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INTERSPECIFIC MUTUALISTIC RELATIONSHIPS

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1 INTERSPECIFIC MUTUALISTIC RELATIONSHIPS
Reciprocally beneficial interactions Please do not use the images in these PowerPoint slides without permission. Photo of clownfish & anemone from Wikipedia Photo of fig & fig wasps from

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 Please do not use the images in these PowerPoint slides without permission. See Janzen’s chapter in D. Boucher, ed. (1985) The Biology of Mutualism, Oxford University Press, Oxford, UK. Harvest mutualisms – one organism harvests resources and converts them to a form usable by the other (e.g., N-fixing bacteria). Photo of Dan Janzen & mutualist(?) from

3 Mutualisms Mutualisms may occur along each of the following continua:
Long-term symbiotic Ephemeral A species of fig & its specialist pollinating wasp A species of fig & one of its many seed dispersers Please do not use the images in these PowerPoint slides without permission. Photo of fig & fig wasps from Photo of bat & figs from

4 Mutualisms Mutualisms may occur along each of the following continua:
Obligate Facultative (non-essential) A species of fig & its specialist pollinating wasp A species of fig & one of its many seed dispersers Please do not use the images in these PowerPoint slides without permission. Photo of fig & fig wasps from Photo of bat & figs from

5 specialist pollinating wasp
Mutualisms Mutualisms may occur along each of the following continua: One-to-one Diffuse (Monophilic Oligophilic Polyphilic) A species of fig & its specialist pollinating wasp A species of fig & its many seed dispersers Please do not use the images in these PowerPoint slides without permission. Photo of fig & fig wasps from Photo of bat & figs from

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 Please do not use the images in these PowerPoint slides without permission. The key is to remember that by-product and investment benefits accrue to an individual from the activities of the benefactor!

7 Both parties receive by-product benefits
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 Please do not use the images in these PowerPoint slides without permission. The 3 mechanisms can be combined into the 6 means by which mutualisms might have arisen (Connor 1995). Mutualist 1 Purloin Investment Adapted from Connor (1995)

8 A parasite confers by-product benefits on its host
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. Please do not use the images in these PowerPoint slides without permission. Mutualist 1 Purloin Investment Adapted from Connor (1995)

9 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. Please do not use the images in these PowerPoint slides without permission. Mutualist 1 Purloin Investment Adapted from Connor (1995)

10 A host begins to parasitize the parasite
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 Please do not use the images in these PowerPoint slides without permission. Mutualist 1 Purloin No examples! Investment Adapted from Connor (1995)

11 A dependent parasite begins to invest in its host
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 Please do not use the images in these PowerPoint slides without permission. E.g., yucca & yucca moth Mutualist 1 Purloin No examples! Moth sp. Investment Adapted from Connor (1995)

12 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 Please do not use the images in these PowerPoint slides without permission. E.g., yucca & yucca moth Mutualist 1 Purloin No examples! E.g., lichens Investment Alga sp. Adapted from Connor (1995)

13 Does Batesian mimicry fit into one of these categories?
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 Please do not use the images in these PowerPoint slides without permission. NOTE: The Batesian mimicry question is a bit of a “trick question”, since the mimic benefits whereas the model is either unaffected (commensalism) or suffers (antagonism). E.g., yucca & yucca moth Mutualist 1 Purloin No examples! E.g., lichens Investment Adapted from Connor (1995)

14 Mutualisms Game-theoretical approach towards understanding the
Evolutionary Stable Strategy (ESS) conditions of mutualisms (Axelrod & Hamilton 1981) Please do not use the images in these PowerPoint slides without permission.

15 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 Sucker’s payoff Cooperate Potential Mutualist 1 Please do not use the images in these PowerPoint slides without permission. To cooperate in this game is to invest in the mutualism; to defect is to withhold investment, but to reap the rewards of the other potential mutualist’s investment. See: Axelrod, R. & W. D. Hamilton The evolution of cooperation. Science 211:1390–1396. See: Hoeksema, Jason D. & Emilio M. Bruna Pursuing the big questions about interspecific mutualism: A review of theoretical approaches. Oecologia 125: T = 3 Temptation to defect P = 1 Punishment for mutual defection Payoffs to 1 are shown with illustrative values Defect E.g., the Prisoner’s Dilemma – 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 Cooperate Defect R = 2 Reward for mutual cooperation S = 0 Sucker’s payoff Cooperate Potential Mutualist 1 Please do not use the images in these PowerPoint slides without permission. To cooperate in this game is to invest in the mutualism; to defect is to withhold investment, but to reap the rewards of the other potential mutualist’s investment. See: Axelrod, R. & W. D. Hamilton The evolution of cooperation. Science 211:1390–1396. See: Hoeksema, Jason D. & Emilio M. Bruna Pursuing the big questions about interspecific mutualism: A review of theoretical approaches. Oecologia 125: T = 3 Temptation to defect P = 1 Punishment for mutual defection Payoffs to 1 are shown with illustrative values Defect The conditions for this particular “game”, i.e., the Prisoner’s Dilemma, are: T > R > P > S, and R > (S + T) / 2

