Paper 209 Disc
Ecology Letters, (2001) 4 : 151±158
REPORT
Emmanuelle Jousselin1,2* and
Finn Kjellberg1
1
CNRS-CEFE (Centre d'Ecologie
Fonctionnelle et Evolutive), 1919
route de Mende, 34293
Montpellier CeÂdex 5, France
2
Biology Department, Universiti
Brunei Darussalam, Tungku Link,
BE 1410, Brunei Darussalam, S.E.
Asia
*Correspondence: E-mail:
Jousselin@cefe.cnrs-mop.fr
The functional implications of active and passive
pollination in dioecious figs
Abstract
Fig-pollinating wasps lay their eggs in fig flowers. Some species of fig-pollinating
wasps are active pollinators, while others passively transfer pollen. In dioecious fig
species, the ovules of male figs produce wasps but no seeds. By observations and
experiments on four dioecious Ficus species we show that (i) passive pollinators
distribute pollen haphazardly within figs, but fertilization of female flowers in male
figs is inhibited. Consequently, wasp larvae will develop in nonfertilized ovules: they
cannot benefit from pollination; (ii) active pollinators efficiently fertilize flowers in
which they oviposit. Lack of pollination increases larval mortality. Hence, fig
pollinators are not obligate seed eaters but ovule gallers. Active pollination has
probably evolved as a way to improve progeny nourishment.
Comparison of pollination and oviposition process in male and female figs,
suggests that stigma shape and function have coevolved with pollination behaviour,
in relation to constraints linked with dioecy.
Keywords
Ficus, agaonid wasps, mutualism, coevolution, dioecy, pollination, active pollination. Ahed
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Ecology Letters (2001) 4 : 151±158
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Table marActive pollination has been documented in three
INTRODUCTION
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specialized plant±pollinator associations: the Yucca/yucca
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moth interaction (Aker & Udovic 1981; Pellmyr et al.
Oviposition site often determines the amount and
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1996), the Senita cactus/senita moth association (Fleming
quality of resources available for offspring development.
& Holland 1998) and the fig/agaonid wasp association
Hence, any maternal behaviour increasing the quality
(Galil & Eisikowitch 1969; Janzen 1979). The fig/agaonid
of a given oviposition site will be favoured by selection.
wasp mutualism is unique among these interactions in that
Insects, such as gall formers, manipulate the growth of
some agaonid species actively pollinate while others
their host tissue during oviposition, to improve larval
passively transfer pollen.
nourishment (Price et al. 1986; Hartley 1998). In other
Figs are closed inflorescences composed of uniovulate
cases, insects use a biological agent. Some parasitoids
female flowers and male flowers. When figs are receptive,
inject viruses to control their host immune system
agaonid wasps lay their eggs in some of the flowers and
(Whithfield 1990) and some insects inoculate fungi on
pollinate them in the process. When figs are mature,
which their larvae will feed (Roy 1994). In a number of
offspring female wasps get loaded with pollen and leave
cases, insects have evolved morphological and betheir natal fig. Half of all Ficus species are monoecious,
havioural adaptations aimed at collecting and depositwith both wasps and seeds produced in the same
ing the biological agent that will benefit their offspring.
inflorescence, while the remaining Ficus species are
Fungus-feeding insects such as gall midges and ambrosia
functionally dioecious. In these species, development of
beetles have specialized `pockets' aimed at storing
insects and seeds occurs on different trees. Female trees
fungal spores (Rohfritsch 1997; see Pellmyr 1997 for
bear figs with long-styled uniovulate flowers. Pollinators
a review). Similarly, some insects whose larvae develop
cannot lay their eggs in these figs because their ovipositor
at the expense of seeds have specialized morphois shorter than the length of the styles and thus cannot
logical and behavioural traits which allow them to
reach the ovule (Galil 1973; Valdeyron & Lloyd 1979).
pollinate their host (Pellmyr 1997). Such a syndrome is
Male trees bear figs with male flowers and short-styled
called active pollination.
