APS 301, Conflict & Cooperation ,lecture 3
Brood site pollination mutualisms: common interests and conflicts between two species
Aims
1. To provide an introduction to modern ideas concerning pollination mutualism.
2. To provide basic factual data sufficient to understand what is going on.
3. To discuss conflicts between plant and pollinator, and how these conflicts are resolved or not-resolved.
Objectives
1. Learn the basic factual information.
2. Think over and understand the basic evolutionary ideas and questions relating to conflict and cooperation.
3. Link in with ideas presented in other lectures in this series.
Big Picture
Many plants are pollinated by insects and other animals. The relationship is normally mutualistic in that both plant and
pollinator benefit. The pollinator typically gains food (nectar, pollen) or some other useful material (oils, chemicals to
attract females). The plant gains pollination. That is, pollen is brought from other plants (male gametes from the
pollen grain fertilize the recipient plant's female gametes) and/or pollen is collected and may fertilize other plants. In
some cases the relationship is not mutualistic. Plants can exploit insects in various ways, for example by attracting an
insect to a flower with no nectar or pollen but that looks or smells like a female, as in many orchids (e.g., the bee
orchid). The male attempts to copulate with the flower and transmits pollen from plant to plant. Similarly, insects can
explot plants, such as by collecting nectar without transmitting pollen. Bees may collect nectar from the side of the
flower. Some bumble bees, such as Bombus terrestris, collect nectar through a hole cut in a flower tube. The bumble
bee does not go anywhere near the anthers (plant part producing pollen) or stigma and is therefore ineffective as a
pollinator.
Most plants and pollinating animals have fairly broad mutualistic relationships. One plant species has many
pollinator species, and one species of pollinator visits many species of plant. However, there are pollinator-plant
relationships which are extremely "tight", and in which the relationship also invlvesa brood site for the insect young.
One is that between fig wasps (small parasitic wasps of the family Agaonidae) and fig plants. Here, in almost all cases
each plant is pollinated by only one wasp species and each wasp species pollinates only one plant species. In addition,
the plant provides the food for the developing larvae of the wasp. The plant and wasp are entirely dependent on each
other, and each would go extinct without the other. The second tight relationship is between yucca moths and plants.
In these brood site pollination mutualistic relationships we expect and find cooperation between the two
species. For example, the insects deliberately collect pollen and deliberately places this on stigmas. Furthermore, the
insect has specialized structures for storing or transmitting pollen. However, there is still the possibility of conflict
between the two parties. The plant will usually benefit if fewer larvae of the pollinator eat its developing seeds. The
pollinator may benefit from overexploiting the plant by laying more eggs. In this lecture we will not concern ourselves
on the important question of how this type of mutualism evolved (i.e., the intermediate steps involved). Instead, we
will concentrate of the conflicts between plant and pollinator and how these may be resolved or not, and the evolution
of cheating by pollinators,
Fig wasps and figs (various sources such as Janzen, D. H. 1979.)
Basic biology fo the mutualism Figs (Ficus) are 800 species of mostly tropical plants. (Amazing fact: the
mediterranean fig has naturalized in Sheffield along the river Don. The hot water from industry allowed it to survive
and reproduce here. This story is one of the great curiosities of the British flora described by Richard Mabey in his
1996 book Flora Britannica.) Individual plants are cross pollinated. Typically, each plant produces its own flowers
synchronously but different plants in the area flower asynchronously. Each plant has many flowers, grouped into
many inflorescences, "figs", each of which has many flowers on the inside. (The technical term for a fig inflorescence
is "synconium".) One or a few female wasps (Agaonidae: Hymenoptera) enter the fig through an opening (technical
term: ostiole). Typically, the female wasp(s) loses her wings on the way in and never leaves the fig. Inside the fig the
female pollinates the stigmas within the fig synconium using pollen stashed in her body that she collected from her
natal fig. The wasp also lays eggs into the styles of many of the flowers she pollinates using her ovipositor. The plant
styles (part between stigma and ovule) vary in length and most eggs are laid in short styled flowers. However, eggs
can be laid in long-styled flowers but this is done less and is probably a slower process. Colonizing female wasps die.
Wasp larvae develop one per developing seed, killing the seed (typically, c. 50% of seeds are killed). If pollinated and
not parasitized, any flower can develop a seed. (But any fig not pollinated is dropped.) Wasps emerge within the fig
and mate, often with brother males. Males are wingless and often fight. (The sex ratio is usually female biased due to
local mate competition). Newly emerged female wasps collect pollen from male flowers which are now present within
the fig. Female wasps leave the natal fig via the ostiole or a hole in the fig cut by males. These young females enter
figs on other plants which they pollinate, thereby continuing the cycle. The fig itself becomes "ripe" after the wasps
leave and may be eaten by various animals who disperse the seeds arising from the flowers pollinated but not
parasitized by wasps.
