The Phylogeny of Hexapoda and the Evolution of Megadiversity

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1 The Phylogeny of Hexapoda and the Evolution of Megadiversity ECE 2018 Napoli Rolf G. Beutel Institut für Spezielle Zoologie und Evolutionsbiologie Entomology Group, Phyletisches Museum

2 Diversity ca described species!!! Hexapoda

3 Pioneer studies in biodiversity research: Dr. T. L. Erwin Canopy fogging, Dr. T.L. Erwin, Smithsonian Institution, National Museum of Natural History ca estimated insect species!!! Stork et al. 2015: species

4 No climate change!!!

Milestone of insect systematics Insect Morphology Willi Hennig, 1913-1976 Grundzüge der

5 Milestone of insect systematics Insect Morphology Willi Hennig, Grundzüge der Theorie einer phylogenetischen Systematik (1950) Die Stammesgeschichte der Insekten (1969)

6 Phylogeny

7 Börner 1904 No consistent and well-defined phylogenetic methods

8 Haeckel 1896 Systematische Phylogenie der wirbellosen Thiere

INSECT PHYLOGENY FROM THE INITIATIVE Methods: Fresh tissue collected in RNAlater Sequenced 103 taxa at BGI Illumina HiSeq2000 250 bp insert-size libraries 150 bp paired-end sequencing ~2.

Nucleotide data modelled by sites Analyzed with RaxML light & ExaML Dates from partitioned BEAST Integration of Morphologists, Embryologists & Palaeontologists Results: 1478 Genes from OrthoDB were

