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

Abstract Background 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 phyl...

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Main Authors: Manuela Sann, Oliver Niehuis, Ralph S. Peters, Christoph Mayer, Alexey Kozlov, Lars Podsiadlowski, Sarah Bank, Karen Meusemann, Bernhard Misof, Christoph Bleidorn, Michael Ohl
Format: Article
Language:English
Published: BMC 2018-05-01
Series:BMC Evolutionary Biology
Subjects:
Online Access:http://link.springer.com/article/10.1186/s12862-018-1155-8
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spelling doaj-6d6fd0fbb92c41ccafaa607b569f31272021-09-02T08:28:14ZengBMCBMC Evolutionary Biology1471-21482018-05-0118111510.1186/s12862-018-1155-8Phylogenomic analysis of Apoidea sheds new light on the sister group of beesManuela Sann0Oliver Niehuis1Ralph S. Peters2Christoph Mayer3Alexey Kozlov4Lars Podsiadlowski5Sarah Bank6Karen Meusemann7Bernhard Misof8Christoph Bleidorn9Michael Ohl10Museum für Naturkunde, Leibniz Institute for Evolution and Biodiversity ScienceCenter for Molecular Biodiversity Research, Zoological Research Museum Alexander KoenigCenter of Taxonomy and Evolutionary Research, Arthropoda Department, Zoological Research Museum Alexander KoenigCenter for Molecular Biodiversity Research, Zoological Research Museum Alexander KoenigHITS gGmbH, Heidelberg Institute for Theoretical StudiesCenter for Molecular Biodiversity Research, Zoological Research Museum Alexander KoenigGeorg-August-Universität Göttingen, Animal Evolution and BiodiversityCenter for Molecular Biodiversity Research, Zoological Research Museum Alexander KoenigCenter for Molecular Biodiversity Research, Zoological Research Museum Alexander KoenigGeorg-August-Universität Göttingen, Animal Evolution and BiodiversityMuseum für Naturkunde, Leibniz Institute for Evolution and Biodiversity ScienceAbstract Background 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. Results 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. Conclusion 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.http://link.springer.com/article/10.1186/s12862-018-1155-8HymenopteraAculeataApoideaApoid waspsBeesAnthophila
collection DOAJ
language English
format Article
sources DOAJ
author Manuela Sann
Oliver Niehuis
Ralph S. Peters
Christoph Mayer
Alexey Kozlov
Lars Podsiadlowski
Sarah Bank
Karen Meusemann
Bernhard Misof
Christoph Bleidorn
Michael Ohl
spellingShingle Manuela Sann
Oliver Niehuis
Ralph S. Peters
Christoph Mayer
Alexey Kozlov
Lars Podsiadlowski
Sarah Bank
Karen Meusemann
Bernhard Misof
Christoph Bleidorn
Michael Ohl
Phylogenomic analysis of Apoidea sheds new light on the sister group of bees
BMC Evolutionary Biology
Hymenoptera
Aculeata
Apoidea
Apoid wasps
Bees
Anthophila
author_facet Manuela Sann
Oliver Niehuis
Ralph S. Peters
Christoph Mayer
Alexey Kozlov
Lars Podsiadlowski
Sarah Bank
Karen Meusemann
Bernhard Misof
Christoph Bleidorn
Michael Ohl
author_sort Manuela Sann
title Phylogenomic analysis of Apoidea sheds new light on the sister group of bees
title_short Phylogenomic analysis of Apoidea sheds new light on the sister group of bees
title_full Phylogenomic analysis of Apoidea sheds new light on the sister group of bees
title_fullStr Phylogenomic analysis of Apoidea sheds new light on the sister group of bees
title_full_unstemmed Phylogenomic analysis of Apoidea sheds new light on the sister group of bees
title_sort phylogenomic analysis of apoidea sheds new light on the sister group of bees
publisher BMC
series BMC Evolutionary Biology
issn 1471-2148
publishDate 2018-05-01
description Abstract Background 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. Results 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. Conclusion 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.
topic Hymenoptera
Aculeata
Apoidea
Apoid wasps
Bees
Anthophila
url http://link.springer.com/article/10.1186/s12862-018-1155-8
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