The Most Relictual Fungus-Farming Ant Species Cultivates the Most Recently Evolved and Highly Domesticated Fungal Symbiont Species

Abstract

Fungus-farming (attine) ant agriculture is made up of five known agricultural systems characterized by remarkable symbiont fidelity in which five phylogenetic groups of ants faithfully cultivate five phylogenetic groups of fungi. Here we describe the first case of a lower-attine ant cultivating a higher-attine fungus based on our discovery of a Brazilian population of the relictual fungus-farming ant Apterostigma megacephala, known previously from four stray specimens from Peru and Colombia. We find that A. megacephala is the sole surviving representative of an ancient lineage that diverged ∼39 million years ago, very early in the ∼55-million-year evolution of fungus-farming ants. Contrary to all previously known patterns of ant-fungus symbiont fidelity, A. megacephala cultivates Leucoagaricus gongylophorus, a highly domesticated fungal cultivar that originated only 2-8 million years ago in the gardens of the highly derived and recently evolved (∼12 million years ago) leaf-cutting ants. Because no other lower fungus-farming ant is known to cultivate any of the higher-attine fungi, let alone the leaf-cutter fungus, A. megacephala may provide important clues about the biological mechanisms constraining the otherwise seemingly obligate ant-fungus associations that characterize attine ant agriculture.

Dry habitats were crucibles of domestication in the evolution of agriculture in ants

“…Additionally, our ancestral reconstructions of ant agriculture returned essentially identical results across the three different models that we tested, with the ER model being statistically favoured (electronic supplementary material, table S10 and figures S12–S14). Our date and trait inferences are largely congruent with previous studies [23,32], except that we recovered slightly older dates for the origin of higher fungus farmers.…”

“…Within the fungus-farming ant clade, there was no topological variability among analyses and nearly all nodes received maximum support. Most relationships are congruent with previous molecular studies [23,32,82], but we recovered a number of novel results within the neoattines. Most importantly, we confidently resolved the positions of major Cyphomyrmex lineages and several enigmatic species of Mycetosoritis for the first time (both genera are non-monophyletic).…”

A Novel, Enigmatic Basal Leafflower Moth Lineage Pollinating a Derived Leafflower Host Illustrates the Dynamics of Host Shifts, Partner Replacement, and Apparent Coadaptation in Intimate Mutualisms

“…Comparative divergence time estimations in other insect-plant mutualisms have revealed likely examples in which insect clades may have replaced each other sequentially in association with the same host plant lineages over macroevolutionary timescales (Althoff et al 2012; Chomicki et al 2015). In a similar and striking example to that reported here, a basal leafcutter ant lineage, Apterostigma megacephala )—known from only a few localities in South America—cultivates a highly derived fungus, Leucoagaricus gongylophorus (Schultz et al 2015). Similar to leafflower-leafflower moth interactions, leafcutter ants show strong fidelity and constraint to particular fungal lineages, with more derived ants being associated with derived, domesticated fungi.…”

Rediscovery of the enigmatic fungus-farming ant "Mycetosoritis" asper Mayr (Hymenoptera: Formicidae): Implications for taxonomy, phylogeny, and the evolution of agriculture in ants

“…Rather than assign them the status of " incertae sedis ," taxonomists often group such species into so-called "dust-bin" genera erected for species of uncertain relationship, even when the species within such genera bear little resemblance to one another. Yet numerous studies have demonstrated that such phylogenetically isolated species may be especially important for understanding deeper relationships of genera, tribes, and subfamilies [1–8]. Including those species in phylogenetic analyses has significant effects on topology, ancestral character-state reconstruction, divergence-time estimation, and inferences of evolutionary rates [9–11].…”