INTERSPECIFIC MUTUALISTIC RELATIONSHIPS

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INTERSPECIFIC MUTUALISTICRELATIONSHIPS
Reciprocally beneficial interactions
Photo of clownfish anemone from Wikipedia Photo
of fig fig wasps from http//www.zoology.ubc.ca
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Mutualisms
Benefits that accrue to one or both
mutualists Cleaning Defense against
enemies Protection from environmental
stresses Transport Trophic enhancement
(energy, nutrients) Etc.
Janzen (1985) recognized five types (1)
Harvest mutualisms (2) Pollination
mutualisms (3) Seed-dispersal mutualisms
(4) Protective mutualisms (5) Human
agriculture / animal husbandry
Photo of Dan Janzen mutualist(?) from
http//www-tc.pbs.org/wgbh/nova/rats/images/janz-0
1-l.jpg
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Mutualisms
Mutualisms may occur along each of the following
continua
Long-term symbiotic
Ephemeral
A species of fig one of its many seed dispersers
A species of fig its specialist pollinating
wasp
Photo of fig fig wasps from http//www.zoology.u
bc.ca Photo of bat figs from http//www.ise5-14.
org.uk/members/Photos/Plants/seed20dispersal/Menu
.htm
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Mutualisms
Mutualisms may occur along each of the following
continua

Obligate Facultative

(non-essential)
A species of fig one of its many seed dispersers
A species of fig its specialist pollinating
wasp
Photo of fig fig wasps from http//www.zoology.u
bc.ca Photo of bat figs from http//www.ise5-14.
org.uk/members/Photos/Plants/seed20dispersal/Menu
.htm
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Mutualisms
Mutualisms may occur along each of the following
continua

