Abstract
Attine ants cultivate fungi as their most important food source and in turn the fungus is nourished, protected against harmful microorganisms, and dispersed by the ants. This symbiosis evolved approximately 50–60 million years ago in the late Paleocene or early Eocene, and since its origin attine ants have acquired a variety of fungal mutualists in the Leucocoprineae and the distantly related Pterulaceae. The most specialized symbiotic interaction is referred to as “higher agriculture” and includes leafcutter ant agriculture in which the ants cultivate the single species Leucoagaricus gongylophorus. Higher agriculture fungal cultivars are characterized by specialized hyphal tip swellings, so-called gongylidia, which are considered a unique, derived morphological adaptation of higher attine fungi thought to be absent in lower attine fungi. Rare reports of gongylidia-like structures in fungus gardens of lower attines exist, but it was never tested whether these represent rare switches of lower attines to L. gonglyphorus cultivars or whether lower attine cultivars occasionally produce gongylidia. Here we describe the occurrence of gongylidia-like structures in fungus gardens of the asexual lower attine ant Mycocepurus smithii. To test whether M. smithii cultivates leafcutter ant fungi or whether lower attine cultivars produce gongylidia, we identified the M. smithii fungus utilizing molecular and morphological methods. Results shows that the gongylidia-like structures of M. smithii gardens are morphologically similar to gongylidia of higher attine fungus gardens and can only be distinguished by their slightly smaller size. A molecular phylogenetic analysis of the fungal ITS sequence indicates that the gongylidia-bearing M. smithii cultivar belongs to the so-called “Clade 1”of lower Attini cultivars. Given that M. smithii is capable of cultivating a morphologically and genetically diverse array of fungal symbionts, we discuss whether asexuality of the ant host maybe correlated with low partner fidelity and active symbiont choice between fungus and ant mutualists.
Highlights
Mutualisms, symbiotic interactions between organisms in which each partner benefits, are widespread across the tree of life [1]
The fungal cultivars collected from three fungus chambers belonging to at least two M. smithii colonies contained gongylidialike structures that were organized in staphylae (Figs. 1B–D)
Our microscopic examination at 400x magnification showed that the gongylidia of this M. smithii fungal cultivar were morphologically very similar to the gongylidia found in fungal cultivars of T. fuscus, Ac. disciger, A. laevigata, and A. sexdens (Fig. 1 E,F,G,H), differing only in their smaller size (Fig. 2)
Summary
Mutualisms, symbiotic interactions between organisms in which each partner benefits, are widespread across the tree of life [1]. Co-evolutionary processes, reciprocal genetic changes in one species in response to changes in the partner species, shape these tight relationships, selecting for ecological specialization and resulting in co-diversification and eventually co-speciation [5,6,7,8,9,10]. It is inherently difficult to study currently co-evolving organisms in order to understand the selective processes and proximate mechanisms underlying obligate interdependencies because currently observed patterns may not necessarily reflect the evolutionary interactions that shaped the symbiosis when it originated. The complex symbiosis of fungus-growing ants with leucocoprineaceous fungi and other associated microorganisms provides a system that is well suited for studying the evolution of mutualistic interactions and the origins of fungiculture in insects [11,12,13,14,15,16,17]. To enable the growth of the fungal symbionts, the ants provide nutrition to the fungus garden and prevent the growth of alien microorganisms [21,27,28,29,30,31]
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