INTERSPECIFIC
MUTUALISTIC
RELATIONSHIPS
Reciprocally
beneficial
interactions
Photo of clownfish & anemone from Wikipedia
Photo of fig & fig wasps from http://www.zoology.ubc.ca
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-01-l.jpg
Mutualisms
Mutualisms may occur along each of the following continua:
Long-term symbiotic
A species of fig & its
specialist pollinating wasp
Ephemeral
A species of fig & one of its
many seed dispersers
Photo of fig & fig wasps from http://www.zoology.ubc.ca
Photo of bat & figs from http://www.ise5-14.org.uk/members/Photos/Plants/seed%20dispersal/Menu.htm
Mutualisms
Mutualisms may occur along each of the following continua:
Obligate
A species of fig & its
specialist pollinating wasp
Facultative
(non-essential)
A species of fig & one of its
many seed dispersers
Photo of fig & fig wasps from http://www.zoology.ubc.ca
Photo of bat & figs from http://www.ise5-14.org.uk/members/Photos/Plants/seed%20dispersal/Menu.htm
Mutualisms
Mutualisms may occur along each of the following continua:
(Monophilic
One-to-one
Oligophilic
A species of fig & its
specialist pollinating wasp
Diffuse
Polyphilic)
A species of fig & its
many seed dispersers
Photo of fig & fig wasps from http://www.zoology.ubc.ca
Photo of bat & figs from http://www.ise5-14.org.uk/members/Photos/Plants/seed%20dispersal/Menu.htm
Mutualisms
Connor’s (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 benefactor’s activities
Investment: An individual benefits from the costly act(s) of the
benefactor
Purloin (“steal”): An individual benefits by partially
consuming the benefactor
Mutualisms
Both parties receive by-product benefits
Mutualist 2
By-product
Bird sp. 1
By-product
Bird sp. 1
Mutualist 1
Purloin
Investment
Adapted from Connor (1995)
E.g., mixed
species flocks;
Mullerian mimicry
Purloin
Investment
Mutualisms
A parasite confers by-product benefits on its host
Mutualist 2
By-product
Purloin
Insect sp.
By-product
Plant sp.
Mutualist 1
Purloin
Investment
Adapted from Connor (1995)
E.g., mixed
species flocks;
Mullerian mimicry
E.g., original
insect pollination
(w/o extra reward)
Investment
Mutualisms
A party receiving by-product benefits begins to invest in the other party
Mutualist 2
By-product
Purloin
Investment
Ant sp.
By-product
Plant sp.
Mutualist 1
Purloin
Investment
Adapted from Connor (1995)
E.g., mixed
species flocks;
Mullerian mimicry
E.g., original
insect pollination
(w/o extra reward)
E.g., ants &
extra-floral
nectaries
Mutualisms
A host begins to parasitize the parasite
Mutualist 2
By-product
By-product
Mutualist 1
Purloin
Investment
Adapted from Connor (1995)
E.g., mixed
species flocks;
Mullerian mimicry
Purloin
E.g., original
insect pollination
(w/o extra reward)
No examples!
Investment
E.g., ants &
extra-floral
nectaries
Mutualisms
A dependent parasite begins to invest in its host
Mutualist 2
By-product
Purloin
Investment
Yucca sp.
By-product
Mutualist 1
Purloin
Moth sp.
Investment
Adapted from Connor (1995)
E.g., mixed
species flocks;
Mullerian mimicry
E.g., original
insect pollination
(w/o extra reward)
E.g., ants &
extra-floral
nectaries
No examples!
E.g., yucca &
yucca moth
Mutualisms
Each party invests in the other, providing safeguards
against “cheating” are possible
Mutualist 2
By-product
Purloin
Investment
Fungus sp.
By-product
Mutualist 1
Purloin
Investment
Alga sp.
Adapted from Connor (1995)
E.g., mixed
species flocks;
Mullerian mimicry
E.g., original
insect pollination
(w/o extra reward)
E.g., ants &
extra-floral
nectaries
No examples!
E.g., yucca &
yucca moth
E.g., lichens
Mutualisms
Does Batesian mimicry fit into one of these categories?
Mutualist 2
By-product
By-product
Mutualist 1
Purloin
Investment
Adapted from Connor (1995)
E.g., mixed
species flocks;
Mullerian mimicry
Purloin
Investment
E.g., original
insect pollination
(w/o extra reward)
E.g., ants &
extra-floral
nectaries
No examples!
