Evolution of cold-tolerant fungal symbionts permits winter fungiculture by leafcutter ants at the northern frontier of a tropical ant–fungus symbiosis

Abstract

The obligate mutualism between leafcutter ants and their Attamyces fungi originated 8 to 12 million years ago in the tropics, but extends today also into temperate regions in South and North America. The northernmost leafcutter ant Atta texana sustains fungiculture during winter temperatures that would harm the coldsensitive Attamyces cultivars of tropical leafcutter ants. Cold-tolerance of Attamyces cultivars increases with winter harshness along a south-to-north temperature gradient across the range of A. texana, indicating selection for cold-tolerant Attamyces variants along the temperature cline. Ecological niche modeling corroborates winter temperature as a key range-limiting factor impeding northward expansion of A. texana. The northernmost A. texana populations are able to sustain fungiculture throughout winter because of their cold-adapted fungi and because of seasonal, vertical garden relocation (maintaining gardens deep in the ground in winter to protect them from extreme cold, then moving gardens to warmer, shallow depths in spring). Although the origin of leafcutter fungiculture was an evolutionary breakthrough that revolutionized the food niche of tropical fungus-growing ants, the original adaptations of this host-microbe symbiosis to tropical temperatures and the dependence on cold-sensitive fungal symbionts eventually constrained expansion into temperate habitats. Evolution of coldtolerant fungi within the symbiosis relaxed constraints on winter fungiculture at the northern frontier of the leafcutter ant distribution, thereby expanding the ecological niche of an obligate hostmicrobe symbiosis.ecological gradient | selection gradient | range limit | frontier mutualism

Metabolism and the Rise of Fungus Cultivation by Ants

“…The resulting cocoons, which appear to have evolved soon after the farming transition, likely protect brood from disease (Armitage et al 2012). Such additional services provided by cultivars have enabled attines to exploit new habitats and niches (Martin and Weber 1969;Mueller et al 2011) and have metabolic costs and benefits that remain to be explored.…”

“…The ants (Hymenoptera: Formicidae) epitomize this trend, with more than 14,000 species whose eusocial hunter-gatherer colonies have anywhere from tens to millions of workers that cooperate to harvest resources and provision developing larvae inside the nest (Hölldob-ler and Wilson 2008). A further transition occurred 50 million years ago (MYA), when ants in the attine lineage adopted fungus cultivation, diversifying over time into more than 230 species common across the New World tropics and subtropics (Weber 1972;Mueller et al 2005Mueller et al , 2011Schultz and Brady 2008). While fungus cultivation is considered a major breakthrough in ant evolution (Mueller and Rabeling 2008;Hölldobler and Wilson 2010), there has been little exploration of the ecological costs and benefits that enabled the transition from hunting and gathering.…”

Heritable symbionts in a world of varying temperature

“…Although the services provided by heritable microbes have been credited with allowing early host range expansion by permitting the exploitation of widespread but nutritionally poor resources (Feldhaar and Gross, 2009;Hansen and Moran, 2011), their narrow temperature requirements have been implicated in restricting host spread. Insects such as aphids may be limited to temperate regions by their intracellular symbionts (Dixon et al, 1987), whereas funguscultivating ants are restricted to tropical environments by the temperature requirements of their obligate cold-susceptible fungal symbiont (Mueller et al, 2011). To date, there has been no formal comparative test of this hypothesis, in which thermal niche breadth of hosts with and without symbionts are compared.…”

Ant-fungal species combinations engineer physiological activity of fungus gardens

“…Atta texana is found throughout central, east and south Texas, western Lousiana and northeastern Mexico (Mueller et al, 2011a;Mueller et al, 2011b;Sanchez-Peña, 2010). Atta texana cultivates a single fungal species typical of the vast majority of leaf-cutting ants (Leucocoprinus gongylophorus) (Fisher et al, 1994;Mikheyev et al, 2006;Mueller et al, 2011a;Mueller, 2002;Pagnocca et al, 2001); however, this species rarely reproduces sexually -we refer to it by its anamorph (asexual) form, Attamyces bromatificus Kreisel Mueller et al, 2011b;Seal et al, 2012;Seal and Mueller, 2014). In contrast, T. arizonensis cultivates a Trachymyces fungus typical for most (but not all) Trachymyrmex species that is placed in a taxonomically unresolved Leucocoprinus clade that is the sister clade to the Attamyces clade.…”