OIKOS 95: 476–484.

Copenhagen 2001

Unbeatable strategy, constraint and coevolution, or how to resolve

evolutionary conflicts: the case of the fig/wasp mutualism

Marie Charlotte Anstett

Anstett, M. C. 2001. Unbeatable strategy, constraint and coevolution, or how to

resolve evolutionary conflicts: the case of the fig/wasp mutualism. – Oikos 95:
476–484.

Constraints and evolution are central for the resolution of conflicts between mutual-
istic species and for the stability of mutualisms. However, proximal causes of the
benevolence of mutualistic species are often unknown. Monoecious fig species and
their specific pollinators are in conflict on the use of fig ovaries, which can either
produce one seed or host one pollinator larva. Here, I provide new data showing
that, probably because of space constraints during the development of both seeds and
wasps, ovaries vary in their quality as a substrate for pollinator development
depending on their location within the fig inflorescence. This constraint may be
responsible for the stability of the fig/wasp mutualism. Moreover, population density
of pollinators and density dependent selection on the pollinators could be sufficient
to explain the observed highly variable seed/wasp ratios produced by figs.

M. C. Anstett, CNRS-CEFE, groupe coé6olution, 1919 route de Mende, F-34293

Montpellier Cedex 5, France (anstett@cefe.cnrs-mop.fr).

In the gradient from antagonistic to mutualistic interac-
tions (Bronstein 1994), mutualisms are characterized by
a reciprocal exploitation in which the net result is
positive for both species (Thompson 1982). Many sym-
biotic mutualisms evolved through the evolution of
parasite benevolence (Margulis and Fester 1991, Black-
stone 1995). Various models have been developed to
explain the evolution of mutualism (Frank 1997). Many
are based on the fact that when parasites are vertically
transmitted their fitness may be correlated with that of
their host (Toft and Karter 1990), even if this is not
always true (Kover and Clay 1998). When this correla-
tion exists, under certain conditions benevolence may
evolve (Yamamura 1993, Frank 1997). Such an evolu-
tionary scenario has been experimentally tested (Bull et
al. 1991), and results consistent with its predictions
have been observed in the field (Herre 1993). Evolution
towards vertical transmission, and then subsequently to
mutualism is also predicted under some conditions (Ya-
mamura 1993, Yamamura, 1996), even when transmis-
sion remains partly horizontal (Lipsitch et al. 1996).
The importance of understanding this evolutionary
trend towards benevolence is illustrated by the evolu-
tion towards benevolence and mutualism of some
strains of fungal pathogens considered for use in bio-
logical control (Freeman and Rodriguez 1993, Hall-
mann and Sikora 1994).
However, many mutualisms have a purely horizontal
transmission (Douglas 1994). For these interactions, the
conditions necessary for the evolution of benevolence
are less well known, especially when conditions for
interdemic selection (Dugatkin et al. 1992) or for the
evolution of reciprocal altruism (Trivers 1971) do not
apply. In these cases, benevolence may be due to a
constraint that limits the exploitation of the partner
(e.g., a trade-off between virulence and transmissibility
[Lipsitch et al. 1995], or unrecognition in an op-
timal foraging game [Mesterton-Gibbons 1991]). The

