Mutualism & Commensalism Please do not use the images in these PowerPoint slides without permission. Wikipedia “Mutualism (biology)” page; accessed 02-X-2014 Photo of hawk moth potentially pollinating Dianthus from Wikimedia Commons

Positive Interactions Facilitation – in other words, “+” means benefits outweigh costs Commensalism = +/0 Mutualism = +/+ What might the benefits and costs be to each partner in a pollination mutualism? Please do not use the images in these PowerPoint slides without permission. Wikipedia “Mutualism (biology)” page; accessed 02-X-2014 From J. Stachowicz (2001) BioScience – “facilitation… encounters between organisms that benefit at least one of the participants and cause harm to neither…” For an individual of one species to have a net “+” outcome for the interaction with an individual of its partner species, the benefits to itself must outweigh the costs to itself, i.e., B > C. The partner(s) who receives the “+” is facilitated by the other (mutually so in mutualisms). Photo of hawk moth potentially pollinating Dianthus from Wikimedia Commons

Obligate vs. Facultative Mutualisms Obligate – not optional, e.g., fig - fig wasp Facultative – optional, e.g., fig - seed disperser Fig & one of its many seed-dispersers (in this case a frugivorous bat) Fig & its pollinating fig wasps Please do not use the images in these PowerPoint slides without permission. Photo of fig & fig wasps from http://www.zoology.ubc.ca; photo of bat & figs from http://www.sserc.org.uk/wwwroot2/members/Photos/Plants/seed%20dispersal/Menu.htm

Types of Benefits to Mutualists Service Mutualisms One partner receives an ecological service from the other – e.g., pollination, seed dispersal, or defense against herbivores, predators, or parasites E.g., ant - bullhorn acacia symbiosis Please do not use the images in these PowerPoint slides without permission. Wikipedia “Vachellia cornigera” page; accessed 18-X-2014  "A-cornigera" by kafka4prez - Flickr here. Licensed under Creative Commons Attribution-Share Alike 2.0 via Wikimedia Commons – http://commons.wikimedia.org/wiki/File:A-cornigera.jpg#mediaviewer/File:A-cornigera.jpg Photo from Wikimedia Commons

Types of Benefits to Mutualists Habitat Mutualisms One partner obtains shelter, a place to live, or favorable habitat from the other E.g., alpheid shrimp - goby symbiosis Please do not use the images in these PowerPoint slides without permission. Wikipedia “Alpheidae” page; accessed 18-X-2014  "Gobi and shrimp" by Steve Childs - Flickr: Gobi and shrimp. Licensed under Creative Commons Attribution 2.0 via Wikimedia Commons – http://commons.wikimedia.org/wiki/File:Gobi_and_shrimp.jpg#mediaviewer/File:Gobi_and_shrimp.jpg Photo from Wikimedia Commons

Types of Benefits to Mutualists Trophic Mutualisms One partner receives energy or nutrients from its partner E.g., mychorrizae – plant root - fungus symbiosis (this type of mutualism probably characterized the very first land plants ~500 mya) Please do not use the images in these PowerPoint slides without permission. Wikipedia “Mychorriza” page; accessed 18-X-2014  "Mycorrhizal root tips (amanita)". Licensed under Creative Commons Attribution 2.5 via Wikimedia Commons – http://commons.wikimedia.org/wiki/File:Mycorrhizal_root_tips_(amanita).jpg#mediaviewer/File:Mycorrhizal_root_tips_(amanita).jpg Photomicrograph from Wikimedia Commons

Types of Benefits to Mutualists Trophic Mutualisms One partner receives energy or nutrients from its partner E.g., E. coli is part of the human microbiome Humans require various essential organic compounds that the organism itself cannot synthesize, including various: purines & pyrimidines amino acids vitamins Please do not use the images in these PowerPoint slides without permission. Photomicrograph of E. coli from “Escherichia coli” Wikipedia page; downloaded 26 Feb. 2018. Photomicrograph from Wikimedia Commons

Mutualists Are Not Altruists Each mutualistic partner seeks to gain net benefit from the other (just like a parasite seeks to gain net benefit from a host); this can create conflicts Yuccas selectively abort flowers into which too many eggs are laid Please do not use the images in these PowerPoint slides without permission. This is one example of how cheaters are penalized or sanctioned. Pellmyr, O. & C. J. Huth. 1994. Evolutionary stability of mutualism between yuccas and yucca moths. Nature 372:257-260. Photo of yucca moth from: http://www.cals.ncsu.edu/course/ent425/images/pollinators_gallery/pages/06_yucca_moth_jpg.htm; Harms’s photo of yuccas in White Sands Nat’l. Park, NM; Bowman, Hacker & Cain (2017), Fig. 15.15 after Pellmyr & Huth (1994) Nature

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) Plant can penalize fungus (for poor P delivery) with low C delivery A B C Please do not use the images in these PowerPoint slides without permission. Kiers, E. T. et al. 2011. Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 333:880-882. Kiers et al. (2011) Science

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. 2011. Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 333:880-882. 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

Mutualisms Can Evolve From Other Types of Species Interactions 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. 1993. Genetic conversion of a fungal plant pathogen to an nonpathogenic, endophytic mutualist. Science 260:75-78. This slide shows how a mutualism can evolve from a parasitic interaction. Can a parasitic interaction evolve from a mutualistic interaction? Original research from Freeman & Rodriguez (1993) Science; photo of anthracnose on cucumber leaf from http://urbanext.illinois.edu/hortanswers/detailproblem.cfm?PathogenID=128

