversity and ultimately
expansion success of the species in the region. Our study
enabled us to reconstruct the first three generations of the
investigated holm oak population, to quantify changes in
allele frequencies across generations, and to assess patterns of
mating and gene flow at the seed and at the recruit stage.
Specifically, we attempted to (i) determine within-population
mating patterns and the contribution of reproductive individuals to the pool of established offspring, (ii) quantify the
frequency of inbreeding and pollen-mediated gene immigration, as well as their connections, and (iii) evaluate
implications for the subsequent evolution of this expanding
pioneer population.
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(a)
10 m
10 m
T4
N
T2
T3
Figure 2. Spatial distribution and genetic structure of the studied Quercus ilex population. (a) Individuals belonging to the F1 (empty circles) and the F2 (filled
circles) generation as inferred from their multi-locus genotypes. Circle sizes are proportional to the stem diameter. (b) Multi-locus genotypes of the F2 plants. Stars
indicate the four parent trees. Coloured semi-circles indicate the local parent trees while white semi-circles indicate that one parent ( putatively the pollen donor)
stems from outside the population.
reproduced in 2003 (T1 and T4, hereafter). Acorns were weighed
and germinated in an incubator, and leaf tissue was used for
DNA isolation.
(c) Molecular analyses
All established plants were genotyped at 13 nuclear microsatellites (simple-sequence repeat, SSR): Msq4, Msq13, Qp9,
Qp15, Qp36, Qp46, Qp104, Qr4, Qr7, Qr11, Qr20, Qr96 and
Qr112 [21 – 23]. All loci except Qp104 were also used for genotyping acorns. The DNeasy Plant Mini Kit (Qiagen) was used
for DNA isolation from fresh buds or leaves. Loci were amplified
individually according to the study of Barreneche et al. [24]. PCR
products were visualized on a Li-Cor model 4000L automatic
DNA sequencer. Gel scoring was performed manually by two
of the authors (M.-H.P. and R.J.P.). All SSRs were amplified
twice and sometimes up to four times to confirm scorings. We
checked for Mendelian segregation of the markers whenever at
least one of the two parent trees studied was a heterozygote, to
detect weak or null alleles as well as linkage between loci.
All field and genotypic data are available in the electronic
supplementary material, appendix S1.
(d) Parentage analysis by genotype exclusion
For the established plants, we used simple rules of inheritance
to manually assign all genotypes to either of two groups:
(i) those that could have been derived by at least one of the
four adult trees and (ii) those that could not be offspring of
any of these four trees. For the latter, we checked for sib
relationships using simple expectations such as the four allele
rule (i.e. no more than four alleles can segregate within a
full-sib family).
For acorn genotypes, a paternity search was conducted
manually by simple exclusion using the four reproductive trees
as candidates. When two or more loci resulted in seedling genotypes that were clearly incompatible with any of the four
candidate fathers, we considered that the acorn had been sired
by a tree from outside the stand. If there was only one mismatch,
we re-amplified the corresponding locus at least once to confirm
that this mismatch was not due to a scoring error. All manual
assignments were subsequently checked and corroborated with
the software GIMLET [25]. Finally, diversity estimates for the
two generations detected (see below) were obtained with
FSTAT v. 2.9.3. [26]. The loci Qp36 and Qp46 were excluded
from this last analysis as they contained null alleles.
3. Results
(a) Established plants
We identified a total of 65 individuals (including the four
reproductive trees) within the surveyed area. Four groups
of saplings had identical genotypes. As saplings from each
group grew close to each other, we concluded that they represent different ramets of the same genet and excluded all but
the largest ramet from subsequent analyses. A total of 58
unique genotypes (i.e. four reproductive trees and 54 recruits)
were therefore available for further studies.
