Distinct male reproductive strategies in two closely related oak species

Distinct male reproductive strategies in two closelyrelated oak species

L �ELIA LAGACHE,*† ETIENNE K. KLEIN,‡ ALEXIS DUCOUSSO*† and R �EMY J. PETIT*†

*INRA, UMR 1202 Biogeco, F-33610 Cestas, France, †Univ. Bordeaux, UMR1202 Biogeco, F-33400 Talence, France,

‡Biostatistique et Processus Spatiaux (BioSP), INRA, UR546, F-84914 Avignon France

Abstract

Reproductive strategies of closely related species distributed along successional gradi-

ents should differ as a consequence of the trade-off between competition and coloniza-

tion abilities. We compared male reproductive strategies of Quercus robur and

Q. petraea, two partly interfertile European oak species with different successional sta-

tus. In the studied even-aged stand, trees of the late-successional species (Q. petraea)grew faster and suffered less from intertree competition than trees of the early-

successional species (Q. robur). A large-scale paternity study and a spatially explicit

individual-based mating model were used to estimate parameters of pollen production

and dispersal as well as sexual barriers between species. Male fecundity was found to

be dependent both on a tree’s circumference and on its environment, particularly so

for Q. petraea. Pollen dispersal was greater and more isotropic in Q. robur than in

Q. petraea. Premating barriers to hybridization were strong in both species, but more

so in Q. petraea than in Q. robur. Hence, predictions based on the competition–coloni-zation trade-off are well supported, whereas the sexual barriers themselves seem to be

shaped by colonization dynamics.

Keywords: ecological speciation, male fecundity, pollen dispersal, Quercus petraea, Quercus

robur, spatially explicit model

Received 6 December 2013; revision received 12 March 2014; accepted 8 April 2014

Introduction

The coexistence of competing populations or species is

often attributed to differing ecological strategies, that is,

specific combinations of life history traits evolved in

response to multiple selective pressures and under mul-

tiple trade-offs (Newell & Tramer 1978; Westoby et al.

2002; Burton et al. 2010). One important trade-off is that

between competition and colonization abilities, resulting

in two distinct ecological strategies, one in which infe-

rior competitors are better colonists and another where

superior competitors are poorer dispersers (Levins &

Culver 1971; Tilman 1994; Harbison et al. 2008). At the

interspecific level, the competition–colonization trade-

off has been used to explain the coexistence of species

characterized by different life history traits along suc-

cessional gradients, including traits related to reproduc-

tion (e.g. Ackerly 2003; Kneitel & Chase 2004; Calcagno

et al. 2006). According to Pickett (1976), ‘the complex,

dynamic pattern of selection pressures in the landscape

[should allow] for the assortment of species into different suc-

cessional positions’, because succession provides a com-

plex gradient of physical and biotic environments to

which a single species cannot be uniformly adapted.

Hence, comparing reproductive strategies of closely

related species with different colonization dynamics

and successional status, and sexual barriers between

them, could help clarify the emergence of distinct eco-

logical strategies.

Traditionally, comparative studies of reproductive

strategies in plants have focused on the female compo-

nent, with fitness estimated by counting the relative

numbers of seeds produced (Primack & Kang 1989). Yet

the fitness of an individual plant is equally determined

by its success as a male parent in fertilizing ovules

(Lloyd 1980a; Morgan & Conner 2001). Moreover, while

dispersal to new patches of habitat requires seedCorrespondence: R�emy Petit, Fax: +33557122881;

E-mail: [email protected]

© 2014 John Wiley & Sons Ltd

Molecular Ecology (2014) 23, 4331–4343 doi: 10.1111/mec.12766

dispersal, subsequent demographic growth depends in

part on pollen immigration as it helps overcome

inbreeding depression (e.g. Hampe et al. 2013; Lesser &

Jackson 2013). For these two reasons, it should be valu-

able to focus on components of male reproductive fit-

ness in species having different successional status.

Comparing male fecundity and pollen dispersal of dif-

ferent species can now be performed using paternity

analysis, taking advantage of methodological develop-

ments in the field (Meagher 1986; Devlin & Ellstrand

1990; Smouse et al. 1999; Burczyk et al. 2002; Oddou-

Muratorio et al. 2005). Theory predicts greater pollen

dispersal, more even pollen production and less strin-

gent mate choice in the pioneer species than in the late-

successional one (e.g. Lloyd 1980b; Richards 1996;

Ronce & Olivieri 1997; Burton et al. 2010). To what

extent this holds for different plant species has not been

explicitly investigated to date.

Here, we compare male reproductive strategies of

two partly interfertile tree species with contrasting colo-

nization dynamics using a large-scale paternity analysis.

Our aim is to evaluate the extent to which their male

reproductive strategies differ in the direction predicted

by theory. The spatially explicit individual-based mat-

ing model introduced by Lagache et al. (2013a) was

used as a starting point for predicting mating events

within and between species. This model was expanded

to control for anisotropic pollen dispersal (Torimaru

et al. 2012) and for variation in male fecundity caused

by tree size (Oddou-Muratorio et al. 2005; Chybicki &

Burczyk 2013), environment (e.g. De Cauwer et al. 2012;

Chybicki & Burczyk 2013) and interplant phenological

overlap (Slavov et al. 2005; Wendt et al. 2011). Using

this expanded mating model, we identify the traits that

affect the mating system of the two species. We then

ask whether differences between species can be inter-

preted in terms of adaptive responses to species coloni-

zation dynamics.