17 shown with illustrative
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 Sucker’s payoff Cooperate Potential Mutualist 1 Please do not use the images in these PowerPoint slides without permission. To cooperate in this game is to invest in the mutualism; to defect is to withhold investment, but to reap the rewards of the other potential mutualist’s investment. See: Axelrod, R. & W. D. Hamilton The evolution of cooperation. Science 211:1390–1396. See: Hoeksema, Jason D. & Emilio M. Bruna Pursuing the big questions about interspecific mutualism: A review of theoretical approaches. Oecologia 125: 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

18 shown with illustrative
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 Sucker’s payoff Cooperate Potential Mutualist 1 Please do not use the images in these PowerPoint slides without permission. To cooperate in this game is to invest in the mutualism; to defect is to withhold investment, but to reap the rewards of the other potential mutualist’s investment. See: Axelrod, R. & W. D. Hamilton The evolution of cooperation. Science 211:1390–1396. See: Hoeksema, Jason D. & Emilio M. Bruna Pursuing the big questions about interspecific mutualism: A review of theoretical approaches. Oecologia 125: 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

19 shown with illustrative
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 Sucker’s payoff Cooperate Potential Mutualist 1 Please do not use the images in these PowerPoint slides without permission. To cooperate in this game is to invest in the mutualism; to defect is to withhold investment, but to reap the rewards of the other potential mutualist’s investment. See: Axelrod, R. & W. D. Hamilton The evolution of cooperation. Science 211:1390–1396. See: Hoeksema, Jason D. & Emilio M. Bruna Pursuing the big questions about interspecific mutualism: A review of theoretical approaches. Oecologia 125: 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 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 negative Neutral Very positive More virulent Less virulent Weak mutualism Strong mutualism Please do not use the images in these PowerPoint slides without permission. See: Ollerton, J "Biological Barter": Patterns of Specialization Compared across Different Mutualisms. pp in: Waser, N.M. & Ollerton, J. (Eds) Plant-Pollinator Interactions: From Specialization to Generalization. University of Chicago Press. 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 either via adaptation (evolution) or a phenotypically plastic response

21 Transport Mutualisms (“mobile links”)
E.g., scatter-hoarding of seeds by rodents Please do not use the images in these PowerPoint slides without permission. Notice that the light-colored confidence limits indicate how well the dark-colored curves account for variation in the data. Jansen, Patrick A. et al Thieving rodents as substitute dispersers of megafaunal seeds. Proceedings of the National Academy of Sciences. “Fig. 1. Dispersal distance and survival of Astrocaryum standleyanum palm seeds handled by scatter-hoarding rodents on BCI, Panama. Curves shown are Kaplan-Meier survivorship estimates (colored lines), with 95% confidence envelopes. (A) Probability of seed dispersal up to a given distance, for the initial movement (red, lower graph) and for the ultimate movement after multiple instances of re-caching (blue, upper graph). Initial seed dispersal was generally limited, with just 18% of the seeds moving >25 m away from the parent tree. However, ultimate dispersal distance, after up to 36 secondary movements, included 35% long-distance dispersal (>100 m). (B) Survivorship of first-order rodent-made caches (red, lower graph) and for the seeds that those caches contained (blue, upper graph). Most caches were recovered within 1 wk, but recovered seeds were usually re-cached rather than eaten, and ultimate survival was nevertheless high, with an estimated 14% survival to 1 y.” Photo of agouti and Astrocaryum palm fruits by Christian Ziegler; Figure from Jansen et al. (2012) PNAS

22 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) Please do not use the images in these PowerPoint slides without permission. Knight, T. M.,  J. A. Steets, J. C. Vamosi, S. J. Mazer, M. Burd, D. R. Campbell, M. R. Dudash, M. O. Johnston, R. J. Mitchell and T.-L. Ashman Pollen limitation of plant reproduction: pattern and process. Annual Reviews of Ecology, Evolution and Systematics 36:467–497. Image of “Darwin’s hawk moth” pollinating its Malagasy orchid from

23 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) Please do not use the images in these PowerPoint slides without permission. An operational definition of pollen limitation – when pollen is artificially added or dispersed to plants, population size increases; when pollen availability is artificially reduced, population size decreases. Knight, T. M.,  J. A. Steets, J. C. Vamosi, S. J. Mazer, M. Burd, D. R. Campbell, M. R. Dudash, M. O. Johnston, R. J. Mitchell and T.-L. Ashman Pollen limitation of plant reproduction: pattern and process. Annual Reviews of Ecology, Evolution and Systematics 36:467–497. See: Ren et al Science; and the Perspective piece by Ollerton & Coulthard. 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.

