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      Transcriptome sequence-based phylogeny of chalcidoid wasps (Hymenoptera: Chalcidoidea) reveals a history of rapid radiations, convergence, and evolutionary success.

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          Abstract

          Chalcidoidea are a megadiverse group of mostly parasitoid wasps of major ecological and economical importance that are omnipresent in almost all extant terrestrial habitats. The timing and pattern of chalcidoid diversification is so far poorly understood and has left many important questions on the evolutionary history of Chalcidoidea unanswered. In this study, we infer the early divergence events within Chalcidoidea and address the question of whether or not ancestral chalcidoids were small egg parasitoids. We also trace the evolution of some key traits: jumping ability, development of enlarged hind femora, and associations with figs. Our phylogenetic inference is based on the analysis of 3,239 single-copy genes across 48 chalcidoid wasps and outgroups representatives. We applied an innovative a posteriori evaluation approach to molecular clock-dating based on nine carefully validated fossils, resulting in the first molecular clock-based estimation of deep Chalcidoidea divergence times. Our results suggest a late Jurassic origin of Chalcidoidea, with a first divergence of morphologically and biologically distinct groups in the early to mid Cretaceous, between 129 and 81 million years ago (mya). Diversification of most extant lineages happened rapidly after the Cretaceous in the early Paleogene, between 75 and 53 mya. The inferred Chalcidoidea tree suggests a transition from ancestral minute egg parasitoids to larger-bodied parasitoids of other host stages during the early history of chalcidoid evolution. The ability to jump evolved independently at least three times, namely in Eupelmidae, Encyrtidae, and Tanaostigmatidae. Furthermore, the large-bodied strongly sclerotized species with enlarged hind femora in Chalcididae and Leucospidae are not closely related. Finally, the close association of some chalcidoid wasps with figs, either as pollinators, or as inquilines/gallers or as parasitoids, likely evolved at least twice independently: in the Eocene, giving rise to fig pollinators, and in the Oligocene or Miocene, resulting in non-pollinating fig-wasps, including gallers and parasitoids. The origins of very speciose lineages (e.g., Mymaridae, Eulophidae, Pteromalinae) are evenly spread across the period of chalcidoid evolution from early Cretaceous to the late Eocene. Several shifts in biology and morphology (e.g., in host exploitation, body shape and size, life history), each followed by rapid radiations, have likely enabled the evolutionary success of Chalcidoidea.

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          Author and article information

          Journal
          Mol. Phylogenet. Evol.
          Molecular phylogenetics and evolution
          Elsevier BV
          1095-9513
          1055-7903
          Mar 2018
          : 120
          Affiliations
          [1 ] Center of Taxonomy and Evolutionary Research, Arthropoda Department, Zoologisches Forschungsmuseum Alexander Koenig, 53113 Bonn, Germany. Electronic address: r.peters@leibniz-zfmk.de.
          [2 ] 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.
          [3 ] Steinmann Institut für Geologie, Mineralogie und Paläontologie, 53115 Bonn, Germany.
          [4 ] Zoological Institute, University of Cologne, Zülpicher Straße 47b, 50674 Cologne, Germany.
          [5 ] Center for Molecular Biodiversity Research, Zoologisches Forschungsmuseum Alexander Koenig, 53113 Bonn, Germany.
          [6 ] Institute of Evolutionary Biology and Ecology, University of Bonn, 53121 Bonn, Germany.
          [7 ] Scientific Computing Group, Heidelberg Institute for Theoretical Studies, 69118 Heidelberg, Germany.
          [8 ] Department of Natural History, Iziko South African Museum, PO BOX 61, Cape Town 8000, South Africa.
          [9 ] 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.
          [10 ] 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.
          [11 ] Department of Entomology, University of California, Riverside, CA 92521, USA.
          [12 ] Entomologie, Staatliches Museum für Naturkunde Stuttgart, 70191 Stuttgart, Germany. Electronic address: lars.krogmann@smns-bw.de.
          Article
          S1055-7903(17)30336-6
          10.1016/j.ympev.2017.12.005
          29247847
          5fb1689c-0f01-4c90-aa9a-ec62842251b3
          History

          evolution,fig wasps,parasitoid wasps,Phylogenomics,biological shifts,egg parasitoids

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