Materials and methods

Study species

We selected the pedunculate (Quercus robur L.) and ses-

sile oaks [Q. petraea (Matt.) Liebl.] as model species pair

for this study. These two long-lived, widespread and

abundant forest tree species are partly interfertile and

have similar geographical distributions in Europe but

contrasting colonization dynamics. Quercus robur is a

pioneer species that can colonize more open environ-

ments, whereas Q. petraea is a more competitive late-

successional species that typically lives in mature

forests (Petit et al. 2003). Quercus robur is therefore

expected to invest a larger share of its energy in female

and male reproduction organs, including attributes

favoring seed and pollen dispersal, than Q. petraea. In

contrast, Q. petraea is expected to invest a larger share

of its energy in growth and competition than Q. robur.

Previous studies have reported greater reserves in the

cotyledons of Q. robur acorns and faster growth of

Q. robur seedlings (Dupouey & Le Bouler 1989; Fried-

man & Barrett 2009; G�erard et al. 2009; Landergott et al.

2012). Furthermore, greater seed dispersal was inferred

in Q. robur than in Q. petraea on the basis of genetic

structure at maternally inherited markers (reviewed in

Petit et al. 2003). Quercus robur and Q. petraea have also

been the target of numerous mating system and parent-

age studies spanning nearly two decades (e.g. Bacilieri

et al. 1996; Streiff et al. 1999; Jensen et al. 2009; Lepais &

Gerber 2011; Chybicki & Burczyk 2013; Lagache et al.

2013a). While these studies suggest greater pollen dis-

persal in the pioneer Q. robur than in the late-succes-

sional Q. petraea, they did not rely on estimated

dispersal kernels (more robust to spatial design, Hardy

2009) and did not investigate male fecundity patterns.

Study site

The study site is a mixed oak stand of 5 ha located in

the Petite Charnie State Forest in western France (lati-

tude: 48.056°N, longitude: 0.168°W). It contains both

Q. petraea and Q. robur adult trees (Fig. 1, Data S1, Sup-

porting Information). We determined the taxonomic sta-

tus of 260 of the 298 trees growing in the stand with

multilocus genetic data using Bayesian assignment

methods (Pritchard et al. 2000). The genetic data

were obtained with a 12-plex microsatellite assay and a

384-plex single-nucleotide polymorphism assay (Guic-

houx et al. 2011, 2013; Lagache et al. 2012, 2013a). For

the 38 remaining trees, for which no tissue was avail-

able for genetic analysis, we relied on previously pub-

lished leaf morphological data (Bacilieri et al. 1995).

Molecular-based and morphologically based taxonomic

approaches have been shown to give largely congruent

results in these oaks (Lagache et al. 2013b). Quercus pet-

raea formed a smaller proportion of the stand than did

Q. robur (40% vs. 55%, the remaining 5% being admixed

trees). In 1995, 3780 seeds were harvested on all adult

trees that had produced a significant acorn crop, that is,

on 22 Q. petraea, 26 Q. robur and three admixed mother

trees. The 51 mother trees were well distributed

throughout the stand (Fig. 1). The resulting seedlings

were grown in a nursery and subsequently planted in a

progeny test located near the adult stand.

The adult stand is situated on a regular slope that

forms an ecological gradient, over humid clay soil in

the lower part up to relatively dry silt and sandy soil in

the upper part. Bacilieri et al. (1995) produced a


4332 L. LAGACHE ET AL.

fine-scale topographical map of the stand by measuring

terrain elevation every two metres across the stand

(Data S2, Supporting Information). We can thus deduce

the approximate terrain elevation at which each tree

was growing, from the bottom (altitude <135 m) to the

top (altitude >146 m), summarized by a class score

between 1, being the lowest class, and 9.

Phenotypic data

Bacilieri et al. (1995) studied the flowering phenology of

the two oak species in this stand during three years

(1989, 1991 and 1992). They found that on average pol-

len shedding from catkins precedes female flowers’

receptivity by 4–7 days. As phenological ranks are very

stable among years (Bacilieri et al. 1995) and leaf phe-

nology is highly heritable in oaks (Alberto et al. 2011),

flowering phenology data from one year should help

predict compatible mating events in other years. We

used data from 1992 because it included most records.

During two months in that year, two ratings of the phe-

nological stages (one for female flowers and one for

male flowers) were made each week for each of the 298

individuals in the stand. For all pairs of candidate trees,

we computed the number of weeks where male flower-

ing of the candidate father k overlapped female flower-

ing of the mother j: OPjk varied between 1 and 4. In

addition, for all adult trees (i.e. 298 individuals), the

height (H) and the circumference at 1.3 m above ground

level (Cir1.3) were measured in 1998 before clear-cutting

of the stand. We used the circumference as a predictor

of male fecundity and the H/DBH index (where DBH =Cir1.3/p) as a life-long indicator of tree competition

(Becker 1992). Trees with a high H/DBH index are con-

sidered to have suffered more from competition than

other trees. Finally, to determine tree ages, the number

of rings was counted on the stump (approximately

25 cm above the ground) after trees were felled.

Paternity analysis

Details on genotyping methods and on paternity analy-

sis are provided in Lagache et al. (2013a). Briefly, using

12 highly polymorphic microsatellite markers, simple

paternity exclusion tests were performed for the 3046

offspring for which genotypic data were available. They

identified a single father for 51.7% of the offspring (615

Q. petraea and 855 Q. robur) and two or more compati-

ble fathers for 1.8% of the offspring (22 Q. petraea and

31 Q. robur). The remaining individuals (427 Q. petraea

and 885 Q. robur, i.e. 46.5% of all offspring) had no

compatible father among the 260 adult trees genotyped.

