Yeast and Invertebrate Associations

Abstract

The genesis of this review occurred at the 23rd International Special Symposium on Yeasts. The meeting was excellent, but, as I listened to the presentations, I was taken by the realization that most of presentations dealing with interactions between yeasts and their environments, especially presentations that could be thought of as applied science, focused on yeast–substrate interactions. This has been noted previ-ously (do Carmo-Sousa 1969). Because the talks and posters presented interesting new data and insights, I did not think this a situation in need of correction but I did feel that yeast–animal interactions were a bit underrepresented. In several instances, yeast–animal interactions could have offered alternative explanations for the data or might have suggested answers to questions generated by the data. What caught my attention was that, in discussing their data, only one of the presenters made specific reference to animals as a possible alternative. Recalling this impression gave me a goal for this review. What I would like to accomplish is to present an argument that yeast–animal interactions are common, understudied, and a necessary part of understanding yeast ecology and evolution. I will not review situations where yeasts are known to be animal parasites or pathogens. However, many interactions are not well understood and the nature of relationships is not fixed but is subject to evolutionary change. This sometimes made it difficult to set a proper boundary for the review and I chose to be inclusive rather than exclusive. It is organized according to the animals that are involved in the inter-actions. This decision was made because the field of study of yeast–animal interac-tions is organized, to the degree one can say that it is organized, in this fashion. The result is that ecological and evolutionary ideas may be revisited within separate sec-tions. The alternative, organizing according to the evolutionary or ecological ideas presented, would mean revisiting animal groups instead of ecological concepts. More importantly, organizing the review by concept would give the impression that some overall scheme for animal–yeast interactions exists at this time. I believe that it would be misleading to imply conceptual unity beyond some broad generalizations. Animal–yeast interactions are varied, from mutualistic endosymbioses to simple phoresy, from pairs of interacting animal and yeast species to interacting animal and yeast communities. So, if I am correct in my belief that much more remains to be discovered about yeast–animal interactions than we currently know, presenting the field as a coherent set of relationships might be premature. Eliminating pathogenic and parasitic interactions has other ramifications. Vertebrate associations receive little attention here owing to a paucity of informa-tion about nonpathogenic interactions, although yeasts can be isolated from verte-brate guts (do Carmo-Sousa 1969; Abranches et al. 1998) and at least one yeast, Cyniclomyces guttulatus (Phaff and Miller 1998), is an endocytobiont. The scope of relationships reviewed here potentially involves fungivory, mutualism, commensal-ism, or amensalism (no interaction, simply co-occurrence). Other categories, such as competition or predation, are not likely. Symbiosis, another descriptor of interac-tions, does not seem to have a universally agreed upon definition. Some use it broadly for any relationship in which two organisms spend significant time in con-tact (parasites and pathogens may then be symbionts) and some authors restrict it to mutualistic or commensal interactions (the caveat about contact applying). Here, I will attempt to use the more restricted meaning when either observational or exper-imental evidence reasonably justifies the implication of a positive interaction. Some broad generalizations are useful to state at the outset. When considered a subset of all fungus–animal interactions, there seems to be little that is unique to yeast–animal interactions. Most relationships are based on yeasts as a food for the animal and the animal as a vector for the yeasts. What is interesting is the wide-spread nature of the association. Table 14.1 is a reasonably complete and up-to-date list of yeasts associated with beetles found in wood and mushrooms. It is over 200-species long. For the vast majority of instances, we do not know if the association is happenstance or significant. I suspect that most are significant but do not involve obligate pairwise interactions between one species of yeast and one species of insect. If true, this would mean that most yeast–animal relationships must be studied in multispecies assemblages if the nature of the relationship is to be fully understood. The number of possible iterations becomes large, especially if variation in environ-mental factors, which may change the nature of yeast–animal interactions, are con-sidered. It is a daunting task but there are also positive sides to the situation. Many necessary techniques have been perfected (obtaining axenic insects and pure cultures of yeasts, efficient means of differential yeast population counts, detection of spa-tial inhomogeneities with differential dye labeling, etc.) that might be applied to experiments on the dynamics of yeast–animal relationships. Both yeast and animal systematics are improving to the point that comparative phylogenetics may be used to generate a subset of testable hypotheses from a much larger set of possible hypotheses. Coalescence theory promises insights into basic ecological parameters (e.g., effective population size, dispersal patterns, and prevalence of recombination) and historical aspects of population biology (e.g., recent bottlenecks and founder events). There have been several excellent reviews of the associations between yeast and animals, often as part of a more general review of yeast habitats (do Carmo-Sousa 1969; Phaff et al. 1978; Phaff and Starmer 1987). Here, I will focus, when possible, on recent additions to the field. Some terminological standards should be set at the