Extensive exchange of fungal cultivars between sympatric species of fungus‐growing ants

Abstract

Fungal cultivars of fungus-growing ants (Attini, Formicidae) are carried by dispersing queens from parent to offspring nest. This vertical cultivar transmission between generations is thought to result in long-term ant-fungus coevolution and selection for beneficial cultivar traits that maximize harvests and thus colony productivity. In contrast to this traditional view of vertical cultivar transmission, frequent horizontal cultivar transmission between ant species is implicated by a phylogenetic analysis of 72 cultivars propagated by two fungus-growing ant species coexisting sympatrically in central Panama. The two ant species are specialized on the same group of closely related cultivars, but in six of 12 cultivar clades identifiable within this group, cultivars from both ant species were united in the same clade. Five of these 'mixed' clades were supported by bootstrap values of about 90% or higher. In one instance, colonies from the two ant species cultivated the same, genetically identical, cultivar clone. These phylogenetic patterns indicate that: (i) cultivar exchanges between the two ant species occur routinely throughout ecological time; and that (ii) coevolutionary processes between ants and their fungi are more diffuse than previously assumed. Because the two ant species are specialized on a narrow group of closely related cultivars that they regularly exchange among each other, but not with other sympatric ant species, cultivar exchanges are constrained, most likely, by ant preferences for their own cultivar group or by stringent selection against transitions of ant lineages to distantly related cultivars.

Cryptic speciation in the fungus-growing ants Cyphomyrmex longiscapus Weber and Cyphomyrmex muelleri Schultz and Solomon, new species (Formicidae, Attini)

“…Each of these fungal cultivars is also employed by other, distantly related attine ants that occupy different microhabitats and that are otherwise quite dissimilar biologically Green et al 2002). Specifically, C. longiscapus shares a narrow group of cultivars of the "Clade 1" type with the sympatric fungus-growing ant Apterostigma auriculatum; molecular data indicate that in one case a cultivar clone has been transferred recently between nests of these two ant species .…”

“…complex; (2) to update the taxonomy of C. longiscapus sensu stricto and to describe the new species; (3) to summarize the morphometrics, distribution, and biology of both species; and (4) to facilitate easy differentiation of these species in the laboratory and the field. The goal of facilitating identification is especially important because, as noted above, C. longiscapus and its relatives are of special biological interest and, as recommended by Mueller and Wcislo (1998), have truly become model organisms in diverse behavioral, ecological, and evolutionary studies Currie et al, 1999Currie et al, a, 1999Villesen et al, 1999;Green et al, 2002;Mueller et al, in press;Villesen et al, in press;Adams et al, unpubl. ;Mehdiabadi and Mueller, unpubl.…”

Symbiont fidelity and the origin of species in fungus-growing ants

“…However, empirical work over the past two decades has shown that cultivars are frequently transmitted horizontally between different ant colonies (sometimes between colonies of different ant species) and that lower-attine cultivars are closely related to, and in some cases identical to, free-living fungal species, suggesting frequent import of fungi into the symbiosis from free-living sources [12][13][14]17,21,23,[25][26][27][28][29] . This apparent absence of one-to-one host fidelity (that is, long-term association of ant and fungal genotypes), combined with the recent discovery that the lower-attine fungal Clade 2 ( Fig.…”

“…Because of the difficulty of obtaining large samples of both ants and fungi from the same nests across the full geographic range of a species, most previous work on the fidelity of association of attine ants and their fungi involved reconstructing phylogenies of fungi but not of their ant hosts, or of ants and fungi drawn from limited localities 12,14,21,26 . A complete understanding of the shared evolutionary history of attine ants and their associated fungi, however, requires detailed understanding of the phylogenies of both interacting partners across their geographic ranges 30 , preferably ant-fungus pairs sampled from the same nests.…”

“…1), even though nests of the two species occur in sympatry and, indeed, may be separated by only a few centimetres in some localities 12,26,[31][32][33] . Based on evidence from morphology and biogeography, it was previously hypothesized that C. muelleri may be derived from an ancestor resembling C. longiscapus s.l.…”