Stability and instability of host-symbiont combinations among higher fungus-gardening ants

Background: A key feature of symbioses is stability and persistence across ecological and evolutionary scales.  Although the so-called ‘higher-attini’ (the leaf-cutter ants (Atta and Acromyrmex spp.) and non-leaf-cutters (Trachymyrmex spp.) were widely considered to be a classic case of 1:1 coevolution because each of these two groups of ants grow distinct clades of derived ant fungi, large scale geographical surveys have shown that there are naturally occurring symbiont switches between these two ant and fungal clades.  The mechanisms that promote or maintain these associations are currently unknown.

Results: We report here the results of experimental symbiont switching (cross-fostering) from six North American fungus gardening-ant species. The six species show three generalized phenotypic responses when growing novel fungi.  Some fail immediately, some sustain growth for several weeks before undergoing irrevocable declines, while others remain stable for 4 years or more.  Because the unstable combinations become invaded by weedy, pathogenic species, we suspect that ant and fungal microbiomes may have a role in stabilizing ant and fungal combinations over ecological and evolutionary time scales.

Significance: Fungus-gardening ants are excellent models to investigate the mechanisms involved in promoting symbiotic stability, because the main partners (ants and fungi) are macroscopic and can thus be disassembled and reassembled with relative ease.  These symbioses are more tractable than other vertically transmitted symbioses where symbionts are often microscopic and reside inside their hosts.  These studies are among the first experiments that examine the stability of host-symbiont pairings in fungus-gardening ants, especially those that involve interspecific switches where ants are paired with a distantly related fungus.