Accepted 11 June 2001

Copyright © OIKOS 2001
ISSN 0030-1299
Printed in Ireland – all rights reserved

476 OIKOS 95:3 (2001)

ultimate form of the constraint is the unbeatable strat-
egy (West and Herre 1994) where one species entirely
controls the other.
Most empirical studies of the evolution of benevo-
lence focus on host parasite interactions. I adopt a
different approach, using a mutualism as a model sys-
tem and focusing on the conflicts between mutualists.
Studies of the resolution of these conflicts could give
insights on the conditions and constraints necessary for
the evolution of benevolence more readily than studies
on host/parasite interactions, where benevolence does
not exist.
Actual causes of benevolence in a mutualism may not
be straightforward to determine. For example coevolu-
tion usually does not occur between two characters, but
between two sets of characters, rendering actual con-
flicts between mutualists more difficult to distinguish.
Once an evolutionary conflict is identified, several alter-
native hypotheses may plausibly explain the stability of
the mutualism. This is the case in the fig/wasp pollina-
tion mutualism.
Fig trees are pollinated solely by species-specific
wasps, and each wasp larva develops at the expense of
one fig ovary (Janzen 1979, Bronstein 1988, Compton
1993). Thus fig trees and their associated fig wasps are
in conflict over predation of fig ovaries (see below for
more details). This conflict was first described more
than 20 years ago (Janzen 1979) and since then, eight
different explanations of the persistence of this mutual-
ism have been published (reviewed by Kathuria 1999).
After a brief review of the three main hypotheses, I will
provide new data that suggest the existence of a trade-
off that could explain why fig pollinators do not occupy
all fig ovaries and allow some seeds to develop.
Fig. 1. Schematic drawing of the interior of the fig just after
pollination, showing the irregular organization of the ovaries.
Ovaries of the outer layer belong to long-styled, short-pedi-
celled flowers. They usually develop into seeds. Ovaries of the
inner layer belong to short-styled, long-pedicelled flowers.
They usually host a pollinator larva.
OIKOS 95:3 (2001)
The conflict
The genus Ficus is characterized by a peculiar inflores-
cence, the fig or syconium (Fig. 1), in which flowers are
enclosed. Figs of each species are pollinated only by a
species-specific wasp that enters the syconium, polli-
nates and lays eggs in some fig flowers. Some Ficus
species are monoecious, others are (gyno)dioecious.
These two reproductive systems impose different con-
flicts on the mutualism (reviewed by Patel et al. 1993,
Anstett et al. 1998). Here monoecious species are
treated. Some traits of dioecious fig pollination systems
have implications for the hypothesis developed and will
be discussed. In monoecious species, each female flower
may either produce one seed or host one pollinator
offspring. Male pollinators are apterous and die just
after they mate with females that developed in the same
syconium. When female pollinators exit the gall where
they developed, they become loaded with pollen (or
load themselves with pollen for species with active
pollination) before leaving the natal syconium. Thus
female pollinators developing in one syconium are the
only dispersers of the pollen produced by this syco-
nium. Reproductive success of fig trees through male
function is (roughly) proportional to their ‘‘produc-
tion’’ of female pollinators.
Thus fig trees and wasps are in conflict over the fate
of female flowers: the fig tree is selected to allocate half
of its reproductive effort to the female function (esti-
mated by seed production) and half to the male func-
tion (estimated by pollen + male and female wasps,
Charnov et al. 1976, Herre 1989). But pollinators do
not have any individual advantage in not laying eggs in
all female flowers. Why do pollinators not occupy all
fig female flowers?
Three hypotheses are currently debated to explain the
seed/wasp production ratio: the unbeatable-seeds hy-
pothesis (West and Herre 1994), the ovipositor length
optimization hypothesis (Ganeshaiah et al. 1995), and
the limited-egg-supply hypothesis (Nefdt and Compton
1996). All of these are supported by data. Five other
hypotheses have been convincingly rejected on grounds
explained by Bronstein (1992) and Kathuria (1999).
In the ‘‘unbeatable-seeds’’ hypothesis (West and
Herre 1994) ‘‘a certain proportion of flowers cannot be
used by any pollinator or parasite wasps, which results
in unbeatable seeds’’. This hypothesis was based on the
fact that some parasitic wasp species that also develop
at the expense of fig ovaries (but do not pollinate)
usually compete with the pollinators and not with the
seeds (West and Herre 1994), even though some para-
sitic species do compete with seeds (Kerdelhué et al.
2000). The ovule dimorphism of Ficus asperifolia, a
(gyno)dioecious species, was wrongly used to support
the unbeatable-seeds hypothesis in monoecious species.
In (gyno)dioecious Ficus, some trees (females) never
host pollinator larvae and only produce seeds, whereas
477
‘‘male’’ trees never produce seeds (they have non-func-
tional ovaries) and only host pollinators (Kjellberg et
al. 1987, Patel and McKey 1998). Ovaries of the female
trees have an integument circumvallating the nucellus,
which is the common situation of anatropous ovules
(Verkerke 1987a, b). The integument may mechanically
protect the ovaries against predation by pollinator lar-
