Comparative Dating of Attine Ant and Lepiotaceous Cultivar Phylogenies Reveals Coevolutionary Synchrony and Discord

Abstract

JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact support@jstor.org.. abstract: The mutualistic symbiosis between fungus-gardening ants and their cultivars has made fundamental contributions to our understanding of the coevolution of complex species interactions. Reciprocal specialization and vertical symbiont cotransmission are thought to promote a pattern of largely synchronous coevolutionary diversification in attines. Here we test this hypothesis by inferring the first time-calibrated multigene phylogeny of the lepiotaceous attine cultivars and comparing it with the recently published fossilanchored phylogeny of the attine ants. While this comparison reveals some possible cases of synchronous origins of ant and fungal clades, there were a number of surprising asynchronies. For example, leafcutter cultivars appear to be significantly younger than the corresponding ant genera. Similarly, a clade of fungi interacting with primitive fungus-gardening ants-thought to be ancestral to the more derived leaf-cutter symbionts-appears instead to be a more recent acquisition from free-living stock. These macroevolutionary patterns are consistent with recent population-level studies suggesting occasional acquisition of novel cultivar types from environmental sources and horizontal transmission of cultivars between different ant species. Horizontal transmission events, even if rare, appear to form loose ecological connections between diffusely coevolving ant and fungus lineages that permit punctuated changes in the topology of the mutualistic ant-fungus interaction network.

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

“…and that the origin of C. muelleri may have coincided with, or even have been driven by, a switch from the Clade 1 to Clade 2 cultivar 31 . The younger evolutionary age of Clade 2 relative to Clade 1 16 is consistent with this scenario, as is experimental work demonstrating that Clade 2-cultivating Panamanian C. muelleri ants accept the cultivar of C. longiscapus, whereas C. longiscapus ants do not readily accept the cultivar of C. muelleri 33,34 , reflecting an asymmetric ancestral/derived host-tolerance pattern also known from insect-plant coevolution 35 .…”

“…Instead, it might best be characterized as narrowly diffuse, 'one-to-few' coevolution. The C. wheeleri ant clade is closely related to the higher Attini 20 , which includes the leafcutting ants whose fungal cultivars are highly derived, obligate symbionts that exhibit coevolved modifications 16,20,22 . If C. wheelerigroup ant-fungus associations are more specific than those found in other lower Attini, they may represent an intermediate condition linking the broadly diffuse associations found in other lower-attine ants with the narrow associations that led to the evolution of higherattine fungiculture.…”

“…Mutualists can be tightly integrated, resulting in coadaptation and cospeciation (that is, speciation in one partner results in simultaneous speciation in the other), or 'diffusely' associated because of frequent host switching. Diffuse coevolution has been proposed to occur in a variety of mutualisms, such as those between figs and fig-wasp pollinators 4,8,9 , squids and their bioluminescent bacterial symbionts 10 , and fungus-growing insects and their cultivated fungi [11][12][13][14][15][16][17] .…”

“…Lower-attine fungi are thought to facultatively associate with ants because the fungi can also live outside the symbiosis 12,21 . In 'higher' attine fungiculture, however, a highly derived group of fungi descended from a lower-attine fungal ancestor is obligately associated with ants and, as far as is known, cannot live outside the symbiosis 13,14,16,17,22,23 .…”

“…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. 1) may be evolutionarily much younger than its ant hosts 16 , has led to a general expectation of low partner fidelity (that is, frequent reassociation of ant and fungal genotypes) in lower-attine fungiculture.…”