One-to-one Diffuse
(Monophilic Oligophilic
Polyphilic)
A species of fig its many seed dispersers
A species of fig its specialist pollinating
wasp
Photo of fig fig wasps from http//www.zoology.u
bc.ca Photo of bat figs from http//www.ise5-14.
org.uk/members/Photos/Plants/seed20dispersal/Menu
.htm
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Mutualisms
Connors (1995) mechanisms by which each organism
benefits
By-product An individual benefits as a
by-product of the selfish act(s) of the
benefactor benefit is incidental to the
benefactors activities
Investment An individual benefits from the
costly act(s) of the benefactor
Purloin (steal) An individual benefits by
partially consuming the benefactor
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Mutualisms
Both parties receive by-product benefits
Mutualist 2
By-product
Purloin
Investment
Bird sp. 1
E.g., mixed species flocks Mullerian mimicry
By-product
Bird sp. 1
Purloin
Mutualist 1
Investment
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Mutualisms
A parasite confers by-product benefits on its host
Mutualist 2
By-product
Purloin
Investment
Insect sp.
E.g., mixed species flocks Mullerian mimicry
E.g., original insect pollination (w/o extra
reward)
By-product
Plant sp.
Purloin
Mutualist 1
Investment
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Mutualisms
A party receiving by-product benefits begins to
invest in the other party
Mutualist 2
By-product
Purloin
Investment
Ant sp.
E.g., mixed species flocks Mullerian mimicry
E.g., original insect pollination (w/o extra
reward)
E.g., ants extra-floral nectaries
By-product
Plant sp.
Purloin
Mutualist 1
Investment
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Mutualisms
A host begins to parasitize the parasite
Mutualist 2
By-product
Purloin
Investment
E.g., mixed species flocks Mullerian mimicry
E.g., original insect pollination (w/o extra
reward)
E.g., ants extra-floral nectaries
By-product
No examples!
Purloin
Mutualist 1
Investment
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Mutualisms
A dependent parasite begins to invest in its host
Mutualist 2
By-product
Purloin
Investment
Yucca sp.
E.g., mixed species flocks Mullerian mimicry
E.g., original insect pollination (w/o extra
reward)
E.g., ants extra-floral nectaries
By-product
E.g., yucca yucca moth
No examples!
Purloin
Mutualist 1
Moth sp.
Investment
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Mutualisms
Each party invests in the other, providing
safeguards against cheating are possible
Mutualist 2
By-product
Purloin
Investment
Fungus sp.
E.g., mixed species flocks Mullerian mimicry
E.g., original insect pollination (w/o extra
reward)
E.g., ants extra-floral nectaries
By-product
E.g., yucca yucca moth
No examples!
Purloin
Mutualist 1
E.g., lichens
Investment
Alga sp.
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Mutualisms
Does Batesian mimicry fit into one of these
categories?
Mutualist 2
By-product
Purloin
Investment
E.g., mixed species flocks Mullerian mimicry
E.g., original insect pollination (w/o extra
reward)
E.g., ants extra-floral nectaries
By-product
E.g., yucca yucca moth
No examples!
Purloin
Mutualist 1
E.g., lichens
Investment
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Mutualisms
Game-theoretical approach towards understanding
the Evolutionary Stable Strategy (ESS)
conditions of mutualisms (Axelrod Hamilton
1981)
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Mutualisms
Game-theoretical approach towards understanding
the Evolutionary Stable Strategy (ESS)
conditions of mutualisms (Axelrod Hamilton
1981)
Potential Mutualist 2
Cooperate
Defect
R 2 Reward for mutual cooperation
S 0 Suckers payoff
Cooperate
Potential Mutualist 1
T 3 Temptation to defect
P 1 Punishment for mutual defection
Payoffs to 1 are shown with illustrative values
Defect
Two players, each of whom can cooperate or defect
(act selfishly)
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Mutualisms
Game-theoretical approach towards understanding
the Evolutionary Stable Strategy (ESS)
conditions of mutualisms (Axelrod Hamilton
1981)
Potential Mutualist 2
Cooperate
Defect
R 2 Reward for mutual cooperation
S 0 Suckers payoff
Cooperate
Potential Mutualist 1
T 3 Temptation to defect
P 1 Punishment for mutual defection
Payoffs to 1 are shown with illustrative values
Defect
The dilemma is whether to cooperate or defect
given the paradox that either player is always
better off defecting, even though if both
cooperated, they would both be better off than if
they both defected
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Mutualisms
Game-theoretical approach towards understanding
the Evolutionary Stable Strategy (ESS)
conditions of mutualisms (Axelrod Hamilton
1981)
Potential Mutualist 2
Cooperate
Defect
R 2 Reward for mutual cooperation
S 0 Suckers payoff
Cooperate
Potential Mutualist 1
T 3 Temptation to defect
P 1 Punishment for mutual defection
Payoffs to 1 are shown with illustrative values
Defect
This is known as the Prisoners Dilemma, whose
conditions are T gt R gt P gt S, and R gt (S T) /
2
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Mutualisms
Game-theoretical approach towards understanding
the Evolutionary Stable Strategy (ESS)
conditions of mutualisms (Axelrod Hamilton
1981)
Potential Mutualist 2
Cooperate
Defect
R 2 Reward for mutual cooperation
S 0 Suckers payoff
Cooperate
Potential Mutualist 1
T 3 Temptation to defect
P 1 Punishment for mutual defection
Payoffs to 1 are shown with illustrative values
Defect
Under these circumstances, an individual can
benefit from mutual cooperation, but it can do
even better by exploiting the cooperative efforts
of others, i.e., mutualism is not an ESS
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Mutualisms
Game-theoretical approach towards understanding
