Horizontal partner exchange does not preclude stable mutualism in fungus-growing ants

Vertical symbiont transmission tends to stabilize mutualisms by aligning the reproductive interests of cooperating species. The attine ants conform well to this principle because all species are nutritionally dependent on vertically transmitted and clonally propagated fungal cultivars. Multiple mechanisms expressed by both partners constrain cultivar transmission between established colonies, but these appear not to preclude horizontal transfer during colony founding, consistent with multiple phylogenetic analyses indicating at least occasional horizontal transfer. The ecological and evolutionary impact of transfers is unknown because, although they can be induced in laboratory experiments, they remain undocumented in natural colonies. In a large-scale field study, we manipulated clusters of newly founded nests and their still portable gardens in two sympatric species of Acromyrmex leaf-cutting ants. This created mosaics of intact nests, queens without a cultivar, and cultivars without a tending queen. We tracked the movements of queens and cultivars through direct observation and microsatellite analysis, respectively. This showed that horizontal acquisition of incipient gardens is surprisingly common because queens actively searched for replacement cultivars and often adopted orphaned gardens. However, these horizontal cultivar exchanges are unlikely to destabilize obligate farming mutualisms when they are restricted to the founding stage, as colonies eventually commit to a single cultivar clone, irreversibly aligning the partners’ fitness interests before colonies reproduce. Inheritance isn’t everything, even a queen resorts to petty theft when down on her luck. Fungus-farming ants rely on a fungal symbiont which a queen inherits from her mother, just as organisms in general acquire their mitochondria maternally. However, most queens are likely to lose this first crop-symbiont and must steal from a neighbor to replace it. Vertical inheritance of symbionts thus appears to be less important for cooperation than often assumed.