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152 E. Jousselin and F. Kjellberg
female flowers in which agaonid wasps can lay their eggs.
Only wasps and pollen are produced in these figs: their
female flowers either produce a wasp or remain empty. As
wasps carry pollen from their natal fig, they contribute to
the fig's male function. Hence male trees are morphologically hermaphroditic but functionally male.
When pollination is active, wasps store pollen from
their natal fig in thoracic structures called pollen pockets
(Galil & Eisikowitch 1969). Each time a wasp lays an egg
in an ovule, it also deposits some pollen grains on the
stigmas (Galil & Eisikowitch 1969; Frank 1984). When
pollination is passive, the pollinator does not show any
pollen collection and deposition behaviour. Associated
figs of these species produce large quantities of pollen so
that the wasps become covered with pollen within their
natal fig (Galil & Neeman 1977; Galil & Meiri 1981).
Molecular phylogenies of fig-pollinating wasps (Machado
et al., 2001) suggest that active pollination has evolved
once and has reverted many times towards passive
pollination. These multiple reversions suggest that the
selective forces favouring active pollination can be relaxed
and that there is a cost to active pollination.
Why do some agaonid wasps pollinate actively?
According to classical descriptions of the mutualism,
fertilized flowers provide a better feeding substrate for
wasp larvae (Verkerke 1989; Anstett et al. 1997; Herre
1999). Active pollination behaviour would have been
selected to allow wasps to pollinate flowers in which they
oviposit. The occurrence of active pollination in dioecious
figs supports this hypothesis. In dioecious figs, wasps can
only benefit from pollination of figs in which they
reproduce, i.e. male figs. For pollination to provide some
benefit to the wasp, it has to result in ovule fertilization.
As male figs do not produce any seeds, it can thus be
predicted that wasp offspring benefit from developing in
fertilized flowers (Kjellberg et al. 1987) and that wasps
only pollinate flowers in which an egg is laid, otherwise
there would be many seeds formed. The situation in
passively pollinated figs is likely to be very different.
Passively pollinating wasps cannot control where pollen is
deposited. It can therefore be predicted that pollen should
be scattered among flowers independent of oviposition
sites. If this prediction were to be verified, then one could
ask what prevents seed production in these figs?
The purpose of this paper is to test hypotheses about
the benefit of pollination for the wasp and examine the
consequences of pollen deposition pattern in both
passively and actively pollinated dioecious fig species.
To do so, we examined whether (i) flowers in which
wasps attempt oviposition are more likely to receive
pollen in male and female figs; (ii) pollination results in
ovule fertilization in male figs and (iii) wasps develop
normally in unpollinated figs.
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MATERIALS AND METHODS
Species and study sites
We studied two actively pollinated species (Ficus fulva and
Ficus condensa) and two passively pollinated species (Ficus
carica and Ficus deltoidea). Ficus condensa (section Sycocarpus, subgenus Sycomorus) and F. fulva (section Ficus,
subgenus Ficus), belong to the two distinct lineages of
dioecious figs (Weiblen 2000). Ficus deltoidea and F. carica
both belong to subgenus Ficus but are pollinated by
different wasp genera.
All observations and experiments on F. condensa, F.
deltoidea and F. fulva were performed in Brunei Darussalam (North Borneo). Experiments on F. carica were
conducted in Montpellier (South of France).
Do fig wasps pollinate flowers in which they attempt
oviposition?
We observed whether pollen grains were mainly deposited
on the stigma of flowers in which pollinators laid an egg
or attempted to lay an egg, i.e. flowers in which they had
inserted their ovipositor.
Figs were picked on F. condensa, F. fulva and F. deltoidea
trees when pollinators were seen on the crop entering
the ostiole. Figs were cut open and those in which a wasp
was still alive were rejected, since foundresses might not
have finished depositing the pollen they transported.
This was done on one male tree and one female tree for
each species.
