Essays on organismal aspects of the fungus-growing ant symbiosis : ecology, experimental symbiont switches and fitness of Atta, and a new theory on the origin of ant fungiculture
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This dissertation includes several experimental approaches aimed at elucidating coadaptations between leaf-cutting ants and their symbiotic fungi. The second chapter provides ecological information on the fungus-growing, leafcutting ant used as study organism, Atta mexicana from Northeastern Mexico. A new commensalistic myrmecophile was discovered: a highly specialized moth, Amydria anceps (Lepidoptera: Acrolophidae), whose larvae live gregariously on the spent fungal substrate of the A. mexicana colony. Although there is an intuitive conception that there is a "high" level of ant-fungus coadaptation in the higher attines (particularly in the leaf-cutters), there are no empirical data on these alleged mutual adaptations. In Chapters 3 and 4, experimental fungal symbiont switches between Atta (derived) and Trachymyrmex (basal) provide the first evidence of tangible coadaptatations and negative effects restricting switches to novel cultivars. Striking effects were observed when Atta ants cultivated the Trachymyrmex symbiotic fungus. These include severely restricted fungus and ant colony growth, with reduced worker sizes and numbers. In Chapter 5 the effect of fungal change on the physiology of leafcutter ants is addressed; specifically, on the mortality of workers upon challenge with the insectpathogenic fungus Beauveria bassiana. I developed and compared two tetratrophic systems (chains) each using a different fungal symbiont; the energy flows in these systems were as follows: plant leaves→fungal symbionts→leafcutter ants→pathogen (B. bassiana). The last chapter proposes a novel theory on the origin of the ant-fungus symbiosis. This mutualism is suggested to originate from the opportunistic consumption, by the attines’ ancestor, of the fungi derived from a preexisting insect-fungus mutualistic symbiosis, such as ambrosia beetles (Coleoptera: Curculionidae) or wood wasps (Hymenoptera: Siricoidea). This subsequently led to conservation of these fungi and to their cultivation. Therefore, theories on the origin of the attine symbiosis can be separated into three groups as follows: 1) “consumption first” hypotheses that propose de novo domestication and cultivation of free-living fungi from different sources; 2) the “phoresyconsumption” hypotheses, which propose a system whereby fungi first utilized the ants as means of transport (phoresy) with subsequent development of consumption and cultivation; and 3) the “exploitation of preexisting symbiosis” hypothesis herein proposed for the first time.