APS 301. Co-operation & Conflict

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APS 301. Co-operation Conflict Professor
Francis L. W. Ratnieks Lecture 3 Brood Site
Pollination Mutualisms Common Interests and
Conflicts Between Two Species
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What is Mutualism?
Relationship Party 1 Party 2 Mutualism
Relationship Actor Recipient Parasitism
Altruism Spite
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What is Mutualism?
Mutualism is an arrangement where all parties
benefit. Many symbiotic (living together)
relationships are mutualistic. For example, many
insects have micro-organisms living in their gut
(e.g., termites and gut protozoa) or
intracellularly which help in nutrition,
particularly in species which live on a
non-balanced or difficult to digest diet such as
wood, plant sap, blood etc.). In previous
lectures we have also seen that genes can usually
be considered as mutualists. However, many
symbiotic relationships are parasitic with one
party exploiting the other.
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Brood Site Pollination Mutualisms
The lecture will focus on obligate mutualistic
relationships involving insect pollinators whose
larvae also develop in the plants they pollinate
(brood site pollination mutualism). Even
though both partners need each other to
reproduce, and even though the relationship is
basically mutualistic, there is often an
incentive for one party to overexploit the other,
and hence conflict. In the next lecture we will
also consider parasitic symbioses and see that
the exploitation of the host by the parasite may
vary from benign to harmful. Symbiotic
relationships are a continuum from mutualism to
parasitism.
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Pollination as a Mutualism
The pollen of many angiosperms is moved between
plants by insects and other animals. The plant,
if it has both male and female function, receives
two benefits. First, its pollen is transmitted to
other plants. Second, it receives pollen from
other plants to fertilise its own eggs. (Many
plants have stigmas that reject their own
pollen.) The pollinator usually receives an
incentive to visit the flower in the form of
nectar. Rewards also include the pollen itself,
oils, and scents (used by male orchid bees,
Euglossinae, to attract female bees).
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Pollination as a Mutualism
Sometimes this relationship is not mutualistic.
Some bees visit plants without pollinating
them. Instead they work the flower from the side
or even chew a hole through the corolla tube in
which to insert their tongue. Some plants
exploit pollinators. Some orchids mimic female
bees and wasps and attract males who try to
copulate with them, spreading pollen via
attempted matings. Kiwi fruit (Actinidia) has
both male and female function plants. Both have
nectar-less flowers with pollen as reward. But
the pollen produced by female function plants is
in fact useless to the bees as food (and also
useless in transmitting genes). It is just the
non-digestible outer coating.
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Insect Cheating Plant
Bumble bee (Bombus terrestris) worker taking
nectar through a hole she has bitten in a
honeysuckle (Lonicera) flower. Honeysuckle is
normally pollinated by long-tongued moths.
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Insects Cheating Plant
Bumble bee (left) and honey bee (right) taking
nectar from base of corolla tube without
pollinating. Some bees (including some bumble
bees but not honey bees) can chew a hole through
the corolla tube.
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Insect Cheating Plant
Left. Honey bee (Apis mellifera) working Brassica
flower from above, a position that results in
pollination. Right. Honey bee inserting tongue
from side in natural gap in flower, a position
that does not pollinate.
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Plants Cheating Insect
Pollination of W. Australian orchid Drakaea
glyptodon by thynnine wasp Zaspilothynnus
trilobatus. Top Left. Pre-mating posture of
wingless female wasp. Top Right. Orchid flower.
Bottom. Male wasp tipped back by flower into
position needed for pollination.
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Plants Cheating Insect
Orchid flower resembles female wasp
Male wasp copulating flower
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Plants Cheating Insect
Insect visitors to Ophrys orchids. Left. Male
solitary wasp Camposcolia ciliata on O. speculum
Centre. Male solitary wasp Argogorytes mystaceus
on fly orchid, O. insectifera Right. Male
solitary bee Andrena maculipes on O. lutea.
