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The Science of Nature

, 103:78 | Cite as

Origin of origami cockroach reveals long-lasting (11 Ma) phenotype instability following viviparity

  • Peter V. Vršanský
  • Lucia Šmídová
  • Daniel Valaška
  • Peter Barna
  • Ľubomír Vidlička
  • Peter Takáč
  • Lubomir Pavlik
  • Tatiana Kúdelová
  • Talia S. Karim
  • David Zelagin
  • Dena Smith
Original Paper

Abstract

Viviparity evolved in bacteria, plants, ˃141 vertebrate lineages (ichthyosaurs, lizards, fishes, mammals, and others), and in 11 of 44 insect orders. Live-birth cockroaches preserved with brood sac (3D recovered two times optically) included Diploptera vladimir, Diploptera savba, Diploptera gemini spp.n., D. sp.1–2, and Stegoblatta irmgardgroehni from Green River, Colorado; Quilchena, Republic; McAbee, Canada; and Baltic amber, Russia (49, 54, and 45 Ma). They evolved from rare and newly evolved Blaberidae; they radiated circumtropically, later expanded into SE Asia, and have now spread to Hawaii and the SE USA. Association of autapomorphic characters that allow for passive and active protections from parasitic insects (unique wing origami pleating identical with its egg case-attacking wasp) suggest a response to high parasitic loads. Synchronized with global reorganization of the biota, morphotype destabilization in roaches lasted approximately 11–22 Ma, including both the adaptation of novel characters and the reduction of others. Thus, while viviparity can be disadvantageous, in association with new Bauplans and/or behaviors, it can contribute to the evolution of taxa with viviparous representatives that are slightly selectively preferred.

Keywords

Fossil insect Cenozoic Eocene Blattaria (=Blattodea) 

Notes

Acknowledgments

We thank Conrad C. Labandeira and Finnegan Marsh (NMNH Washington, DC) for allowing the study and support, Nataša Halásiová (ESISAS Banská Bystrica) for SEM assistance, Roman Hergovits, Vít Kubáň, and Ján Kodada for collecting the living materials, Lena Lukashevich (PIN Moscow) for anisopodid fly determination, and anonymous reviewers for revisions. Earth Relief: Google Maps, 2010 (license Creative Commons CC0—maps-for-free.com). Supported by the Slovak Research and Development Agency under the contracts no. APVV-0436-12, APVV 0692-12; UNESCO-Amba; VEGA 0012-14, 0186/13, 2/0125/09; MVTS; Literary Fund. Support of PB’s work at UCM, fossil curation, and digitization of specimens were supported by National Science Foundation under award numbers EAR 13002622 and EF 13004574. PV designed research and performed NMNH research and wrote paper; PB performed CU research including SEMs and hindwing of living species; LŠ revised viviparity over zoological system; ĽV collected literature and new data of living individuals; MK performed the cladistical analysis; DV provided the 3D reconstructions and visualizations and confocal profiling (www.5s.sk); LP provided the confocal and optical profiling; DS revised text, enabled the study, and provided fossil material and its stratigraphy.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

114_2016_1398_MOESM1_ESM.mp4 (35.8 mb)
ESM 1 SI1: Optical 3D model (cockroach Diploptera vladimir; and synsedimented fly Anisopodidae sp.1, indetermined psocopteran and indetermined insect fragment) with overlay of 16,384/ 16,384 pixel calibrated color texture. (MP4 36,639 kb)
114_2016_1398_MOESM2_ESM.docx (21 kb)
ESM 2 SI3 (SI Tab 1) Phylogenetically annotated morphological character matrix for Diplopteridae (Diploptera, Diplopterina and Stegoblatta and Gyna as outgroup). (DOCX 21 kb)

