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      Phylogenomic analysis of Apoidea sheds new light on the sister group of bees

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          Apoid wasps and bees (Apoidea) are an ecologically and morphologically diverse group of Hymenoptera, with some species of bees having evolved eusocial societies. Major problems for our understanding of the evolutionary history of Apoidea have been the difficulty to trace the phylogenetic origin and to reliably estimate the geological age of bees. To address these issues, we compiled a comprehensive phylogenomic dataset by simultaneously analyzing target DNA enrichment and transcriptomic sequence data, comprising 195 single-copy protein-coding genes and covering all major lineages of apoid wasps and bee families.


          Our compiled data matrix comprised 284,607 nucleotide sites that we phylogenetically analyzed by applying a combination of domain- and codon-based partitioning schemes. The inferred results confirm the polyphyletic status of the former family “Crabronidae”, which comprises nine major monophyletic lineages. We found the former subfamily Pemphredoninae to be polyphyletic, comprising three distantly related clades. One of them, Ammoplanina, constituted the sister group of bees in all our analyses. We estimate the origin of bees to be in the Early Cretaceous (ca. 128 million years ago), a time period during which angiosperms rapidly radiated. Finally, our phylogenetic analyses revealed that within the Apoidea, (eu)social societies evolved exclusively in a single clade that comprises pemphredonine and philanthine wasps as well as bees.


          By combining transcriptomic sequences with those obtained via target DNA enrichment, we were able to include an unprecedented large number of apoid wasps in a phylogenetic study for tracing the phylogenetic origin of bees. Our results confirm the polyphyletic nature of the former wasp family Crabonidae, which we here suggest splitting into eight families. Of these, the family Ammoplanidae possibly represents the extant sister lineage of bees. Species of Ammoplanidae are known to hunt thrips, of which some aggregate on flowers and feed on pollen. The specific biology of Ammoplanidae as predators indicates how the transition from a predatory to pollen-collecting life style could have taken place in the evolution of bees. This insight plus the finding that (eu)social societies evolved exclusively in a single subordinated lineage of apoid wasps provides new perspectives for future comparative studies.

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          The online version of this article (10.1186/s12862-018-1155-8) contains supplementary material, which is available to authorized users.

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          Most cited references 82

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          MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability

          We report a major update of the MAFFT multiple sequence alignment program. This version has several new features, including options for adding unaligned sequences into an existing alignment, adjustment of direction in nucleotide alignment, constrained alignment and parallel processing, which were implemented after the previous major update. This report shows actual examples to explain how these features work, alone and in combination. Some examples incorrectly aligned by MAFFT are also shown to clarify its limitations. We discuss how to avoid misalignments, and our ongoing efforts to overcome such limitations.
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            RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies

            Motivation: Phylogenies are increasingly used in all fields of medical and biological research. Moreover, because of the next-generation sequencing revolution, datasets used for conducting phylogenetic analyses grow at an unprecedented pace. RAxML (Randomized Axelerated Maximum Likelihood) is a popular program for phylogenetic analyses of large datasets under maximum likelihood. Since the last RAxML paper in 2006, it has been continuously maintained and extended to accommodate the increasingly growing input datasets and to serve the needs of the user community. Results: I present some of the most notable new features and extensions of RAxML, such as a substantial extension of substitution models and supported data types, the introduction of SSE3, AVX and AVX2 vector intrinsics, techniques for reducing the memory requirements of the code and a plethora of operations for conducting post-analyses on sets of trees. In addition, an up-to-date 50-page user manual covering all new RAxML options is available. Availability and implementation: The code is available under GNU GPL at https://github.com/stamatak/standard-RAxML. Contact: alexandros.stamatakis@h-its.org Supplementary information: Supplementary data are available at Bioinformatics online.
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              PAML 4: phylogenetic analysis by maximum likelihood.

               Ziheng Yang (2007)
              PAML, currently in version 4, is a package of programs for phylogenetic analyses of DNA and protein sequences using maximum likelihood (ML). The programs may be used to compare and test phylogenetic trees, but their main strengths lie in the rich repertoire of evolutionary models implemented, which can be used to estimate parameters in models of sequence evolution and to test interesting biological hypotheses. Uses of the programs include estimation of synonymous and nonsynonymous rates (d(N) and d(S)) between two protein-coding DNA sequences, inference of positive Darwinian selection through phylogenetic comparison of protein-coding genes, reconstruction of ancestral genes and proteins for molecular restoration studies of extinct life forms, combined analysis of heterogeneous data sets from multiple gene loci, and estimation of species divergence times incorporating uncertainties in fossil calibrations. This note discusses some of the major applications of the package, which includes example data sets to demonstrate their use. The package is written in ANSI C, and runs under Windows, Mac OSX, and UNIX systems. It is available at -- (http://abacus.gene.ucl.ac.uk/software/paml.html).

                Author and article information

                BMC Evol Biol
                BMC Evol. Biol
                BMC Evolutionary Biology
                BioMed Central (London )
                18 May 2018
                18 May 2018
                : 18
                [1 ]ISNI 0000 0001 2293 9957, GRID grid.422371.1, Museum für Naturkunde, Leibniz Institute for Evolution and Biodiversity Science, ; Invalidenstraße 43, 10115 Berlin, Germany
                [2 ]ISNI 0000 0001 2216 5875, GRID grid.452935.c, Center for Molecular Biodiversity Research, Zoological Research Museum Alexander Koenig, ; Adenauerallee 160, 53113 Bonn, Germany
                [3 ]GRID grid.5963.9, University of Freiburg, Institute of Biology I (Zoology), Evolutionary Biology and Animal Ecology, ; Hauptstr. 1, 79104 Freiburg, Germany
                [4 ]ISNI 0000 0001 2216 5875, GRID grid.452935.c, Center of Taxonomy and Evolutionary Research, Arthropoda Department, Zoological Research Museum Alexander Koenig, ; Adenauerallee 160, 53113 Bonn, Germany
                [5 ]ISNI 0000 0001 2275 2842, GRID grid.424699.4, HITS gGmbH, Heidelberg Institute for Theoretical Studies, ; Schloss-Wolfsbrunnenweg 35, 69118 Heidelberg, Germany
                [6 ]ISNI 0000 0001 2364 4210, GRID grid.7450.6, Georg-August-Universität Göttingen, Animal Evolution and Biodiversity, ; Untere Karspüle 2, 37073 Göttingen, Germany
                [7 ]GRID grid.421064.5, German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, ; Deutscher Platz 5e, 04103 Leipzig, Germany
                © The Author(s). 2018

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. 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.

                Funded by: FundRef http://dx.doi.org/10.13039/501100001659, Deutsche Forschungsgemeinschaft;
                Award ID: OH81/9-1
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                Research Article
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                © The Author(s) 2018


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