Mutualisms Can Evolve From Other Types of Species Interactions 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. Freeman, S. & Rodriguez, R. J. 1993. Genetic conversion of a fungal plant pathogen to an nonpathogenic, endophytic mutualist. Science 260:75-78. Considerable potential exists to tailor endophytes as biocontrol agents; an example of Darwinian Agriculture Original research from Freeman & Rodriguez (1993) Science; 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

Species Interactions Can Vary Geographically, Temporally, or in Other Context-Dependent Ways Cattail facilitated small-flowered forget-me-not at low soil temp. (possibly owing to soil aeration) Please do not use the images in these PowerPoint slides without permission. Callaway, R. M. & L. King. 1996. Temperature-driven variation in substrate oxygenation and the balance of competition and facilitation. Ecology 77:1189-1195. Wikipedia “Typha” page; accessed 19-X-2014  "Typha-cattails-in-indiana". Licensed under Public domain via Wikimedia Commons – http://commons.wikimedia.org/wiki/File:Typha-cattails-in-indiana.jpg#mediaviewer/File:Typha-cattails-in-indiana.jpg Photo of cattail from Wikimedia Commons; Bowman, Hacker & Cain (2017), Fig. 15.8, after Callaway & King (1996) Ecology

Cattail competed with small-flowered forget-me-not at high soil temp. Species Interactions Can Vary Geographically, Temporally, or in Other Context-Dependent Ways Cattail facilitated small-flowered forget-me-not at low soil temp. (possibly owing to soil aeration) Please do not use the images in these PowerPoint slides without permission. Callaway, R. M. & L. King. 1996. Temperature-driven variation in substrate oxygenation and the balance of competition and facilitation. Ecology 77:1189-1195. Wikipedia “Typha” page; accessed 19-X-2014  "Typha-cattails-in-indiana". Licensed under Public domain via Wikimedia Commons – http://commons.wikimedia.org/wiki/File:Typha-cattails-in-indiana.jpg#mediaviewer/File:Typha-cattails-in-indiana.jpg Cattail competed with small-flowered forget-me-not at high soil temp. Photo of cattail from Wikimedia Commons; Bowman, Hacker & Cain (2017), Fig. 15.8, after Callaway & King (1996) Ecology

*When is it Coevolution? Reciprocal adaptive evolution in each of 2 interacting species in response to adaptations in the other species “Darwin’s hawk moth” potentially pollinating its Malagasy orchid Daniel H. Janzen e.g., ant-acacia mutualism Please do not use the images in these PowerPoint slides without permission. Photo of Janzen from http://www.fbbva.es/TLFU/tlfu/ing/microsites/ premios/fronteras/galardonados/2011/ecologia.jsp; image of “Darwin’s hawk moth” pollinating its Malagasy orchid from http://botany.si.edu/events/sbsarchives/sbs2008; *original idea from Janzen (1980) Evolution

Imagine a world without corals! Positive interactions can influence individuals, populations, interactions between species, communities & ecosystems Zoxanthellae = unicellular algal protist symbionts with corals; algae receive N, corals receive carbohydrates A world without zoxanthellae would be a world without most shallow-water corals Imagine a world without corals! Please do not use the images in these PowerPoint slides without permission. Positive interactions can influence individuals, populations, communities & ecosystems (and, of course, we could also say this about negative interactions etc.). Wikipedia “Symbiodinium” page; accessed 18-X-2014  "Symbiodinium Wikipedia v2 (1)" by Allison m lewis - Own work. Licensed under Creative Commons Attribution-Share Alike 3.0 via Wikimedia Commons – http://commons.wikimedia.org/wiki/File:Symbiodinium_Wikipedia_v2_(1).png#mediaviewer/File:Symbiodinium_Wikipedia_v2_(1).png Photomicrograph from Wikimedia Commons

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). Mutualisms often involve substantial resources that could be exploited by an opportunistic third party. 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. 1985. Cheating and taking advantage in mutualistic associations. In D. Boucher, ed., The Biology of Mutualism. The Oxford University Press, Oxford, UK. Photo from http://www.pbs.org/wnet/nature/episodes/the-queen-of-trees/photo-essay-an-extraordinary- ecosystem/1356/attachment/gal23/

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. 2000. Pollen viability reduction as a potential cost of ant association for Acacia constricta (Fabaceae). American Journal of Botany 87:711-715. Willmer, P. B. & G. N. Stone. 1997. How aggressive ant-guards assist seed-set in Acacia flowers. Nature 388:165-167. Photo from http://coronadetucson.blogspot.com/2009_03_01_archive.html

“The enemy of my enemy is my friend” 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

Indirect Mutualisms Cartoon and examples from Degenhardt (2009) Please do not use the images in these PowerPoint slides without permission. Jörg Degenhardt. 2009. Indirect defense responses to herbivory in grasses. Plant Physiology 149:96-102. Cartoon and examples from Degenhardt (2009)

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 + + + + 1 Please do not use the images in these PowerPoint slides without permission. Note that in the earlier case of ant-plant mutualism the ants adversely affected the pollinator, which illustrates how the outcome of certain indirect effects are often unpredictable (see Wootton…).

Indirect Mutualisms +/+ + + + + Please do not use the images in these PowerPoint slides without permission. K. Harms’s photo of strangler fig, Queensland, Australia; photo of fig & fig wasps from http://www.zoology.ubc.ca; photo of bat & figs from http://www.sserc.org.uk/wwwroot2/members/Photos/Plants/seed%20dispersal/Menu.htm