the Evolutionary Stable Strategy (ESS)
conditions of mutualisms (Axelrod Hamilton
1981)
Potential Mutualist 2
Cooperate
Defect
R 2 Reward for mutual cooperation
S 0 Suckers payoff
Cooperate
Potential Mutualist 1
T 3 Temptation to defect
P 1 Punishment for mutual defection
Payoffs to 1 are shown with illustrative values
Defect
However, mutualism (cooperation) is a possible
ESS in the Iterated Prisoners Dilemma, e.g.,
Tit-for-Tat, in which an individual cooperates on
the first move and then adopts its opponents
previous action for each future move
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Mutualisms
Ever-present conflict within mutualisms each
party constantly tests opportunities to cheat
(cf. biological barter Ollerton 2006)
Therefore, mutualisms can evolve into parasitic
relationships (and vice versa)
Sliding scale of impact of one species (that
always acts to benefit itself) on another
Very negative
Very positive
Neutral
Less virulent
More virulent
Weak mutualism
Strong mutualism
Pairwise species interactions are often condition
dependent, i.e., they could shift between
mutualistic and parasitic depending on
environmental conditions
The location on the above scale can therefore
change in either evolutionary or ecological time
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Transport Mutualisms(mobile links)
Pollinator mutualisms (bird-, bat-, bee-, etc.
syndromes) Benefits to pollinators include
pollen, nectar, oil, resin, fragrances
(e.g., Euglossine bees), oviposition sites, food
supply for larvae, etc. Can significantly impact
plant-community structure when pollen limitation
occurs (which is often see Knight et al.
2005)
Image of Darwins hawk moth pollinating its
Malagasy orchid from http//botany.si.edu/events/s
bsarchives/sbs2008
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Transport Mutualisms(mobile links)
Pollinator mutualisms (bird-, bat-, bee-, etc.
syndromes) Benefits to pollinators include
pollen, nectar, oil, resin, fragrances
(e.g., Euglossine bees), oviposition sites, food
supply for larvae, etc. Can significantly impact
plant-community structure when pollen limitation
occurs (which is often see Knight et al.
2005)
Artists reconstruction of Mesozoic (250 mya to
65 mya ended with K-T extinction event)
scorpionfly pollination of a member of the
extinct order Czekanowskiales from Ollerton
Coulthard (2009) Science.
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Transport Mutualisms(gone bad, i.e., no longer
mutualistic!)
Pollination by deception likely often arises from
a reward-based mutualism
Photo of a Bee Orchid (Ophrys apifera) from
Wikipedia
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Transport Mutualisms(mobile links)
Seed-dispersal mutualisms (bird-, bat-,
megafauna-, etc. syndromes primary
secondary) Endozoochory inside animals
Exozoochory outside animals
Mymecochory by ants Can significantly impact
plant-community structure when seed-dispersal
limitation occurs (which is often see Hubbell
et al. 1999)
Photos of dung beetles, Proboscidea parviflora
Trillium recurvatum with elaisomes from Wikipedia
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Transport Mutualisms
Fig syconium Flowers are on the inside
Female wasp enters fig through ostiole carrying
pollen Female lays eggs on some flowers
pollinates others Scales grow over ostiole
Wasp larvae feed on fig seeds as they grow and
develop Newly hatched male wasps fertilize
newly hatched female wasps cut escape holes
females collect pollen in specialized structures
prior to dispersing
Photo of fig fig wasps from http//www.zoology.u
bc.ca
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Transport Mutualisms
Benefits to plant Highly effective
pollination Benefits to wasp Larval
provisioning Costs to plant Larval
provisioning maintaining appropriate fig
temperature for wasp development Costs to
wasp Pollen transport, competition for
oviposition sites when multiple foundresses
enter a fig
Mutualism conflict Production of fig seeds is
negatively correlated with production of fig
wasps (biological barter along an
inter-specific trade-off axis)
Photo of fig fig wasps from http//www.zoology.u
bc.ca
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Trophic Mutualisms
Mycorrhizae fungus-plant interactions that
influence nutrient ( water?) uptake by the plant
Present in 92 of plant families (80 of
species) see Wang Qiu (2006)
Mycorrhizal associations occur throughout the
sliding scale, depending on ontogeny,
environment, identity of fungus and plant (see
Johnson et al. 1997)
These considerations suggest that mycorrhizae
could have substantial effects on plant
communities, as they may influence the
colonization and competitive abilities of plant
species in complex ways (see Bever 2003)
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Trophic Mutualisms
Photosynthate can pass from source plants to
sink plants via the mycorrhizal hyphal
net This could have a major impact on
competitive interactions among plants
Grime et al. (1987) were the first to show the
influence of mycorrhizae on competition (in a
microcosm) isotopically labeled photosynthate
passed from a dominant species (Festuca) to less
abundant species
Photo of Phil Grime from http//archive.sciencewat
ch.com/interviews/philip_grime.htm
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Trophic Mutualisms
Mycorrhizae An explanation for yield decline
under continuous cropping? (Johnson et al. 1992)
Distinctly different VAM communities in plots
with continuous corn vs. continuous soybeans
since VAM influence nutrient uptake,
differences can influence yield Under some
circumstances declining yield of continuous
monocultures reflects proliferation of
mycorrhizae that provide inferior benefits to
their host plants (sliding towards
parasitism) Crop rotation reduces the relative
