Introduction
Fungi are important components of many model systems in evolutionary ecology. Some members of all four phyla of Eumycota have the capacity to form symbiotic associations with diverse and often phylogenetically distant organisms. These relationships span the continuum of mutualism to parasitism and thus they may contribute to the understanding of co-evolutionary processes. Likewise, the type of symbiosis found in any given pair of interacting symbionts is also likely to vary with host/fungus genotype and with environmental conditions.
Chytridiomycota
Parasites
The Chytridiomycota phylum contains many parasites that are often associated with aquatic or wet environments. For example, the global decline of amphibians has been attributed to many factors, particularly environmental degradation (acids rain, ozone depletion and global warming) and infection by a chytrid fungus, Batrachochytrium dendrobatidis. Typically chytrids feed on algae, plant material, and keratin, being rather benign superficial parasites in animals. However, the current view of this disease is that it is that chytrid infection of amphibians has recently emerged and did not evolve from a less virulent amphibian parasite. Likewise, the interaction between the fungus and human dominated may be responsible for the host shift of the fungus by increasing susceptibility in physiologically stressed amphibians.
Mutualists
Chytrids can also play a mutualistic role in symbioses. Ungulates diets consist primarily of grasses. Grasses unfortunately are poor quality forage because they consist of many complex carbohydrates that indigestible to most herbivores. Therefore, the rumen-inhabiting chytrids play important role by enhancing the digestion efficiency of their hosts by predigesting their food (Alexopolus et al. 1996). While this relationship is clearly mutualistic, it would interesting to know how the association first evolved and whether it was initially parasitic.
Zygomycota
Parasites
Insect destroyer fungi are obligate pathogens of arthropods found in the family Entomophthoraceae (Zygomycota) This association is fascinating because these fungi can often manipulate the behavior of the host by mycelial penetration of the brain. For example, common houseflies infected with Entomophthora muscae land on a surface and climb as high as possible prior to death. These manipulations help ensure successful dissemination of fungal spores by more effectively utilizing wind currents. In addition, some members of the Massospora genus have achieved amazing adaptations to their hosts such as the ability to survive a 17-year dormancy in their cicada hosts. Upon emergence of the cicadas, some of these infection lead to a dramatic synchronized deaths in the population by the first afternoon, while others are less virulent and disseminate their spores from their living hosts for an more extended and variable duration. (Alexopolus et al. 1996) Further studies are necessary to determine what ecological factors influence the level of virulence in this genus.
Mutualists
Members of class Trichomycetes are all obligate associates of arthropods that typically inhabit the hindgut. While most species within this class are parasites, a few are involved in a context dependent mutualism. For example, when mosquito larvae are nutritionally deprived of sterols and certain B-vitamins, larvae infected with Smittium culisetae exhibit faster growth and better survival than uninfected individual. Conversely, larval infections of S. morbosum are always lethal (Horn & Lichtwardt 1981).
Ascomycota
Grass endophytes: Mutualists or parasites?
Neotyphodium endophytes are obligate, asexual, seed-borne symbionts, which live within grass plant tissues. Although evolutionary theory predicts that asexual symbionts should be strong mutualists, the direction of the interaction found in many grasses is highly variable. This association has been widely recognized to be mutualistic in a few agronomic grasses, in terms of increased growth, drought tolerance, and herbivore and pathogen resistance. However, these grass/endophyte cultivars have been artificially selected and thus are quite genetically uniform. As such, the association found in these domesticated grasses may not be representative of the interactions in natural populations. Again, the direction of the symbiosis in native grasses may vary with host/fungal genotypes and also within the lifetime of the host depending upon the environmental context in which it occurs (water, nutrients, herbivory stress) (Faeth 2002).
