TY - JOUR
T1 - The molecular phylogenetics of Trachymyrmex Forel ants and their fungal cultivars provide insights into the origin and coevolutionary history of ‘higher-attine’ ant agriculture
AU - Solomon, Scott E.
AU - Rabeling, Christian
AU - Sosa-Calvo, Jeffrey
AU - Lopes, Cauê T.
AU - Rodrigues, André
AU - Vasconcelos, Heraldo L.
AU - Bacci, Maurício
AU - Mueller, Ulrich G.
AU - Schultz, Ted R.
N1 - Funding Information:
We are very grateful to the following colleagues for providing samples that were used in this study and/or for facilitating field work: Rachelle Adams, Donat Agosti, Roberto C.F. Brandão, Cameron Currie, Jacques Delabie, Ana Harada, Anna Himler, John Lattke, Inara Leal, Alexandre Marchesi, Antonio Mayhé-Nunes and Eduardo Salomão. We are thankful to Marek Borowiec for sharing his unpublished manuscript to generate the files for submitting sequences to GenBank, and to Eugenia Okonski for creating the images for Fig. This work was supported by the U.S. National Science Foundation (International Research Fellowship Program award 07012333 to SES; DEB-0949689 to TRS; DEB-1456964 and DEB-1654829 to CR and TRS; DEB-0919519 and DEB-1354666 to UGM), the W.M. Wheeler Endowment from the University of Texas at Austin, and Smithsonian Scholarly Studies and CGPS grants to TRS and a Smithsonian Institution Peter Buck Pre-Doctoral Fellowship to JSC. Field work in Brazil was conducted under permit numbers 14789-1, 14789-2, 14789-3, 14789-4, 14789-5, 14789-9, 33487-2 and 33487-4 issued by the Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis (IBAMA) and the Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio). The authors state that there are no conflicts of interest.
Publisher Copyright:
© 2019 The Authors. Systematic Entomology published by John Wiley & Sons Ltd on behalf of Royal Entomological Society.
PY - 2019/10/1
Y1 - 2019/10/1
N2 - The fungus-growing ants and their fungal cultivars constitute a classic example of a mutualism that has led to complex coevolutionary dynamics spanning c. 55–65 Ma. Of the five agricultural systems practised by fungus-growing ants, higher-attine agriculture, of which leaf-cutter agriculture is a derived subset, remains poorly understood despite its relevance to ecosystem function and human agriculture across the Neotropics and parts of North America. Among the ants practising higher-attine agriculture, the genus Trachymyrmex Forel, as currently defined, shares most-recent common ancestors with both the leaf-cutter ants and the higher-attine genera Sericomyrmex Mayr and Xerolitor Sosa-Calvo et al. Although previous molecular-phylogenetic studies have suggested that Trachymyrmex is a paraphyletic grade, until now insufficient taxon sampling has prevented a full investigation of the evolutionary history of this group and limited the possibility of resolving its taxonomy. Here we describe the results of phylogenetic analyses of 38 Trachymyrmex species, including 27 of the 49 described species and at least 11 new species, using four nuclear markers, as well as phylogenetic analyses of the fungi cultivated by 23 species of Trachymyrmex using two markers. We generated new genetic data for 112 ants (402 new gene sequences) and 95 fungi (153 new gene sequences). Our results corroborate previous findings that Trachymyrmex, as currently defined, is paraphyletic. We propose recognizing two new genera, Mycetomoellerius gen.n. and Paratrachymyrmex gen.n., and restricting the continued use of Trachymyrmex to the clade of nine largely North American species that contains the type species [Trachymyrmex septentrionalis (McCook)] and that is the sister group of the leaf-cutting ants. Our fungal cultivar phylogeny generally corroborates previously observed broad patterns of ant–fungus association, but it also reveals further violations of those patterns. Higher-attine fungi are divided into two groups: (i) the single species Leucoagaricus gongylophorus (Möller); and (ii) its sister clade, consisting of multiple species, recently referred to as Leucoagaricus Singer ‘clade B’. Our phylogeny indicates that, although most non-leaf-cutting higher-attine ants typically cultivate species in clade B, some species cultivate L. gongylophorus, whereas still others cultivate fungi typically associated with lower-attine agriculture. This indicates that the attine agricultural systems, which are currently defined by associations between ants and fungi, are not entirely congruent with ant and fungal phylogenies. They may, however, be correlated with as yet poorly understood biological traits of the ants and/or of their microbiomes.
AB - The fungus-growing ants and their fungal cultivars constitute a classic example of a mutualism that has led to complex coevolutionary dynamics spanning c. 55–65 Ma. Of the five agricultural systems practised by fungus-growing ants, higher-attine agriculture, of which leaf-cutter agriculture is a derived subset, remains poorly understood despite its relevance to ecosystem function and human agriculture across the Neotropics and parts of North America. Among the ants practising higher-attine agriculture, the genus Trachymyrmex Forel, as currently defined, shares most-recent common ancestors with both the leaf-cutter ants and the higher-attine genera Sericomyrmex Mayr and Xerolitor Sosa-Calvo et al. Although previous molecular-phylogenetic studies have suggested that Trachymyrmex is a paraphyletic grade, until now insufficient taxon sampling has prevented a full investigation of the evolutionary history of this group and limited the possibility of resolving its taxonomy. Here we describe the results of phylogenetic analyses of 38 Trachymyrmex species, including 27 of the 49 described species and at least 11 new species, using four nuclear markers, as well as phylogenetic analyses of the fungi cultivated by 23 species of Trachymyrmex using two markers. We generated new genetic data for 112 ants (402 new gene sequences) and 95 fungi (153 new gene sequences). Our results corroborate previous findings that Trachymyrmex, as currently defined, is paraphyletic. We propose recognizing two new genera, Mycetomoellerius gen.n. and Paratrachymyrmex gen.n., and restricting the continued use of Trachymyrmex to the clade of nine largely North American species that contains the type species [Trachymyrmex septentrionalis (McCook)] and that is the sister group of the leaf-cutting ants. Our fungal cultivar phylogeny generally corroborates previously observed broad patterns of ant–fungus association, but it also reveals further violations of those patterns. Higher-attine fungi are divided into two groups: (i) the single species Leucoagaricus gongylophorus (Möller); and (ii) its sister clade, consisting of multiple species, recently referred to as Leucoagaricus Singer ‘clade B’. Our phylogeny indicates that, although most non-leaf-cutting higher-attine ants typically cultivate species in clade B, some species cultivate L. gongylophorus, whereas still others cultivate fungi typically associated with lower-attine agriculture. This indicates that the attine agricultural systems, which are currently defined by associations between ants and fungi, are not entirely congruent with ant and fungal phylogenies. They may, however, be correlated with as yet poorly understood biological traits of the ants and/or of their microbiomes.
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U2 - 10.1111/syen.12370
DO - 10.1111/syen.12370
M3 - Article
AN - SCOPUS:85066053092
SN - 0307-6970
VL - 44
SP - 939
EP - 956
JO - Systematic Entomology
JF - Systematic Entomology
IS - 4
ER -