abundance of detrimental VAM
An example of Darwinian Agriculture (see Denison
et al. 2003)
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Defense Mutualisms
Endophytic fungi fungi that inhabit plant parts
without causing disease Hyperdiverse and common
Arnold et al. (2000) isolated 347 distinct
genetic taxa of endophytes from 83 leaves from 2
tropical tree species gt 50 of taxa were only
collected once
What are they doing in there? At least some are
apparently mutualist symbionts might have
dramatic effects on coexistence, especially by
indirectly affecting competitive ability through
resistance to disease herbivory
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Defense Mutualisms
Clay and Holah (1999) examined an endophytic
fungus in a successional old-field community
the host-specific fungus grows intercellularly
in introduced Tall Fescue (Festuca arundinacea),
and is transmitted through seeds
Infected plants have greater vigor, toxicity to
herbivores drought tolerance
Methods 8 plots (20 x 20 m) were mown cleared,
sown with infected (E) or uninfected (-E) Tall
Fescue a mixture of other species germinated
from the soil-seed bank Results Species
diversity declined in E plots over time relative
to -E plots
Photomicrograph of endophyte in Festuca from
http//www.goatworld.com/articles/nutrition/tallf
escuetoxicosis.shtml
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Defense Mutualisms
Freeman and Rodriguez (1993) The heart-warming
tale of a reformed parasite...
Notorious filamentous fungal pathogen,
Colletotrichum magna, causes anthracnose disease
in cucurbits
Member of a large clade of pathogens capable of
infecting the majority of agricultural crops
worldwide Infection occurs when spores adhere to
host tissue, enter a cell and subsequently grow
through the host leaving a trail of necrotic
tissue
Photo of anthracnose on cucumber leaf from
http//urbanext.illinois.edu/hortanswers/detailpro
blem.cfm?PathogenID128
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Defense Mutualisms
Freeman and Rodriguez (1993) The heart-warming
tale of a reformed parasite...
Path-1 single-locus mutant of C. magna that
spreads throughout the host (albeit more slowly)
without necrosis is a non-sporulating endophyte
Plants infected with Path-1 were protected from
the wild-type were immune to an unrelated
pathogenic fungus, Fusarium oxysporum
Path-1 may induce host defenses against pathogens
or may outcompete other fungi
Considerable potential exists to tailor
endophytes as biocontrol agents another example
of Darwinian Agriculture
Photo of cucurbits grown without (left) and with
(right) Path-1 C. magna, both in the presence of
Fusarium, from http//wfrc.usgs.gov/research/conta
minants/STRodriguez4.htm
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Trophic-Protection-Defense Mutualisms
Leaf-cutter (attine) ants and fungi Ants produce
proteolytic compounds while masticating leaves
fungus further breaks down the leaves and
produces food bodies from hyphal tips on which
ants feed
Ants carry a species of bacterium (Streptomyces)
on their cuticles that controls growth of a
parasitic fungus (Escovopsis) (the tripartite
mutualism of Currie et al. 2003)
Photo from Wikipedia
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Trophic-Protection-Defense Mutualisms
Ecosystem-level effects A single Atta colony
can harvest 5 of annual net primary production
over 1.4 ha (summarized in Leigh 1999)
Photo from Wikipedia
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Mutualism does not occur in isolation from other
species interactions
E.g., Aprovechados (parasites of
mutualisms) sensu Mainero Martinez del Rio 1985
Parasitic fig wasp
Photo from http//www.pbs.org/wnet/nature/episodes
/the-queen-of-trees/photo-essay-an-extraordinary-
ecosystem/1356/attachment/gal23/
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Mutualism does not occur in isolation from other
species interactions
E.g., Aprovechados (parasites of
mutualisms) sensu Mainero Martinez del Rio 1985
Parasitic fig wasp
An herbivorous jumping spider (Bagheera kiplingi)
that exploits an ant-plant mutualism (Vachellia
formerly Acacia Pseudomyrmex)
Figure 1.c from Meehan et al. (2009)
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Mutualism does not occur in isolation from other
species interactions
E.g., Interactions among mutualists of
semi-independent function E.g., Ants that act as
defense mutualists against herbivores may
influence pollinators activities pollination
success (see Wagner 2000 Willmer Stone 1997)
Photo from http//coronadetucson.blogspot.com/2009
_03_01_archive.html
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Mutualism does not occur in isolation from other
species interactions
Indirect mutualisms The enemy of my enemy is my
friend (e.g., plants whose defenses enlist the
services of the third trophic level)
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-

2


-

Me
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Mutualism does not occur in isolation from other
species interactions
Indirect mutualisms The friend of my friend may
be my friend too (e.g., a seed-disperser may be
an indirect mutualist of a pollinator of the same
plant)

Me
2




3
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Phylogenies can help us understand the historical
context of mutualisms
Do mutualisms generally arise from close
associations?
Do mutualisms generally arise from initially
parasitic interactions?
Do mutualisms spawn adaptive radiations?
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Mutualisms through time
Cospeciation
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Ghosts of Mutualism Past
E.g., Janzen Martin (1982) Neotropical
anachronisms the fruits the gomphotheres ate.
Science 21519-27.
Image from http//www.karencarr.com