We could distinguish two generations of plants and infer a
third one by reconstructing the relationships among the
unique multi-locus genotypes of all individuals (figure 2a;
see also pedigree reconstruction in electronic supplementary
material, figure S2). All except two individuals could be
unequivocally assigned to their respective generation from
their multi-locus genotypes. The combined genotypic and
plant size data for the two remaining plants allowed us also
to infer their respective generations also with high confidence.
First, we identified a total of 33 recruits as offspring of
either one or two of the four reproductive trees (figure 2b).
Both parents could be identified for 24 of these recruits.
Proc R Soc B 280: 20131070
T1
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N
3
(b)
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generation
n
no. immigrant genotypes (%)
no. foreign alleles
RS
HE
FIS
F1
25
3 (12%)
16
3.7
0.44
20.24***
F2
33
9 (27%)
33
4.2
0.44
20.24***
***p , 0.001.
mother tree
T1
T2
T3
T4
immigrant
total
T1
T4
1 (0.7)
0
5 (3.7)
0
62 (45.9)
0
58 (43.0)
113 (94.2)
9 (6.7)
7 (5.8)
135
120
Nine recruits had at least two (and upto seven) alleles not
found in any of the four reproductive trees, pointing to
pollen immigration events (table 1). Among the 33 recruits,
no less than 28 (85%) were offspring of tree T1. Trees T2
and T3 had 12 –13 and 8–9 offspring, respectively (one
recruit could be offspring of either of these trees). One offspring of T2 stemmed from a selfing event (and died
shortly after the study). Tree T4 had only six offspring.
The remaining 21 recruits had genotypes indicating that
they could not have been sired by any of the four reproductive trees. Instead, we could infer a single full-sib family
that encompasses the four reproductive trees as well as 18
of these 21 recruits (figure 2a). The three remaining recruits
had genotypes suggesting that they could be half-sibs of
this family. We consequently hypothesized that two
unknown parental trees had produced this family group by
either mating with each other (for the full-sib family) or
receiving immigrant pollen from outside the population
(for the putative half-sibs; table 1). We were able to reconstruct the multi-locus genotypes of the two hypothesized
trees from these 25 individuals (i.e. the four reproductive
trees plus the 21 other recruits), finding a unique and fully
consistent solution that comforted our hypothesis.
Based on our inferences, we concluded therefore that:
(i) two now absent ‘ghost’ trees were the founders of the
study population; (ii) these mated either with each other or
were sired by immigrant pollen, generating an F1 generation
of 22 full-sibs (including the four reproductive trees) and
three half-sibs; and (iii) the four reproductive trees of the F1
generation produced an F2 generation of 33 established
recruits by either mating with each other (24 individuals) or
receiving immigrant pollen (nine individuals). In line with
these conclusions, first-generation plants were on average
larger than those belonging to the second generation
(mean + s.d.: 67.4 + 139.0 mm versus 5.6 + 5.1 mm; t-test:
t ¼ 2.56, d.f. ¼ 56, p ¼ 0.01; see also figure 2a).
Diversity estimates of the generations F1 and F2 are shown
in table 1. Both generations showed similar levels of moderate
gene diversity (HE) and marked heterozygote excess (FIS).
Interestingly, the F2 generation contained a higher number
of immigrant alleles and showed a higher allelic richness
than the F1 generation ( paired t-test: t ¼ 2.37, d.f. ¼ 9,
p ¼ 0.04).
(b) Acorns
The reproductive trees were homozygous at three loci (Qr7,
Qr112 and Msq4), whereas Mendelian segregation could be
assessed at the nine remaining loci on at least one tree. Null
alleles were identified for loci Qp36 and Qp46 (see above).
