Newly discovered sister lineage sheds light on early ant evolution

Ants are the world's most conspicuous and important eusocial insects and their diversity, abundance, and extreme behavioral specializations make them a model system for several disciplines within the biological sciences. Here, we report the discovery of a new ant that appears to represent the sister lineage to all extant ants (Hymenoptera: Formicidae). The phylogenetic position of this cryptic predator from the soils of the Amazon rainforest was inferred from several nuclear genes, sequenced from a single leg. Martialis heureka (gen. et sp. nov.) also constitutes the sole representative of a new, morphologically distinct subfamily of ants, the Martialinae (subfam. nov.). Our analyses have reduced the likelihood of long-branch attraction artifacts that have troubled previous phylogenetic studies of early-diverging ants and therefore solidify the emerging view that the most basal extant ant lineages are cryptic, hypogaeic foragers. On the basis of morphological and phylogenetic evidence we suggest that these specialized subterranean predators are the sole surviving representatives of a highly divergent lineage that arose near the dawn of ant diversification and have persisted in ecologically stable environments like tropical soils over great spans of time.

[1]  Jonathan P. Bollback,et al.  Bayesian model adequacy and choice in phylogenetics. , 2002, Molecular biology and evolution.

[2]  C. Brandão,et al.  The Earliest Known Fossil Ant(First Southern Hemisphere Mesozoic Record)(Hymenoptera: Formicidae: Myrmeciinae) , 1989 .

[3]  P. S. Ward,et al.  Phylogeny and biogeography of the ant subfamily Myrmeciinae (Hymenoptera: Formicidae) , 2003 .

[4]  D. Grimaldi,et al.  Primitive New Ants in Cretaceous Amber from Myanmar, New Jersey, and Canada (Hymenoptera: Formicidae) , 2005 .

[5]  C. Peeters,et al.  Worker reproduction in the ponerine ant Ophthalmopone berthoudi: an alternative form of eusocial organization , 1985, Behavioral Ecology and Sociobiology.

[6]  Edward O Wilson,et al.  The rise of the ants: a phylogenetic and ecological explanation. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[7]  A. Rasnitsyn,et al.  The first Late Cretaceous ants (Hymenoptera: Formicidae) from southern Africa, with comments on the origin of the Myrmicinae , 2004 .

[8]  R. Crozier,et al.  The reproductive cycle of the queenless ant pristoMyrmex pungens , 1984, Insectes Sociaux.

[9]  A. Rodrigo,et al.  Likelihood-based tests of topologies in phylogenetics. , 2000, Systematic biology.

[10]  J. Bergsten.  A review of long‐branch attraction , 2005, Cladistics : the international journal of the Willi Hennig Society.

[11]  Hidetoshi Shimodaira,et al.  Multiple Comparisons of Log-Likelihoods with Applications to Phylogenetic Inference , 1999, Molecular Biology and Evolution.

[12]  D. Grimaldi,et al.  Fossiliferous Cretaceous Amber from Myanmar (Burma): Its Rediscovery, Biotic Diversity, and Paleontological Significance , 2002 .

[13]  W. Gotwald,et al.  Taxonomy and Biology of a New West African Ant Belonging to the Genus Amblyopone (Hymenoptera: Formicidae) , 1972 .

[14]  B. Bolton.  The higher classification of the ant subfamily Leptanillinae (Hymenoptera: Formicidae) , 1990 .

[15]  John P. Huelsenbeck,et al.  MRBAYES: Bayesian inference of phylogenetic trees , 2001, Bioinform..

[16]  K. Masuko.  Behavior and ecology of the enigmatic antLeptanilla japonica Baroni Urbani (Hymenoptera: Formicidae: Leptanillinae) , 1990, Insectes Sociaux.

[17]  C. Beaulieu.  The oldest ant in the Lower Cretaceous amber of Charente-Maritime (SW France) (Insecta: Hymenoptera: Formicidae) , 2004 .

[18]  E. Wilson.  Ants From the Cretaceous and Eocene Amber of North America , 1985 .

[19]  B. Fisher,et al.  Dracula ant phylogeny as inferred by nuclear 28S rDNA sequences and implications for ant systematics (Hymenoptera: Formicidae: Amblyoponinae). , 2004, Molecular phylogenetics and evolution.

[20]  E. Wilson,et al.  The First Mesozoic Ants , 1967, Science.

[21]  G. Dlussky.  Ants (Hymenoptera: Formicidae) from Burmese Amber , 1996 .

[22]  E. Wilson,et al.  The First Mesozoic Ants, with the Description of a New Subfamily , 1967 .

[23]  P. S. Ward,et al.  The internal phylogeny of ants (Hymenoptera: Formicidae) , 1992 .

[24]  Jeremy M. Brown,et al.  The importance of data partitioning and the utility of Bayes factors in Bayesian phylogenetics. , 2007, Systematic biology.

[25]  P. S. Ward.  Phylogeny, classification, and species-level taxonomy of ants (Hymenoptera: Formicidae)* , 2007 .

[26]  W. L. Brown.  Remarks on the internal phylogeny and subfamily classification of the familyFormicidae , 1954, Insectes Sociaux.

[27]  B. Fisher,et al.  Molecular systematics of basal subfamilies of ants using 28S rRNA (Hymenoptera: Formicidae). , 2006, Molecular phylogenetics and evolution.

[28]  B. Bolton.  Synopsis and classification of Formicidae , 2003 .

[29]  E. Wilson.  The Insect Societies , 1974 .

[30]  D. Grimaldi,et al.  A formicine in New Jersey cretaceous amber (Hymenoptera: formicidae) and early evolution of the ants. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[31]  Derrick J. Zwickl.  Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion , 2006 .

[32]  James M. Carpenter,et al.  New and rediscovered primitive ants (Hymenoptera: Formicidae) in Cretaceous amber from New Jersey, and their phylogenetic relationships , 1997 .

[33]  E. J. Fittkau,et al.  On biomass and trophic structure of the central Amazonian rain forest ecosystem , 1973 .

[34]  Brian L. Fisher,et al.  Evaluating alternative hypotheses for the early evolution and diversification of ants , 2006, Proceedings of the National Academy of Sciences.

[35]  P. S. Ward.  The ant subfamily Pseudomyrmecinae (Hymenoptera: Formicidae): generic revision and relationship to other formicids , 1990 .

[36]  J. Huelsenbeck,et al.  Bayesian phylogenetic analysis of combined data. , 2004, Systematic biology.

[37]  R. Matthews,et al.  Ants. , 1898, Science.

[38]  Insemination controls the reproductive division of labour in a ponerine ant , 2004, Naturwissenschaften.

[39]  P. S. Ward.  Adetomyrma, an enigmatic new ant genus from Madagascar (Hymenoptera: Formicidae), and its implications for ant phylogeny , 1994 .

[40]  Robert W. Taylor,et al.  Nothomyrmecia macrops: A Living-Fossil Ant Rediscovered , 1978, Science.

[41]  S. Lacau,et al.  Fossil evidence for the early ant evolution , 2008, Naturwissenschaften.

[42]  Piotr Naskrecki,et al.  Bolton's Catalogue of Ants of the World: 1758-2005 , 1995 .

[43]  C. Moreau,et al.  Phylogeny of the Ants: Diversification in the Age of Angiosperms , 2006, Science.

[44]  Jeremy M. Brown,et al.  PuMA: Bayesian analysis of partitioned (and unpartitioned) model adequacy , 2009, Bioinform..