vae. Ovaries of the ‘‘male’’ trees have a thicker raphe
and shorter integument, two characteristics that are
very likely to facilitate oviposition and development of
pollinator larvae by providing more food for the larva
just after hatching and by facilitating movement of the
larvae to the endosperm (Verkerke 1987a). However,
no such dimorphism exists among the ovaries of a
monoecious fig (Verkerke 1987a). All ovaries of monoe-
cious figs have the same structure as those of ‘‘male’’
figs of dioecious species. They thus have the same
adaptations for pollinator development, and lack the
ovary protection of a continuous integument present in
flowers of female figs. In the absence of description of
any actual biological traits characterizing these puta-
tively ‘‘unbeatable flowers’’ in any monoecious fig, this
hypothesis is not testable or refutable.
When the pollinator lays eggs, it inserts its ovipositor
through the style, and precisely deposits each egg next
to the nucellar epidermis (Verkerke 1987a). Thus the
relative distributions of style length and ovipositor
length give the percentage of flowers accessible for egg
laying. Comparisons of ovipositor length and style
length show that in monoecious species female wasps
have access to only 50% to 90% of female flowers
(Nefdt and Compton 1996, Kathuria 1999). The o6ipos-
itor-length-optimization hypothesis (Ganeshaiah et al.
1995, Kathuria et al. 1995) supposes a cost of a longer
ovipositor, making it too costly to evolve an ovipositor
capable of reaching all female ovaries. In this hypothe-
sis, the number of wasp eggs is never limiting, which is
clearly an oversimplification (Nefdt and Compton
1996). Moreover, this hypothesis does not explain the
highly variable seed/wasp ratios observed (from 0 to
100% of seeds within a crop, Bronstein and Hossaert-
McKey 1996), and a cost of having a longer ovipositor
has never been demonstrated.
The limited-egg-supply hypothesis (Nefdt and Comp-
ton 1996) suggests that on average, there are not
enough eggs deposited in one syconium to occupy all
female flowers. This is clearly true in some cases
(Anstett et al. 1996, Nefdt and Compton 1996), but the
hypothesis cannot explain why some seeds are still
produced when the number of eggs is clearly saturating
(Anstett et al. 1996, Bronstein and Hossaert-McKey
1996). Moreover, the number of foundresses, and thus
the egg supply, greatly varies within individual figs
(from 1 to 24 in F. aurea [Bronstein and Hossaert-
McKey 1996] while five foundresses are clearly saturat-
ing [Anstett et al. 1996]), and among crops (mean
number of foundresses per fig ranges from 1.4 to 7.6,
478
data from 12 crops at the same date [Bronstein and
Hossaert-McKey 1996]), showing that egg supply is not
always limiting.
Within a fig, there are several irregular layers of
ovaries. Because style and pedicel are both approxi-
mately straight, with all stigmata being at the same
height during fig receptivity, lengths of style and pedicel
of each flower are highly negatively correlated. Thus
female flowers of the outer layers (near the fig wall)
have a long style and a short pedicel and female flowers
of the inner layers (near the fig lumen) have a short
style and a long pedicel (Fig. 1). Because ovary organi-
zation is irregular, style length distribution is unimodal.
Seeds and pollinators can develop in any layer of
ovaries (Kerdelhué and Rasplus 1996, Nefdt and
Compton 1996). However, ovaries of the outer layer
(near the fig wall) are more likely to develop into seeds,
whereas ovaries of the inner layer are more likely to
host a wasp larva (pollinator or parasite). This is the
only point that was observed by all the authors that
proposed the above hypotheses (West and Herre 1994,
Ganeshaiah et al. 1995, Nefdt and Compton 1996) and
others (Kerdelhué and Rasplus 1996).
This spatial distribution is thought to be the result of
a choice by the pollinator during oviposition that could
be based on style length and shape. This choice could
also be due to differences in the quality of flowers
within each fig. Understanding the causes of this choice
may help us to examine the three existing plausible
hypotheses for why pollinators do not lay eggs
everywhere.
Here I address the following questions: Does the fate
of an ovary depend on its position (i.e. ovary layer, as
defined by pedicel length, see below) or on female
flower style length? Does duration of pollinator devel-
opment depend on the position of its gall? Does gall
seed size vary with the position of the ovary? In light of
these new results, I will discuss the reasons why pollina-
tors are benevolent to their host tree and whether this
benevolence is due to an evolutionarily stable strategy,
an evolutionary constraint or an unbeatable strategy of
one of the partners.
Materials and methods
Ficus microcarpa (Linn. f.) is native to Asia and intro-
duced as an ornamental tree in many countries (McKey
1989). Its pollinator, Eupristina 6erticillata (Waterston)
has also established in many areas of introduction
(McKey 1989). On three different trees planted in
Sevilla (Spain), I collected figs just before wasp emer-
gence, then placed them in glass vials. The number of
foundresses per fig is unknown since they can re-exit
the fig they visit (pers. obs.), as in many species (Giber-
nau et al. 1996). When male wasps started to emerge,
OIKOS 95:3 (2001)
Table 1. Results of a multiple regression explaining pedicel length. This model explains 67.4% of the total variance.