Paternity assignments of the analysed acorns are shown
in table 2. Nine (6.7%) out of the 135 acorns collected on
tree T1 and seven (5.8%) of the 120 acorns collected on tree
T4 contained at least two (and upto nine) loci with alleles
not present in any of the four reproductive trees, and were
hence inferred to result from pollen immigration. The remaining 126 acorns of tree T1 could be unequivocally assigned to a
single father tree: tree T3 in 46 per cent and tree T4 in 43 per
cent of the cases. Interestingly, the 113 non-immigrant acorns
of tree T4 were interpreted to result exclusively from selfing
events. Of these, 106 individuals were in full agreement
with this hypothesis across all 12 loci, and seven individuals
showed just one mismatch. Mismatches occurred exclusively
at loci for which the mother tree was homozygous or had
a putative null allele and were interpreted as resulting
from artefacts of the amplification process (e.g. three acorns
carried a similar PCR product at Msq13 that was not found
elsewhere in the population).
The overall frequency of immigrant genotypes in the analysed acorns (6%) did not differ statistically from that
observed in the F1 generation of established plants (12%;
x 2-test: x 2 ¼ 1.18, d.f. ¼ 1, p ¼ 0.28). On the contrary, it was
lower than that observed in the F2 generation (27%;
x 2 ¼ 16.3, d.f. ¼ 1, p , 0.001).
The two seed trees produced acorns of different weight
(mean + s.d.: T1, 2.04 + 0.40 g versus T4, 2.44 + 0.68 g;
t-test: t ¼ 5.68, d.f. ¼ 253, p , 0.001), pointing to maternal
effects [25]. However, we also found within each seedlot
differences in seed weight depending on paternal origin.
First, for tree T1, acorns originating from immigrant pollen
Proc R Soc B 280: 20131070
Table 2. Pollen donors assigned for acorns collected on the two major reproductive trees T1 and T4. Immigrant refers to acorns with at least two loci
containing alleles not present in the adult population and hence inferred to stem from pollen immigration. Numbers in parentheses denote percentages.
4
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Table 1. Diversity estimates for the F1 and F2 generations identified among the established plants. The number and percentage of immigrant genotypes refer
to individuals with alleles not found in the local parent trees (and hence assumed to originate from pollen immigration). The number of foreign alleles refers to
the alleles not present in the local parent trees (F1, n ¼ 2; F2, n ¼ 4). We report the multi-locus averages of allelic richness (RS, standardized to n ¼ 23),
gene diversity (HE) and heterozygote deficit (FIS). Differences of FIS from zero were tested using 10 000 permutations (Bonferroni-corrected).
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4. Discussion
(a) Disparate mating behaviour and the reproductive
dominance of one tree
All genotyped acorns of tree T4 resulted either from selfing or
from siring by immigrant pollen. Regular selfing is very rare in
trees, which are highly susceptible to inbreeding depression
and depend relatively little on reproductive assurance because
of their long lifespan [28,29]. The reduced seed weight of
selfed acorns compared with outcrossed ones from the same
tree and the quasi-absence of selfed seedlings in the established F2 generation (despite the abundant production of
selfed acorns by tree T4) point indeed towards the existence
of strong inbreeding depression (which is further confirmed
by a very low germination rate of selfed acorns; R. J. Petit
2004, unpublished data). The high selfing rate of tree T4 was
probably caused by reduced pollen availability, as self pollen
is typically out-competed by outcross pollen [30].
Overall, a small proportion of the potential crosses were
observed. For instance, few acorns of tree T1 were sired by
tree T2 (3.7%), although both trees are located within a few
metres of each other. More strikingly, effective pollen flow
between the two largest trees was completely uni-directional
(from T4 to T1). A phenological difference in the reproduction of trees T1 and T4 is unlikely to have caused this
pattern: while holm oak is protandrous, the delay between
male and female flowers on the same branch is only 2–3
days, much less than the temporal variation in flower
anthesis that exists across the tree crown [31]. The combination of predominant winds and unequal canopy size
(and hence uneven pollen production) could possibly result
in such an asymmetric gene flow. In any case, regardless of
the mechanism involved, asymmetric mating patterns are a
source of departure from panmixia, thereby reducing
effective population size.