Following Lagache et al. (2013a), we decomposed off-

spring whose fathers were not found into two groups:

offspring sired by ‘ghost’ fathers located inside the

stand, for which taxonomic status (species assignment

based on morphological markers), circumference and

terrain elevation were available but for which genotypic

data were missing; and offspring sired by fathers

located outside the stand (i.e. immigration), for which

no information at all was available.

Spatially explicit mating model

We used a spatially explicit individual-based mating

model to investigate intra- and interspecific mating

events with pollen from inside and outside the studied

stand (Data S3, Supporting Information). This allows a

simultaneous estimation of all the parameters influenc-

ing male fecundity and pollen dispersal using a classi-

cal likelihood approach (e.g. Oddou-Muratorio et al.

2003; De Cauwer et al. 2012; DiFazio et al. 2012). In this

approach, the probability that a seed o from mother johas genotype go is:

Pðgo j gjoÞ ¼ sTðgo j gjo ;gjoÞþ ð1� sÞ½migjoPTðgo j gjo ;AFPÞþmigjoRTðgo j gjo ;AFRÞþ

Xk:candidates

pjokTðgo j gjo ;gkÞ�

ðeqn 1Þ

where s is the selfing rate; T(go|.,.) are the Mendelian

probabilities of generating the offspring’s genotype go

Fig. 1 Map of the study stand. Quercus robur trees are repre-

sented by grey diamonds, Q. petraea trees by black squares and

intermediate trees by white triangles. Sampled mother trees

are circled. Ghost trees (for which genotypic data were miss-

ing) are represented in light grey diamonds for Q. robur, light

grey squares for Q. petraea and light grey triangles for interme-

diate trees.


MALE REPRODUCTIVE STRATEGIES IN OAKS 4333

from the known genotypes of the two parents; AFR and

AFP are the microsatellite allelic frequencies of Q. robur

and Q. petraea; migjR and migjP correspond to the two

apparent migration rates (Q. robur and Q. petraea) on

mother j (‘apparent’ because they include pollen from

ghost trees); and pjk is the relative contribution of the

candidate father k to the pollen pool of mother j

(detailed below). As in Lagache et al. (2013a), we mod-

elled pollen immigration from outside the stand using a

mass-action law (Holsinger 1991). Migration rates can

thus vary across mothers (see details below).

Modelling the relative contributions of the candidatefathers to the pollen pools (pjk)

The relative contribution pjk of the candidate father k to

the pollen pool of mother j results from the competition

with pollen from all other candidate fathers together

with pollen from all ghost trees and with immigrant

pollen. Following Smouse & Sork (2004), we considered

two kinds of factors determining the pollen pool avail-

able to each mother tree j: factors affecting the male

fecundity of each father tree k of the stand (Fk) and fac-

tors affecting the cross-compatibility between each

mother j and father k (Compatjk):

where qP(DEj) and qR(DEj) are the relative amounts of

Q. petraea and Q. robur pollen coming from outside the

stand received by the mother j, at a distance DEj of the

edges of the plot. The measures qP(DEj) and qR(DEj) are

relative to a tree with a male fecundity equal to one

and present at the edge of the plot. hspj,R and hspj,P rep-

resent the postdispersal relative fertilization successes

on mother j of each Q. robur pollen grain (hspj,R) and of

each Q. petraea pollen grain (hspj,P).

The fecundity component (Fk) in eqn. 2 includes the

effects of circumference and terrain elevation following:

Fk ¼exp aCir1:3 ;spk Cir1:3;k � Cir1:3� ��

expðaspk þ bspkELkÞ1þ expðaspk þ bspkELkÞ

ðeqn 3Þ

where Cir1.3,k and ELk are the circumference and terrain

elevation for tree k, and Cir1:3 is the average circumfer-

ence of trees in the study site. One set of parameters

(a, b, aCir1:3 ) applies to each of the three categories

(Q. petraea, Q. robur and admixed trees). The circumfer-

ence parameter (aCir1:3 ) measures the direction and

strength of the effect of circumference on fecundity (0:

no effect, >0: bigger trees are more fecund; < 0: bigger

trees are less fecund). Elevation parameters (a, b) deter-

mine the inflection point (i.e.�a/b) and the slope (i.e. if

b is small, the slope is weak) of the sigmoidal curve

relating fecundity to elevation. Finally, spk is the species

of tree k.

The compatibility component in eqn. 2 includes

effects of spatial distance between parents, overlapping

phenology and interspecific sexual barriers:

compatjk ¼ cPOjkhspj;spk fEPðdjk; azjk; dspk ; bspk ; jspk ; hspkÞ

ðeqn 4Þwhere POjk, djk and azjk are the distance, phenological

overlap and azimuth between trees j and k, respectively,

and fEP is the anisotropic exponential power dispersal

kernel (detailed below). Different sets of parameters (d, b,j, h) apply to the three groups (Q. petraea, Q. robur and

admixed trees) and must be estimated. Six h parameters

quantify the intensities of sexual barriers for an allospeci-

fic pollen grain relative to a conspecific pollen grain (two

between Q. robur and Q. petraea, one in each direction).

Four c parameters quantify the relative pollination suc-

cess for pairs of trees with different overlapping periods.

Parameters c and h also need to be estimated.