df Type III SS F P

Style 1 77.5 72.3 B1×10−4

Ovary length 1 16.2 15.1 B1×10−4
Tree 2 10.2 5.12 B9×10−3
Fig(tree) 13 40.7 2.9 B5×10−4
Style×content 1 45.6 42.6 B1×10−4
Ovary length×content 1 109.6 102.2 B1×10−4
Style×fig (tree) 15 35.5 2.21 B6×10−3
Error 347 371

each fig was immediately cut open and put into 70% Results
ethanol, with all the wasps. I thus stopped emergence of
wasps at a point when some females had already exited Does the content of an ovary depend on its
their galls whereas others were still inside. For five figs position (i.e. ovary layer or pedicel length) or on
per tree, I measured style length, pedicel length, seed or style length?
gall length and width for at least 30 flowers per fig.
There was an overall correlation between style and
Since styles and pedicels are approximately straight
pedicel length (r= − 0.643, p B10 − 4, n=398). A mul-
(especially for pedicels), and since they stay intact dur-
tiple regression analysis (Table 1) shows that pedicel
ing fig development, measurement is quite easy in spite
length depended on style length and ovary (i.e. seed or
of their small size. During fig receptivity all stigmata
gall) length. Pedicel length also depended on tree, fig
are at the same height and form a stigmatic platform
(tree) and an interaction term style × fig (tree). It also
for the pollinators. However, after pollination the style
depended on the interactions ovary length × content
no longer has a function. When wasps emerge, stigmata
and style × content (Table 1), showing that the regres-
may be at any height and do not form a platform
sion line was different for flowers containing a seed and
anymore. On the other hand, pedicels are likely to
flowers containing a gall. Pedicel length decreased more
ensure circulation of nutrients during the whole devel- with ovary length for seeds than for galls. This may be
opment of the fig. When wasp emerge, pedicels are still due to very different size (see below) and shape of galls
straight and perpendicular to the fig wall and thus and seeds, seeds being longer and larger. Fig. 2 shows
provide an accurate measurement of the distance be- the variability of the regression between style and
tween the ovary and the fig wall, i.e. of ovary position. pedicel length for each fig and each content (seed or
I also recorded content of each flower: seed, female wasp). Besides the overall correlation between pedicel
pollinator inside a closed gall, female pollinator inside a and style length, the high number of variables signifi-
gall with a hole, empty gall. No parasites were present cantly explaining pedicel length indicates the intricate
in these figs. Within a fig, male pollinators exit their developmental factors responsible for the final pedicel
galls first, then mate females by piercing a small hole in length.
the gall of each female wasp and inserting the abdo-
men. Thus a female pollinator inside a gall with a small
hole is a mated female. It is only after being mated that
female pollinators exit their galls and then their natal
fig.
Continuous variables (seed or gall length and width)
were analysed using general linear models (proc GLM,
SAS 1999) and type III SS. Qualitative variables with
two levels (seed or wasp, closed or open gall, full or
empty gall) were analysed by logistic regression (bino-
mial distribution and logit link function, proc GEN-
MOD, SAS 1999), and qualitative variables with three
levels (closed, open or empty gall) by a log linear model
(Poisson distribution and log link function, proc GEN-
MOD, SAS 1999). For these analyses LR statistics for
type III analysis are provided (proc GENMOD, SAS
1999). I used forward model selection, keeping only
significant variables and interactions in the models (p B
0.05, unless to show the non-significance of some vari- Fig. 2. Regression lines between style and pedicel length for
each fig (black lines for flowers containing a wasp and gray
ables). In all analyses backwards selection gave the lines for flowers containing a seed), showing the overall nega-
same final model. tive correlation and the variability of the relationship.