(b) Pollen-mediated gene immigration and the rescue
of genetic diversity
The above findings suggest that the population should be
experiencing strong genetic drift. Along with the strong relatedness detected in the F1 generation and the strong inbreeding
depression characteristic of long-lived trees, this should result
in severe founder effects. However, our results show that
these expected founder effects are in fact alleviated by a nonnegligible amount of long-distance pollen inflow. More than
six per cent of all genotyped acorns were fathered by immigrant pollen, a notable fraction given that no adult holm oak
exists within 5 km around our population and the nearest
major stands are more than 30 km away. A rapidly increasing
body of evidence indicates that pollen gene flow over many
kilometres could indeed be a widespread phenomenon,
especially in wind-pollinated tree species [3,35].
The fraction of immigrant genotypes among the established plants of the F2 generation (27%) exceeded by far
that observed at the acorn stage (6%). This difference could
in principle arise from the increase in local pollen production
as trees grow older. This should in turn increase competition
for access to ovules, and hence decrease the likelihood of
immigration events through time. However, we consider it
more likely that the purging of inbred individuals during
early plant recruitment has contributed to this result [28].
This interpretation is backed by the facts that (i) inbred
seeds were lighter than outbred ones (an indicator for lower
fitness [36]), (ii) selfed individuals were virtually absent
from the established recruits and (iii) the F1 generation did
not contain significantly more immigrant genotypes than the
acorn cohort. In fact, the two founder trees are not close
relatives, according to our genotype reconstruction, and inbreeding effects in the F1 generation should therefore be
negligible, in contrast to what we expect in the F2 generation.
(c) Insights into the evolution of leading-edge
populations
Overall, our results, along with those of Lesser & Jackson [4],
suggest that leading-edge populations of wind-pollinated
trees could restore their genetic diversity within very few
generations owing to the combination of efficient longdistance pollen flow and marked inbreeding depression
during plant recruitment. Allelic richness is expected to be
more immediately affected by this recovery than heterozygosity [15]. The comparison of the F1 and F2 generations
supports this prediction (table 2). Various models have
recently addressed the evolution of genetic diversity of
5
Proc R Soc B 280: 20131070
While the role of long-distance dispersal events during range
expansions has been an object of intense research in the
past [5,6,8], empirical evidence for the mechanisms involved
in the subsequent establishment of leading-edge populations
remains scant (reviewed for plants in [4,27]). Our pedigree
reconstruction of a recently founded leading-edge population
revealed five phenomena with potentially relevant evolutionary implications: (i) all individuals are closely related; (ii) the
four reproductive trees show disparate mating patterns,
despite being full-sibs; (iii) one tree strongly dominates the
population’s reproduction; (iv) long-distance pollen flow
causes a non-negligible amount of gene immigration; and
(v) there is a remarkably high fraction of immigrant genotypes in the established recruits of the F2 generation.
Overall, our results suggest that the study population
should be able to recover high levels of genetic diversity
within very few generations, as also found in the case of
colonizing Pinus ponderosa populations [4].
Finally, 85 per cent of the established plants of the F2 generation were offspring of tree T1. The strong reproductive
dominance of tree T1 during the initial stage of population
establishment is likely to leave a strong imprint on the future
genetic composition and diversity of the study population
[32,33]. In addition, most of the corresponding seedlings
must have been mothered by this tree, considering that eight
of the nine F2 recruits sired by immigrant pollen had been
mothered by tree T1. In view of the expectation of strong
maternal effects in trees [34], the influence of tree T1 on the
next generation is likely to be even stronger than what one
might expect from considerations based only on Mendelian
inheritance.
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were heavier than acorns sired by local trees (2.28 + 0.41 g
versus 2.02 + 0.39 g; t-test: t ¼ 2.05, d.f. ¼ 133, p ¼ 0.04).
