Termitidae comprises ∼80% of all termite species [1] that play dominant decomposer roles in tropical ecosystems [2, 3]. Two major events during termite evolution were the loss of cellulolytic gut protozoans in the ancestor of Termitidae and the subsequent gain in the termitid subfamily Macrotermitinae of fungal symbionts cultivated externally in "combs" constructed within the nest [4, 5]. How these symbiotic transitions occurred remains unresolved. Phylogenetic analyses of mitochondrial data previously suggested that Macrotermitinae is the earliest branching termitid lineage, followed soon after by Sphaerotermitinae [6], which cultivates bacterial symbionts on combs inside its nests [7]. This has led to the hypothesis that comb building was an important evolutionary step in the loss of gut protozoa in ancestral termitids [8]. We sequenced genomes and transcriptomes of 55 termite species and reconstructed phylogenetic trees from up to 4,065 orthologous genes of 68 species. We found strong support for a novel sister-group relationship between the bacterial comb-building Sphaerotermitinae and fungus comb-building Macrotermitinae. This key finding indicates that comb building is a derived trait within Termitidae and that the creation of a comb-like "external rumen" involving bacteria or fungi may not have driven the loss of protozoa from ancestral termitids, as previously hypothesized. Instead, associations with gut prokaryotic symbionts, combined with dietary shifts from wood to other plant-based substrates, may have played a more important role in this symbiotic transition. Our phylogenetic tree provides a platform for future studies of comparative termite evolution and the evolution of symbiosis in this taxon.

Department for Materials and Environment BAM Federal Institute for Materials Research and Testing Unter den Eichen 87 12205 Berlin Germany

Evolutionary Biology and Ecology CP 160 12 Université Libre de Bruxelles Avenue F D Roosevelt 50 1050 Brussels Belgium

Faculty of Forestry and Wood Sciences Czech University of Life Sciences Kamycka 129 16521 Prague Czech Republic

Institute of Biology Freie Universität Berlin Königin Luise Strasse 1 3 14195 Berlin Germany

Institute of Organic Chemistry and Biochemistry Flemingovo nám 2 166 10 Prague Czech Repubic

Marie Bashir Institute for Infectious Diseases and Biosecurity Charles Perkins Centre School of Life and Environmental Sciences and Sydney Medical School The University of Sydney Sydney NSW 2006 Australia

Okinawa Institute of Science and Technology Graduate University 1919 1 Tancha Onna son Okinawa 904 0495 Japan

School of Life and Environmental Sciences University of Sydney Sydney NSW 2006 Australia

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