9 INSECT PHYLOGENY FROM THE INITIATIVE Methods: Fresh tissue collected in RNAlater Sequenced 103 taxa at BGI Illumina HiSeq bp insert-size libraries 150 bp paired-end sequencing ~2.5Gb per taxon Assembled with SOAPdenovo-trans Orthology prediction with modified HaMStR Hidden Markov models from OrthoDB Alignment masking with Aliscore Amino acid data partitioned by domains Nucleotide data modelled by sites Analyzed with RaxML light & ExaML Dates from partitioned BEAST Integration of Morphologists, Embryologists & Palaeontologists Results: 1478 Genes from OrthoDB were shared among all taxa Average coverage: 98% of genes recovered from new taxa Results shown at the right - > Same tree from both nucleotide and amino acid analyses More to come: ~1000 new insect transcriptomes completed * Bernhard Misof 1 Shanlin Liu 2,3, Karen Meusemann 1,4, Ralph S. Peters 5, Christoph Mayer 1, Alexander Donath 1, Paul B. Frandsen 6, Jessica Ware 7, Rolf G. Beutel 8, Oliver Niehuis 1, Malte Petersen 1, Tomas Flouri 9, Fernando Izquierdo-Carrasco 9, Torsten Wappler 10, Jes Rust 10, Andre J. Aberer 9, Ulrike Aspöck Horst Aspöck 13, Alexander Blanke 1, Daniela Bartel 12, Simon Berger 9, Alexander Böhm 12, Thomas Buckley 14, Brett Calcott 15, Junqing Chen 3, Frank Friedrich 16, Makiko Fukui 17, Mari Fujita 18, Carola Greve 1, Peter Grobe 1, Shengchang Gu 3, Ying Huang 2,3, Lars S. Jermiin 19, Akito Y. Kawahara 20, Lars Krogmann 21, Martin Kubiak 16, Robert Lanfear 15,22, Harald Letsch 23, Yiyuan Li 2,3, Zhenyu Li 3, Jiguang Li 3, Haorong Lu 3, Ryuichiro Machida 18, Yuta Mashimo 18, Duane McKenna 24, Guanliang Meng 2,3, Yasutaka Nakagaki 18, José Luis Navarrete-Heredia 25, Michael Ott 26, Yanxiang Ou 3, Günther Pass 12, Lars Podsiadlowski 27, Hans Pohl 8, Björn M. v. Reumont 28, Kai Schütte 29, Kaoru Sekiya 18, Shota Shimizu 18, Adam Slipinski 4, Alexandros Stamatakis 9, 30, Wenhui Song 2,3, Xu Su 2,3, Nikolaus U. Szucsich 12, Meihua Tan 2,3, Xuemei Tan 3, Min Tang 2,3, Jingbo Tang 3, Gerald Timelthaler 12, Shigekazu Tomizuka 18, Michelle Trautwein 31, Xiaoli Tong 32, Toshiki Uchifune 18,33, Manfred Walzl 12, Brian Wiegmann 34, Jeanne Wilbrandt 1, Benjamin Wipfler 8, Thomas K. F. Wong 19, Qiong Wu 2,3, Gengxiong Wu 3, Yinlong Xie 3, Shenzhou Yang 2,3, Qing Yang 2,3, David K. Yeates 4, Kazunori Yoshizawa 35, Qing Zhang 2,3, Rui Zhang 2,3, Wenwei Zhang 3, Yunhui Zhang 3, Jing Zhao 2,3, Chengran Zhou 2,3, Lili Zhou 2,3, Tanja Ziesmann 1, Shijie Zou 3, Yingrui Li 3, Xun Xu 3, Yong Zhang 2,3, Huanming Yang 3, Jian Wang 3, Jun Wang 3,37,38,39,40,*, Karl M. Kjer 36,*, Xin Zhou 1,2,3,*, * = Speaker = Major contributor 1 Museum Koenig (ZFMK), Bonn, Germany 2 China National GeneBank, BGI-Shenzhen 3 BGI-Shenzhen, China 4 CSIRO,Canberra, Australia 5 Museum Koenig (ZFMK) 6 Rutgers University, New Brunswick, NJ 7 Rutgers University, Newark, NJ, USA, 8 FSU Jena, Phyletischem Museum Germany 9 Heidelberg Inst. for Theoretical Studies 10 Universität Bonn, Germany 11 Naturhistorisches Museum Wien, Austria 12 Universität Wien, Vienna, Austria 13 Medizinische Universität Wien, Vienna 14 Manaaki Whenua Landcare Research, Auckland, New Zealand 15 Johns Hopkins University, Baltimore, MD 16 Universität Hamburg, Germany 17 Ehime University, Japan 18 University of Tsukuba, Japan 19 CSIRO Canberra, ACT, Australia 20 University of Florida, Gainesville, FL 21 Staatliches Museum für Naturkunde Stuttgart 22 Australian National University, Canberra 23 University of Vienna, Austria 24 University of Memphis, TN 25 Universidad de Guadalajara, México 26 Leibniz Supercomputing, Garching, Germany 27 University of Bonn, Germany 28 The Natural History Museum, London 29 Universität Hamburg, Germany 30 Karlsruher Institut für Technologie, Germany 31 North Carolina Museum of Nat. Sci., Raleigh 32 South China Agricultural University 33 Yokosuka City Museum, Kanagawa, Japan 34 North Carolina State University, Raleigh, 35 Hokkaido University, Sapporo, Japan 36 Rutgers University, New Brunswick,NJ 37 University of Copenhagen, Denmark. 38 Abdulaziz University, Jeddah Saudi Arabia. 39 Macau University of Science & Tech., China 40 Dept. of Medicine, University of Hong Kong Misof et al. 2014

10 Tracheata (?): switch to terrestrial lifestyle in the Silurian (ca. 400 my) Tracheal system Malpighian tubules Spermatophores no aquatic larvae.

11 Arthropod phylogeny based on EST data Pancrustacea =Tetraconata Meusemann et al. 2010

12 Hexapoda + Remipedia? Brain anatomy (Fanenbruck et al. 2014)

13 Independent invasions of the terrestrial environment Remipedia ( 30 spp) in an evolutionary dead end street ) v. Reumont et al (also Misof et al. 2014)

14 Pancrustacea: independent invasion of terrestrial habitats by Hexapoda (1KITE: Ordovician, ca. 470 my ago) Terrestrial adapatations like the * tracheal system * Malpiphian tubules Sperm transfer via spermatophore Must have evolved independently (also in Arachnida) Even very plausible evolutionary scenario are only as good as the underlying phylogeny!!!

