The Evolutionary Ecology of Mutualisms: Introduction
Edited by Frank Messina
Mutualisms occur when two species receive benefits by virtue of their association, and these benefits often translate into increased population densities or greater persistence in a particular habitat. Mutualism has traditionally received less attention than competition or predation, and was for a time considered the neglected stepchild of community ecology (Boucher et al. 1982). Although that characterization is no longer true, much remains to be learned about the origin and maintenance of these ubiquitous and complex relationships. It has become apparent, for example, that many purported mutualisms can easily be converted to commensalistic (+/0) or parasitic (+/-) interactions in response to changing local conditions. More attention has recently been paid to the costs associated with mutualistic interactions, in addition to the reciprocal benefits. Because benefits received by one partner typically require a significant investment by the other, the relative magnitudes of costs and benefits can determine the likelihood of “cheating” (Bronstein 2001).
This virtual issue gathers 17 recent Functional Ecology papers that address the evolutionary ecology of mutualisms. The compilation is in part intended to coincide with two symposia (“Mutualistic Interactions: Causes and Consequences” and “Coevolution across the Parasitism-Mutualism Continuum”) at the 13th Congress of the European Society for Evolutionary Biology in 2011. The selected articles cover a wide variety of taxa and examine mutualistic interactions from the scale of a single pair of species to an entire ecological community.
Several studies tackle the issue of specificity. What ecological, morphological, or other kinds of “filters” explain why some interactions are highly specialized while others remain diffuse? In pollination systems, specificity is often thought to be mediated by unusual flower morphology. Shuttleworth & Johnson (2009) demonstrated how a milkweed with open flowers and exposed nectar nevertheless maintains an efficient, specialized interaction with pollinating wasps by combining cryptic flower colour, a distinctive floral scent, and a nectar that is unpalatable to generalist visitors. Similarly, Burger et al. (2010) found that a specialist bee requires an interplay between visual and olfactory floral cues (and multiple sensory modalities) to discriminate between host and non-hosts. In contrast, extreme species-specificity in a fig-fig wasp interaction appeared to depend on a single volatile compound that is rare in the floral scent of most fig species, and thus serves as a “private channel” (Chen et al. 2009). The Functional Ecology Special Feature, “Floral Scent in a Whole Plant Context,” further elaborated the important role of plant volatiles in maintaining pollinator specificity (Wright & Schiestl 2009) and the Haldane Award-winning paper in 2009 confirmed experimentally that variation in floral scent indeed influences plant fitness (Majetic et al. 2009). More recently, an investigation of orchid pollination revealed that phenotypic selection on flower morphology can be quite complex, as multiple, alternative combinations of floral characters yielded the highest rates of fitness gain (Cuartas-Domínguez & Medel 2010).
Figs and fig wasps provide a classic model system for examining conflicts of interest in mutualisms because wasps are seed predators as well as obligate pollinators (Bronstein 2001). This “nursery-pollination” interaction could therefore tend toward parasitism if seed predation is high relative to pollination service. In the system studied by Chen et al. (2009), rapid deterioration of the olfactory signal following pollination may prevent overexploitation of seeds. In another nursery-pollination system, evolutionary stability may be increased because nectar-feeding male moths provide effective pollination but, unlike ovipositing females, do not cause a loss of seeds (Labouche & Bernasconi 2010). In general, conflicts of interest can lead to “deception” and a mutualism breakdown. Deception is well known in the context of pollination; some orchids offer no rewards but attract pollinating insect males by mimicking the sex pheromones of females. Pfeiffer et al. (2010) discovered similar deception in a seed-dispersal mutualism. Myrmecochorous plants typically produce elaiosomes, lipid-rich seed appendages that are consumed by seed-dispersing ants. However, some plants “cheat” by simply mimicking the chemical cues of elaiosomes. Interestingly, Pfeiffer et al. (2010) suggest that cheating may actually stabilize bona fide mutualisms because it favors greater discrimination on the part of the ants.