To model pollen dispersal, we took into account not

only the distance but also the azimuth between trees,

following Torimaru et al. (2012). As the pollen dispersal

curves of the two species were known to differ (Lagache

et al. 2013a), we modelled different anisotropic exponen-

tial power pollen dispersal kernels for each species:

fEPðd;az;d;b;j;hÞ/ exp � dCð3=bÞdCð2=bÞ

� �b" #

exp½jcosðaz�hÞ�;

ðeqn 5Þwhere d is the mean dispersal distance, b the shape

parameter, j the intensity of anisotropy and h (in radian

with east as starting point) the main direction of anisot-

ropy.

Modelling apparent and true pollen immigration

As in Lagache et al. (2013a), our model allowed immi-

grant pollen to compete with pollen produced inside the

stand, resulting in immigration rates that can vary across

mother trees following the mass-action law (Holsinger

pjk ¼ Fk � CompatjkPl:candidates Fl � Compatjl þ

Pl:ghosts Fl � Compatjl þ qPðDEjÞhspj;P þ qRðDEjÞhspj;R

ðeqn 2Þ



1991). The model also accounts for the positions of ghost

trees relative to each mother tree. While the offspring

sired by the different ghost trees cannot be distinguished

from each other nor from offspring sired by immigrant

pollen on an individual basis, the explicit inclusion of

ghost trees in the model enabled us to estimate the

amounts of true immigrant pollen after statistically

removing (i.e. partialling out) the pollen from ghost trees

from the set of unassigned seeds. To take into account

possible edge effects (e.g. a mother tree near the edge of

the stand might receive more immigrant pollen than a

mother tree located in the middle), we considered that

the amount of true immigrant pollen from each species

qR and qP decreased with the distance to the edges of the

plot. We therefore computed DEj, the distance of mother

tree j to the closest edge of the stand, and defined:

qPðDEjÞ ¼ qPexpðam;P þ bm;PDEjÞ

1þ expðam;P þ bm;PDEjÞ and

qRðDEjÞ ¼ qRexpðam;R þ bm;RDEjÞ

1þ expðam;R þ bm;RDEjÞðeqn 6Þ

where qP(0) and qR(0) are the amounts of pollen of

Q. petraea and Q. robur at the edge of the plot (i.e.

DEj = 0). The parameters qP and qR correspond to the

amount of pollen from each species received per unit

area relative to the total emission of a tree with a fecun-

dity equal to 1. am,P, bm,P, am,R, bm,R are parameters of

pollen dilution with distance to the edge of the plot.

The Q. robur and Q. petraea apparent immigration

rates on a mother tree j (i.e. migjR and migjP) were then

calculated by summing true immigration with contribu-

tions from ghost trees:

Parameter estimation

The log-likelihood of the full genotypic data set was

computed by summing the logarithm of eqn. 1 for the

3046 genotyped offspring. All computations necessary

to derive the likelihood were conducted with MATHEMATI-

CA 8.1 (Wolfram Research Inc. 2010). We maximized the

log-likelihood using a quasi-Newton algorithm to obtain

maximum-likelihood estimates for all parameters con-

sidered. The maximization was repeated several times

using different initial values in order to be confident

that we had reached a global maximum.

Likelihood ratio tests

Thirteen submodels were fitted to the data to investi-

gate different biological hypotheses by omitting or fix-

ing different parameters of interest. Likelihood ratio

tests were then used to test the hypotheses (i.e. to

investigate the significance of fixed parameters in the

full model), following Oddou-Muratorio et al. (2005).

First, the general effect and species-specific effect of

circumference on male fecundity were studied by con-

trasting the full model with a model without this effect

of circumference on male fecundity and with a model

with the same effect of circumference on the male

fecundity for both species. Second, the full model was

compared with a model without the effect of terrain

elevation on male fecundity and with a model where

the effect of terrain elevation on male fecundity is the

same for both species. Third, we contrasted the full

model with one with no phenological effect on cross-

ing probability. Fourth, we compared the full model

with one where the sexual barriers are symmetric

between Q. robur and Q. petraea (hPR = hRP). Fifth, the

effect of pollen dispersal on mating events was studied

by contrasting the full model with an unlimited dis-

persal model and with a model with the same dis-

persal parameters for both species. Sixth, the full

model was compared with a model where there is no

anisotropic effect on pollen dispersal and with a model

where this anisotropic effect is the same for both spe-

cies. Seventh, we tested whether different amounts of

Q. robur and Q. petraea pollen come from outside the

stand by fitting a model with the same amounts of

immigrant pollen for the two species [qP(0) = qR(0)].

Eighth, we compared the full model with a model

without edge effect on the amount of immigrant pol-

len, assuming that whatever the position of a mother

tree, it receives the same amount of Q. robur or of

Q. petraea immigrant pollen. Ninth, we compared the

full model with a model where the edge effect is the

same for both species.

We also explored two other more complex models by

extending the full model described above. First, we cre-

ated a model where pollen dispersal curves can differ

migjR ¼P

l:robur ghosts Fl � Compatjl þ qRðDEjÞHybjRPl:candidates Fl � Compatjl þ

Pl:ghosts Fl � Compatjl þ qPðDEjÞHybjP þ qRðDEjÞHybjR

ðeqn 7Þ

migjP ¼P

l:petraea ghosts Fl � Compatjl þ qPðDEjÞHybjPPl:candidates Fl � Compatjl þ

Pl:ghosts Fl � Compatjl þ qPðDEjÞHybjP þ qRðDEjÞHybjR

ðeqn 8Þ



for groups of trees that flower at different times. Sec-

ond, we studied whether relatedness between father

trees and mother trees modifies fertilization success

within each species, as detailed in Appendix S1 (Sup-

porting Information).