Second, for tree T4, acorns originating from immigrant
pollen were heavier than those originating from selfing
(2.95 + 0.65 g versus 2.39 + 0.67 g; t-test: t ¼ 2.53, d.f. ¼ 118,
p ¼ 0.01).
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could have a great influence on the colonization process
itself, two factors that have only recently been incorporated
in models of range expansions [38,39].
Finally, our results underpin that, once a few trees have
successfully established, long-distance pollen gene flow
appears sufficient to rapidly restore the genetic diversity
lost during initial establishment [40]. This conclusion supports the widely held but under-investigated idea that
range expansions of forest trees are primarily constrained
by the initial arrival of viable propagules rather than by
subsequent gene flow by pollen [4,8,27].
Funding statement. This work was partially funded by the EU projects
QLRT-2001-01594 (CREOAK) and BiodivERsA2012-15 (TipTree), as
well as the Spanish Ministry of Science project CGL2010-18381
(PERSLIM).
References
1.
Chen IC, Hill JK, Ohlemüller R, Roy DB, Thomas CD.
2011 Rapid range shifts of species associated with
high levels of climate warming. Science 333,
1024–1026. (doi:10.1126/science.1206432)
2. Petit RJ, Hu FS, Dick CW. 2008 Forests of the past:
a window to future changes. Science 320,
1450–1452. (doi:10.1126/science.1155457)
3. Kremer A et al. 2012 Long-distance gene flow and
adaptation of forest trees to rapid climate change.
Ecol. Lett. 15, 378–392. (doi:10.1111/j.1461-0248.
2012.01746.x)
4. Lesser MR, Jackson ST. 2003 Contributions of longdistance dispersal to population growth in
colonising Pinus ponderosa populations. Ecol. Lett.
16, 380–389. (doi:10.1111/ele.12053)
5. Dytham C. 2009 Evolved dispersal strategies at
range margins. Proc. R. Soc. B 276, 1407 –1413.
(doi:10.1098/rspb.2008.1535)
6. Excoffier L, Foll M, Petit RJ. 2009 Genetic
consequences of range expansions. Annu. Rev. Ecol.
Evol. Syst. 40, 481–501. (doi:10.1146/annurev.
ecolsys.39.110707.173414)
7. Roques L, Garnier J, Hamel F, Klein ET. 2012
Allee effect promotes diversity in traveling waves
of colonization. Proc. Natl Acad. Sci. USA
109, 8828 –8833. (doi:10.1073/pnas.
1201695109)
8. Nathan R. 2006 Long-distance dispersal of plants.
Science 313, 786–788. (doi:10.1126/science.
1124975)
9. Slatkin M, Excoffier L. 2012 Serial founder effects
during range expansion: a spatial analog of genetic
drift. Genetics 191, 171–181. (doi:10.1534/
genetics.112.139022)
10. Courchamp F, Clutton-Brock T, Grenfell B. 1999
Inverse density dependence and the Allee effect.
Trends Ecol. Evol. 14, 405– 410. (doi:10.1016/
S0169-5347(99)01683-3)
11. Grant PR, Grant BR, Petren K. 2001 A population
founded by a single pair of individuals:
establishment, expansion, and evolution. Genetica
112 – 113, 359–382. (doi:10.1007/978-94-0100585-2_22)
12. Thomas CD, Bodsworth EJ, Wilson RJ, Simmons AD,
Davies ZG, Musche M, Conradt L. 2001 Ecological
and evolutionary processes at expanding range
margins. Nature 441, 577 –581. (doi:10.1038/
35079066)
13. Vilà C et al. 2003 Rescue of a severely bottlenecked
wolf (Canis lupus) population by a single
immigrant. Proc. R. Soc. Lond. B 270, 91 –97.
(doi:10.1098/rspb.2002.2184)
14. Pujol B, Pannell JR. 2008 Reduced responses to
selection after species range expansion. Science 321,
96. (doi:10.1126/science.1157570)
15. Dlugosch KM, Parker IM. 2008 Founding events in
species invasions: genetic variation, adaptive
evolution, and the role of multiple introductions.