OIKOS 95:3 (2001) 479


Fig. 3. Style length distribution according to ovary content.
Both seeds and pollinators develop in flowers of all style
length. The mode of the style length distribution is smaller for
pollinators than for seeds. n= 117 for flowers containing a
seed and n =343 for flowers containing a pollinator.
Female flowers of the entire range of style lengths
can be occupied by either a seed or a pollinator (Fig.
3). Pollinators occupied flowers of the entire range of
pedicel lengths, but seeds mainly occupied flowers
with short pedicels (Fig. 4). However some seeds did
(rarely) develop in flowers with long pedicels.
The content of the ovaries (seed or gall) depended
significantly on the fig and on pedicel length, with a
marginal effect of pedicel ×tree (Table 2, two figs
without seeds were excluded from this analysis).
When added to this model, the variable style length
Fig. 4. Pedicel length distribution according to ovary content.
Both seeds and pollinators develop in flowers of all style
lengths. However, very few seeds develop in flowers with a
long pedicel. n = 117 for flowers containing a seed and n =273
for flowers containing a pollinator.
480
Table 2. LR statistics for type 3 analysis of a logistic regres-
sion of the content of the ovaries (seed or wasp). Only
significant variables are retained in the model. The content of
the ovaries depended on pedicel length and on the fig but not
on style length. n = 403.
Variable df x2 P
Pedicel length 1 109 B10−4
Fig (tree) 14 44 B10−4
Pedicel×tree 2 9 0.01
did not have a significant effect (df = 1, x2 = 0.27,
p \ 0.6). However, in a simple logistic model with
style length and fig as the only independent variables,
style length did explain the content of the ovaries
(df = 1, x2 = 62.9, pB0.0001). In this case, style
length did not enter into the final model because the
part of variance it explains is included in the variance
explained by the variable pedicel length (since pedicel
and style length are correlated). This underlines the
importance of measuring both variables. Fig. 4 illus-
trates that flowers containing a seed had a shorter
pedicel.
Does rapidity of pollinator emergence depend on
the position of its gall?
The different gall states (closed, with hole and a pol-
linator inside or empty) reflect the rapidity of emer-
gence, i.e. the time of wasp development plus the
time spent waiting for males when development is
already completed. The gall state depended on the fig
and on pedicel length (Table 3). When added to this
model, style length did not significantly affect gall
state (df =1, x2 = 0.25, p\ 0.6). Pedicels of empty
galls were longer than those of galls with a hole and
pollinators inside, which were in turn longer than
those of closed galls (Fig. 5). Thus wasps of the inner
layer of ovaries emerged first. This is due to the fact
that females occupying flowers with longer pedicels
were mated first (Table 4), and exited their gall first
(Table 5). I found no significant effect of style length
on these variables. Thus rapidity of pollinator emer-
gence depended on the position of the ovary within
the fig.
Table 3. LR statistics for type 3 analysis of a log linear model
of the gall state (closed, with a hole, empty). Pedicel length
significantly explained the gall state. For this analysis, I only
retained figs with galls in all three states. n = 94.
Variable df x2 P
Pedicel length 1 6.43 0.011
Fig (tree) 3 6.78 0.079
OIKOS 95:3 (2001)
 Table 5. LR statistics for type 3 analysis of a logistic regres-
sion on whether or not the pollinator had exited from its gall.
Above a tree and a fig effect, pedicel length significantly
explained the pollinators’ exit status.

Variable df x2 P

Tree 2 5.9 0.05

Fig (tree) 12 56.2 1×10−3
Pedicel length 1 9.7 B10−4

characteristics but also to the quantity and quality of

pollinator visits.

