Evolutionary History of the Hymenoptera.
Hymenoptera (sawflies, wasps, ants, and bees) are one of four mega-diverse insect orders, comprising more than 153,000 described and possibly up to one million undescribed extant species [1, 2]. As parasitoids, predators, and pollinators, Hymenoptera play a fundamental role in virtually all terrestrial ecosystems and are of substantial economic importance [1, 3]. To understand the diversification and key evolutionary transitions of Hymenoptera, most notably from phytophagy to parasitoidism and predation (and vice versa) and from solitary to eusocial life, we inferred the phylogeny and divergence times of all major lineages of Hymenoptera by analyzing 3,256 protein-coding genes in 173 insect species. Our analyses suggest that extant Hymenoptera started to diversify around 281 million years ago (mya). The primarily ectophytophagous sawflies are found to be monophyletic. The species-rich lineages of parasitoid wasps constitute a monophyletic group as well. The little-known, species-poor Trigonaloidea are identified as the sister group of the stinging wasps (Aculeata). Finally, we located the evolutionary root of bees within the apoid wasp family "Crabronidae." Our results reveal that the extant sawfly diversity is largely the result of a previously unrecognized major radiation of phytophagous Hymenoptera that did not lead to wood-dwelling and parasitoidism. They also confirm that all primarily parasitoid wasps are descendants of a single endophytic parasitoid ancestor that lived around 247 mya. Our findings provide the basis for a natural classification of Hymenoptera and allow for future comparative analyses of Hymenoptera, including their genomes, morphology, venoms, and parasitoid and eusocial life styles.
Center of Taxonomy and Evolutionary Research, Arthropoda Department, Zoologisches Forschungsmuseum Alexander Koenig, 53113 Bonn, Germany. Electronic address: r.peters@leibniz-zfmk.de.
Ralph S
RS
Peters
Entomologie, Staatliches Museum für Naturkunde Stuttgart, 70191 Stuttgart, Germany.
Lars
L
Krogmann
Center for Molecular Biodiversity Research, Zoologisches Forschungsmuseum Alexander Koenig, 53113 Bonn, Germany.
Christoph
C
Mayer
Center for Molecular Biodiversity Research, Zoologisches Forschungsmuseum Alexander Koenig, 53113 Bonn, Germany.
Alexander
A
Donath
Steinmann Institut für Geologie, Mineralogie und Paläontologie, 53115 Bonn, Germany.
Simon
S
Gunkel
Center for Molecular Biodiversity Research, Zoologisches Forschungsmuseum Alexander Koenig, 53113 Bonn, Germany; Department of Evolutionary Biology and Ecology, Institute for Biology I (Zoology), University of Freiburg, 79104 Freiburg (Brsg.), Germany; Australian National Insect Collection, CSIRO National Research Collections Australia (NRCA), Acton, ACT 2601, Australia.
Karen
K
Meusemann
Scientific Computing Group, Heidelberg Institute for Theoretical Studies, 69118 Heidelberg, Germany.
Alexey
A
Kozlov
Institute of Evolutionary Biology and Ecology, University of Bonn, 53121 Bonn, Germany.
Lars
L
Podsiadlowski
Center for Molecular Biodiversity Research, Zoologisches Forschungsmuseum Alexander Koenig, 53113 Bonn, Germany.
Malte
M
Petersen
Ecology, Evolution and Genetics, Research School of Biology, Australian National University, Canberra, ACT 2601, Australia; School of Biological Sciences, Macquarie University, Sydney, NSW 2109, Australia.
Robert
R
Lanfear
Centro de Investigaciones y Transferencia de Catamarca, CITCA-CONICET/UNCA, 4700 Catamarca, Argentina.
Patricia A
PA
Diez
Department of Entomology, University of California, Riverside, Riverside, CA 92521, USA.
John
J
Heraty
Department of Biological Sciences, Rutgers University, Newark, NJ 07102, USA.
Karl M
KM
Kjer
Naturhistorisches Museum der Burgergemeinde Bern, 3005 Bern, Switzerland.
Seraina
S
Klopfstein
Department of Biological Sciences and Lee Kong Chian Natural History Museum, National University of Singapore, Singapore 117543, Singapore.
Rudolf
R
Meier
Instituto de Ciencias Ambientales (ICAM), Universidad de Castilla-La Mancha, 45071 Toledo, Spain.
Carlo
C
Polidori
Department of Animal Ecology and Tropical Biology, University of Würzburg, 97074 Würzburg, Germany.
Thomas
T
Schmitt
China National GeneBank-Shenzhen, BGI-Shenzhen, Shenzhen, Guangdong Province, 518083, People's Republic of China; BGI-Shenzhen, Shenzhen, Guangdong Province, 518083, People's Republic of China; Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, Øster Voldgade 5-7, 1350 Copenhagen, Denmark.
Shanlin
S
Liu
Beijing Advanced Innovation Center for Food Nutrition and Human Health, China Agricultural University, Beijing 100193, People's Republic of China; Department of Entomology, China Agricultural University, Beijing 100193, People's Republic of China.
Xin
X
Zhou
Steinmann Institut für Geologie, Mineralogie und Paläontologie, 53115 Bonn, Germany.
Torsten
T
Wappler
Steinmann Institut für Geologie, Mineralogie und Paläontologie, 53115 Bonn, Germany.
Jes
J
Rust
Center for Molecular Biodiversity Research, Zoologisches Forschungsmuseum Alexander Koenig, 53113 Bonn, Germany.
Bernhard
B
Misof
Center for Molecular Biodiversity Research, Zoologisches Forschungsmuseum Alexander Koenig, 53113 Bonn, Germany; Department of Evolutionary Biology and Ecology, Institute for Biology I (Zoology), University of Freiburg, 79104 Freiburg (Brsg.), Germany; School of Life Sciences, Arizona State University, Tempe, AZ 85287, USA. Electronic address: oliver.niehuis@biologie.uni-freiburg.de.
Oliver
O
Niehuis
D000818:Animals; D005075:Biological Evolution; D006927:Hymenoptera / Q000145:classification* / Q000235:genetics / Q000502:physiology; D019476:Insect Proteins / Q000235:genetics*; D010802:Phylogeny
D019476:Insect Proteins
Hymenoptera; RNA-seq; evolution; herbivory; life history; molecular dating; parasitoidism; phylogenomics; phylogeny; transcriptomes