Mol. Ecol. 17, 431–449. (doi:10.1111/j.1365-294X.
2007.03538.x)
16. Badeau V, Dupouey JL, Cluzeau C, Drapier J, Le Bas
C. 2010 Climate change and the biogeography of
French tree species: first results and perspectives. In
Forests, carbon cycle and climate change (ed. QuaeINRA), pp. 231– 252. Versailles, France: INRA
Versailles.
17. Lumaret R, Mir C, Michaud H, Raynal V. 2002
Phylogeographical variation of chloroplast DNA
in holm oak (Quercus ilex L.). Mol. Ecol. 11, 2327–
2336. (doi:10.1046/j.1365-294X.2002.01611.x)
18. DAISIE. 2009 Handbook of alien species in Europe.
Dordrecht, The Netherlands: Springer.
19. Gómez-Casero MT, Hidalgo PJ, Garcı́a-Mozo H,
Domı́nguez E, Galán C. 2004 Pollen biology in four
Mediterranean Quercus species. Grana 43, 22 –30.
(doi:10.1080/00173130410018957)
20. Gómez JM. 2003 Spatial patterns in long-distance
dispersal of Quercus ilex acorns by jays in a
heterogeneous landscape. Ecography 26, 573 –584.
(doi:10.1034/j.1600-0587.2003.03586.x)
21. Dow BD, Ashley MV, Howe HF. 1995 Characterization
of highly variable (GA/CT)n microsatellites in the bur
oak, Quercus macrocarpa. Theor. Appl. Gen. 91,
137–141. (doi:10.1007/BF00220870)
22. Steinkellner H, Fluch S, Turetschek E, Lexer C, Streiff
R, Kremer A, Burk K, Glössl J. 1997 Identification
and characterization of (GA/CT)n—microsatellite
locus from Quercus petraea. Plant Mol. Biol. 33,
1093– 1096. (doi:10.1023/A:1005736722794)
23. Kampfer S, Lexer C, Glössl J, Steinkellner H. 1998
Characterization of (GA)n microsatellite loci from
Quercus robur. Hereditas 129, 183– 186. (doi:10.
1111/j.1601-5223.1998.00183.x)
24. Barreneche T, Casasoli M, Russell K, Akkak A,
Meddour H, Plomion C, Villani F, Kremer A. 2004
Comparative mapping between Quercus and
Castanea using simple-sequence repeats (SSRs).
Theor. Appl. Gen. 108, 558–566. (doi:10.1007/
s00122-003-1462-2)
25. Valière N. 2002 GIMLET: a computer program for
analysing genetic individual identification data. Mol.
Ecol. Notes 2, 377 –379. (doi:10.1046/j.1471-8286.
2002.00228.x)
26. Goudet J. 2001 FSTAT, a program to estimate
and test gene diversities and fixation indices, v.
2.9.3. See http://www.unil.ch/izea/softwares/
fstat.html.
27. Hampe A. 2011 Plants on the move: the role
of seed dispersal and initial population
establishment for climate-driven range expansions.
Acta Oecol. 37, 666– 673. (doi:10.1016/j.actao.
2011.05.001)
28. Petit RJ, Hampe A. 2006 Some evolutionary
consequences of being a tree. Annu. Rev. Ecol. Evol.
Proc R Soc B 280: 20131070
Acknowledgements. We are most indebted to Marjorie Battle and Didier
Bert for their help during fieldwork, to Vincent Badeau for providing
us with figure 1, and to Etienne Klein, Francisco Rodrı́guez-Sánchez
and two anonymous reviewers for insightful comments on the
manuscript.