Controlled pollination experiments were performed on
F. carica. To obtain receptive male figs at the same time as
receptive female figs, we induced the early development
of male figs by removing the apical bud of several
branches. On the same day, we introduced one foundress
per fig into male and female figs (method as in Khadari et al.
1995). Foundresses were collected from a single male tree.
Figs were collected 24 h after pollinator introduction.
Flowers were observed on the day of fig collection. In
all species studied, the styles of flowers in which
pollinators had inserted their ovipositor presented a
conspicuous bruise. For each fig, we removed a set of
flowers haphazardly chosen within the inflorescence. For
each flower, we first assessed from the darkening of the
style whether pollinators had attempted to oviposit in it.
On 10 randomly chosen ``oviposited'' flowers and 10
randomly chosen ``virgin'' flowers, we assessed the
presence/absence of pollen grains on stigmas. Flowers
were stained with 0.01% aniline blue in 0.1 M K3PO4.
Then, the stigma of each flower was removed from the
ovule and squashed on a slide in order to visualize pollen
grains under an epifluorescence microscope (Kearns &
Inouye 1993).
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Active and passive pollination in figs 153
Do wasp larvae develop in fertilized ovules?
On one male tree of F. condensa, we made controlled
pollinator introductions. Figs were enclosed before
pollination in a fine-mesh nylon bag to prevent wasp
and parasite visits. When figs became receptive, we
introduced one foundress per fig in 10 figs. Foundresses
were collected from a single donor tree. Figs were
collected 2 days after pollinator introduction and were
preserved in FAA (formalin, acetic acid, ethanol).
For F. deltoidea and F. fulva, figs were collected when
pollinators were seen entering through the ostiole on a single
male tree for each species. To let pollen tubes grow, collected
figs were then kept for two days in a plastic vial with wet
cotton inside. After two days, figs were put into FAA.
For each species, 7±11 figs were embedded in paraffin
blocks. A portion of each fig was cut into 15 mm transverse
serial sections. Slices were then stained with 0.01% aniline
blue in 0.1 M K3PO4 and observed under an epifluorescence
microscope. For each fig, the fate of the ovules viewed on
the median section of the portion of the fig cut (15±30
ovules per fig), was determined by compiling the
information from 20 to 30 slides. For each ovule we noted
(i) presence or absence of a pollinator egg and (ii) presence
or absence of pollen tubes penetrating the ovule.
Can fig wasp larvae develop in unpollinated figs?
In F. condensa, we introduced wasps without pollen. To
prevent wasps from collecting pollen, we removed the
stamens of figs in which mated female wasps were about
to emerge from their gall. Wasps were then allowed to
emerge in fine-mesh bags. A subsample of 20 females used
in each treatment were squashed on a slide and the
presence of pollen grains in their pollen pockets was
checked under a light microscope. The 20 from the sample
of wasps used in the control experiment carried numerous
pollen grains in their pockets (4 400 pollen grains per
wasp). Two wasps out of 20 of the sample used in the
`pollen free' experiment carried pollen grains.
On one male tree, figs at the prepollination stage were
enclosed in a fine-mesh nylon bag. On the day figs became
receptive we either introduced a pollen-free wasp or a
normally pollen loaded wasp into randomly chosen fig.
All foundresses emerged from figs from the same male
tree. A drop of nontoxic glue was applied to the ostiole
after pollinator introduction to prevent foundress exit
from a fig and re-entry into another fig (see Gibernau et
al. 1996). Mesh bags were then replaced around figs to
prevent attacks by parasitoids.
Figs were collected 4 weeks later just before maturation. In each, the numbers of male wasps, female wasps,
undeveloped flowers and bladders (swollen but empty
flowers) were counted. In a few cases, wasps had already
emerged from the fig prior to its collection. The number
of galls that had been exited by wasps was then counted to
assess total wasp production in these figs.