24 Transport Mutualisms (“gone bad”, i.e., no longer mutualistic!)
Pollination by deception likely often arises from a reward-based mutualism Please do not use the images in these PowerPoint slides without permission. Photo of a Bee Orchid (Ophrys apifera) from Wikipedia

25 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) Please do not use the images in these PowerPoint slides without permission. An operational definition of seed or dispersal limitation – when seed is artificially added or dispersed, population size increases; when seed availability is artificially reduced, population size decreases. Hubbell, S. P., R. B. Foster, S. T. O’Brien, K. E. Harms, R. Condit, B. Wechsler, S. J. Wright & S. Loo de Lao Light-gap disturbances, recruitment limitation, and tree diversity in a neotropical forest. Science 283: Photos of dung beetles, Proboscidea parviflora, & Trillium recurvatum with elaisomes from Wikipedia

26 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 Please do not use the images in these PowerPoint slides without permission. 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

27 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 Please do not use the images in these PowerPoint slides without permission. 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

28 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) Please do not use the images in these PowerPoint slides without permission. Photo from Wikimedia Commons, “Mycorrhiza” page – downloaded Feb. 13, 2016: By Msturmel - MS Turmel, University of Manitoba, Plant Science DepartmentTransferred from en.wikipedia; Transfer was stated to be made by User:Vojtech.dostal., Public Domain, Bever, J. D.  2003.  Soil community dynamics and the coexistence of competitors: Conceptual frameworks and empirical tests.  New Phytologist 157: Johnson, N. C., P. J. Copeland, R. K. Crookston & F. L. Pfleger Mycorrhizae: Possible explanation for yield decline with continuous corn and soybean. Agronomy Journal 84: Wang, B. & Y. L. Qiu Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16:299–363. Photo of arbuscular mycorrhiza from Wikimedia Commons

29 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) Please do not use the images in these PowerPoint slides without permission. Bever, J. D.  2003.  Soil community dynamics and the coexistence of competitors: Conceptual frameworks and empirical tests.  New Phytologist 157: Johnson, N. C., P. J. Copeland, R. K. Crookston & F. L. Pfleger Mycorrhizae: Possible explanation for yield decline with continuous corn and soybean. Agronomy Journal 84: Wang, B. & Y. L. Qiu Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16:299–363. Photo of mycorrhizae from Wikimedia Commons

30 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 Please do not use the images in these PowerPoint slides without permission. Grime, P. J., J. M. L. Mackey, S. H. Hillier & D. J. Read Floristic diversity in a model system using experimental microcosms. Nature 328: Photo of Phil Grime from

31 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 Please do not use the images in these PowerPoint slides without permission. Denison, R. Ford, E. Toby Kiers & Stuart A. West Darwinian agriculture: when can humans find solutions beyond the reach of natural selection? Quart. Review Biol. 78: An example of Darwinian Agriculture (see Denison et al. 2003)

32 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 Please do not use the images in these PowerPoint slides without permission. Arnold, A. E., Z. Maynard, G. Gilbert, P. D. Coley & T.A. Kursar Are tropical fungal endophytes hyperdiverse? Ecology Letters 3:

33 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 Please do not use the images in these PowerPoint slides without permission. Photomicrograph of endophyte in Festuca from

34 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 Please do not use the images in these PowerPoint slides without permission. Freeman, S. & Rodriguez, R. J Genetic conversion of a fungal plant pathogen to an nonpathogenic, endophytic mutualist. Science 260:75-78. Photo of anthracnose on cucumber leaf from

35 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 Please do not use the images in these PowerPoint slides without permission. 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

36 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 Please do not use the images in these PowerPoint slides without permission. Currie, Cameron R., Bess Wong, Alison E. Stuart, Ted R. Schultz, Stephen A. Rehner, Ulrich G. Mueller, Gi-Ho Sung, Joseph W. Spatafora & Neil A. Straus Ancient tripartite coevolution in the attine ant-microbe symbiosis. Science 299: 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

37 Trophic-Protection-Defense Mutualisms
Please do not use the images in these PowerPoint slides without permission. 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