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Bee Orchid
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Bee Orchid
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Brood Site Pollination Mutualism
Most plants are visited by many pollinator
species, and pollinators visit many plant
species. Some pollination mutualisms are more
specific. In some the plant provides a home for
the larvae of the pollinating insects instead of
or in addition to the more traditional rewards of
pollen and nectar. We will look at two of these.
We will see how the relationship between figs and
fig wasps has less conflict in it that that
between yucca plants and yucca moths. Fig/Fig
wasp mutualism Fig plants (Ficus spp.) and Fig
wasps (Agaonidae) Where worldwide in tropical
and subtropical countries Yucca/Yucca moth
mutualism Yucca plants (Yucca spp.) and Yucca
moths (Tegeticula spp) Where N. America
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Fig - Fig Wasp Mutualism
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Strangler fig from SE Asia. The fig climbs an
existing tree which it eventually kills. Figs are
perennial plants ranging in size from a small
bush to a massive tree. Photo courtesy Steve
Compton
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Female fig wasp entering fig via ostiole. Panama
Photo courtesy Allen Herre
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Cross section of fig at time of entry of mother
wasps. Panama. Photo courtesy Allen Herre
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Fig Wasps Figs
Top Left. Female fig wasp, Blastophaga
quadraticeps. Bottom Left. Male of same
species. Right. Female fig wasp, Ceratosolen
arabicus, laying an egg inside fig. Forelegs are
raised to extract pollen from thoracic pockets,
where it is stored by the wasp.
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Fig Wasp Life Cycle
2. Wasp larvae develop
3. Male (wingless) and female offspring wasps
emerge mate
1. Mated female wasp enters fig lays eggs in
fig flowers inside fig
4. Mated female wasps disperse to fig flowers on
other fig plants.
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Cross section of fig at time of emergence of
progeny wasps. Panama.
Photo courtesy Allen Herre
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Male fig wasps showing absence of wings and large
mandibles for male-male fighting. Panama. Photo
courtesy Allen Herre.
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Fig Wasps Figs
The life cycle is complex, but you must
understand it. A fig is an inflorescence
arranged so that the flowers are all on the
inside of a cavity (synconium). The flowers
inside are connected to the outside world by a
small hole in the fig (ostiole). One or more
mated and pollen carrying female fig wasps,
usually of a particular species per fig species,
enter the ostiole. They pollinate the flowers,
which are all female at this point, and lay eggs
in some of them. The wasp larvae develop into
adults as parasites of some of the fig flowers.
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Fig Wasps Figs
Offspring male and female wasps emerge inside the
fig and mate. Male fig wasps often fight with
each other. The female wasps collect pollen from
male flowers that mature inside the fig at this
time. The mated, pollen-carying, females now
leave their natal fig through a hole in the side
cut by the male wasps. They disperse to other fig
plants which have young figs to enter. The fig
matures after the wasps leave. Figs are eaten by
vertebrates who disperse the seeds in their
faeces. The mother fig wasps did not lay eggs in
all female flowers, so the fig does produce
seeds.
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Fig Wasps Figs
In addition to pollinating fig wasps there are
species of fig wasp (Torymidae) which do not
enter the fig to lay their eggs. Instead they
use a long ovipositor to lay eggs through the
outer coat of the fig without having to enter.
These do not pollinate the fig and so are
parasites. They are parasites of both the fig
plant and the fig wasp. They need the pollinating
(mutualistic) fig wasp to pollinate the fig that
they lay eggs into. They need the fig for their
developing larvae.
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Mutualistic Parasitic Fig Wasps
Parastic fig wasp
Outer coat of fig
Flowers
Ostiole
Pollinating fig wasp
Flowers
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Mutualistic Parasitic Fig Wasps
Parasitic female fig wasp (above), with long
ovipositor and pollinating fig wasp (below), with
shorter ovipositor. Panama. Photo courtesy Allen
Herre
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Cost to Fig of Parasitism by fig wasps
Even though a large proportion of the figs
ovules are parasitized by wasp larvae, the cost
to the plant is small. Why? Because most ovules
result in female wasps that transmit pollen from
the same plant. Optimal sex ratio is normally
5050. So if half the flowers result in female
wasps (male function for the plant) and half in
seeds this is fine for the plant. However, some
wasps reared are males. Males do not transmit
pollen. But they help by cutting exit holes in
the fig. (In many fig wasps there is LMC, so most
of their offspring are females anyway.)