Mutualisms cannot be understood in isolation; the costs and benefits of any pairwise interaction will of course depend on which other species are present in the local habitat, as well as on abiotic conditions. For example, changes in plant chemistry induced by herbivory can have simultaneous negative effects on a plant’s floral attractiveness (Kessler & Halitschke 2009). Context-dependence is especially evident in intersecting mutualisms, which occur when a focal species simultaneously engages in mutualistic interactions with multiple and potentially competing partners. Like most plants, grasses establish associations with soil mycorrhizae, which improve plant nutrition, but they are also frequently infected with fungal endophytes, which can boost plant defence against herbivores and even improve seedling recruitment (Omacini et al. 2009). Liu et al. (in press) document a clear antagonistic relationship between endophytes and mycorrhizae in the same grass host. Moreover, because their relative effects on plant performance depend on available soil nutrients and levels of herbivory, both of these “mutualistic” fungi may instead act as plant parasites. In another antagonistic interaction between mutualists, mycorrhizal colonization was found to deter some flower visitors in a Geranium species, possibly by altering nectar composition (Varga & Kytöviita 2010). On the other hand, mycorrhizae appeared to enhance the inducibility of host defences against herbivores in several dicots and grasses (Kempel et al. 2010). Jaber & Vidal (2009) provide a final example of the many contingencies that can arise when mutualisms collide. They noted that the presence of endophytic fungi could either increase or decrease production of extrafloral nectaries in bean plants, depending on whether plants were simultaneously attacked by herbivores. Jaber & Vidal (2009) also speculated that extrafloral nectaries, which attract plant-defending ants, will not be effective if plants are colonized by honeydew-producing insects, which represent a diverting and more attractive partner for ants.
Two additional papers provide rare examples of mutualism studies at the level of whole communities. Some tree-dwelling ants establish “ant-gardens” by forming nests from dead organic matter and seeds. Roots of germinating seeds help anchor the arboreal nest, and ants protect plants from herbivores. For a bromeliad species found only in ant gardens, plant shape was found to depend on the identity of the ant partner, because the two ant species established arboreal nests in different light environments (Céréghino et al., in press). Variation in the shape of the plant and the light regime in turn led to differences in the composition and diversity of aquatic organisms living in the wells of bromeliad leaves. Hence, the food-web structure and functioning of an entire aquatic community was affected by the particular makeup of a two-species mutualism. Another community-level study applied network theory to a “mutualistic community” in the same way that it has been used to study predator-prey communities (Chamberlain & Holland 2009) These authors established that a single ant character (body size) is a reasonably good predictor of degree, i.e., the number of local plant species with which a given ant species interacts (in this case, by visiting extrafloral nectaries). It is unclear whether the mechanism underlying the positive degree-body size correlation in this system is similar to that underlying the relationship in predator-prey food webs. Network theory can be similarly applied to understand plant-pollinator and plant-seed disperser mutualisms at the community level.
Virtually all species engage in mutualistic interactions at least one other species, and the papers listed above illustrate the variety of approaches that have been used to study them. More theoretical work is needed to explain how mutualisms form and persist in the face of inherent conflicts (Ferrière et al. 2007), and empirical studies will continue to provide new (and sometimes surprising) examples of beneficial interactions between species. For example, we have only begun to uncover the breadth of mutualistic interactions involving symbiotic microorganisms, but rapidly improving genomic tools should help elucidate the critical roles of microbes in the nutrition and metabolism of their multicellular hosts (Douglas 2009, as part of a Special Feature on “Nutritional Ecology”). We hope this virtual issue serves to remind readers of the importance and diversity of mutualistic interactions in ecological communities.
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Boucher, D.H., James, S. & Keeler, K.H. (1982) The ecology of mutualism. Annual Review of Ecology and Systematics, 13, 315-347.
Bronstein, J.L. (2001) Mutualisms. Evolutionary Ecology: Concepts and Case Studies (eds C.W. Fox, D.A. Roff & D.J. Fairbairn), pp. 315-330. Oxford University Press, New York.
Ferrière, R., Gauduchon, M. & Bronstein, J.L. (2007) Evolution and persistence of obligate mutualists and exploiters: competition for partners and evolutionary immunization. Ecology Letters, 10, 115-126.
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