FORUM New View on Origin of Attine Ant–Fungus Mutualism: Exploitation of a Preexisting Insect–Fungus Symbiosis (Hymenoptera: Formicidae) SERGIO R. SA ´ NCHEZ -PEN ˜ A 1 University of Texas at Austin, Austin, TX 78712, and Universidad Auto ´ noma Agraria Antonio Narro, Saltillo, Coahuila, Mexico Ann. Entomol. Soc. Am. 98(2): 151Ð164 (2005) ABSTRACT Current hypotheses on the origin of the fungusÐattine ant (Hymenoptera: Formicidae) symbiosis propose, as an ancestral Þrst step in the development of fungal cultivation, fortuitous feeding on fungi growing adventitiously on substrates such as rotting wood, insect parts, seeds stored by ants in nests, regurgitated infrabuccal pellets, free-living soil fungi, or mycorrhizae. However, feeding- deterrent fungi regularly colonize these substrates. De novo feeding on these fungi by the attine ancestor is unlikely because the almost universal presence of mycotoxins on adventitious fungi is a formidable barrier to mycophagy. In addition, there is no evolutionary history of mycophagy in the Hymenoptera. Instead, I propose that attine mycophagy began from opportunistic, selective feeding on wood-colonizing fungi previously “domesticated” by other insects: ambrosia beetles: (Coleoptera: Curculionidae: Scolytinae or Platypodinae); and less likely, woodwasps (Hymenoptera: Siricoidea). Attine ancestors foraged for beetle brood and fungal biomass in the galleries of those insects, which provided the attine ancestor with fungi that were nutritious and nontoxic to insects. The invading antsÕ debris (fecal spots, exuviae, meconia, and saliva) possibly allowed the growth of the “good” domes- ticated fungi in galleries, while ants mechanically eliminated undesirable ones. Feeding on beetle fungi Þrst allowed the development of broad mycophagy in ants, and, later, of the gardening habits. Subsequently, more restricted, speciÞc mycophagy evolved. Only after serious barriers were overcome did incipient mycophagy develop, followed by cultivation. The ambrosia fungi-lined beetle galleries in wood provide one location favorable for this sequence. An analogous progression in mycophagy and incipient fungus manipulation, departing from the omnivore diet has occurred in Megalomyrmex ants that feed parasitically on brood and/or fungus gardens of attines. Colonies of the ancestral attine nested in wood and adopted mated foundress queens after mating ßights, and colonies reproduced by budding. Queen adoption by established colonies allowed the chronological continuation of the incipient symbiosis. Mycophagy preadapted the ants to test free-living fungi in wood and soil as cultivars. The fortuitous Þnding of more adequate lepiotaceous strains in soil allowed the adaptive radiation exhibited in present-day attines. The cultivation, by the primitive attine Apterostigma, of wood-colonizing Basidiomycotina is possibly of ancestral signiÞcance. KEY WORDS Fungus-growing ants, mycophagy, symbiosis, origin FUNGUS-GROWING ANTS (Hymenoptera: Formicidae: Attini) are a fascinating and diverse group comprising 210 species in 13 genera. A monophyletic clade (Currie et al. 2003), all the Attini share the habit of cultivating mycelia of fungi (Basidiomycotina: Agari- cales: Agaricaceae (formerly Lepiotaceae) and Pteru- laceae) for food (Weber 1972, Chapela et al. 1994, Mueller et al. 1998). Both Lepiotaceae and “lepiota- ceous” are used here to refer to the attine symbionts that were classiÞed in that family (Lepiotaceae), which has recently been transferred to the Agari- caceae (Vellinga et al. 2003). Survival of attine ants depends on the successful cultivation and production of their symbiontÕs fungal biomass, which is very prob- ably the only food of attine larvae. Fungus-growing ants live only in the American continents. They are vastly more diverse in the warm, humid rainforests of Central and South America (Weber 1972, Garcia et al. 2002). Although fungus-growing ants in general are usually conservative cultivators, they may change their orig- inal fungal symbiont stocks occasionally when cata- strophic events lead to the loss of their original cultivar (Chapela et al. 1994, Mueller et al. 1998, Adams et al. 2000). Hypotheses on Origin of Fungus-Growing Symbiosis of Attines The main hypotheses on the origin of the fungusÐ attine ant symbiosis were thoroughly reviewed by 1 E-mail: elcheco@usa.net; sergiosp@mail.utexas.edu. 0013-8746/05/0151Ð0164$04.00/0  2005 Entomological Society of America