Statistical analysis
Test of independence between pollination and oviposition
Data were classified in a contingency table according to
three factors: fig, oviposition (presence/absence), pollen
tube or pollen grains (presence/absence). We then fitted a
log-linear model to the data assuming a Poisson error
distribution and a log link function in the Glim statistical
package (Glim 3.7i, 1985). To assess the significance of
association between oviposition and pollination, we
removed the two-way interaction term from the full
model. The difference in deviance between two nested
models follows a w2 distribution, with number of degrees
of freedom equal to the difference in number of
parameters between the two models (Crawley 1993).
Pollen free experiment
The effect of lack of pollen on fig production was tested
with an analysis of covariance with number of flowers in a
fig as a covariate and treatment as a fixed effect. We used
the GLM procedure from the SAS statistical package
(SAS 1992).
RESULTS
Do fig wasps pollinate flowers in which they attempt
oviposition?
Actively pollinated figs
In both F. condensa and F. fulva, in male figs, most flowers
in which pollinators had inserted their ovipositor were
pollinated while those in which pollinators had not
inserted their ovipositor were mostly not pollinated (Fig.
1). Pollen deposition and oviposition attempt were
strongly associated (Table 1). Furthermore, most of the
pollen grains had started to germinate (80% of all pollen
grains observed for F. condensa and F. fulva).
In female figs, about 60% of the ovules in which the
wasps had attempted to oviposit were pollinated,
compared to 50% of those that had not been probed.
Nevertheless, oviposition attempt and pollination were
dependent (Table 1). In female figs of F. fulva and F.
condensa, stigmas stick together forming a synstigma (Fig.
2a) and we frequently observed for both species, pollen
grains that landed on one stigma growing into a
neighbouring style (Fig. 2b). In male figs of both species,
stigmas were well separated and no such phenomenon was
observed (Fig. 2c).
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154 E. Jousselin and F. Kjellberg
Figure 1 Pollen grain distribution among
flowers of male and female figs of actively
pollinated species.
Table 1 Values of w2 for two-way inter-
Data set
Number of figs
(number of flowers)
w2
(1 d.f.)
Test
Actively pollinated figs
F. condensa, male
F. condensa, female
F. fulva, male
F. fulva, female
29
16
14
14
(560)
(320)
(280)
(280)
236
4.51
184
5.58
P 55 1074
P = 0.03
P 55 1074
P = 0.02
Passively pollinated figs
F. carica, male
F. carica, female
F. deltoidea, male
F. deltoidea, female
6
7
13
10
(120)
(140)
(260)
(60)
0.37
0.73
0.10
all flowers
pollinated
and probed
P = 0.54
P = 0.39
P = 0.74
Passively pollinated figs
The probability of a flower receiving pollen grains was
the same whether or not wasps had inserted their ovipositor in the style of the flower for male and female figs
of F. carica and male figs of F. deltoidea (Fig. 3, Table 1).
In F. deltoidea male figs, only 20% of all pollen grains
observed had germinated. Moreover, 70% of the resulting
pollen tubes were blocked by a callose plug. In female figs
of F. deltoidea, there are very few flowers (from 8 to 15)
and all styles were darkened and had received numerous
pollen grains that were germinating normally.
For F. carica, although the number of female flowers in
male figs and female figs is similar (& 1200; F. Kjellberg
unpublished data), the percentage of pollinated flowers
was higher for female figs (65 + 30%, 20 flowers per fig,
7 figs) than for male figs (18 + 8%, 20 flowers per fig, 6
figs) (w21df = 16.29; P 5 1074). The number of pollen
grains per pollinated flower was significantly higher in
female figs (mean = 3.3, SD = 2.5) than in male figs
(mean = 1.4, SD = 0.5) (w21df = 7.29; P 5 1072). In
female figs of F. deltoidea and F. carica, the stigmas do not
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action between pollen grain presence and
oviposition attempt
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stick together (Fig. 2d), pollen germination from one style Ref start
into another is thus morphologically impossible. In male
figs, stigmas are well individualized and many pollen
grains had fallen between the flowers, on the sepals.