Effective male population size

To test whether intertree variation in male fecundity

differs between species, we first estimated the fecundity

of each tree with the complete model. As the absolute

amounts of pollen produced by individual trees are not

known, we present relative fecundities with reference to

a tree of average circumference (1.73 m) growing in ter-

rain elevation class nine. We then computed the coeffi-

cient of variation (CV) of relative male fecundities

within each species and its confidence interval (for

a = 0.05) and compared them. All else being equal, the

species with the more heterogeneous male fecundities

across individuals (i.e. a larger CV) should have a smal-

ler male effective population size.

The effective number of fathers (Ke) provides another

estimate of effective population size. It corresponds to

the number of offspring that need to be examined in a

given maternal progeny to find two offspring sired by

the same father (i.e. the inverse of the probability of

copaternity). We used the unbiased estimate of Ke pro-

posed by Nielsen et al. (2003) to compute the effective

number of fathers in the progeny of a tree:

Ke ¼ ðn� 1Þ2Pnk¼1 p

2kðnþ 1Þðn� 2Þ þ 3� n

ðeqn 9Þ

where pk and n are, respectively, the proportion of off-

spring sired by a given father tree k and the number of

offspring sampled in the progeny of a given mother

tree. A simple paternity exclusion analysis for each

mother tree was used to compute the average Ke for

each species and a Kruskal–Wallis test was used to

evaluate the significance of the difference between spe-

cies. Note that in the computation of Ke, we excluded

fathers located outside the plot. For a full picture of the

diversity in the maternal progeny of each individual,

differences in immigration rates ought to be accounted

for. Here, they were investigated separately through a

comparison of immigration parameters.

Results

Direct comparison of growth and phenology

In the studied stand, Quercus petraea trees are larger on

average (Cir1.3: 1.84 m; height: 26.5 m) than Q. robur

trees (Cir1.3: 1.67 m; height: 25.1 m; both P-val-

ues < 10�4; Table 1 and Data S4A, Supporting Informa-

tion), that is, by 10.2% for circumference and by 5.6%

for height. Yet, on the basis of ring counts, both species

have the same age (mean of 100 years in 1998 for each

species, P-value = 0.74; Table 1). The tree competition

index H/DBH also differs between the two species (45.2

for Q. petraea vs. 47.2 for Q. robur; P-value = 0.002;

Table 1), suggesting that Q. petraea trees suffered less

than Q. robur trees from competition. Quercus petraea

trees are more frequent in high terrain elevation classes

than Q. robur trees (6.9 vs. 4.7, P-value < 10�4; Table 1

and Data S4B, Supporting Information). There is also a

slight phenological shift between the two species with

Q. petraea trees flowering later than Q. robur trees (first

record of mature male and female flowers for Q. petraea:

3.5 and 3.9 vs. 3.0 and 3.3 for Q. robur; both

P-values < 10�4; Table 1 and Data S4C, Supporting

Information).

Comparisons based on the spatially explicit matingmodel

Our main interest was to study the fecundity and mat-

ing behaviour of pure bred individuals from each spe-

cies. Because the admixed category includes few

individuals (n = 14) and is very heterogeneous, with

some individuals in this category being very similar to

either Q. robur or Q. petraea, the average parameters

estimated for this category are not presented.

Male fecundity parameters

Individual male fecundity depends on tree circumfer-

ence (Table 2). In both species, larger trees are more

fecund (positive values of aCir1.3 in Table 3). However,

the effect is stronger on Q. robur trees than on Q. petraea

trees (Table 2 and Fig. 2a). Terrain elevation also has a

Table 1 Main characteristics of Quercus petraea and Q. robur

trees

Phenotypic data Q. petraea* Q. robur* P-value†

Circumference (m) 1.84 (0.42) 1.67 (0.24) <10�4

Height (m) 26.5 (1.6) 25.1 (1.6) <10�4

H/DBH 45.2 (2.0) 47.2 (1.8) 0.002

Age (years) 100 (4) 100 (4) 0.74

Terrain elevation (m) 6.9 (1.3) 4.7 (1.7) <10�4

1st record of a mature ♂

flower

3.5 (0.6) 3.0 (0.7) <10�4

1st record of a mature ♀

flower

3.9 (0.4) 3.3 (0.7) <10�4

*Mean values with standard deviation in brackets.†Comparison between species: Kruskal–Wallis test for indepen-

dent samples.



significant effect on male fecundity (Table 2), with trees

located higher on the slope being more fecund

(Table 3). Interestingly, this effect differs for the two

species (Table 2), with male fecundity of Q. petraea trees

being more reduced at low terrain elevation than male

fecundity of Q. robur trees (Fig. 2b).

Mating compatibility between trees

Distance between trees has the greatest influence on

observed mating patterns (Table 2). Moreover, pollen

dispersal curves are not the same for both species

(Table 2). Indeed, we found that Q. petraea trees dis-

persed their pollen over shorter distances within the

study site (mean pollination distance of 97 m, with a

thinner-tailed dispersal kernel: b = 0.48) than Q. robur

trees (137 m, b = 0.25) (Table 3 and Fig. 3a). Pollen dis-

persal is directional in both species (i.e. models without

anisotropy have a lower likelihood than models in which

anisotropy is included, Table 2), but the directionality of

crosses is stronger in Q. petraea than in Q. robur

(jP = 1.21 > jR = 0.66; P-value < 10�4; Table 2). The

preferential direction is from east to west in Q. petraea

(hP = 0.17 rad; Table 2 and Fig. 3b) and from northeast

to southwest in Q. robur (hR = 1.14 rad; Table 2 and

Fig. 3b).

