Somatic incompatibility and genetic structure of fungal crops in sympatric Atta colombica and Acromyrmex echinatior leaf-cutting ants

Abstract

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.

Biogeography of mutualistic fungi cultivated by leafcutter ants

“…Recent studies argued that L. gongylophorus fungi (i.e., Clade-A fungi) cultivated by Atta and Acromyrmex ants in Panam a represent separate gene pools (Kooij, Poulsen, Schiøtt, & Boomsma, 2015) First, at most of the locations at which we obtained adequate samples of L. gongylophorus fungi from both Atta and Acromyrmex nests, we found Atta-cultivated and Acromyrmex-cultivated fungal clones that were identical in all alleles across the five microsatellite loci (Table S3). Atta and Acromyrmex nests cultivating identical fungal clones (as defined by our five markers) were located typically within 50 km of each other, but there were also instances of apparent cultivar identity between Atta and Acromyrmex nests about 1,200 km distant (Brazil) and 1,900 km distant in Mexico/United States (Table S3).…”

“…Second, structure analyses of fungi from Panamá, the best‐sampled region in our survey, indicates that Atta ‐ vs. Acromyrmex ‐cultivated fungi do not form genetically distinct clusters, but are admixed (Figure a–d), regardless of whether we analyse regional fungal diversity (Colombia, Panamá, Costa Rica; n = 125 samples), within‐country diversity (only Panamá; n = 89 samples), provincial diversity (Panamá Canal Zone; n = 42 samples) or the local diversity in Gamboa ( n = 27) also studied by Kooij, Poulsen, et al. () (Figure a–d; see additional discussion in the Supporting Information). Our structure analyses therefore agree with the findings of three previous studies: Mikheyev et al.…”

“…Recent studies argued that L. gongylophorus fungi (i.e., Clade‐A fungi) cultivated by Atta and Acromyrmex ants in Panamá represent separate gene pools (Kooij, Poulsen, Schiøtt, & Boomsma, ) and that two L. gongylophorus fungi cultivated by Atta vs. Acromyrmex ants in Panamá diverged from each other 7.2 Ma (confidence interval 5.4–9.0 Ma; Nygaard et al., ; pages 43 & 44 in the Supplementary Methods of Nygaard et al.). Because we did not find differences between Atta ‐cultivated vs. Acromyrmex ‐cultivated L. gongylophorus fungi in our phylogenetic analyses (Figures –), we tested for possible differences using our faster‐evolving microsatellite markers, which should have adequate resolution to detect Nygaard et al.…”

Small genome of the fungus Escovopsis weberi , a specialized disease agent of ant agriculture

“…There are several important considerations in the case of complex symbiotic systems such as that of the fungus-growing ant symbiosis, however. First, the cultivar, likely under the strongest selection to evolve defenses to counteract Escovopsis attack, reproduces mostly asexually, and somatic incompatibilities limit genetic exchange between strains (29,30); the cultivar may be constrained to not evolve rapidly so as to maintain a mutualism with the ants [i.e., Red King hypothesis for slow evolution of mutualistic partners (31)]. Second, Escovopsis too can benefit from symbionts [e.g., black yeast that inhibit growth of antibioticproducing bacteria (32)], which in turn themselves could evolve in response to changing defenses.…”

The good, the bad and the tasty: The many roles of mushrooms

“…Research is ongoing to resolve the phylogeny of the Leucoagaricus genus, which appears to be polyphyletic (Johnson, 1999, Vellinga et al., 2003, Kooij et al., 2014b, Pereira et al., 2015), and to decipher the specific relationships of the leaf-cutter ant genera with their fungal symbiont, as there are some indications that Atta and Acromyrmex are cultivating different clades of L. gongylophorus (Mikheyev et al., 2010, Kooij et al., 2015a, Kooij et al., 2015b). …”