Do fig wasp larvae develop in fertilized ovaries?
In male figs of F. fulva and F. condensa, about 90% of the
flowers in which an egg was laid were fertilized and few
fertilized flowers did not contain a wasp egg (5% of all
flowers) (Fig. 4). The presence of a pollen tube and the
presence of a wasp egg in an ovule were closely associated
(Table 2). In contrast, for F. deltoidea, among the 123
flowers analysed, only two were fertilized (Fig. 3).
Do actively pollinating fig wasps develop normally in
unpollinated figs?
In F. condensa, male figs with and without pollen developed
normally. Rates of fig abortion were identical in both treatments (3 figs out of 16). Unpollinated figs produced
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Active and passive pollination in figs 155
Figure 2 (a) Synstigma in female figs of F.
condensa: the stigmas are fused together. (b)
Lateral pollen tube: growth on flowers of F.
fulva female figs: pt, pollen tube; sty, style; stg,
stigma. (c) Female flowers of male figs of F.
condensa: stigmas are individualised. (d) Female
fig of F. carica: stigmas are elongate and
individualised.
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Figure 3 Pollen grain distribution among flowers of male and female flowers of passively
pollinated species.
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significantly (F1,23 = 5.10; P = 0.03) fewer agaonid offspring
(mean = 67, S.D. = 57) than pollinated ones (mean = 110,
S.D. = 55). The number of bladders was similar in pollinated
and unpollinated figs (respectively, mean = 66, S.D. = 23;
mean = 44, S.D. = 38; F1,23 = 0.94, P = 0.34). The number
of flowers had no effect on fig production and did not need to
be considered as a covariate. The proportion of males in the
broods did not differ between treatments (unpollinated figs:
mean = 0.30; S.D. = 0.11 n = 13; pollinated figs:
mean = 0.22, S.D. = 0.09, n = 7; Mann±Whitney U-test,
P = 0.69). If some foundresses considered as `pollen free' had
carried some pollen then our results would give an underestimate of the cost of lack of pollination.
DISCUSSION
In dioecious fig species, as summarized in Table 3, passive
and active pollination result in a strikingly different
functioning of the fig/fig wasp mutualism.
Active pollination and functional dioecy
In the two actively pollinated fig species studied, in male
figs, wasps mainly pollinate the flowers in which they
oviposit. As a result, most flowers into which an egg has
been laid are fertilized. In F. condensa, some wasps manage
to develop in unpollinated figs, hence in unfertilized
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156 E. Jousselin and F. Kjellberg
behaviour is similar in male and female figs (Galil 1973).
We suggest that the tight packing of stigmas in female figs
may limit the precision of pollen deposition.
flowers, but brood size is strongly reduced by lack of
pollination. Together, these observations imply that wasp
offspring benefit from pollination and that this benefit is
probably linked to the fertilization of the ovule in which
the egg has been deposited. Fertilized ovules may provide
a better feeding substrate for the developing larvae.
Our observations also partly explain why there are no
seed produced in actively pollinated male figs: the strong
association between pollination and oviposition in male
figs ensures that nearly every fertilized flower contains a
wasp egg; thus, all fertilized flowers will develop as a gall.
Interestingly, in female figs, much more pollen was
deposited on flowers that had not been probed by the
wasps than in male figs, despite the fact that wasp
Passive pollination and functional dioecy
In passively pollinated fig species, pollen is homogeneously distributed between probed and unprobed
flowers in male and female figs. However, in male figs,
flower fertilization is limited by poor adherence of pollen
to the stigmas (data on F. carica) and limited pollen tube
growth (F. deltoidea our data, F. carica, Beck & Lord
1988). This implies that most pollinators of F. deltoidea
and F. carica will develop in unfertilized flowers.
Consequently, they are true ovule gallers.
The observation that ovule fertilization is partly
prevented in passively pollinated male figs explains the
lack of seed production and hence functional dioecy.
