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      The rise of army ants and their relatives: diversification of specialized predatory doryline ants

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          Abstract

          Background

          Army ants are dominant invertebrate predators in tropical and subtropical terrestrial ecosystems. Their close relatives within the dorylomorph group of ants are also highly specialized predators, although much less is known about their biology. We analyzed molecular data generated from 11 nuclear genes to infer a phylogeny for the major dorylomorph lineages, and incorporated fossil evidence to infer divergence times under a relaxed molecular clock.

          Results

          Because our results indicate that one subfamily and several genera of dorylomorphs are non-monophyletic, we propose to subsume the six previous dorylomorph subfamilies into a single subfamily, Dorylinae. We find the monophyly of Dorylinae to be strongly supported and estimate the crown age of the group at 87 (74–101) million years. Our phylogenetic analyses provide only weak support for army ant monophyly and also call into question a previous hypothesis that army ants underwent a fundamental split into New World and Old World lineages. Outside the army ants, our phylogeny reveals for the first time many old, distinct lineages in the Dorylinae. The genus Cerapachys is shown to be non-monophyletic and comprised of multiple lineages scattered across the Dorylinae tree. We recover, with strong support, novel relationships among these Cerapachys-like clades and other doryline genera, but divergences in the deepest parts of the tree are not well resolved. We find the genus Sphinctomyrmex, characterized by distinctive abdominal constrictions, to consist of two separate lineages with convergent morphologies, one inhabiting the Old World and the other the New World tropics.

          Conclusions

          While we obtain good resolution in many parts of the Dorylinae phylogeny, relationships deep in the tree remain unresolved, with major lineages joining each other in various ways depending upon the analytical method employed, but always with short internodes. This may be indicative of rapid radiation in the early history of the Dorylinae, but additional molecular data and more complete species sampling are needed for confirmation. Our phylogeny now provides a basic framework for comparative biological analyses, but much additional study on the behavior and morphology of doryline species is needed, especially investigations directed at the non-army ant taxa.

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          Most cited references 37

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          Bayesian selection of continuous-time Markov chain evolutionary models.

          We develop a reversible jump Markov chain Monte Carlo approach to estimating the posterior distribution of phylogenies based on aligned DNA/RNA sequences under several hierarchical evolutionary models. Using a proper, yet nontruncated and uninformative prior, we demonstrate the advantages of the Bayesian approach to hypothesis testing and estimation in phylogenetics by comparing different models for the infinitesimal rates of change among nucleotides, for the number of rate classes, and for the relationships among branch lengths. We compare the relative probabilities of these models and the appropriateness of a molecular clock using Bayes factors. Our most general model, first proposed by Tamura and Nei, parameterizes the infinitesimal change probabilities among nucleotides (A, G, C, T/U) into six parameters, consisting of three parameters for the nucleotide stationary distribution, two rate parameters for nucleotide transitions, and another parameter for nucleotide transversions. Nested models include the Hasegawa, Kishino, and Yano model with equal transition rates and the Kimura model with a uniform stationary distribution and equal transition rates. To illustrate our methods, we examine simulated data, 16S rRNA sequences from 15 contemporary eubacteria, halobacteria, eocytes, and eukaryotes, 9 primates, and the entire HIV genome of 11 isolates. We find that the Kimura model is too restrictive, that the Hasegawa, Kishino, and Yano model can be rejected for some data sets, that there is evidence for more than one rate class and a molecular clock among similar taxa, and that a molecular clock can be rejected for more distantly related taxa.
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            A Total-Evidence Approach to Dating with Fossils, Applied to the Early Radiation of the Hymenoptera

            Phylogenies are usually dated by calibrating interior nodes against the fossil record. This relies on indirect methods that, in the worst case, misrepresent the fossil information. Here, we contrast such node dating with an approach that includes fossils along with the extant taxa in a Bayesian total-evidence analysis. As a test case, we focus on the early radiation of the Hymenoptera, mostly documented by poorly preserved impression fossils that are difficult to place phylogenetically. Specifically, we compare node dating using nine calibration points derived from the fossil record with total-evidence dating based on 343 morphological characters scored for 45 fossil (4--20 complete) and 68 extant taxa. In both cases we use molecular data from seven markers (∼5 kb) for the extant taxa. Because it is difficult to model speciation, extinction, sampling, and fossil preservation realistically, we develop a simple uniform prior for clock trees with fossils, and we use relaxed clock models to accommodate rate variation across the tree. Despite considerable uncertainty in the placement of most fossils, we find that they contribute significantly to the estimation of divergence times in the total-evidence analysis. In particular, the posterior distributions on divergence times are less sensitive to prior assumptions and tend to be more precise than in node dating. The total-evidence analysis also shows that four of the seven Hymenoptera calibration points used in node dating are likely to be based on erroneous or doubtful assumptions about the fossil placement. With respect to the early radiation of Hymenoptera, our results suggest that the crown group dates back to the Carboniferous, ∼309 Ma (95% interval: 291--347 Ma), and diversified into major extant lineages much earlier than previously thought, well before the Triassic. [Bayesian inference; fossil dating; morphological evolution; relaxed clock; statistical phylogenetics.]
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              Phylogeny of the ants: diversification in the age of angiosperms.

               C. Moreau (2006)
              We present a large-scale molecular phylogeny of the ants (Hymenoptera: Formicidae), based on 4.5 kilobases of sequence data from six gene regions extracted from 139 of the 288 described extant genera, representing 19 of the 20 subfamilies. All but two subfamilies are recovered as monophyletic. Divergence time estimates calibrated by minimum age constraints from 43 fossils indicate that most of the subfamilies representing extant ants arose much earlier than previously proposed but only began to diversify during the Late Cretaceous to Early Eocene. This period also witnessed the rise of angiosperms and most herbivorous insects.
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                Author and article information

                Contributors
                Journal
                BMC Evol Biol
                BMC Evol. Biol
                BMC Evolutionary Biology
                BioMed Central
                1471-2148
                2014
                1 May 2014
                : 14
                : 93
                Affiliations
                [1 ]Department of Entomology, National Museum of Natural History, Smithsonian Institution, Washington, D.C., USA
                [2 ]Department of Entomology, California Academy of Sciences, San Francisco, CA, USA
                [3 ]Department of Entomology and Nematology, University of California, Davis, CA, USA
                Article
                1471-2148-14-93
                10.1186/1471-2148-14-93
                4021219
                Copyright © 2014 Brady et al.; licensee BioMed Central Ltd.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                Categories
                Research Article

                Evolutionary Biology

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