Taking the phenological overlap between mother trees

and father trees into account significantly improves

model fit (Table 2). As expected, the longer the overlap

Table 2 Likelihood ratio test of the significance of each sub-

model

Model* �log DlogL ddl† P-value‡

Full model 61423 – 37 –

Diameter effect on male

fecundity

aCirc1:3;P= aCirc1:3;R= 0 ?

61513 90 3 <10�4

Species-specific diameter effect

on male fecundity

aCirc1:3;P= aCirc1:3;R ?

61432 9 1 0.027

Terrain elevation effect on

male fecundity

bP = bR = 0 ?

61448 25 6 <10�3

Species-specific terrain

elevation effect on male

fecundity

bP = bR ?

61442 19 2 <10�4

Phenology effect on cross-

compatibility

cPOJk=1 = cPOJk=2 = cPOJk=3

= cPOJk=4 = 1 ?

61448 25 3 <10�4

Asymmetric hybridization

hPR = hRP ?

61431 8 1 0.0047

Distance effect on cross-

compatibility

dP = dR = ∞ ?

62565 1142 6 <10�4

Species-specific pollen

dispersal

dP = dR and bP = bR ?

61433 10 2 0.0067

Anisotropic pollen dispersal

jP = jR = 0 ?

61606 183 6 <10�4

Species-specific anisotropy of

pollen dispersal

jP = jR and hP = hR ?

61495 72 2 <10�4

Species-specific pollen

immigration rates

qP(0) = qR(0) ?

61432 9 1 0.0027

Immigration rate with edge

effects

bmP = bmP = 0 ?

61449 26 4 <10�4

Species-specific edge effects

bmP = bmR and amP = amR ?

61432 9 3 0.029

*All models listed are based on the full model modified in one

respect to yield the corresponding submodel.†ddl is the number of estimated parameters for the full model

and for all other cases the number of parameters that are fixed

and not estimated.‡P-values lower than 0.05 indicate that the full model is signifi-

cantly more informative than the tested submodel.

Table 3 Parameters estimated from the spatially explicit

mating model

Parameter* Estimated value

aCirc1:3;P 0.0075

aCirc1:3;R 0.0161

aP �5.7

aR �2.5

bP 0.81

bR 2.17

cPOJk=1 0.57

cPOJk=2 0.69

cPOJk=3 1

cPOJk=4 0.68

hPR 0.00095

hRP 0.035

dP (m) 97

dR (m) 137

bP 0.48

bR 0.25

jP 1.21

jR 0.66

hP 0.17

hR 1.14

qP(0) 0.0010

qR(0) 0.0018

amP �8.3

bmP �0.017

amR �4.1

bmR �0.005

*In total, 37 parameters were estimated, but the 11 parameters

for hybrid/intermediate trees (hIP, hIR, hPI, hRI, dI, bI, jI, hI, aI, bIand aCirc1:3;I ), are not shown in this table.



between male and female flowering, the greater the likeli-

hood of mating between the trees (except for the fourth

overlap class that was under-represented; Table 3). The

sexual barriers to hybridization are on average 37 times

more porous in Q. robur than in Q. petraea mother trees

(hRP = 0.035 vs. hPR = 0.00095, P-value < 10�4; Tables 2

and 3). In comparison with the study of Lagache et al.

(2013a) based on the same genotypic data but a much

simpler model, the estimates of pollen dispersal parame-

ters and sexual barriers tend to vary in the same direction

(Appendix S2, Supporting Information).

We did not find any effect of trees relatedness on

mating success within species (Appendix S1, Support-

ing Information). In contrast, we found that in Q. robur,

early- and mid-season-flowering trees have their pollen

dispersed at shorter distances than late-flowering trees

(mean pollen dispersal of 95, 114 and 193 m for the

early, intermediate and late periods, P-value < 10�4).

This difference seems to be due to an increase in the

proportion of pollen dispersing to long distances in

late-flowering trees, as suggested by differences in the

parameter b of the dispersal curve (0.60, 0.23 and 0.16

for the early, intermediate and late periods). On the

contrary, the pollen dispersal curve for Q. petraea does

not change significantly during the season (mean pollen

dispersal of 96 and 100 m for mid-season- and late-

flowering trees; P-value = 0.27).

Immigration

In the studied flowering episode, immigrant pollen was

approximately half as abundant in Q. petraea as in

Q. robur (at the edge of the stand: qP(0) = 0.0010 vs.

qR(0) = 0.0018, P-value = 0.003, Tables 2 and 3). As

expected, immigration rates were larger at the edge

than inside the stand for both species (Table 2 and

Fig. 3c). However, the difference is greater in Q. petraea

than in Q. robur (Table 2).

Distribution of male fecundities and effective numberof males

The coefficient of variation of male fecundities is signifi-

cantly lower for Q. robur (CVR = 43% � 2%) than for

Q. petraea (CVP = 57% � 2%; P-value < 0.05; Data S5,

Supporting Information). The greater heterogeneity of

male fecundities in Q. petraea and its lower pollen dis-

persal and immigration rates should result in Q. petraea

being sired by a less diverse cohort of pollen grains

than Q. robur. Accordingly, for the fraction of maternal

progenies sired by fathers from inside the plot, we

found that the effective number of fathers is signifi-

cantly lower in Q. petraea (KeP = 11) than in Q. robur

(KeR = 45) (P-value = 0.004, Kruskal–Wallis test).

