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      A DNA and morphology based phylogenetic framework of the ant genus Lasius with hypotheses for the evolution of social parasitism and fungiculture

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          Abstract

          Background

          Ants of the genus Lasius are ecologically important and an important system for evolutionary research. Progress in evolutionary research has been hindered by the lack of a well-founded phylogeny of the subgenera, with three previous attempts disagreeing. Here we employed two mitochondrial genes ( cytochrome c oxidase subunit I, 16S ribosomal RNA), comprising 1,265 bp, together with 64 morphological characters, to recover the phylogeny of Lasius by Bayesian and Maximum Parsimony inference after exploration of potential causes of phylogenetic distortion. We use the resulting framework to infer evolutionary pathways for social parasitism and fungiculture.

          Results

          We recovered two well supported major lineages. One includes Acanthomyops, Austrolasius, Chthonolasius, and Lasius pallitarsis, which we confirm to represent a seventh subgenus, the other clade contains Dendrolasius, and Lasius sensu stricto. The subgenus Cautolasius, displaying neither social parasitism nor fungiculture, probably belongs to the second clade, but its phylogenetic position is not resolved at the cutoff values of node support we apply. Possible causes for previous problems with reconstructing the Lasius phylogeny include use of other reconstruction techniques, possibly more prone to instabilities in some instances, and the inclusion of phylogenetically distorting characters.

          Conclusion

          By establishing an updated phylogenetic framework, our study provides the basis for a later formal taxonomic revision of subgenera and for studying the evolution of various ecologically and sociobiologically relevant traits of Lasius, although there is need for future studies to include nuclear genes and additional samples from the Nearctic. Both social parasitism and fungiculture evolved twice in Lasius, once in each major lineage, which opens up new opportunities for comparative analyses. The repeated evolution of social parasitism has been established for other groups of ants, though not for temporary social parasitism as found in Lasius. For fungiculture, the independent emergence twice in a monophyletic group marks a novel scenario in ants. We present alternative hypotheses for the evolution of both traits, with one of each involving loss of the trait. Though less likely for both traits than later evolution without reversal, we consider reversal as sufficiently plausible to merit independent testing.

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          Most cited references108

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          Bayesian phylogenetic analysis of combined data.

          The recent development of Bayesian phylogenetic inference using Markov chain Monte Carlo (MCMC) techniques has facilitated the exploration of parameter-rich evolutionary models. At the same time, stochastic models have become more realistic (and complex) and have been extended to new types of data, such as morphology. Based on this foundation, we developed a Bayesian MCMC approach to the analysis of combined data sets and explored its utility in inferring relationships among gall wasps based on data from morphology and four genes (nuclear and mitochondrial, ribosomal and protein coding). Examined models range in complexity from those recognizing only a morphological and a molecular partition to those having complex substitution models with independent parameters for each gene. Bayesian MCMC analysis deals efficiently with complex models: convergence occurs faster and more predictably for complex models, mixing is adequate for all parameters even under very complex models, and the parameter update cycle is virtually unaffected by model partitioning across sites. Morphology contributed only 5% of the characters in the data set but nevertheless influenced the combined-data tree, supporting the utility of morphological data in multigene analyses. We used Bayesian criteria (Bayes factors) to show that process heterogeneity across data partitions is a significant model component, although not as important as among-site rate variation. More complex evolutionary models are associated with more topological uncertainty and less conflict between morphology and molecules. Bayes factors sometimes favor simpler models over considerably more parameter-rich models, but the best model overall is also the most complex and Bayes factors do not support exclusion of apparently weak parameters from this model. Thus, Bayes factors appear to be useful for selecting among complex models, but it is still unclear whether their use strikes a reasonable balance between model complexity and error in parameter estimates.
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            Inconsistency of phylogenetic estimates from concatenated data under coalescence.

            Although multiple gene sequences are becoming increasingly available for molecular phylogenetic inference, the analysis of such data has largely relied on inference methods designed for single genes. One of the common approaches to analyzing data from multiple genes is concatenation of the individual gene data to form a single supergene to which traditional phylogenetic inference procedures - e.g., maximum parsimony (MP) or maximum likelihood (ML) - are applied. Recent empirical studies have demonstrated that concatenation of sequences from multiple genes prior to phylogenetic analysis often results in inference of a single, well-supported phylogeny. Theoretical work, however, has shown that the coalescent can produce substantial variation in single-gene histories. Using simulation, we combine these ideas to examine the performance of the concatenation approach under conditions in which the coalescent produces a high level of discord among individual gene trees and show that it leads to statistically inconsistent estimation in this setting. Furthermore, use of the bootstrap to measure support for the inferred phylogeny can result in moderate to strong support for an incorrect tree under these conditions. These results highlight the importance of incorporating variation in gene histories into multilocus phylogenetics.
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              Stochastic mapping of morphological characters.

              Many questions in evolutionary biology are best addressed by comparing traits in different species. Often such studies involve mapping characters on phylogenetic trees. Mapping characters on trees allows the nature, number, and timing of the transformations to be identified. The parsimony method is the only method available for mapping morphological characters on phylogenies. Although the parsimony method often makes reasonable reconstructions of the history of a character, it has a number of limitations. These limitations include the inability to consider more than a single change along a branch on a tree and the uncoupling of evolutionary time from amount of character change. We extended a method described by Nielsen (2002, Syst. Biol. 51:729-739) to the mapping of morphological characters under continuous-time Markov models and demonstrate here the utility of the method for mapping characters on trees and for identifying character correlation.
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                Author and article information

                Journal
                BMC Evol Biol
                BMC Evolutionary Biology
                BioMed Central
                1471-2148
                2008
                19 August 2008
                : 8
                : 237
                Affiliations
                [1 ]Department of Zoology, National Science Museum, Hyakunin-chô 3-23-1, Shinjuku-ku, Tokyo 169-0073, Japan
                [2 ]Department of Zoology, Field Musem of Natural History, 1400 South Lake Shore Drive, Chicago IL 60605-2496, USA
                [3 ]Institute of Zoology, Department of Integrative Biology and Biodiversity Research, Boku, University of Natural Resources and Applied Life Sciences Vienna, 1180 Vienna, Austria
                [4 ]Institute of Forest Entomology, Forest Pathology and Forest Protection, Department of Forest and Soil Sciences, Boku, University of Natural Resources and Applied Life Sciences Vienna, 1190 Vienna, Austria
                [5 ]School of Marine and Tropical Biology, James Cook University, Townsville, Queensland 4811, Australia
                [6 ]Laboratory of Insect Behavior, National Institute of Agrobiological Sciences, Ôwasi 1-2, Tsukuba-shi 305-8634, Japan
                Article
                1471-2148-8-237
                10.1186/1471-2148-8-237
                2542377
                18710580
                8aea913f-759e-4bcc-aecc-c95550b90ef0
                Copyright © 2008 Maruyama 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 cited.

                History
                : 18 December 2007
                : 19 August 2008
                Categories
                Research Article

                Evolutionary Biology
                Evolutionary Biology

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