An advantage of developing in the inner ovaries

Fig. 5. Percentage of the different gall states for each pedicel
length class, showing that galls with a wasp already exited
have longer pedicels than galls with a mated wasp inside.
Virgin wasps tend to occupy galls with the shortest pedicels.
Sample size is in parentheses above the bars.
Do gall and seed size vary with the position of
the ovary?
Both gall and seed size (height ×width) depended on
the tree, on the fig and on pedicel length but not on
style length (Tables 6, 7). However, gall size increased
with pedicel length (Fig. 6a) whereas seed size decreased
with pedicel length (Fig. 6b). Thus the outer ovaries
(Fig. 1) produced many large seeds and a few small
galls, whereas inner ovaries produced few small seeds
and many large galls. Once more, position of the ovary
(i.e. pedicel length) and not style length was responsible
for these differences.
Discussion
In this study I demonstrate that pollinators developing
in flowers with long pedicels and short styles (i.e. with
ovaries near the lumen of the fig) will tend to develop in
a larger gall. Female wasps developing in the innermost
layer of ovaries will be mated first, and will exit their
gall, and probably their natal fig, earlier than those
developing in ovaries in other positions. I will discuss
below how this results in a fitness advantage in laying
eggs in flowers that will develop in the inner layers. In
most of our analyses there is either a tree and/or a fig
effect. These are likely to be due not only to plant
Table 4. LR statistics for type 3 analysis of a logistic regres-
sion of mating status of female pollinators. Whether the
female was mated or not depended on pedicel length and on
the host tree. n=126.
Variable df x2 P Style
Pedicel length 1 15.7 B10−4
Tree 2 13.0 B2×10−3
Several advantages are associated with development in
the inner galls. First, inner galls are larger than outer
galls, and are likely to host larger pollinators. Larger
pollinators have a higher probability of reaching a
receptive syconium and laying eggs (Herre 1989). More-
over, larger species of pollinators have a higher number
of eggs (Herre, 1989). This pattern is likely to be
maintained at the intra-specific level and to add an
advantage of larger size. Second, female pollinators
developing in the outer galls should have a lower
probability of mating. When I opened the figs, most
males had already exited, and at that time, the proba-
bility of mating of virgin females should be low. Un-
mated females can lay eggs but will only have sons,
resulting in zero fitness if the female is the only
foundress. Third, females developing in the inner
ovaries will exit the fig first, just after the males, which
could possibly aid in escaping ant predation. Duration
of wasp emergence from a single fig was about 1 h.
However, after emergence pollinators of Ficus micro-
carpa live less than 5 h (pers. obs.). A small difference
in the timing of emergence is likely to have a strong
impact on pollinator fitness.
After pollination, enlarging seeds and galls fill the
lumen of the fig, leading to its disappearance and to the
tight packing of the ovaries. In some species fruits may
sometimes even burst before maturity (F. racemosa;
pers. obs.). At the beginning of fruit development, just
after pollination, there is some free space near the fig
wall and near the lumen. Near the fig wall only between
Table 6. Results of a GLM model explaining gall size. Gall
size depended on the tree, on the fig and on pedicel length, but
not on style length. This model explains 40.7% of the total
variance.
Variable df Type III SS F P
Pedicel 1 33.1 25.6 B10−4
1 1.1 0.9 0.33
Tree 2 63.5 24.6 B10−4
Fig (tree) 13 76.4 4.5 B10−4
Error 253 326.8

OIKOS 95:3 (2001) 481

Table 7. Results of a GLM model explaining seed size. Seed wasps emerge from their galls, the fig enlarges and the
size depended on the tree, on the fig and on pedicel length, but lumen reappears in the centre. When male wasps exit, it
not on style length. This model explains 50.1% of the total
variance. should be easier for them to move in the lumen than
between compacted galls and seeds, which would explain
Variable df Type III SS F P why they mate first with females in the inner layers of
Pedicel 1 45.8 10.6 0.001 ovaries. As a consequence, these females will be the first
Style 1 11.0 2.55 0.11 to exit their galls and then the fig. These space constraints
Tree 2 86.8 10.0 B10−4 could explain the observed differences in gall size and
Fig (tree) 11 205.9 4.32 B10−4 development, and why these differences are more closely
Error 95 411.2
related to pedicel than to style length.

