INTERSPECIFIC MUTUALISTIC RELATIONSHIPS Photo of clownfish & anemone from Wikipedia Photo of fig & fig wasps from Reciprocally

INTERSPECIFIC MUTUALISTIC

RELATIONSHIPS

Photo of clownfish & anemone from WikipediaPhoto of fig & fig wasps from http://www.zoology.ubc.ca

Reciprocally beneficial

interactions

Benefits that accrue to one or both mutualists:CleaningDefense against enemiesProtection from environmental stressesTransport 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

Mutualisms

Photo of Dan Janzen & mutualist(?) from http://www-tc.pbs.org/wgbh/nova/rats/images/janz-01-l.jpg

Mutualisms may occur along each of the following continua:

Long-term symbiotic Ephemeral

Mutualisms

A species of fig & its specialist pollinating wasp

Photo of fig & fig wasps from http://www.zoology.ubc.caPhoto of bat & figs from http://www.ise5-14.org.uk/members/Photos/Plants/seed%20dispersal/Menu.htm

A species of fig & one of itsmany seed dispersers

Obligate Facultative (non-essential)


Mutualisms


A species of fig & one of itsmany seed dispersers


One-to-one Diffuse



(Monophilic Oligophilic Polyphilic)

Mutualisms

A species of fig & itsmany seed dispersers


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

By-product Purloin Investment

By-product

Purloin

Investment

Mutualist 2

Mutualist 1

E.g., mixed species flocks;Mullerian mimicry

Bird sp. 1

Bird sp. 1

Mutualisms

Both parties receive by-product benefits

By-product

Purloin

Investment

Mutualist 2

Mutualist 1


E.g., original insect pollination (w/o extra reward)


Insect sp.

Plant sp.

Mutualisms

A parasite confers by-product benefits on its host

By-product

Purloin

Investment

Mutualist 2

Mutualist 1



E.g., ants & extra-floral nectaries


Ant sp.

Plant sp.

Mutualisms

A party receiving by-product benefits begins to invest in the other party

By-product

Purloin

Investment

Mutualist 2

Mutualist 1




No examples!


Mutualisms

A host begins to parasitize the parasite

By-product

Purloin

Investment

Mutualist 2

Mutualist 1




E.g., yucca & yucca mothNo examples!


Yucca sp.

Moth sp.

Mutualisms

A dependent parasite begins to invest in its host

By-product

Purloin

Investment

Mutualist 2

Mutualist 1




No examples!E.g., yucca & yucca moth

E.g., lichens


Fungus sp.

Alga sp.

Mutualisms

Each party invests in the other, providing safeguardsagainst “cheating” are possible

By-product

Purloin

Investment

Mutualist 2

Mutualist 1




No examples!E.g., yucca & yucca moth

E.g., lichens


Mutualisms

Does Batesian mimicry fit into one of these categories?

Game-theoretical approach

towards understanding the

Evolutionary Stable Strategy

(ESS) conditions of mutualisms

(Axelrod & Hamilton 1981)

Mutualisms

Cooperate Defect

Cooperate

Defect

Potential Mutualist 2







R = 2

Reward for mutual cooperation

S = 0

Sucker’s payoff

T = 3

Temptation to defect

P = 1

Punishment for mutual defection

Two players, each of whom can cooperate or defect (act selfishly)

Payoffs to 1 areshown with illustrative

values

Mutualisms

Cooperate Defect

Cooperate

Defect








R = 2


S = 0

Sucker’s payoff

T = 3


P = 1


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


values

Mutualisms

Cooperate Defect

Cooperate

Defect








R = 2


S = 0

Sucker’s payoff

T = 3


P = 1


This is known as the Prisoner’s Dilemma, whose conditions are:T > R > P > S, and R > (S + T) / 2


values

Mutualisms

Cooperate Defect

Cooperate

Defect








R = 2


S = 0

Sucker’s payoff

T = 3


P = 1


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


values

Mutualisms

Cooperate Defect

Cooperate

Defect








R = 2


S = 0

Sucker’s payoff

T = 3


P = 1


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


values

Mutualisms

Therefore, mutualisms can evolve into parasitic relationships (and vice versa)

Very negative Very positiveNeutral

Less virulentMore virulent Weak mutualism Strong mutualism

Ever-present conflict within mutualisms: each party constantly tests opportunities to cheat (cf. “biological barter” – Ollerton 2006)

Sliding scale of impact of one species (that always acts to benefit itself) on another:

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

Mutualisms

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 orchidfrom http://botany.si.edu/events/sbsarchives/sbs2008


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!)