References

  1. Angert ER, Clements KD (2004) Initiation of intracellular offspring in Epulopiscium. Mol Microbiol 51:827–835CrossRefPubMedGoogle Scholar
  2. Anisyutkin LN (2002) Notes on the cockroaches of the subfamilies Pycnoscelinae and Diplopterinae from South-East Asia with description of three new species (Dictyoptera: Blaberidae). Zoosystematica Rossica 10:351–359Google Scholar
  3. Anisyutkin LN (2007) A new species of the genus Diploptera Saussure, 1864 from Borneo (Dictyoptera: Blaberidae: Diplopterinae). Zoosystematica Rossica 16:173–175Google Scholar
  4. Anisyutkin LN, Gröhn C (2012) New cockroaches (Dictyoptera: Blattina) from Baltic amber, with the description of a new genus and species: Stegoblatta irmgardgroehni. Proc Zool Inst RAS 316:193–202Google Scholar
  5. Archibald SB, Mathewes RW (2000) Early Eocene insects from Quilchena, British Columbia, and their paleoclimatic implications. Can J Zool 78:1441–1462CrossRefGoogle Scholar
  6. Bainbridge DRJ (2014) The evolution of pregnancy. Early Hum Dev 90:741–745CrossRefPubMedGoogle Scholar
  7. Benoit JB, Hansen IA, Attardo GM, Michalková V, Mireji PO, Bargul JL, Drake LL, Masiga DK, Aksoy S (2014) Aquaporins are critical for provision of water during lactation and intrauterine progeny hydration to maintain tsetse fly reproductive success. PLOS Neglected Tropical Diseases 8(4):e2517. doi: 10.1371/journal.pntd.0002517
  8. Benoit JB, Attardo GM, Baumann AA, Michalkova V, Aksoy S (2015) Adenotrophic viviparity in tsetse flies: potential for population control and as an insect model for lactation. Annu Rev Entomol 60:351–371CrossRefPubMedGoogle Scholar
  9. Blackburn DG (1999) Viviparity and oviparity: evolution and reproductive strategies. In: Knobil TE (ed) Encyclopedia of reproduction 4. Academic, London, pp. 994–1003Google Scholar
  10. Blackburn DG (2015) Evolution of vertebrate viviparity and specializations for fetal nutrition: a quantitative and qualitative analysis. J Morphol 276:961–990CrossRefPubMedGoogle Scholar
  11. Blackburn DG, Sidor CA (2014) Evolution of viviparous reproduction in Paleozoic and Mesozoic reptiles. Int J Dev Biol 58:935–948CrossRefPubMedGoogle Scholar
  12. Brunner de Wattenwyl C (1865) Noueau systeme des Blattaires. G. Braumüller, ViennaGoogle Scholar
  13. Brunner de Wattenwyl C (1882) Prodromus der Europäischen Orthopteren. Verlag von Wilhelm Engelmann, LeipzigGoogle Scholar
  14. Brunner von Wattenwyl K (1893) Révision du Système des Orthoptères et description des Espèces rapportées par M. Léonardo Fea de Birmanie. Annali del Museo Civico di Storia Naturale di Genova 2(13):75–101Google Scholar
  15. Buckley D (2012) Evolution of viviparity in salamanders (Amphibia, Caudata). John Wiley & Sons, Ltd, Chichester. doi: 10.1002/9780470015902.a0022851 Google Scholar
  16. Cai CY et al. (2014) Early origin of parental care in Mesozoic carrion beetles. Proc Natl Acad Sci U S A 111:14170–14174. doi: 10.1073/pnas.1412280111 CrossRefPubMedPubMedCentralGoogle Scholar
  17. Caldwell MW, Lee MSY (2001) Live birth in cretaceous marine lizards (mosasauroids). Proc Roy Soc Lond B 268:2397–2401CrossRefGoogle Scholar