APS 301, Conflict & Cooperation ,lecture 3
Non-pollinating wasps In addition to pollinating wasps there are two kinds of wasps that develop in figs without
pollinating: (1) those that parasitize the developing seeds in the fig from the outside using a long ovipositor
(Torymidae: Hymenoptera); (2) those that enter the fig and parasitize from the inside. Non-pollinators may variously
eat the developing seeds, parasitize the fig wasp larva, form galls on the fig etc.
Cost to fig of parasitism by fig wasps Even though a large proportion of ovules are parasitized by fig wasp larvae,
this will not be a great cost to the plant. This is because most ovules result in female wasps which transmit pollen
collected from the same plant (actually the same fig on the same plant). Most outcrossing organisms will have an
optimum sex-allocation ratio of 50:50 (i.e., equal investment to male and female function). Thus having 50% of
ovules parasitized is about right for the plant. However, some wasps reared are male and do not perform pollination,
though they do help the female wasps disperse.
Obviously, the fig benefits by having many but not all of its ovules parasitized. Janzen (1979) suggests a
variety of ways in which plants may control wasp entry into figs over evolutionary time (i.e., via feedback mediated
by natural selection leading to phenotypic change in the plant). For example, if too many flowers are oviposited in
there will be selection to reduce wasp entry (e.g., tighter ostiole, shorter open period of ostiole, more rapid
development of fig etc.) See also Herre (1996). In a study of 8 species of Costa Rican figs, Janzen (Janzen, D. H.
1979. How many babies do figs pay for babies? Biotropica 11: 48-50) found that 41-77% of seeds per fig species
were killed (mean of means 55%). This seems about right for the plant, but seed parasitism by pollinating and nonpollinating wasps were not distinguished.
Non-pollinating wasps: plant defences Plants may be relatively powerless to evolve mechanisms preventing nonpollinating wasps of type (2) because adaptations keeping out these wasps will likely also keep out the needed
pollinating fig wasps. Non-pollinators of type (1) may be kept out by thicker skin on fig. However, this may be
realtively expensive and in an arms race wasps can evolve longer ovipositors.
Some Old World fig species are "Gynodioecious". That is, some plants produce figs with
Gynodioecious figs
only female flowers, and others with both male and female flowers.
In figs with only female flowers a wasp(s) enters and pollinates. All flowers have long styles and the wasp
cannot lay its eggs. Thus the female wasp pollinates the plant but leaves no offspring. These figs produce seeds but no
pollinating wasps and are functionally and actually female, in that they transmit their genes through seeds and produce
no pollen..Good for plant but bad for wasp! In figs with both sexes of flowers a wasp(s) enters, pollinates and lays
eggs. Almost all female flowers are parasitized so these figs produce pollinating wasps but no seeds. These plants are
functionally male, in that they transmit their genes through male function (pollen carrying female wasps). Good for
both plant and wasp!
Gynooecious figs exploit fig wasps attracted to the female-flower-only figs. Why don't wasps learn to avoid
such figs? Presumably, the plants make it difficult for the wasps to tell which is which.
Overall Figs appear not to be overexploited by pollinating fig wasps given that about half the seeds are parasitized.
Wasps are exploited by female only figs in gynodioecious species. Both fig plants and fig wasps are exploited by nonpollinating wasps which parasitize ovules and kill fig wasp larvae directly or by competition for brood sites. How it is
that the fig wasps do not overexploit the plant is not yet known, but probably involves the fig wasps being unable to
parasitize all the developing seeds. But this begs the question of why the wasps have not evolved a way to
"overcome" such a defence (Herre, E. A. 1996. An overview of studies on a comunity of Panamanian figs. J. Biogeog.
23: 593-607). Its still a puzzle!
Yucca plants and yucca moths (various sources)
Yucca (Yucca spp.) plants are agaves and live particularly in western N. America. The moths (Tegeticula spp.) collect
pollen from one plant, visit another plant, lay eggs in the plant ovary using a piercing ovipositor, then deliberately
pollinate the stigma using a special organ (the maxillary tentacles). The moth larva develops in the seed pod of the
plant. When it has completed development the larva of the moth pupates away from the plant. Next year the moths
emerge and mate, and the females collect pollen which they use to pollinate stigmas and continue the cycle. However,
unlike the case of the fig wasp, the female yucca moth probably does not get her pollen from the plant she developed
on as a larva. Thus, unlike the fig plant, a yucca plant does not get a pollination benefit from the actual larvae that
feed on it. Yucca plants abort (= drop, abscise) a great many of their flowers along with any yucca moth eggs in the
flower. Abortion occurs because the plants are typically resource limited not pollination limited. That is, more flowers
are pollinated than the plant has the resources to turn into seeds. The plant does not abort flowers at random.
Stabilization of the mutualism Even more than in the wasp-fig mutualism there is potential conflict between plant
and pollinator because the insects developing on the plant probably do not benefit the plant by transmitting pollen.