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Cost to Fig of Parasitism by fig wasps
The fig benefits by having some but not all of
its ovules parasitized Janzen (1979) suggests
ways in which plants can control wasp entry over
evolutionary time (also Herre 1996) e.g. tighter
ostiole, shorter ostiole opening period, more
rapid fig development How many babies do figs
pay for babies? 41-77 of seeds per fig killed
(mean of means 55) (but pollinating and
non-pollinating wasps were not distinguished)
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Defence Against Non-Pollinating Wasps
These wasps have a long ovipositor. Fig may keep
them out by evolving a thicker skin. Could be
expensive to do this Will probably cause an arms
race. With wasps evolving longer ovipositors.
Who would win? Fig or parasitic wasp?
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Gynodioecious figs. Figs from 2 plants. Left
female function plant has only long stigmas and
nowhere for wasp to lay her eggs Right male
function plant has short stigmas allowing
oviposition by wasps. SE Asia. Photo by Steve
Compton.
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Gynodioecious figs

• Some Old World figs are gynodioecious
• Some plants have only female flowers
• Some plants have female and male flowers
• Female only plants all flowers have long styles
  
• Female wasp enters, pollinates but cannot lay
  eggs
• Fig produces seeds but no wasps functionally
  female
• GOOD FOR PLANT, BAD FOR WASPS
• Why do female wasps enter female-function figs?

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Yucca - Yucca Moth Mutualism References Pellmyr,
O., Huth, C. J. 1994. Evolutionary stability of
mutualism between yuccas and yucca moths. Nature
372 257-260. Pellmyr, O., Leebens-Mack, J.,
Huth, C. J. 1996. Non-mutualistic yucca moths and
their evolutionary consequences. Nature 380
155-156.
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Female yucca moth taking pollen from stamens of a
yucca plant. USA.
Photo courtesy National Geographic magazine
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Yucca moth with bundle of pollen in her maxillary
tentacles, ready to pollinate yucca flowers.
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Female yucca moth pollinating the stigma of a
yucca plant. USA.
Photo courtesy National Geographic magazine
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Female yucca moth using ovipositor to lay eggs
below stigma of yucca plant. USA.
Photo courtesy National Geographic magazine
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Yucca Plant Yucca Moth
Left. Yucca flower. The stigma is centrally
located and surrounded by stamens that produce
pollen. Middle. Yucca moth deliberately
obtaining pollen from stamens. Right. Moth
mouthparts are specially modified for handling
pollen.
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Yucca moths Yucca plants
The life cycle is less complex that in the fig
wasps. Yucca plants live in N. America,
particularly in the arid western states. Each
spring a plant produces an inflorescence of many
flowers. Yucca moths hatch from their pupae in
the soil and mate. The females deliberately
collect pollen from the stamens of plants and
deliberately use this to pollinate the stigmas of
the flowers of other plants.The moths have
specialised mouthparts for handling the pollen.
The pollinating moth also saws a slit in the
ovary of the flower it is pollinating and lays
eggs. The eggs develop into larvae which feed on
some of the developing seeds.
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Yucca moths Yucca plants
Plants can drop (abort) flowers into which too
many eggs have been laid or which have not been
pollinated adequately. Moth larvae pupate away
from the plant. Thus, a female moth will probably
not pollinate the plant on which it develops. In
contrast, a fig wasp does transmit the pollen of
the plant in which it developed. Thus, the
interests of plant and insect are more closely
aligned in the fig system than in the yucca
system. As with the fig wasps, there are species
of yucca moths which do not pollinate.
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Abortion (Dropping) of Yucca Flowers
The graph (Pellmyr Huth 1994) shows that when
flowers are aborted, they are normally dropped
before the moth eggs hatch. In this way the plant
can prevent itself from being overexploited by
having too many eggs laid, which would result in
most developing seeds being eaten.
