Biogeography of mutualistic fungi cultivated by leafcutter ants

Authors: MUELLER, ULRICH - University Of Texas; ISHAK, HEATHER - University Of Texas; BRUSCHI, SOFIA - Universidade Estadual Paulista (UNESP); SMITH, CHAD - University Of Texas; HERMAN, JACOB - University Of Texas; MIKHEYEV, ALEXANDER - Okinawa Prefectural Institute; RABELING, CHRISTIAN - Arizona State University; SCOTT, JAROD - University Of Texas; COOPER, MICHAEL - University Of Texas; RODRIGUES, ANDRE - Universidade Estadual Paulista (UNESP); BRANDAO, CARLOS - Universidad De Sao Paulo; LATTKE, JOHN - Universidade Federal Do Parana; PAGNOCCA, FERNANDO - Universidade Estadual Paulista (UNESP); Rehner, Stephen; SCHULTZ, TED - Smithsonian Institute; VASCONCELOS, HERALDO - Universidade Federal De Uberlândia; ADAMS, RACHELLE - University Of Texas; BOLLAZI, M - Universidad De La República; CLARK, REBECCA - University Of California; HIMLER, ANNA - The College Of Idaho; LAPOLLA, JOHN - Towson University; LEAL, INARA - Federal University Of Pernambuco; JOHNSON, ROBERT - Arizona State University; ROCES, FLAVIO - University Of Wurzburg; SOSA-CALVO, JEFFREY - Smithsonian Institute; WIRTH, R - University Of Konstanz; BACCI, MAURICIO - Universidade Estadual Paulista (UNESP); SOLOMON, SCOTT - University Of Texas; ORTIZ, ADRIANA - University Of Texas

Submitted to: Molecular Ecology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/4/2017
Publication Date: 12/2/2017
Citation: Mueller, U.G., Ishak, H.D., Bruschi, S.M., Smith, C.C., Herman, J.J., Mikheyev, A.S., Rabeling, C., Scott, J.J., Cooper, M., Rodrigues, A., Brandao, C.R., Lattke, J.E., Pagnocca, F.C., Rehner, S.A., Schultz, T.R., Vasconcelos, H.L., Adams, R.M., Bollazi, M., Clark, R.M., Himler, A.G., Lapolla, J.S., Leal, I.R., Johnson, R.A., Roces, F., Sosa-Calvo, J., Wirth, R., Bacci, M., Solomon, Scott E., Ortiz, A. 2017. Biogeography of mutualistic fungi cultivated by leafcutter ants. Molecular Ecology. 26:6921-6937. https://doi.org/10.1111/mec.14431

Interpretive Summary: Because they often completely defoliate plants, leafcutter ants are a major agricultural problem because they annually cause billions of dollars in damage to trees and herbaceous plants from Argentina through the southern United States. These ants carry plant leaves to their nests, where the leaves are fed to fungi cultivated by the ants. This paper describes an international study by a large group of scientists examining the nature of the relationships between different species of ants and the different species of fungi cultivated by the ants. Specifically, the researchers examined the DNA sequences of 474 kinds of fungi from different geographical areas. The researchers discovered that there were two major groups of fungi, each being associated with two different groups of ants--those that preferentially attack grasses versus those that attack broadleaved plants, especially trees. The results are significant because they provide remarkably new information about the adaptation and co-evolution of these ants and fungi to different plants. This research will be utilized by biologists, entomologists, and other researchers seeking to minimize agricultural losses caused by leafcutter ants.

Technical Abstract: Leafcutter ants propagate co-evolving fungi for food. The nearly 50 species of leafcutter ants (Atta, Acromyrmex) range from Argentina to the USA, with the greatest species diversity in southern South America. We elucidate the biogeography of fungi cultivated by leafcutter ants using DNA-sequence and microsatellite-marker analyses of 474 cultivars collected across the leafcutter range. Fungal cultivars belong to two clades (Clade-A, Clade-B). The dominant and widespread Clade-A cultivars form three genotype-clusters, with their relative prevalence corresponding to southern South America, northern South America, and Central & North America. Admixture between Clade:A populations support genetic exchange within a single species, Leucocoprinus gongylophorus. Some leafcutter species that cut grass as fungicultural substrate arespecialized to cultivate Clade-B fungi, whereas leafcutters preferring dicot plants appear specialized on Clade-A fungi. Cultivar sharing between sympatric leafcutter species occurs frequently, such that cultivars of Atta are not distinct from those of Acromyrmex. Leafcutters specialized on Clade-B fungi occur only in South America. Diversity of Clade-A fungi is greatest in South America, but minimal in Central & North America. Maximum cultivar diversity in South America is predicted by the Kusnezov-Fowler hypothesis that leafcutter ants originated in subtropical South America and only dicot-specialized leafcutter ants migrated out of South America, but the cultivar diversity becomes also compatible with a recently-proposed hypothesis of Central American origin by postulating that leafcutter ants acquired novel cultivars from other fungus-growing ants during their migrations from Central America across South America. We evaluate these biogeographic hypotheses in light of estimated dates for the origins of leafcutter ants and their cultivars.