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INTERSPECIFIC MUTUALISTIC RELATIONSHIPS

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  1. INTERSPECIFIC MUTUALISTICRELATIONSHIPS Reciprocally beneficial interactions Photo of clownfish & anemone from Wikipedia Photo of fig & fig wasps from http://www.zoology.ubc.ca

  2. 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

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

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

  5. Mutualisms Mutualisms may occur along each of the following continua: One-to-oneDiffuse (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.ubc.ca Photo of bat & figs from http://www.ise5-14.org.uk/members/Photos/Plants/seed%20dispersal/Menu.htm

  6. 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

  7. Mutualisms Both parties receive by-product benefits Mutualist 2 Investment Purloin By-product Bird sp. 1 E.g., mixed species flocks; Mullerian mimicry By-product Bird sp. 1 Purloin Mutualist 1 Investment

  8. Mutualisms A parasite confers by-product benefits on its host Mutualist 2 Investment Purloin By-product 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

  9. Mutualisms A party receiving by-product benefits begins to invest in the other party Mutualist 2 Investment Purloin By-product 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

  10. Mutualisms A host begins to parasitize the parasite Mutualist 2 Investment Purloin By-product 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

  11. Mutualisms A dependent parasite begins to invest in its host Mutualist 2 Investment Purloin By-product 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

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

  13. Mutualisms Does Batesian mimicry fit into one of these categories? Mutualist 2 Investment Purloin By-product 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

  14. Mutualisms Game-theoretical approach towards understanding the Evolutionary Stable Strategy (ESS) conditions of mutualisms (Axelrod & Hamilton 1981)

  15. Mutualisms Game-theoretical approach towards understanding the Evolutionary Stable Strategy (ESS) conditions of mutualisms (Axelrod & Hamilton 1981) Potential Mutualist 2 Defect Cooperate S = 0 Sucker’s payoff R = 3 Reward for mutual cooperation Cooperate Potential Mutualist 1 P = 1 Punishment for mutual defection T = 5 Temptation to defect Payoffs to 1 are shown with illustrative values Defect Two players, each of whom can cooperate or defect (act selfishly)

  16. Mutualisms Game-theoretical approach towards understanding the Evolutionary Stable Strategy (ESS) conditions of mutualisms (Axelrod & Hamilton 1981) Potential Mutualist 2 Defect Cooperate S = 0 Sucker’s payoff R = 3 Reward for mutual cooperation Cooperate Potential Mutualist 1 P = 1 Punishment for mutual defection T = 5 Temptation to defect 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

  17. Mutualisms Game-theoretical approach towards understanding the Evolutionary Stable Strategy (ESS) conditions of mutualisms (Axelrod & Hamilton 1981) Potential Mutualist 2 Defect Cooperate S = 0 Sucker’s payoff R = 3 Reward for mutual cooperation Cooperate Potential Mutualist 1 P = 1 Punishment for mutual defection T = 5 Temptation to defect Payoffs to 1 are shown with illustrative values Defect This is known as the Prisoner’s Dilemma, whose conditions are: T > R > P > S, and R > (S + T) / 2

  18. Mutualisms Game-theoretical approach towards understanding the Evolutionary Stable Strategy (ESS) conditions of mutualisms (Axelrod & Hamilton 1981) Potential Mutualist 2 Defect Cooperate S = 0 Sucker’s payoff R = 3 Reward for mutual cooperation Cooperate Potential Mutualist 1 P = 1 Punishment for mutual defection T = 5 Temptation to defect 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

  19. Mutualisms Game-theoretical approach towards understanding the Evolutionary Stable Strategy (ESS) conditions of mutualisms (Axelrod & Hamilton 1981) Potential Mutualist 2 Defect Cooperate S = 0 Sucker’s payoff R = 3 Reward for mutual cooperation Cooperate Potential Mutualist 1 P = 1 Punishment for mutual defection T = 5 Temptation to defect Payoffs to 1 are shown with illustrative values Defect 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

  20. 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 positive Very negative Neutral More virulent 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

  21. Transport Mutualisms Pollinator mutualisms (bird-, bat-, bee-, etc. syndromes): Benefits to pollinators include pollen, nectar, oil, resin, fragrances (e.g., Euglossine bees), ovipositionsites, foodsupplyforlarvae, 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

  22. Transport Mutualisms 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

  23. 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

  24. 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

  25. 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)

  26. 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

  27. 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)

  28. 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

  29. 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 (Festucaarundinacea), 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

  30. Defense Mutualisms Freeman and Rodriguez (1993): The heart-warming tale of a reformed parasite... Notorious filamentous fungal pathogen, Colletotrichummagna, 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

  31. 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, Fusariumoxysporum 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

  32. 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

  33. 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

  34. 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/

  35. 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

  36. Mutualism does not occur in isolation from other species interactions… Indirect mutualisms E.g., “the enemy of my enemy is my friend” (recall plants whose defenses enlist the services of the “third trophic level”) 3 - + + 2 + - + Me

  37. Mutualism does not occur in isolation from other species interactions… Indirect mutualisms E.g., “the friend of my friend may be my friend too” (a seed-disperser may be an indirect mutualist of a pollinator of the same plant) + 2 Me + + + + 3

  38. 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?

  39. Hostswitch Duplication Host Mutualist Failure to speciate Missing the boat Extinction Coexistence Mutualisms through time Cospeciation

  40. 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