38 Positive interactions can foster coexistence & species diversity
Cleaning Mutualisms Positive interactions can foster coexistence & species diversity Please do not use the images in these PowerPoint slides without permission. Wikipedia “Bluestreak cleaner wrasse” page; accessed 10-III-2015 ["Cleaner wrasse with a client" by Alexander Vasenin - Own work. Licensed under CC BY-SA 3.0 via Wikimedia Commons - Grutter, Alexandra S., Jan Maree Murphy & J. Howard Choat Cleaner fish drives local fish diversity on coral reefs. Current Biology 13:64-67. “Figure 1. Mean (s.e.) Visiting Client Fish Numbers per Reef at Two Sites Counted by Remote Video and by a Snorkeler (A) The number of visiting species on reefs with (closed symbols) and without (open symbols) cleaner fish at Casuarina Beach (circles) and Lagoon (squares) sites. (B) The log10 (x+1) abundance of visiting client fish per reef. Symbols are as in (A). Counts in (A) and (B) were pooled across different times of the day.” “reefs with (closed symbols) and without (open symbols) cleaner fish at Casuarina Beach (circles) and Lagoon (squares) sites Figure from Grutter et al. (2003) Current Biology; photo of cleaner wrasse & client from Wikimedia Commons

39 Cheaters can be Penalized or Sanctioned
Split-plate design: (A) plant roots labeled with 14C; (B) mycorrhizal fungus without P; (C) mycorrhizal fungus with P (either 35 M or 700 M) Title of the project: “Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis” Plant can penalize fungus (for poor P delivery) with low C delivery A B C Fungus can penalize plant (for poor C delivery) with low P delivery Please do not use the images in these PowerPoint slides without permission. Kiers, E. T. et al Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 333: Split-plate design: (A) fungal hyphae labeled with 33P; (B) roots with no access to sucrose; (C) roots with access to sucrose (either 5 mM or 25 mM) Kiers et al. (2011) Science, Fig. 2

40 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 Please do not use the images in these PowerPoint slides without permission. Mutualism does not occur in isolation from other species interactions. This is obviously the case in some types of mutualism (e.g., defense). Kyle once thought “aprovechosos” should be used for the organisms that are taking advantage of the mutualism, even though the original article uses the term “aprovechados” for these organisms, but “aprovechosos” is not a word in Spanish; in Spanish one who takes advantage of others is commonly referred to as an “aprovechado,” so it makes sense that Mainero & Martinez del Rio (1985) would have used that term; even so, Sandra Galeano found the following, potentially even better term: “aprovechador” – found in the Diccionario de la Lengua Espanola.” See: Mainero, Jorge S. & Carlos Martinez del Rio Cheating and taking advantage in mutualistic associations. In D. Boucher, ed., The Biology of Mutualism. The Oxford University Press, Oxford, UK. Photo from ecosystem/1356/attachment/gal23/

41 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) Please do not use the images in these PowerPoint slides without permission. Wagner, Diane Pollen viability reduction as a potential cost of ant association for Acacia constricta (Fabaceae). American Journal of Botany 87: Willmer, P. B. & G. N. Stone How aggressive ant-guards assist seed-set in Acacia flowers. Nature 388: Photo from

42 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 + Please do not use the images in these PowerPoint slides without permission. - + Me

43 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 + + + + Please do not use the images in these PowerPoint slides without permission. 3

44 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? Please do not use the images in these PowerPoint slides without permission.

45 Mutualisms through time Ghost of Mutualism Past?
Cospeciation Host switch Duplication Host Mutualist Failure to speciate Missing the boat Extinction Coexistence Please do not use the images in these PowerPoint slides without permission. Phylogenies can help us understand the time courses of species interactions. This is the same slide I used in the predation/parasitism lecture; it also illustrates possible time-courses for interacting mutualists; the original slide was from Jason Weckstein. The red box indicates conditions that might create a “Ghost of Mutualism Past.” Ghost of Mutualism Past?

46 Ghosts of Mutualism Past
E.g., Janzen & Martin (1982) Neotropical anachronisms: the fruits the gomphotheres ate. Science 215:19-27. Please do not use the images in these PowerPoint slides without permission. See: Barlow, Connie The Ghosts of Evolution. Basic Books, New York, NY. See: Janzen, Daniel H. & Paul S. Martin Neotropical anachronisms: the fruits the gomphotheres ate. Science 215:19-27. Note that Connell (1980) was critical of invoking “Ghosts of Competition Past” too readily, but when the criteria for establishing the role of a “ghost” are met, “ghosts” (of competition, predation, mutualism past) are entirely possible. Image from: 46


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