6
rspb.royalsocietypublishing.org
leading-edge populations, but few have been confronted with
empirical data. Given the marked reproductive dominance of
tree T1, our results could in principle be interpreted as a
snapshot of an ongoing process of allele surfing [6], although
this phenomenon should be partly counteracted by the elevated gene immigration observed. More importantly, our
results support the idea that negative demographic consequences of Allee effects can be counter-balanced by their
beneficial impacts on gene flow. A good example of this seemingly paradoxical conclusion is the work of Roques et al. [7],
which modelled a scenario of expansion with Allee effects
(but without long-distance gene flow). Our expectation is
that most leading-edge populations of tree species that managed to establish and eventually expand should have
benefitted from this rescue effect, in view of their typically
high inbreeding depression (that make them prone to Allee
effects). To date, the literature on range expansions typically
focuses on the negative consequences of Allee effects [4,37].
On the other hand, our study also suggests that mating patterns and kin competition within leading-edge populations
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30.
32.
34.
35.
36.
37. Tobin PC, Berec L, Liebhold AM. 2011 Exploiting
Allee effects for managing biological invasions. Ecol.
Lett. 14, 615–624. (doi:10.1111/j.1461-0248.2011.
01614.x)
38. Shine R, Brown GP, Phillips BL. 2011 An
evolutionary process that assembles phenotypes
through space rather than through time. Proc. Natl
Acad. Sci. USA 108, 5708–5711. (doi:10.1073/pnas.
1018989108)
39. Kubisch A, Fronhofer EA, Poethke HJ, Hovestadt T.
2013 Kin competition as a major driving force for
invasions. Am. Nat. 181, 700–706. (doi:10.1086/
670008)
40. Breed MF, Ottewell KM, Gardner MG, Lowe AJ. 2011
Clarifying climate change adaptation responses for
scattered trees in modified landscapes. J. Appl. Ecol.
48, 637 –641. (doi:10.1111/j.1365-2664.2011.
01969.x)
7
Proc R Soc B 280: 20131070
31.
33.
genetic rescue during limiting environmental
conditions in an isolated wolf population.
Proc. R. Soc. B 278, 3336 –3344. (doi:10.1098/rspb.
2011.0261)
Moran E, Clark JS. 2012 Causes and consequences of
unequal seedling production in forest trees: a case
study in red oaks. Ecology 93, 1082 –1094. (doi:10.
1890/11-1428.1)
Revardel E, Franc A, Petit RJ. 2010 Adaptive parental
effects promoted by sex-biased dispersal. BMC Evol.
Biol. 10, 217. (doi:10.1186/1471-2148-10-217)
Buschbom J, Yanbaev Y, Degen B. 2011 Efficient
long-distance gene flow into an isolated relict oak
stand. J. Hered. 102, 464– 472. (doi:10.1093/
jhered/esr023)
Gómez JM. 2004 Bigger is not always better:
conflicting selective pressures on seed size in Quercus
ilex. Evolution 58, 71–80. (doi:10.1554/02-617)
rspb.royalsocietypublishing.org
29.
Syst. 37, 187 –214. (doi:10.1146/annurev.ecolsys.
37.091305.110215)
Duminil J, Hardy OJ, Petit RJ. 2009 Plant traits
correlated with generation time directly affect
inbreeding depression and mating system and
indirectly genetic structure. BMC Evol. Biol. 9, 177.
(doi:10.1186/1471-2148-9-177)
Holsinger KE. 1991 Mass-action models of plant
mating systems: the evolutionary stability of mixed
mating systems. Am. Nat. 138, 606– 622. (doi:10.
1086/285237)
Varela MC, Brás R, Barros IR, Oliveira P, Meierrose C.
2008 Opportunity for hybridization between two oak
species in mixed stands as monitored by the timing
and intensity of pollen production. For. Ecol. Manage.
256, 1546–1551. (doi:10.1016/j.foreco.2008.06.049)
Adams JR, Vucetich LM, Hedrick PW, Peterson RO,
Vucetich JA. 2011 Genomic sweep and potential