Discussion

We compared the male reproductive strategies of two

closely related oak species. The mating model used

relies on individual characteristics of trees and of pairs

of trees (circumference, intertree distance, phenological

overlap, etc.) and an accurate paternity analysis. Con-

sidering several characteristics of the mating system

simultaneously in a spatially explicit mating model and

testing the marginal effects of each characteristic (i.e.

type III tests) avoids possible confusions among effects

of nonindependent environmental variables. This

approach allowed the estimation of important yet rarely

available reproductive parameters that could then be

compared between species. Our goal here is to interpret

the corresponding findings in the light of existing theo-

ries on ecological strategy.

a

b

Fig. 2 Effect of tree circumference and terrain elevation on Quer-

cus robur and Q. petraea predicted male fecundity. Quercus robur

relative fecundity is symbolized by a dotted line and Q. petraea

by a full line. In a, the reference is the fertility of a tree with a

circumference equal to the mean circumference of the population

(1.73 m). In b, the reference is the fertility of a tree growing in

terrain elevation class 9.



Q. robur and Q. petraea: two species with contrastingecological dynamics

We found that Q. petraea trees grow faster than Q. ro-

bur trees. We also found indications that Q. petraea

trees better tolerate competition than Q. robur trees, as

suggested by previous studies (Becker 1992; Jensen

2000; Landergott et al. 2012; L�evy et al. 1992; reviewed

in Petit et al. 2003). Furthermore, we confirmed that

trees of these two species occupy different ecological

niches, as Q. petraea trees are found preferentially at

the top of the slope, whereas Q. robur trees are found

everywhere but are most abundant at the bottom.

Interestingly, the environment was shown to affect

male fecundity: trees of both species growing in the

lower part of the stand, where anoxic conditions pre-

vail, had decreased male fecundities, regardless of

tree size. Moreover, this effect was stronger for Q. pet-

raea than for Q. robur. This is consistent with knowl-

edge on the ecological preferences of these two

species: Q. robur, unlike Q. petraea, is tolerant of root

waterlogging (Ponton et al. 2002; Parelle et al. 2006; Le

Provost et al. 2011). In a recent study of the mating

system of these species in Poland, male reproductive

success was also found to vary spatially within the

studied plantation, with trees located lower in the

plot being characterized by lower male reproductive

success (Chybicki & Burczyk 2013). Such a confirma-

tion in another independent study is important

because inferences from a single site are difficult to

generalize.

Q. robur’s ecological strategy favours dispersal

According to our expanded model, mean pollen dis-

persal distance was 40% greater in Q. robur than in

a

b

c

Fig. 3 Pollen dispersal in Quercus robur

and Q. petraea. (a) Pollen dispersal kernel

of Q. robur (symbolized by a dotted line)

and Q. petraea (symbolized by a full line).

Right panel: along the main direction of

dispersal, left panel: in the direction

opposite to the main direction of dis-

persal. (b) Anisotropic pollen dispersal

modelling for Q. petraea (left) and Q. ro-

bur (right). (c) Amount of immigrant pol-

len as a function of the distance from the

edge to Q. robur (symbolized by a dotted

line) and to Q. petraea (symbolized by a

full line).



Q. petraea. Furthermore, Q. robur pollen was over-

represented among immigrant pollen and dilution with

distance from the edge of the stand was three times

lower for Q. robur pollen than for Q. petraea pollen, also

suggesting that Q. robur pollen travels greater distances

and is therefore less quickly diluted by locally pro-

duced pollen. These findings support those of Lagache

et al. (2013a) based on the same data but using a sim-

pler model and those of Jensen et al. (2009) based on

realized pollen dispersal distances in another study plot

during two different mating episodes. We also found

that pollen dispersal differs throughout the flowering

season in Q. robur, with late-flowering trees dispersing

their pollen twice as far as early-flowering trees. No

such trend was detected in Q. petraea. Interestingly,

interspecific differences in pollen dispersal are detected

only among late-flowering trees. While differences in

pollen dispersal might in principle be caused by differ-

ences in pollen size between species (Rushton 1976), as

dispersal is known to depend on pollen size (Niklas

1985), they could also be due to interspecific differences

in the timing of pollen release relative to leafing and

canopy closure and to the position of the stigmas borne

by short vs. long and erect peduncles in these decidu-

ous trees (Nathan & Katul 2005; Miller�on et al. 2012).

Regardless of its origin, the difference in pollen dis-

persal between species might explain why we found a

lower effective number of fathers in Q. petraea than in

Q. robur.

In the studied year (1995), pollen dispersal events

inferred from paternity analysis were predominantly

from east to west in Q. petraea and from northeast to

southwest in Q. robur. One hypothesis is that wind is

responsible for this anisotropy (e.g. Shen et al. 1981;

Burczyk & Prat 1997; Pluess et al. 2009; Torimaru et al.

2012). However, this does not explain why the direction

is not the same for both species. Moreover, the prevail-

ing winds in this area blow mainly from west to east in

spring (Meteo France database), that is, in a direction

different from that inferred for the pollen. The finding

that the direction of intraspecific crosses is independent

of the predominant wind direction is not without prece-

dent (e.g. Burczyk et al. 2004; Robledo-Arnuncio & Gil

2005), suggesting that landscape features (e.g. topogra-

phy) could be involved in pollen anisotropic dispersal.

In addition, crosses were more anisotropic in Q. petraea

than in Q. robur. This observation could be caused by

the different locations of the species within the stand.

Whatever the reason for this difference, it has conse-

quences for mating opportunities (i.e. anisotropic dis-

persal should decrease mating opportunities).