pedicels is there any free space, whereas ovaries touch

each other and are more compacted. Thus ovaries can
develop either towards the lumen or towards the fig wall.
This would explain why galls, which develop mostly in
inner flowers, are bigger when they are nearest the centre,
while seeds, which develop mostly near the fig wall, are
bigger when they are nearest the fig wall. Just before
How can foundresses choose flowers with a long
pedicel?
Space constraints do not explain why pedicel length also
better explains the distribution of seeds and wasps than
does style length. During oviposition, foundresses could
conceivably assess style length and shape, but not pedicel
length. Foundresses could respond to length and curva-
ture of the style as an indicator of pedicel length, but this
seems unlikely. An alternative hypothesis is that there is
a differential development of the pedicel depending on
the position or on the content of the ovary. Due to the
same space constraints as discussed above, inner ovaries
would grow and be pushed towards the lumen, resulting
in a longer pedicel, whereas outer ovaries would develop
towards the fig wall and would have a shorter pedicel.
This consideration, and the different regression lines
between style and pedicel length, suggest that pedicel
growth is smaller for ovaries that contain a seed. Thus
foundresses preferentially lay eggs in flowers with a short
style (the content of the ovary depends on style length
when pedicel is not in the model, see Results). These
flowers have also a long pedicel and will grow and be
pushed towards the inside of the fig during development.
According to this reasoning, the pedicel of long-styled
flowers (especially those that contain a seed) will grow
less during post-pollination development. This could
explain why pedicel length is a better predictor of ovary
content than is style length.

A new hypothesis explaining pollinator

Fig. 6. a) Relationship between gall size and pedicel length; b)
Relationship between seed size and pedicel length. For both
graphs each line represents one fig and the bold line the
relation for all flowers.
benevolence
These results confirm that pollinators can develop in all
flowers, whatever the lengths of their styles (Fig. 3) and
pedicels (Fig. 4). They also show that flowers are of
different quality for pollinator development depending
on their position (i.e. pedicel length). The preference of
foundresses for short-styled, long-pedicelled flowers, il-
lustrated by Figs 3 and 4, is now explained, since there
is a cost in laying eggs in ovaries close to the fig wall.
The only data supporting the ‘‘unbeatable-seeds’’
hypothesis (West and Herre 1994) is the apparent com-
petition between fig pollinators and some species of

482 OIKOS 95:3 (2001)

parasitic wasps. However, the existence within the fig of
flowers of different quality as larval hosts for both
pollinators and parasites, is sufficient and more parsi-
monious to explain this competition. Thus no data
exclusively support the unbeatable-seed hypothesis.
The ovipositor-length-optimization hypothesis (Gane-
shaiah et al. 1995, Kathuria et al. 1995) is lacking a
demonstrated cost of the ovipositor length. Different
quality of flowers depending on their position could fill
this gap. An ovipositor too long could increase the
percentage of eggs laid in long-styled, low-quality flow-
ers and could entail a cost of ovipositor length. More
work is needed to test for the existence of such a cost.
Based on these hypothesis I propose a new explana-
tion of pollinator benevolence in the fig/wasp mutual-
ism that synthesizes the ovipositor-length-optimization
and the limited-egg-supply hypothesis. Selection on
ovipositor length could be frequency dependent: in the
absence of competition for egg laying sites (i.e. in
single-foundress figs) there would be an advantage in
having a short ovipositor (long enough to permit laying
of all the foundress’ eggs but short enough to prevent
laying of eggs in the outer layers of ovaries) whereas in
situations with competition (i.e., several foundresses),
pollinators with a longer ovipositor would be favoured
since they would have access to more ovaries. The
resulting ovipositor length would depend on fig struc-
ture (style length distribution, number of female flowers
per fig) and on fig wasp population dynamics (distribu-
tion in space and time of the number of foundresses per
fig). Thus the proximate cause of seed/wasp production
ratios at the syconium level would depend on the
number of foundresses per fig: with one or few
foundresses the number of eggs would be limiting,
whereas with many foundresses, wasp production
would be limited by the ovipositor length. This hypoth-
esis seems congruent with currently published data but
needs further testing.
Acknowledgements – I thank Martine Hossaert and Doyle
McKey for helpful comments on the manuscript, and Edmond
Dounias for preparing Fig. 1.
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