Mutualists
Lichens are composite organisms that consist of a fungal partner, the mycobiont, and an algal or bacterial partner, the photobiont. The fungus benefits from the photosynthates produced by the photobiont, whereas, the photobiont receives protection from UV and desiccation from the fungus. Although the situation seems unquestionably mutualistic, it invariably depends on the environmental context in which this relationship occurs. Typically, lichens occur in harsh environments where water and nutrients are not readily accessible to most organisms. However, lichens are known to “evict” their photosynthetic partner when these circumstances change and resources are more readily available. In these cases, fungi may “steal” a more efficient or less costly photobionts or exist in a free-living state (Richardson 1999). As such, these algal/fungal associations are also context dependent.
Basidiomycota
Parasites
The Urediniomycetes (rusts) are a class within Basidiomycota that consists of facultative parasites. The exhibit a complex lifecycle with up to 5 spore types and typically have 2 hosts within their lifecycle. One species, Puccinia graminis, is an economically important parasite of wheat and barberry respectively. Although measures have been taken to reduce the incidence of the disease by removing the alternate host, barberry, these measures have been largely unsuccessful. Typically the teliospores produces on the barberry hosts are the only ones that can overwinter. However in warmer climates the urediniospores that cycle through wheat hosts can often survive the winter and are subsequently wind dispersed to more northern locales to reinfect wheat. In addition, urediniospore production within wheat fields has been exacerbated by agricultural practices. Wheat is typically planted in dense genetically uniform monocultures, the density and similar susceptibility of plants within the plot can allow urediniospores to rapidly cycle between wheat hosts. In addition, flood irrigation increases humidity and can facilitate fungal growth. While rust species always form parasitic associations with their hosts, environmental condition can dictate the severity of the disease (Watkins & Gaussoin 1992).
Mutualists
Many social insects have evolved mutualistic relationships with Basidiomycetes. These insects typically exploit the fungi’s ability to degrade cellulose and other complex plant carbohydrates that are not accessible to them naturally. In return, the fungi are fed and protected by the colony. For example, Attine ants form mutualistic associations with Leucoagaricus and Lepiota species mushrooms. These ants are economically devastating pests that harvest mass quantities of leaves from the forest trees, however, they don not consume them directly. Instead, these leaves along with fecal matter are fed to the colony’s fungus. Subsequently, the ants consume the fungal mycelia in order to utilize the enzymatically-liberated nutrients. Similarly, termite species such as Macrotermes bellicosus have evolved an association with Termitomyces species. However, these species predigest wood products instead of leaves. The lack of variability found in these symbioses may be due to the fact that neither partner can survive alone (Kendrick 1992).
Conclusion
Clearly, symbiotic fungi can teach us a lot about co-evolutionary processes. Most importantly, these studies reveal that many fungal symbionts cannot be pigeonholed into distinct categories of mutualists or parasites. These interactions are dynamic and not only evolve in response to their partner but also are influenced by environmental factors. Presumably, all symbiotic associations incur a cost and thus the cost-benefit ratio will change with the environmental context in which the interaction is played out.
Additional Resources
Alexopoulos, Mimms & Blackwell. 1996. Introductory Mycology (4th edition) Daszak P, Cunningham AA.2003. Anthropogenic change, biodiversity loss, and a new agenda for emerging diseases. Journal of Parasitology 89 (Suppl): S37-S41.
Faeth, SH. 2002. Are endophytic fungi defensive plant mutualists? Oikos 98: 25-36
Horn BW, Lichtwardt RW. 1981. Studies on the nutritional relationship of larval Aedes aegypti (Diptera: Culicidae) with Smittium culisetae (Trichomycetes). Mycologia 73: 724-740
Kendrick B. 1992 The Fifth Kingdom (2nd edition).
Law, R. 1985. Evolution in a mutualistic environment. In: The Biology of Mutualisms. Croom Helm, London, 145-170
Richardson, D. H. S. 1999. War In The World Of Lichens: Parasitism And Symbiosis As Exemplified By Lichens And Lichenicolous Fungi Mycological Research 103:6 p 641 – 650
Watkins, J.E. and Gaussoin, R. 1992. Rust diseases of turfgrass. Cooperative Extension, Institute of Agriculture and Natural Resources, University of Nebraska – Lincoln. NebGuide G92-1119-A.