15 Devonohexapodus bocksbergiensis Haas et al. (2003)

16 Wingertshelicus backesi Kühl & Rust 2009

17 Monophyletic Hexapoda: 3 tagmata, head (6), thorax (3), abdomen (11) Division of labour in the postcepalic body

18 General rule: If a character has independently evolved in 2 non-related successful groups it has contributed to the diversification in both cases. Does not help in this case

19 Apterygote hexapods: 4 of 5 groups with a low species number

20 Pancrustacea (=Tetraconata) Additional apomorphies of Hexapoda: Tracheal system Malpighian tubules Sperm transfer with spermatophore No primary aquatic larva Relatively compact fat body Loss of nephridial organs Loss of midgut glands Loss of 2nd antenna..

21 Hennig (1969): Entognatha (and Ellipura)

22 Collembola: ca spp.! * Great variety of habitats: marine tide pools, hot springs, glaciers, tree canopies, caves, leave litter * Jumping mechanism * High reproductive rate (parthenogenesis)

23 Cercophora (Kukalová-Peck 1991) Diplura + Insecta (=Ectognatha), (Collembola + Protura) Cerci Paired claws Sperm axoneme pattern 9 + 9x2 + 2 No solution with morphology and transcriptomes

24 More molecular data: Entognatha or Cercophora??? 1KITE? still ambiguous

25 Insecta = Ectogntha * Ovipositor * Subdivision of the tarsus

26 Thysanura? silverfish (Zygentoma) rock crawlers (Archaeognatha)

27 Dicondylia * dicondylic mandible! Much broader variety of food, e.g., solid plant materials!

Pterygota, ca. 1.000.000 spp.! Ca. 99% of all spp. * Flight, 2 pairs of wings!

28 Pterygota, ca spp.! Ca. 99% of all spp. * Flight, 2 pairs of wings!!! - Flight mechanism - Access to 3-dimensional space Plant surfaces!!! - Dispersal

29 Passive flight in juvenile spiders using silk rafts (dipsersal) Passive flight and dispersal over long distances with silk rafts in spiders and spider mites

30 Carboniferous ca mya First great wave of diversification!

31 Copulation internal sperm transfer by an intromittent organ external transfer in apterygotes internal transfer with male pedipalps in spiders

32 Lock-and-key mechanism??? exact fit of genitalia

33 Sexual selection (Charles Darwin) cryptic female choice Modification of female and male genitalia: evolutionary arms race

34 Basal branching pattern in Pterygota? Hennig (1969): Palaeoptera (Odonata + Ephemeroptera)

35 Chiastomyaria: Ephemeroptera + Neoptera (Boudreaux 1979) Indirect flight musculature Direct fertilization with aedeagus Metapterygota: Odonata + Neoptera (Staniczek 2000) Modifications of the mandible, anterior ball-and-socket joint modified mandibular musculature Loss of the subimago

36 Palaeoptera Blanke et al. 2012a,b

37 Neoptera: folding back of wings Penetration of relatively narrow spaces possible!

38 Attachment structures: Arolium Friedemann, Schneeberg & Beutel 2014

39 Evolutionary arms race: plant surfaces insect attachment structures Aphids (Sternorrhyncha)

40 Neoptera - Polyneoptera - Paraneoptera (=Acercaria) - Holometabola Wheeler et al. 2001

41 Polyneoptera?

42 Kjer et al s rdna Dermaptera Plecoptera Orthoptera Grylloblattodea Mantophasmatodea Phasmatodea Embioptera Dictyoptera Acercaria Holometabola Polyneoptera Beutel & Gorb 2001 Morphologie Plecoptera Dictyoptera Phasmatodea Orthoptera Grylloblattodea Phasmatodea Embioptera Dermaptera Zoraptera Acercaria Holometabola Ishiwata et al DPD1, RPB1, RPB2 Dictyoptera Zoraptera Orthoptera Dermaptera Plecoptera Mantophasmatodea Grylloblattodea Embioptera Phasmatodea Acercaria Holometabola Misof et al s rdna Holometabola Dictyoptera Dermaptera Plecoptera Zoraptera Embioptera Orthoptera Phasmatodea Grylloblattodea Acercaria Dermaptera Yoshizawa 2011 Flügel Gelenk Phasmatodea Orthoptera Dermaptera Plecoptera Dictyoptera Embioptera Zoraptera Holometabola Acercaria Beutel & Gorb 2006 Morphologie Plecoptera Embioptera Phasmatodea Orthoptera Dictyoptera Grylloblattodea Mantophasmatodea Dermaptera Zoraptera Acercaria Holometabola