Evolution of pollination mode in dioecious figs
Actively pollinating wasps are probably selected to
pollinate flowers in which they lay an egg in order to
enhance larval nutrition. Nevertheless, oviposition alone
has the capacity to induce the development of ovule tissue
necessary to support the development of some wasps.
This suggests that there is no absolute barrier to the loss
of active pollination behaviour. This is consistent with the
observation that reversions to passive pollination are
numerous (Machado et al., in press). Although, the
pathway leading to the loss of active pollination is still
unknown, we can hypothesize that costs associated with
pollination behaviour (time spent collecting and depositing pollen) sometimes exceed costs associated with
development in unfertilized flowers.
Figure 4 Pollen tube and wasp egg distribution across ovaries of
male figs of F. condensa, F. fulva, F. deltoidea.
Table 2 Values of w2 for two way
Ficus species
Number of figs
(number of flowers)
w2
(1 d.d.f.)
F. condensa
F. fulva
F. deltoidea
9 (215)
11 (230)
7 (120)
174.4
24.7
only two flowers
were fertilized
Test
P 55 1074
P 55 1074
interaction between pollen tube presence
and wasp egg presence in male figs
Table 3 Summary of results on pollen dispersion, flowers fertilization and benefit of pollen transport for the wasp
Mode of
pollination
Fig sexual
function
Pollen dispersion
Flower fertilization
Benefit of pollination
for the wasps
Active
Male
Female
Male
Female
Depends strongly of oviposition site
Depends slightly of oviposition site
Haphazardly distributed
Haphazardly distributed
Yes + no lateral pollen tube growth
Yes + lateral pollen tube growth
Rare
Yes + no lateral pollen tube growth
Inc.brood size
None
None
None
Passive
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Active and passive pollination in figs 157
The observation that, in passively-pollinated male figs,
pollen germination is prevented, suggests that active
pollination cannot re-evolve from passive pollination in
dioecious figs; in such figs, wasps will simply never
benefit from developing in fertilized flowers. This
prediction is in agreement with the phylogenetic reconstruction of mode of pollination in fig wasps and the
phylogenetic reconstruction of the reproductive system of
the host fig (Machado et al., in press). Active pollination
has evolved in the monoecious ancestors of dioecious figs,
and it has been lost several times (in monoecious and
dioecious figs). So far there is no evidence of reacquisition
of active pollination in dioecious figs.
flowers in which they oviposit while the host fig would be
selected to ensure seed production. Indeed, actively
pollinated monoecious figs present a synstigmatic structure (Jousselin and Kjellberg, unpublished observations
on sections Americana, Conosycea, Galoglychia, Urostigma)
and this structure is lacking in lineages of monoecious figs
that have evolved passive pollination independently
(Jousselin and Kjellberg, unpublished observations on
sections Pharmacosycea and Conosycea). Hence, investigations of pollen distribution by actively pollinating wasps
on monoecious figs will be necessary to test our
hypothesis that synstigmas evolve in response to precise
pollen deposition by the wasps.
Coadaptation of wasp pollination behaviour and stigma
morphology
CONCLUSIONS
In all male figs we have observed, including representatives of all dioecious Ficus sections, the stigmas are well
separated and in all female figs of actively pollinated
species we have observed, stigmas are cohesive (observations on sections Sycocarpus, Neomorphe, Ficus, Rhizocladus
and Sycidium). In all female figs of passively pollinated figs
we have observed, the stigmas are non cohesive
(observations on sections Ficus, Rhizocladus and Kalosyce).
Hence, according to available data, the style shapes
described for actively and passively pollinated fig species
are representative of dioecious figs. The difference in
stigma structure between male figs and female figs,
suggests that cohesive stigmas enhance female function
(i.e. seed production). Furthermore, the lack of cohesive
stigmas in passively pollinated female figs suggests that
this structure is maintained by selection for increasing
pollen dispersion when wasps actively pollinate, i.e. when
they control where the pollen is deposited. Such a
morphology would have no selective value in passively
pollinated species, in which pollen is homogeneously
distributed among flowers. Formal comparative analysis
will be necessary to conclude on the coadaptation between
stigma shape and wasp behaviour.