What is to prevent the pollinator from laying so many eggs that the entire content of the seed pod is eaten, something
APS 301, Conflict & Cooperation ,lecture 3
which would be of no benefit to the plant? Research (Pellmyr, O., Huth, C. 1994. Evolutionary stability of mutualism
between yuccas and yucca moths. Nature 372: 257-260) on one pair of species, Yucca filamentosa and Tegeticula
yuccasella growing in a botanic garden in Ohio, shows that the plant preferentially aborts flowers with more eggs on.
(Most aborted flowers are dropped from the plant within 5 days of oviposition, before larvae hatch.) However, up to a
point, increased oviposition scarring tends to reduce abortion. Scarring occurs when a moth pierces the ovary with its
ovipositor. Not every piercing results in egg laying but is followed by pollen transfer. Scar number is more a
reflection of pollination intensity than oviposition intensity. The proximal mechanism underlying abortion is not
known, but presumably the plant has some way of determing egg load per flower. Pretty smart for a plant.
Non-mutualistic yucca moths (Pellmyr et al. 1996) As in the fig example there are pollinators that take advantage.
Distinct "cheater" (=non-pollinator Tegeticula) species have evolved within the yucca moth complex and inflict a
heavy cost on the plant by consuming seeds but not pollinating. (76% of seeds are eaten in a population of plants with
both early cheater and pollinator moths but only 26% with only the pollinator.) Historically, there were thought to be
two species of pollinator moths but more detailed studies reveal T.yuccasella to be more complex, and containing both
cheater and pollinator species. Cheaters oviposit into developing seed pods approximately a few days (early cheaters)
or two weeks (late cheaters) after they have been pollinated by moths of the others pecies and so need pollinators to
actually pollinate the plant. There are two types of cheater:
• Early cheaters: Adults are active during the latter part of flowering, ovipositing into the fruit wall a few days
after pollination and after the abortion period.
• Late cheaters: Females use an elongated ovipositor to cut into full-sized fruit. Where both types of cheaters
occur up to 85% of seeds may be destroyed.
Phylogenetic analysis of T. yuccasella (Pellmyr et al. 1996) Phylogeny based on base pair sequences in 2.1kbases of
mitochondrial DNA. The main inferences from the phylogenty are.
• monophyly of T. yuccasella
• active pollination is ancestral and evolved just once
• one origin of early cheaters and one or two origins of late cheaters
• cheaters evolved c. 61-66% of time since origin of T. yuccasella complex
• host shifts are rather common
How has the obligate mutualism persisted or how does cheating evolve? (Pellmyr et al. 1996) There are two basic
ideas behind the evolution of cheating in an obligate mutualism: (1) intraspecific reversal, in which there is only one
pollinator species and within this species some individuals cheat; (2) reversal of one species in a complex of two or
more pollinators, in which one species evolves cheating.
Scenario (1) may be a dead end because it may lead to extinction. That is, intraspecific cheating may not be
stable. If there is a cost to pollinating the non-pollinating strategy should go to fixation and the population will go to
extinction because there will be no pollination. However, there may be some conditions under which both pollinator
and non-pollinator strategies occur in the same species of insect.
Scenario (2) avoids this problem because one species remains as a pollinator. The idea is that there are
multiple species of plants and pollinators, and that for some reason (e.g., range shift, migration) one of the pollinators
starts to pollinate another plant as well. A population of the plant now has two pollinators, both of which pollinate
only that one plant species in that area. Cheating can now evolve in one pollinator species. The pollinator flying later
is pre-adapted for the cheating role, because it can take advantage of the pollination already carried out by the earlier
species. Cheating may be a very advantageous strategy in the yucca system because later oviposition defeats the
plants' abortion mechanism. The phylogeny supports pathway (2) inasmuch as a cheater and a pollinator of the same
plant are not each other's sister group. (For example compare the early cheater and the pollinator feeding on Y.
filamentosa in Ohio, the 3rd and 7th topmost branches from the right hand side of the tree.) The only documented case
of a reversal of mutualism in fig wasps also seems to follow host shift in that the cheater agaonid wasp coexists with a
distantly related pollinator agaonid fig wasp. (In most cases, each fig species has just one pollinating wasp species.)
Overview & summary
It seems that both figs and yuccas are pretty good at keeping their obligate pollinators in line, but are rather less
successful in keeping other species of non-pollinators in line. In the yucca moths the cheaters have evolved from
pollinating moths. But in the fig situstion most non-pollinating wasps have not evolved within the fig wasp complex
(Agaonidae). In the yucca plants research suggests that flower abortion prevents overexploitation of plants by
pollinators. In fig wasps the mechanism, if any, by which plants prevent overexploitation by fig wasps is unknown but
probably is something to do with the wasps being unable, or finding it difficult, to lay eggs in all the flowers within a
fig. Figs and fig wasps are less in conflict that yuccas and yucca moths because the young fig wasp female always
APS 301, Conflict & Cooperation ,lecture 3
collects pollen from the natal fig, thereby providing a direct benefit to the fig plant whose seed she ate as a larva. In
contrast, a yucca moth will not normally collect pollen from the plant in which it develops.