TY - JOUR
T1 - Phylogenomic reconstruction reveals new insights into the evolution and biogeography of Atta leaf-cutting ants (Hymenoptera: Formicidae)
AU - Barrera, Corina A.
AU - Sosa-Calvo, Jeffrey
AU - Schultz, Ted R.
AU - Rabeling, Christian
AU - Bacci, Maurício
N1 - Funding Information:
We wish to thank the following colleagues that sent specimens and assisted us in museum visits, field trips and/or laboratory work, for their generous help: André Rodrigues, Antônio Mayhé-Nunes, Carlos R. Brandão, Clarisa Decuyper, Clarissa Knoechelmann, Corrie S. Moreau, Daniela M. Rodríguez, Eder B. França, Emília Z. Albuquerque, Fabricio B. Baccaro, Felipe Vivallo, Geancarlo Alarcon, Graziele Santiago, Heraldo L. Vasconcelos, Inara R. Leal, Itanna O. Fernandes, Jack T. Longino, Jacques H. C. Delabie, Janiele P. da Silva, Janete Andrade, John E. Lattke, Júlio Chaul, Kelli Ramos, Kyle Gray, Lívia P. do Prado, Marcio L. de Oliveira, Mariane Nickele, Martín Bolazzi, Matheus T. Fontanelle, Matthew Prebus, Mayara L. Pessoa, Milene Ferro, Mônica A. Ulysséa, Paulo R. de Souza, Pedro Elias, Pedro Senna, Philip S. Ward, Rodolfo Probst, Renata Z. Aquino, Ricardo Vicente, Rodrigo M. Feitosa, Rogério R. da Silva, Sabrina Simon, and Steven Messer. We are also grateful to Andrés F. Sánchez-Restrepo (FuEDEI, Argentina) and Ivan L. F. Magalhaes (MACN, Argentina) for assistance with biogeobears scripts; Milene Ferro (UNESP, Brazil) for help with the biogeographical analyses; Andrés F. Sánchez-Restrepo, Fernando Fernández, Gabriela Camacho, Heraldo L. Vasconcelos, and Scott Solomon for their constructive comments and advice on earlier versions of this manuscript; and the editor Bonnie Blaimer, Rodrigo M. Feitosa, and two anonymous reviewers for providing valuable suggestions and feedback on the manuscript. Permission to collect samples in Brazil (SISBio 33487-5) was granted by the Chico Mendes Institute for Biodiversity Conservation (ICMBio). This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – Brasil (CAPES) – Financing Code 001 (CB; PhD scholarship); Fundação de Apoio à Pesquisa do Estado de São Paulo (FAPESP) [2019/03746-0, 2019/24470-2 (MB)]; Universidade Estadual Paulista (UNESP) (CB & MB); Arizona State University (CR & CB); the Smithsonian National Museum of Natural History Small Grants Program (JSC & TRS); and the U.S. National Science Foundation [NSF CAREER DEB-1943626 (CR), NSF DEB-1654829 (CR & TRS), and NSF DEB-1927161 (TRS & JSC)]. The authors declare that there are no conflicts of interest.
Funding Information:
We wish to thank the following colleagues that sent specimens and assisted us in museum visits, field trips and/or laboratory work, for their generous help: André Rodrigues, Antônio Mayhé‐Nunes, Carlos R. Brandão, Clarisa Decuyper, Clarissa Knoechelmann, Corrie S. Moreau, Daniela M. Rodríguez, Eder B. França, Emília Z. Albuquerque, Fabricio B. Baccaro, Felipe Vivallo, Geancarlo Alarcon, Graziele Santiago, Heraldo L. Vasconcelos, Inara R. Leal, Itanna O. Fernandes, Jack T. Longino, Jacques H. C. Delabie, Janiele P. da Silva, Janete Andrade, John E. Lattke, Júlio Chaul, Kelli Ramos, Kyle Gray, Lívia P. do Prado, Marcio L. de Oliveira, Mariane Nickele, Martín Bolazzi, Matheus T. Fontanelle, Matthew Prebus, Mayara L. Pessoa, Milene Ferro, Mônica A. Ulysséa, Paulo R. de Souza, Pedro Elias, Pedro Senna, Philip S. Ward, Rodolfo Probst, Renata Z. Aquino, Ricardo Vicente, Rodrigo M. Feitosa, Rogério R. da Silva, Sabrina Simon, and Steven Messer. We are also grateful to Andrés F. Sánchez‐Restrepo (FuEDEI, Argentina) and Ivan L. F. Magalhaes (MACN, Argentina) for assistance with biogeobears scripts; Milene Ferro (UNESP, Brazil) for help with the biogeographical analyses; Andrés F. Sánchez‐Restrepo, Fernando Fernández, Gabriela Camacho, Heraldo L. Vasconcelos, and Scott Solomon for their constructive comments and advice on earlier versions of this manuscript; and the editor Bonnie Blaimer, Rodrigo M. Feitosa, and two anonymous reviewers for providing valuable suggestions and feedback on the manuscript. Permission to collect samples in Brazil (SISBio 33487‐5) was granted by the Chico Mendes Institute for Biodiversity Conservation (ICMBio). This study was financed in part by the (CAPES) Financing Code 001 (CB; PhD scholarship); (FAPESP) [2019/03746‐0, 2019/24470‐2 (MB)]; (UNESP) (CB & MB); Arizona State University (CR & CB); the Smithsonian National Museum of Natural History Small Grants Program (JSC & TRS); and the U.S. National Science Foundation [NSF CAREER DEB‐1943626 (CR), NSF DEB‐1654829 (CR & TRS), and NSF DEB‐1927161 (TRS & JSC)]. The authors declare that there are no conflicts of interest. Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – Brasil – Fundação de Apoio à Pesquisa do Estado de São Paulo Universidade Estadual Paulista
Publisher Copyright:
© 2021 The Authors. Systematic Entomology published by John Wiley & Sons Ltd on behalf of Royal Entomological Society.