E.g., yucca &
yucca moth
E.g., lichens
Mutualisms
Game-theoretical approach
towards understanding the
Evolutionary Stable Strategy
(ESS) conditions of mutualisms
(Axelrod & Hamilton 1981)
Mutualisms
Game-theoretical approach
towards understanding the
Evolutionary Stable Strategy
(ESS) conditions of mutualisms
(Axelrod & Hamilton 1981)
Potential Mutualist 2
Defect
Cooperate
Cooperate
Potential
Mutualist 1
Payoffs to 1 are
shown with illustrative
values
Defect
R=2
S=0
Reward for
mutual
cooperation
Sucker’s payoff
T=3
P=1
Temptation to
defect
Punishment for
mutual defection
E.g., the Prisoner’s Dilemma – two players, each of whom can
cooperate or defect (act selfishly)
Mutualisms
Game-theoretical approach
towards understanding the
Evolutionary Stable Strategy
(ESS) conditions of mutualisms
(Axelrod & Hamilton 1981)
Potential Mutualist 2
Defect
Cooperate
Cooperate
Potential
Mutualist 1
Payoffs to 1 are
shown with illustrative
values
Defect
R=2
S=0
Reward for
mutual
cooperation
Sucker’s payoff
T=3
P=1
Temptation to
defect
Punishment for
mutual defection
The conditions for this particular “game”, i.e., the Prisoner’s Dilemma, are:
T > R > P > S, and R > (S + T) / 2
Mutualisms
Game-theoretical approach
towards understanding the
Evolutionary Stable Strategy
(ESS) conditions of mutualisms
(Axelrod & Hamilton 1981)
Potential Mutualist 2
Defect
Cooperate
Cooperate
Potential
Mutualist 1
Payoffs to 1 are
shown with illustrative
values
Defect
R=2
S=0
Reward for
mutual
cooperation
Sucker’s payoff
T=3
P=1
Temptation to
defect
Punishment for
mutual defection
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
Mutualisms
Game-theoretical approach
towards understanding the
Evolutionary Stable Strategy
(ESS) conditions of mutualisms
(Axelrod & Hamilton 1981)
Potential Mutualist 2
Defect
Cooperate
Cooperate
Potential
Mutualist 1
Payoffs to 1 are
shown with illustrative
values
Defect
R=2
S=0
Reward for
mutual
cooperation
Sucker’s payoff
T=3
P=1
Temptation to
defect
Punishment for
mutual defection
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
Mutualisms
Game-theoretical approach
towards understanding the
Evolutionary Stable Strategy
(ESS) conditions of mutualisms
(Axelrod & Hamilton 1981)
Potential Mutualist 2
Defect
Cooperate
Cooperate
Potential
Mutualist 1
Payoffs to 1 are
shown with illustrative
values
Defect
R=2
S=0
Reward for
mutual
cooperation
Sucker’s payoff
T=3
P=1
Temptation to
defect
Punishment for
mutual defection
However, mutualism (cooperation) is a possible ESS in the Iterated Prisoner’s
Dilemma, e.g., Tit-for-Tat, in which an individual cooperates on the first move
and then adopts its opponent’s previous action for each future move
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
More virulent
Very positive
Neutral
Less 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
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 “Darwin’s hawk moth” pollinating its Malagasy orchid
from http://botany.si.edu/events/sbsarchives/sbs2008
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)
Artist’s 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.
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
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
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.ubc.ca
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.ubc.ca
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)
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.sciencewatch.com/interviews/philip_grime.htm
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)
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; >
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
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/tallfescuetoxicosis.shtml
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/detailproblem.cfm?PathogenID=128
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/contaminants/STRodriguez4.htm
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
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
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-extraordinaryecosystem/1356/attachment/gal23/
Mutualism does not occur in isolation
from other species interactions…
An herbivorous jumping spider
(Bagheera kiplingi) that exploits
an ant-plant mutualism
(Vachellia [formerly Acacia] &
Pseudomyrmex)
Figure from Meehan et al. (2009)
Proxy for Trophic Level
E.g., “Aprovechados” (parasites of mutualisms)
sensu Mainero & Martinez del Rio 1985
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
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”)
3
-
+
+
+
2
-
Me
+
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
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?
Mutualisms through time
Cospeciation
Host switch
Duplication
Host
Mutualist
Failure to speciate
Missing the boat
Extinction
Coexistence
Ghosts of Mutualism Past
E.g., Janzen & Martin (1982) Neotropical anachronisms: the fruits the
gomphotheres ate. Science 215:19-27.
Image from: http://www.karencarr.com