Photo of a Bee Orchid (Ophrys apifera) from Wikipedia

Pollination by deception likely often arises from a reward-based mutualism

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

Photo of fig & fig wasps from http://www.zoology.ubc.ca

Fig = syconium

Flowers are on the inside

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

Female wasp enters fig through ostiole carrying pollen

Female lays eggs on some flowers & pollinates others

“Scales” grow over ostiole

Mutualism conflict: Production of fig seeds is negatively correlatedwith production of fig wasps

(“biological barter” along an inter-specific trade-off axis)

Transport Mutualisms

Photo of fig & fig wasps from http://www.zoology.ubc.ca

Benefits to plant: Highly effective pollinationBenefits to wasp: Larval provisioningCosts to plant: Larval provisioning & maintaining appropriate fig temperature for wasp developmentCosts to wasp: Pollen transport, competition for oviposition sites when multiple foundresses enter a fig

Present in 92% of plant families (80% of species); see Wang & Qiu (2006)

Mycorrhizae = fungus-plant interactions that influencenutrient (& water?) uptake by the plant

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

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

Trophic Mutualisms

Photo of Phil Grime from http://archive.sciencewatch.com/interviews/philip_grime.htm

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

Distinctly different VAM communitiesin 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

Trophic Mutualisms

Mycorrhizae: An explanationfor yield decline under continuouscropping? (Johnson et al. 1992)

An example of Darwinian Agriculture (see Denison et al. 2003)

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

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

Defense Mutualisms

Methods:8 plots (20 x 20 m) were mown & cleared, sownwith 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

Infected plants have greater “vigor,” toxicity to herbivores & drought tolerance

Photomicrograph of endophyte in Festuca from http://www.goatworld.com/articles/nutrition/tallfescuetoxicosis.shtml

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

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

Defense Mutualisms

Freeman and Rodriguez (1993): The heart-warming tale of a reformed parasite...

Photo of anthracnose on cucumber leaf from http://urbanext.illinois.edu/hortanswers/detailproblem.cfm?PathogenID=128

Plants infected with Path-1 were protected from the wild-type & were immune to an unrelated pathogenic fungus, Fusarium oxysporum

“Path-1” = single-locus mutant of C. magna that spreads throughout the host (albeit more slowly) without necrosis & is a non-sporulating endophyte

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

Defense Mutualisms

Freeman and Rodriguez (1993): The heart-warming tale of a reformed parasite...

Photo of cucurbits grown without (left) and with (right) Path-1 C. magna, both in the presence of Fusarium, fromhttp://wfrc.usgs.gov/research/contaminants/STRodriguez4.htm

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)

Trophic-Protection-Defense Mutualisms

Photo from Wikipedia

Leaf-cutter (attine) ants and fungi

Ants produce proteolytic compoundswhile masticating leaves; fungus further breaks down the leaves and produces food bodies from hyphal tips on which ants feed

Ecosystem-level effects: A single Atta colony can harvest ~ 5% of annual net primary production over 1.4 ha

(summarized in Leigh 1999)

Trophic-Protection-Defense Mutualisms

Photo from Wikipedia

Mutualism does not occur in isolationfrom other species interactions…

E.g., “Aprovechados” (parasites of mutualisms)sensu Mainero & Martinez del Rio 1985

Photo from http://www.pbs.org/wnet/nature/episodes/the-queen-of-trees/photo-essay-an-extraordinary-ecosystem/1356/attachment/gal23/

Parasitic fig wasp


E.g., “Aprovechados” (parasites of mutualisms)sensu Mainero & Martinez del Rio 1985

Parasitic fig wasp

Figure 1.c from Meehan et al. (2009)

An herbivorous jumping spider (Bagheera

kiplingi) that exploits an ant-plant mutualism (Vachellia [formerly

Acacia] & Pseudomyrmex)


Photo from http://coronadetucson.blogspot.com/2009_03_01_archive.html

E.g., Interactions among mutualists of semi-independent function

E.g., Ants that act as defense mutualists againstherbivores may influence pollinators’

activities & pollination success(see: Wagner 2000; Willmer & Stone 1997)


Indirect mutualisms“The enemy of my enemy is my friend”

(e.g., plants whose defenses enlist the services of the “third trophic level”)

2

Me

3

- +

- +

++


Indirect mutualisms“The friend of my friend may be my friend too”

(e.g., a seed-disperser may be an indirect mutualist of apollinator of the same plant)

3

+ +

Me + 2

+ +

Do mutualisms generally arise from close associations?

Do mutualisms generally arise from initially parasitic interactions?

Do mutualisms spawn adaptive radiations?

Phylogenies can help us understand the historical context of mutualisms…

Cospeciation Host switch Duplication

Missing the boat Extinction

Host

Failure to speciate

Mutualist

Coexistence

Mutualisms through time

Ghosts of Mutualism Past

Image from: http://www.karencarr.com

E.g., Janzen & Martin (1982) Neotropical anachronisms: the fruits the gomphotheres ate. Science 215:19-27.

Documents

INTERSPECIFIC MUTUALISTIC RELATIONSHIPS Photo of clownfish & anemone from Wikipedia Photo of fig & fig wasps from Reciprocally