PY - 2022/1
Y1 - 2022/1
N2 - Atta Fabricius is an ecologically dominant leaf-cutting ant genus, the major herbivore of the Neotropics, and an agricultural pest of great economic importance. Phylogenetic relationships within Atta have until now remained uncertain, and the delimitation and identification of a subset of Atta species are problematic. To address these phylogenetic uncertainties, we reconstruct the most comprehensive phylogenetic estimate to date of Atta by employing ultraconserved elements (UCEs). We recovered 2340 UCE loci from 224 Atta specimens, which include 14 out of the 15 identifiable species from across their geographic distributions, and 49 outgroup specimens. Our results strongly support the monophyly of Atta and of the four clades that coincide with the previously recognized subgenera Archeatta Gonçalves, Atta s.s. Emery, Epiatta Borgmeier, and Neoatta Gonçalves. The Archeatta clade contains three species occurring in North and Central America and the Caribbean and is the sister group of the remainder of all other Atta species. The Atta s.s. clade is composed of two species occupying North, Central, and South America. The Epiatta clade contains seven entirely South American species and the two species of the Neoatta clade occur in Central and South America. Divergence-dating analyses identify a series of major events in the Miocene, such as the divergence of Acromyrmex Mayr and Atta 16.7 million years ago (Ma) and the crown-group origin of Atta around 8.5 Ma. Extant Atta species evolved very recently, originating in the early Pleistocene, approximately 1.8–0.3 Ma (crown-group ages). We provide the first evidence that Atta goiana Gonçalves belongs to the Epiatta clade and that Atta robusta Borgmeier is the species with the youngest crown-group age of 0.3 Ma. The very young ages of Atta and its component species indicate a recent, rapid radiation. Biogeographic analyses suggest that the range of the most recent common ancestor of Atta consisted of the combined North/Central America and NW South America bioregions and that one daughter lineage subsequently dispersed into South America, rapidly diversifying in the newly formed Cerrado biome and Chaco, and further dispersing into the Atlantic Forest, Caatinga, and Pampas bioregions.
AB - Atta Fabricius is an ecologically dominant leaf-cutting ant genus, the major herbivore of the Neotropics, and an agricultural pest of great economic importance. Phylogenetic relationships within Atta have until now remained uncertain, and the delimitation and identification of a subset of Atta species are problematic. To address these phylogenetic uncertainties, we reconstruct the most comprehensive phylogenetic estimate to date of Atta by employing ultraconserved elements (UCEs). We recovered 2340 UCE loci from 224 Atta specimens, which include 14 out of the 15 identifiable species from across their geographic distributions, and 49 outgroup specimens. Our results strongly support the monophyly of Atta and of the four clades that coincide with the previously recognized subgenera Archeatta Gonçalves, Atta s.s. Emery, Epiatta Borgmeier, and Neoatta Gonçalves. The Archeatta clade contains three species occurring in North and Central America and the Caribbean and is the sister group of the remainder of all other Atta species. The Atta s.s. clade is composed of two species occupying North, Central, and South America. The Epiatta clade contains seven entirely South American species and the two species of the Neoatta clade occur in Central and South America. Divergence-dating analyses identify a series of major events in the Miocene, such as the divergence of Acromyrmex Mayr and Atta 16.7 million years ago (Ma) and the crown-group origin of Atta around 8.5 Ma. Extant Atta species evolved very recently, originating in the early Pleistocene, approximately 1.8–0.3 Ma (crown-group ages). We provide the first evidence that Atta goiana Gonçalves belongs to the Epiatta clade and that Atta robusta Borgmeier is the species with the youngest crown-group age of 0.3 Ma. The very young ages of Atta and its component species indicate a recent, rapid radiation. Biogeographic analyses suggest that the range of the most recent common ancestor of Atta consisted of the combined North/Central America and NW South America bioregions and that one daughter lineage subsequently dispersed into South America, rapidly diversifying in the newly formed Cerrado biome and Chaco, and further dispersing into the Atlantic Forest, Caatinga, and Pampas bioregions.
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U2 - 10.1111/syen.12513
DO - 10.1111/syen.12513
M3 - Article
AN - SCOPUS:85114153681
SN - 0307-6970
VL - 47
SP - 13
EP - 35
JO - Systematic Entomology
JF - Systematic Entomology
IS - 1
ER -