The phylogeny of Ficus (Weiblen 2000) is not yet
sufficiently resolved to establish whether passive pollination evolved several times in dioecious figs. Thus, we
cannot test whether independent losses of active pollination lead to the loss of synstigma in female figs. Hence, no
general conclusion may be drawn from the sole investigation of dioecious fig species. Hypothesized coadaptation
of stigma arrangement with mode of pollination may,
however, be tested by investigating monoecious species
which produce both seeds and wasps in the same figs. The
selective pressures in monoecious figs could be convergent with those evidenced for female figs. Actively
pollinating wasps may be selected to only fertilize the
The evolution of active pollination in the fig/fig wasp
mutualism does not follow the same pathway as that in the
Yucca/yucca moth and the Senita/senita moth interactions.
In these latter, pollinator larvae feed on several seeds
produced in their natal flower. Hence, in the absence of
copollinators, pollination of the host by the mother is
essential for larval survivorship. In contrast, agaonid wasp
larvae complete their development in a single ovule of the
fig inflorescence, and response to selection for increasing
the quality of their oviposition site includes fertilization of
the ovule but also manipulation of the flowers. Studies on
other actively pollinating insect lineages had concluded
that seed eating was a prerequisite for the evolution of
active pollination (Pellmyr et al. 1996). Active pollination
in the fig/agaonid wasp mutualism is more likely to have
evolved from ovule parasitism.
ACKNOWLEDGEMENTS
This research was supported by a Brunei Shell Environmental Studies Fellowship. The authors are grateful to Dr
D. Edwards and to the Biology Department staff at
Universiti Brunei Darussalam for their help. They also
acknowledge the Director of the Brunei Museum and the
Forestry Department for allowing them to export specimens. Many thanks to C. Maycock and all the staff at the
Kuala Belalong Field Studies Center for field assistance,
and to C. Brouat, M. Hossaert-Mckey, Doyle Mckey,
John Thompson, for critically reading earlier versions of
this manuscript.
REFERENCES
Aker, C.L. & Udovic, D. (1981) Oviposition and pollination
behavior of the yucca moth, Tegeticula maculata, (Lepidoptera:
Prodoxidae) and its relation to the reproductive biology of
Yucca whipplei (Agavacae). Oecologia, 49, 96±101.
#2001 Blackwell Science Ltd/CNRS
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Paper 209 Disc
158 E. Jousselin and F. Kjellberg
Anstett, M.-C., Hossaert-McKey, M. & Kjellberg, F. (1997) Figs
and fig pollinators: evolutionary conflicts in a coevolved
mutualism. Trends Ecol. Evol., 12, 94±99.
Beck, N.G. & Lord, E.M. (1988) Breeding system in Ficus carica,
the common fig. II Pollination events. Am. J. Botany, 75,
1913±1922.
Crawley, M.J. (1993) GLIM for Ecologists. Blackwell Scientific
Publications, Oxford, UK.
Fleming, T.H. & Holland, J.N. (1998) The evolution of obligate
pollination mutualisms: Senita cactus and Senita moth.
Oecologia, 114, 368±375.
Frank, S.A. (1984) The behaviour and morphology of the fig
wasps Pegoscapus assuetus and P. jimenezi: descriptions and
suggested behavioral characters for phylogenetic studies.
Psyche, 91, 289±308.
Galil, J. (1973) Pollination in dioecious figs. Pollination of Ficus
fistulosa by Ceratosolen hewitii. Gardens' Bulletin, 26, 303±311.
Galil, J. & Eisikowitch, D. (1969) Further studies on the
pollination ecology of Ficus sycomorus L. (Hymenoptera,
Chalcidoidea, Agaonidae). Tijdschrift Voor Entomologie, 112,
1±13.
