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Attine ants evolved farming 55-60 My before humans. Although evolutionarily derived leafcutter ants achieved industrial-scale farming, extant species from basal attine genera continue to farm loosely domesticated fungal cultivars capable of pursuing independent reproductive interests. We used feeding experiments with the basal attine Mycocepurus smithii to test whether reproductive allocation conflicts between farmers and cultivars constrain crop yield, possibly explaining why their mutualism has remained limited in scale and productivity. Stoichiometric and geometric framework approaches showed that carbohydrate-rich substrates maximize growth of both edible hyphae and inedible mushrooms, but that modest protein provisioning can suppress mushroom formation. Worker foraging was consistent with maximizing long-term cultivar performance: ant farmers could neither increase carbohydrate provisioning without cultivars allocating the excess toward mushroom production, nor increase protein provisioning without compromising somatic cultivar growth. Our results confirm that phylogenetically basal attine farming has been very successful over evolutionary time, but that unresolved host-symbiont conflict may have precluded these wild-type symbioses from rising to ecological dominance. That status was achieved by the evolutionarily derived leafcutter ants following full domestication of a coevolving cultivar 30-35 Mya after the first attine ants committed to farming., Competing Interests: The authors declare no conflict of interest.

The mutualism between leaf-cutting ants and their fungal symbionts revolves around processing and inoculation of fresh leaf pulp in underground fungus gardens, mediated by ant fecal fluid deposited on the newly added plant substrate. As herbivorous feeding often implies that growth is nitrogen limited, we cloned and sequenced six fungal proteases found in the fecal fluid of the leaf-cutting ant Acromyrmex echinatior and identified them as two metalloendoproteases, two serine proteases and two aspartic proteases. The metalloendoproteases and serine proteases showed significant activity in fecal fluid at pH values of 5-7, but the aspartic proteases were inactive across a pH range of 3-10. Protease activity disappeared when the ants were kept on a sugar water diet without fungus. Relative to normal mycelium, both metalloendoproteases, both serine proteases and one aspartic protease were upregulated in the gongylidia, specialized hyphal tips whose only known function is to provide food to the ants. These combined results indicate that the enzymes are derived from the ingested fungal tissues. We infer that the five proteases are likely to accelerate protein extraction from plant cells in the leaf pulp that the ants add to the fungus garden, but regulatory functions such as activation of proenzymes are also possible, particularly for the aspartic proteases that were present but without showing activity. The proteases had high sequence similarities to proteolytic enzymes of phytopathogenic fungi, consistent with previous indications of convergent evolution of decomposition enzymes in attine ant fungal symbionts and phytopathogenic fungi.

Maintaining symbiosis homeostasis is essential for mutualistic partners. Leaf-cutting ants evolved a long-term symbiotic mutualism with fungal cultivars for nourishment while using vertical asexual transmission across generations. Despite the ants’ efforts to suppress fungal sexual reproduction, scattered occurrences of cultivar basidiomes have been reported. Here, we review the literature for basidiome occurrences and associated climate data. We hypothesized that more basidiome events could be expected in scenarios with an increase in temperature and precipitation. Our field observations and climate data analyses indeed suggest that Acromyrmex coronatus colonies are prone to basidiome occurrences in warmer and wetter seasons. Even though our study partly depended on historical records, occurrences have increased, correlating with climate change. A nest architecture with low (or even the lack of) insulation might be the cause of this phenomenon. The nature of basidiome occurrences in the A. coronatus–fungus mutualism can be useful to elucidate how resilient mutualistic symbioses are in light of climate change scenarios. [ABSTRACT FROM AUTHOR]