Altogether, Q. robur appears to have higher dispersal

ability than Q. petraea, whether through pollen (this

study) or through seed (Petit et al. 2003). While it would

now be important to conduct full parentage studies in

mixed stands to investigate not only pollen but also

acorn dispersal, these findings are consistent with mod-

els of the colonization of disturbed environment in

which Q. robur establishes first at low density, whereas

Q. petraea establishes only after, in areas already colo-

nized by Q. robur (Petit et al. 1997, 2003; Lepais &

Gerber 2011). Note that this scenario requires that

Q. petraea has sufficiently strong sexual barriers against

Q. robur so as not to be swamped out by allospecific

pollen during forest succession while still at low den-

sity, in forests dominated by Q. robur.

Interspecific sexual barriers

The flowering phenologies of the two oak species are

not exactly the same, with flowers of Q. petraea matur-

ing later on average than those of Q. robur (Bacilieri

et al. 1995). This phenological shift should thus help

limit interspecific crosses between these two species. It

is also responsible for part of the observed asymmetry

of interspecific crosses, given that these oaks are protan-

drous, that is, that pollen shedding precedes the peak

of stigmata receptivity (Appendix S2, Supporting Infor-

mation). However, we also identified asymmetric sexual

barriers between species in addition to the isolation

effect conferred by phenology. This interspecific sexual

barrier was 37 times stronger on Q. petraea mother trees

than on Q. robur mother trees, a finding consistent with

results from a previous study (Chybicki & Burczyk

2013) and from interspecific controlled crosses (e.g.

Steinhoff 1993; Lepais et al. 2013), which point to asym-

metric mating compatibility in the same direction. It fits

also with predictions that mating system should be

more relaxed in early-successional than in late-succes-

sional species (e.g. Richards 1996).

In principle, the superior siring ability of Q. petraea

pollen could be caused by its larger pollen grains

(Delph et al. 1997). However, it seems difficult to attri-

bute the marked asymmetry in interspecific mating com-

patibility, confirmed in controlled crosses (e.g. Steinhoff

1993; Lepais et al. 2013), solely to differences in pollen

grain size, as these are quite weak between the studied

species (Rushton 1976). Yet another scenario is that

this asymmetric prezygotic barrier is the consequence of

asymmetric reinforcement, due to differences in inter-

specific mating opportunities resulting from ecological

succession, a directional process. From this perspec-

tive, Q. petraea trees colonizing stands of Q. robur would

initially face conditions conducive to massive hybridiza-

tion while the species is still at low density (Lepais et al.

2009). This should result in a strong and asymmetric

selection against interspecific mating events, as recently

described in Drosophila (Yukilevich 2012).



Conclusions

The differences observed in terms of pollen dispersal

(greater in Q. robur than in Q. petraea) and male fecun-

dity (more stable across environments in Q. robur than in

Q. petraea) fit with the more pioneering character of

Q. robur and the more competitive character of Q. pet-

raea. Differentiation between these two closely related

oak species could additionally be shaped by differing

adaptation to the environment, as shown by differences

in male fitness as a function of terrain elevation. Such

cases of multiple selection pressures (i.e. of ‘multifarious

divergent selection’), caused by interrelated selection

trade-offs, have been shown to be particularly conducive

to ecological speciation (Nosil et al. 2009; Nosil 2012).

Interestingly, the more competitive character of mature

Q. petraea than of Q. robur trees also extends to interspe-

cific mating relationships, as the siring success of Q. pet-

raea appears greater than that of Q. robur. More empirical

and theoretical studies of closely related species with dif-

ferent successional status could help assess whether dif-

fering selection pressures and asymmetric interaction

during succession trigger or reinforce speciation.

Acknowledgements

We are grateful to G�erard Nepveu and Maryline Harrou�e for

sharing tree-ring data. We also thank Jean-Marc Louvet, ONF

office of Le Mans, ONF Research and Development Depart-

ment in Fontainebleau and the ONF manager of La Petite

Charnie (Gabriel Faramin) for construction and maintenance

of the stands. We are particularly grateful to Da-Yong Zhang,

Olivier Lepais, Berthold Heinze and three anonymous referees

for their constructive comments on previous versions of the

manuscript and to Didier Bert and C�eline Meredieu for help

in interpreting tree rings and tree growth. Funding was

provided by the LinkTree project (ANR BIODIVERSA), the

EU Network of Excellence EvolTree and ANR-10-EQPX-16

XYLOFOREST.

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A.D. established the progeny test and shared informa-

tion about tree characteristics. R.J.P. initially conceived

the study, which evolved significantly with the help of

all authors. L.L. gathered and analysed the data. E.K.

performed the modelling. L.L. and R.J.P. wrote the

paper; E.K. wrote part of the methods. All four authors

reviewed the complete manuscript.

Data accessibility

Microsatellite data can be found in the Dryad data

repository at http://datadryad.org, doi:10.5061/dryad.

n50b4 (Lagache et al. 2012).

Morphological data can be found in the TreePop data-

base at http://bioinfo.orleans.inra.fr/TreePop/tmp/

export_20121002141319506ada5f6da21.txt.

Supporting information

Additional supporting information may be found in the online ver-

sion of this article.

Data S1 Spatial coordinates of the trees in the stand.

Data S2 Topographic map of the stand and definition of ter-

rain elevation classes.

Data S3 Mathematica Notebook.

Data S4 Distribution of individual circumferences (A), terrain

elevation class (B) and first record of male and female mature

flowers (C) for each species.

Data S5 Model prediction of individual male fecundities by

species.

Appendix S1 Model including a relatedness effect

between father and mother trees on male fecundity.

Appendix S2 Dependence of parameter estimation on

the model used.



Distinct male reproductive strategies in two closely related oak species

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