Galil, J. & Meiri, L. (1981) Number and structure of anthers in
fig syconia in relation to behaviour of the pollen vectors. New
Phytologist, 88, 83±87.
Galil, J. & Neeman, G. (1977) Pollen transfer and pollination in
the common fig (Ficus carica L.). New Phytologist, 79, 163±171.
Gibernau, M., Hossaert-McKey, M., Anstett, M.-C. & Kjellberg, F. (1996) Consequences of protecting flowers in a fig: a
one-way trip for pollinators? J. Biogeogr., 23, 425±432.
Hartley, S.E. (1998) The chemical composition of plant gals: are
levels of nutrients and secondary compounds controlled by
the gall-former? Oecologia, 113, 492±501.
Herre, E.A. (1999) Laws governing species interactions?
Encouragements and caution from figs and their associates.
Levels of Selection (by Keller, L.). Princeton University Press,
Princeton, NJ, USA.
Janzen, D.H. (1979) How to be a fig. Ann. Rev. Ecol. Syst, 10,
13±51.
Kearns, C.A. & Inouye, D.W. (1993) Techniques for Pollination
Biologists. University Press of Colorado, Niwot, CO.
Khadari, B., Gibernau, M., Anstett, M.C., Kjellberg, F. &
Hossaert-McKey, M. (1995) When figs wait for pollinators:
the length of fig receptivity. Am. J. Botany, 82, 992±999.
Kjellberg, F., Michaloud, G. & Valdeyron, G. (1987) The Ficus±
pollinator mutualism: how can it be evolutionary stable? Insect
#2001 Blackwell Science Ltd/CNRS
Plants (eds Labeyrie, V., Fabres, G. & Lachaise, D.), pp. 335±
340. W. Surck Publishers, Dordrecht, The Netherlands.
Machado, C., Jousselin, E., Kjellberg, F., Compton, S.G. &
Herre, E.A. (2001) Phylogenetic relationships, historical
biogeography and character evolution of fig pollinating
wasps. Proc. Roy. Soc. Lond. B., 268, 1±10.
Pellmyr, O. (1997) Pollinating seed eaters: why is active
pollination so rare? Ecology, 78, 1655±1660.
Pellmyr, O., Thompson, J.N., Brown, J.M. & Harrison, R.G.
(1996) Evolution of pollination and mutualism in the yucca
moth lineage. Am. Nat., 148, 828±845.
Price, P.W., Waring, G.L. & Fernandes, G.W. (1986) Hypotheses on the adaptive nature of galls. Proc. Entomol. Sic. Wash.,
88, 361±363.
Rohfritsch, O. (1997) Morphological and behavioural adaptations of the gall midge Lasioptera arundinis (Schiner) (Diptera,
Cecidomyiidae) to collect and transport conidia of its fungal
symbiont. Tijdschrift Voor Entomologie, 140, 59±66.
Roy, B.A. (1994) The use and abuse of pollinators by fungi.
Trend Ecol. Evolut., 9, 335±339.
SAS (1992) SAS User's Guide. SAS Institute Inc, Cary, NC, USA.
Valdeyron, G. & Lloyd, D.G. (1979) Sex differences and
flowering phenology of the common fig, Ficus carica L.
Evolution, 33, 673±685.
Verkerke, W. (1989) Structure and function of the fig.
Experientia, 45, 612±622.
Weiblen, G.D. (2000) Phylogenetic relationships of functinally
dioecious Ficus (Moraceae) based on ribosomal DNA
sequences and morphology. Am. J. Botany, 87, 1342±1357.
Whithfield, J.B. (1990) Parasitoids, polydnaviruses and endosymbiosis. Parasitol. Today, 6, 381±384.
BIOSKETCH
Emmanuelle Jousselin's main research interest is the evolutionary ecology of mutualistic interactions. Her research
involves experimental ecology but also phylogeny and
comparative analysis.
Editor, M. Parker
Manuscript received 25 October 2000
First decision made 7 December 2000
Manuscript accepted 9 January 2001
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