43 Kristensen s comb (1981, 1991) Polyneoptera (?): Kristensen s comb Grylloblattodea Dictyoptera Dermaptera Orthoptera Zoraptera Phasmatodea Embioptera Plecoptera Holometabola Acercaria

44 Zoraptera belong to monophyletic Polyneoptera! Embryological data: * Blastoderm formation by fusion of paired regions with higher cellular density * blastokinesis accompanied by full elongation of the embryo on the egg surface Mashimo et al. (2013)

45 Polyneoptera: diversity?

46 Compact thorax with strong musculature: precondition for the evolution of a flight apparatus

47 Wheeler et al. 2001

48 Cyrptocercus + Isoptera * Subsocial (groundplan) * wood-feeding habits * Specific endosymbiontic gut flagellelates * Morpological and molecular data (e.g., Klass 2003; Lo et al. 2000, 2003) Cyrptocercus Implies the non-monophyly of roaches in the traditional sense ( Blattaria )! Mastotermes

49 Polyneoptera monophyletic Zoraptera + Dermaptera basal Misof et al. 2014

50 Grylloblattodea (ice crawlers), ca. 20 spp., Japan, northern North America, Siberia Mantophasmatodea ( heelwalker ), ca. 30 spp.??? (taxonomy uncertain southern Africa

51 Paraneoptera (=Acercaria) ca spp. Wheeler et al. 2001

52 Paraneoptera (=Acercaria) ca. 120,000 spp. Psocoptera Ca spp. Phthiraptera Ca spp. Thysanoptera Ca spp. Auchenorrhyncha Ca spp. Sternorrhyncha Ca spp. Coleorrhyncha Ca. 30 spp. Heteroptera Ca spp.

53 ? Paraneoptera paraphyletic? Psocodea + Holometabola? Misof et al. 2014, ongoing analyses in 1KITE

54 Acercaria project: head structures and attachment devices Psocodea Acercaria Condylognatha Friedemann et al. (2013): 110 characters

55 Hemiptera: ca spp.! (ca. 80% of Paraneoptera) Pentatomorpha: phytophagous

56 Cicada, ca spp., evolutionary parallels to Orthoptera Jumping capacity Accoustic communication systems close association with plants

57 Great diversification of Hemiptera started in the Cretaceous, linked with the diversification of angiosperm plants Archaefructus Great variety of attachment structure (Friedemann et al. 2014)

58 K. Friedemann, PhD project, Friedemann et al. 2015

59 Eumetabola * Loss of ocelli in immatures Psocodea + Holometabola? Misof et al. 2014, ongoing analyses in 1KITE

60 ca. 850,000 described species Holometabola

61 Diversity of organisms Holometabola

62 Hymenoptera + Aparaglossata Neuropterida + (Coleoptera + Strepsiptera) Mecopterida: Amphiesmenoptera + Antliophora Misof et al. 2014

63 Monophyly of Mecoptera? Nannochoristidae + (Boreidae + Pistiliifera) (mol. + morph.) Boreidae + (Nannochoristidae + Pistillifera) (morph.) Nannochoristidae + fleas (mol.) Nannochoristidae + fleas + Diptera (morph.) Nannochoristidae, 7 spp., Gondwanan distribution from Grimaldi & Engel (2005)

64 Holometabola complete metamorphosis Pupa: evolutionary costs Reduced intraspecific competition: evolutionary benefits

65 Endopterygotism Evolutionary benefits: ability to penetrate very narrow crevices or plant tissues including wood

66 356 morphological characters, Beutel et al. in 2011 Megadiversification 4 times independently: BIG4

67 Excellent flight capacity with functional or anatomical dipterism!!! Peltosynidae, Yan et al Strong mechanical protection!

68 Parasitism in Hymenoptera: ca known species Large hidden diversity

69 Co-evolution angiosperms insects!!! Lepidoptera (Moths and butterflies), ca species

70 Morphology in the age of Phylogenomics?

71 Great thanks to all my collaboration partners and to 1KITE Big4 DFG AvH DAAD

Unit 3 Insect Orders

Unit 3 Insect Orders General Directions: 1. To complete this study guide, please read the assigned readings for Unit 3 and watch the lecture. If you need additional information to complete this study guide,