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

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 Mutualisms Photo of Dan Janzen & mutualist(?) from

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 Photo of bat & figs from A species of fig & one of its many seed dispersers

Obligate Facultative (non-essential) Mutualisms may occur along each of the following continua: Mutualisms A species of fig & its specialist pollinating wasp A species of fig & one of its many seed dispersers Photo of fig & fig wasps from Photo of bat & figs from

One-to-one Diffuse Mutualisms may occur along each of the following continua: A species of fig & its specialist pollinating wasp (Monophilic Oligophilic Polyphilic) Mutualisms A species of fig & its many seed dispersers Photo of fig & fig wasps from Photo of bat & figs from

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 Mutualisms Both parties receive by-product benefits

By-product Purloin Investment Mutualist 2 Mutualist 1 E.g., mixed species flocks; Mullerian mimicry E.g., original insect pollination (w/o extra reward) By-product Purloin Investment Insect sp. Plant sp. Mutualisms A parasite confers by-product benefits on its host

By-product Purloin Investment Mutualist 2 Mutualist 1 E.g., mixed species flocks; Mullerian mimicry E.g., original insect pollination (w/o extra reward) E.g., ants & extra-floral nectaries By-product Purloin Investment 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 E.g., mixed species flocks; Mullerian mimicry E.g., original insect pollination (w/o extra reward) E.g., ants & extra-floral nectaries No examples! By-product Purloin Investment Mutualisms A host begins to parasitize the parasite

By-product Purloin Investment Mutualist 2 Mutualist 1 E.g., mixed species flocks; Mullerian mimicry E.g., original insect pollination (w/o extra reward) E.g., ants & extra-floral nectaries E.g., yucca & yucca moth No examples! By-product Purloin Investment Yucca sp. Moth sp. Mutualisms A dependent parasite begins to invest in its host

By-product Purloin Investment Mutualist 2 Mutualist 1 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 By-product Purloin Investment Fungus sp. Alga sp. Mutualisms Each party invests in the other, providing safeguards against “cheating” are possible

By-product Purloin Investment Mutualist 2 Mutualist 1 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 By-product Purloin Investment 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 Potential Mutualist 1 Game-theoretical approach towards understanding the Evolutionary Stable Strategy (ESS) conditions of mutualisms (Axelrod & Hamilton 1981) 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 are shown with illustrative values Mutualisms

Cooperate Defect Cooperate Defect Potential Mutualist 2 Potential Mutualist 1 Game-theoretical approach towards understanding the Evolutionary Stable Strategy (ESS) conditions of mutualisms (Axelrod & Hamilton 1981) R = 2 Reward for mutual cooperation S = 0 Sucker’s payoff T = 3 Temptation to defect P = 1 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 Payoffs to 1 are shown with illustrative values Mutualisms

Cooperate Defect Cooperate Defect Potential Mutualist 2 Potential Mutualist 1 Game-theoretical approach towards understanding the Evolutionary Stable Strategy (ESS) conditions of mutualisms (Axelrod & Hamilton 1981) R = 2 Reward for mutual cooperation S = 0 Sucker’s payoff T = 3 Temptation to defect P = 1 Punishment for mutual defection This is known as the Prisoner’s Dilemma, whose conditions are: T > R > P > S, and R > (S + T) / 2 Payoffs to 1 are shown with illustrative values Mutualisms

Cooperate Defect Cooperate Defect Potential Mutualist 2 Potential Mutualist 1 Game-theoretical approach towards understanding the Evolutionary Stable Strategy (ESS) conditions of mutualisms (Axelrod & Hamilton 1981) R = 2 Reward for mutual cooperation S = 0 Sucker’s payoff T = 3 Temptation to defect P = 1 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 Payoffs to 1 are shown with illustrative values Mutualisms

Cooperate Defect Cooperate Defect Potential Mutualist 2 Potential Mutualist 1 Game-theoretical approach towards understanding the Evolutionary Stable Strategy (ESS) conditions of mutualisms (Axelrod & Hamilton 1981) R = 2 Reward for mutual cooperation S = 0 Sucker’s payoff T = 3 Temptation to defect P = 1 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 Payoffs to 1 are shown with illustrative values Mutualisms

Therefore, mutualisms can evolve into parasitic relationships (and vice versa) Very negative Very positive Neutral Less virulent More virulent Weak mutualismStrong 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 orchid from

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!) 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 (“mobile links”)

Transport Mutualisms Photo of fig & fig wasps from 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 correlated with production of fig wasps (“biological barter” along an inter-specific trade-off axis) Transport Mutualisms Photo of fig & fig wasps from 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

Present in 92% of plant families (80% of species); see Wang & Qiu (2006) Mycorrhizae = fungus-plant interactions that influence nutrient (& 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 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 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 Trophic Mutualisms Mycorrhizae: An explanation for yield decline under continuous cropping? (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, 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 Infected plants have greater “vigor,” toxicity to herbivores & drought tolerance Photomicrograph of endophyte in Festuca from 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

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, from

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 compounds while 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 isolation from other species interactions… E.g., “Aprovechados” (parasites of mutualisms) sensu Mainero & Martinez del Rio 1985 Photo from ecosystem/1356/attachment/gal23/ Parasitic fig wasp

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 Figure 1.c from Meehan et al. (2009) An herbivorous jumping spider (Bagheera kiplingi) that exploits an ant-plant mutualism (Vachellia [formerly Acacia] & Pseudomyrmex)

Mutualism does not occur in isolation from other species interactions… Photo from 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)

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”) 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

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