Abstract
Stable associations between partners over time are critical for the evolution of mutualism. Hosts employ a variety of mechanisms to maintain specificity with bacterial associates. Acromyrmex leaf-cutting ants farm a fungal cultivar as their primary nutrient source. These ants also carry a Pseudonocardia Actinobacteria exosymbiont on their bodies that produces antifungal compounds that help inhibit specialized parasites of the ants' fungal garden. Major workers emerge from their pupal cases (eclose) symbiont-free, but exhibit visible Actinobacterial coverage within 14 days post-eclosion. Using subcolony experiments, we investigate exosymbiont transmission within Acromyrmex colonies. We found successful transmission to newly eclosed major workers fostered by major workers with visible Actinobacteria in all cases (100% acquiring, n = 19). In contrast, newly eclosed major workers reared without exosymbiont-carrying major workers did not acquire visible Actinobacteria (0% acquiring, n = 73). We further show that the majority of ants exposed to major workers with exosymbionts within 2 hours of eclosion acquired bacteria (60.7% acquiring, n = 28), while normal acquisition did not occur when exposure occurred later than 2 hours post-eclosion (0% acquiring, n = 18). Our findings show that transmission of exosymbionts to newly eclosed major workers occurs through interactions with exosymbiont-covered workers within a narrow time window after eclosion. This mode of transmission likely helps ensure the defensive function within colonies, as well as specificity and partner fidelity in the ant-bacterium association.
Highlights
Symbiosis, the living together of unlike organisms [1], has been and remains critically important to the evolution of life on Earth
We explored the natural conditions under which newly eclosing Acromyrmex echinatior ants acquire Actinobacteria exosymbionts
No Acromyrmex echinatior ants lived longer than five days post-eclosion (0% survival, n = 4 subcolonies), so all results reported here are for Acromyrmex octospinosus (58% survival, n = 12 subcolonies)
Summary
The living together of unlike organisms [1], has been and remains critically important to the evolution of life on Earth. The success of symbiosis depends on the host’s ability to properly acquire and maintain suitable symbionts. Constrained transmission allows few opportunities for partner switching. Symbiont transmission can be constrained by the need for physical interactions, temporal acquisition windows, and molecular specificity [2,3]. Constrained transmission allows fewer opportunities for partner switching, increasing partner fidelity, which is important for maintaining stable interactions in specialized symbioses [4]. This type of evolutionary constraint can be imposed through several mechanisms, including recognition through partner-mediated molecular patterns by hosts and/or symbionts [2]. Establishing a symbiosis may rely on a critical bacterial acquisition window. Limited symbiont acquisition periods likely function to increase colonization specificity [2] and are likely more common than currently recognized
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