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Abortion (Dropping) of Yucca Flowers
The graph below (Pellmyr Huth 1994) shows
Left, that flowers with more eggs are
preferentially dropped. Right, that flowers with
very few oviposition scars are also more likely
to be dropped. This suggests that the plant is
sensitive to being overexploited (too many eggs)
but also drops flowers that may not have been
sufficiently pollinated (few scars meaning not
much visitation by moths). Plants do not have the
resources to mature all flowers so selectively
abort those of least benefit.
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Non-Mutualistic Yucca Moths
As in figs, some pollinators take
advantage Cheater non-pollinating species of
Tegeticula have evolved Consume seeds but do
not pollinate 76 seeds eaten in population of
plants with pollinator and non-pollinator speces
26 with pollinator only Tegeticula yuccasella
is probably a complex of numerous species, both
pollinators and cheaters
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Non-Mutualistic Yucca Moths
There are two types of cheater Early
cheaters Adults active during latter part of
flowering Oviposit into fruit wall a few days
after pollination Late cheaters Use elongated
ovipositor to cut into full-sized fruit This is
ca. 2 weeks after pollination AND after the
abortion phase (cunning!) If both types occur,
up to 85 of seeds may be destroyed
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Phylogeny of Yucca Moth Strategies
The phylogeny of yucca moths on the following
slide (Pellmyr et al. 1996) was constructed using
2100 base pairs of mitochondrial DNA. Each end
point represents a moth. Above this are the names
of its host plant and the USA State in which they
live. The phylogeny enables the following
inferences to be made. 1. There is a single
origin of active pollination of yucca plants by
moths. 2. There is a single origin of
non-pollinating via early cheating. (Early
cheaters lay their eggs in yucca flowers a few
days after they have been pollinated, and after
the flower abortion period.)
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Phylogeny of Yucca Moth Strategies
3. There is either one or two origins of
non-pollinating via late cheating. (Late
cheaters have an elongated ovipositor and lay
their eggs in the swollen seed pod of the plant
c. 2 weeks after pollination.) 4. Within a
single plant population with two moth species,
one pollinating and one non-pollinating, the two
moths are not closely related phylogenetically.
This suggests that non-pollinating arose when one
moth species colonised an area in which plants
were pollinated by another species, allowing one
species to evolve to be a non-pollinator, rather
than a single species both pollinating and
non-pollinating. 5. Non-pollination evolved
c.61-66 of the time since active pollination.

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Phylogeny of Yucca Moth Strategies
Late Cheaters (non-pollinators)
Early cheaters (non-pollinators)
Y. schidigera CA
Y. utahensis UT
Y. intermedia NM
Y. baccata NM
Y. elata AZ
Y. torreyi TX
Y. brevifolia NV
Y. whipplei sCA
Outgroup
Y. whipplei nCA
Evolution of Tegeticula yucasella complex of
yucca moths
Evolution of active pollination of yucca plants
by yucca moths
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Effect of Cheating on Plants
The figure below (Pellmyr et al. 1996) shows the
proportion of seeds of Yucca filamentosa
destroyed by yucca moths in populations with and
without cheaters ( non-pollinating moth species)
in Ohio and Tennessee. A sample of 25 fruits were
collected in each population. Two populations had
cheaters and six did not. The proportion of seeds
destroyed was only 26 without cheaters but role
to 76 with cheaters.
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Things to Ponder

• Why dont fig wasps avoid female function figs?
• Why dont fig wasps over-exploit the plant by
  laying eggs into all the flowers?
• How might a fig plant be able to able to prevent
  over-exploitation?
• What are the similarities and differences between
  the fig/wasp and yucca/moth mutualisms?
• How can a plant make decisions, such as when a
  yucca plant aborts flowers with excess eggs?
• Parasites have evolved in both mutualisms. Why is
  this? Is it inevitable?
• This is an ongoing area of research see
  references, search Web of Science etc. if
  interested