Obligate mutualistic symbioses rely on mechanisms that secure host-symbiont commitments to maximize host benefits and prevent symbiont cheating. Previous studies showed that somatic incompatibilities correlate with neutral-marker-based genetic distances between fungal symbionts of Panamanian Acromyrmex leaf-cutting ants, but the extent to which this relationship applies more generally remained unclear. Here we showed that genetic distances accurately predicted somatic incompatibility for Acromyrmex echinatior symbionts irrespective of whether neutral microsatellites or AFLP markers were used, but that such correlations were weaker or absent in sympatric Atta colombica colonies. Further analysis showed that the symbiont clades maintained by A. echinatior and A. colombica were likely to represent separate gene pools, so that neutral markers were unlikely to be similarly correlated with incompatibility loci that have experienced different selection regimes. We suggest that evolutionarily derived claustral colony founding by Atta queens may have removed selection for strong incompatibility in Atta fungi, as this condition makes the likelihood of symbiont swaps much lower than in Acromyrmex , where incipient nests stay open because queens have to forage until the first workers emerge. [ABSTRACT FROM AUTHOR]

Abstract: Though inconspicuous in healthy nests, Pseudoxylaria species are almost always present and overgrow deteriorating fungus-growing termite gardens. Whether these fungi are detrimental to the fungus-garden, benign, or even beneficial is unclear. We hypothesize that Pseudoxylaria is a stowaway that practices a sit-and-wait strategy to survive in the termite nest. Using isolates from three different termite genera to test our hypothesis, we compared Pseudoxylaria’s growth on 40 carbon sources with that of Termitomyces and tested its interaction with Termitomyces. The C-source use of both fungi largely overlapped, indicating potential for competition. One-to-one interactions between Pseudoxylaria, Termitomyces and free-living relatives showed that Pseudoxylaria and Termitomyces strains interacted differently with each other than with each other’s free-living relatives. Both fungi grew less together than when growing alone, confirming that they compete. Pseudoxylaria was more strongly inhibited by Termitomyces than free-living Xylariaceae were. The results suggest that the symbiotic lifestyle adopted by Pseudoxylaria goes together with reduced antagonism towards Termitomyces, consistent with Pseudoxylaria being a stowaway. [Copyright &y& Elsevier]

Animal gut microbiota affect host physiology and behaviour. In social insects, where colony level integrity is preserved via a nestmate discrimination system based on cuticular hydrocarbon mixtures, microorganismal effects may therefore influence social dynamics. Although nestmate recognition has undergone a thorough exploration during the last four decades, few studies have investigated the putative role of gut microbes. Here, we integrated 16S rRNA-based microbial community profiling, chemical and behavioural approaches to test whether gut microbes affect nestmate recognition in Acromyrmex echinatior leaf-cutting ants. Treating workers with a sterile diet or with antibiotics resulted in a substantial alteration of their gut microbial communities. In pairwise social interactions, untreated versus antibiotic-treated nestmates behaved more aggressively than other nestmate and non-nestmate pairs, suggesting that bacterial suppression may alter chemical social cues and trigger aggressive behaviour. Chemical analyses of treated individuals revealed a decrease in the abundance of two metapleural gland antifungal compounds, and confirmed the correspondence between aggression levels and chemical profile differences. Feeding microbiota-remodelled ants with conspecific faecal droplets partially restored the original bacterial communities. Ants fed with faecal droplets from different colonies were unusually aggressive compared to pairs fed with faecal droplets from the same colony. We cannot exclude confounding effects resulting from the potentially harmful action of antibiotics on ant hosts. However, our results suggest a correlation between chemical profiles and the presence of certain microbial species in the gut, which may affect nestmate recognition and division of labour. This opens novel questions about the role of symbiotic microorganisms in the evolution of social insect behaviour. Highlights • We tested whether gut microbes influence nestmate recognition in leaf-cutting ants. • Gut microbiota suppression appears to affect aggression and cuticular hydrocarbons. • Partial microbiota restoration partly reverses induced changes in aggression. • 3-way interactions of gut microbes, cuticular hydrocarbons and aggression may exist. [ABSTRACT FROM AUTHOR]