  18. Carayon J (1966) Traumatic insemination and the paragenital system, pp. 81–166. In: Usinger RL (ed) Monograph of Cimicidae. Philadelphia, Entomol Soc Am, Thomas Say FoundationGoogle Scholar
  19. Cheng YN, Wu XC, Ji Q (2004) Triassic marine reptiles gave birth to live young. Nature 432:383–386CrossRefPubMedGoogle Scholar
  20. Comstock JH, Needham JG (1898) The wings of insects. Am Nat 32:43–48, 81–89, 231–257, 335–340, 413–424, 561–565, 769–777, 903–911Google Scholar
  21. Comstock JH, Needham JG (1899) The wings of insects. Am Nat 33:117–126, 573–582, 845–860Google Scholar
  22. Cota-Sánchez JH (2004) Vivipary in the Cactaceae: its taxonomic occurrence and biological significance. Flora 199:481–490CrossRefGoogle Scholar
  23. Crespi BJ (1989) Causes of assortative mating in arthropods. Anim Behav 38:980–1000CrossRefGoogle Scholar
  24. de Fraipont M, Clobert J, Barbault R (1996) The evolution of oviparity with egg guarding and viviparity in lizards and snakes: a phylogenetic analysis. Evolution 50:391–400CrossRefGoogle Scholar
  25. Djernæs M, Klass KD, Eggleton P (2014) Identifying possible sister groups of Cryptocercidae + Isoptera: a combined molecular and morphological phylogeny of Dictyoptera. Mol Phylogenet Evol. doi: 10.1016/j.ympev.2014.08.019 PubMedGoogle Scholar
  26. Eisner T (1958) Spray mechanism of the cockroach Diploptera punctata. Science 128:148–149CrossRefPubMedGoogle Scholar
  27. Eschscholtz JF (1822) Entomographien. Erste Lieferung. Berlin: G. Reimer, iii + 128 pp, 2 plsGoogle Scholar
  28. Feldman A et al. (2015) The geography of snake reproductive mode: a global analysis of the evolution of snake viviparity. Glob Ecol Biogeogr 24:1433–1442CrossRefGoogle Scholar
  29. Flegr J (2015) Evoluční tání aneb o původu rodů. Academia, PrahaGoogle Scholar
  30. Franzen JL, Aurich C, Habersetzer J (2015) Description of a Well Preserved Fetus of the European Eocene Equoid Eurohippus messelensis. PLoS ONE:e0137985Google Scholar
  31. Gabriš R, Kundrata R, Trnka F (2016) Review of Dolichostyrax Aurivillius (Cerambycidae, Lamiinae) in Borneo, with descriptions of three new genera and the first case of (ovo)viviparity in the long-horned beetles. ZooKeys 587:49–75. doi: 10.3897/zookeys.587.7961 CrossRefPubMedGoogle Scholar
  32. Gasmi L, Boulain H, Gauthier J, Hua-Van A, Musset K, Jakubowska AK, et al. (2015) Recurrent domestication by Lepidoptera of genes from their parasites mediated by Bracoviruses. PLoS Genet 11:e1005470CrossRefPubMedPubMedCentralGoogle Scholar
  33. Gingerich PD, Ul-Haq M, von Koenigswald, Sanders WJ, Smith BH, Zalmout IS (2009) New protocetid whale from the middle Eocene of Pakistan: birth on land, precocial development, and sexual dimorphism. PLoS ONE:e4366Google Scholar
  34. Grandcolas P (1996) The phylogeny of cockroach families: a cladistic appraisal of morpho-anatomical data. Can J Zool 74:508–527CrossRefGoogle Scholar
  35. Greenwood GR, Archibald SB, Mathewes RW, Moss PT (2005) Fossil biotas from the Okanagan highlands, southern British Columbia and northeastern Washington state: climates and ecosystems across an Eocene landscape. Can J Earth Sci 42:167–185CrossRefGoogle Scholar
  36. Griffith OW, Blackburn DG, Brandley MC, Van Dyke JU, Whittington CM, Thompson MB (2015) Ancestral state reconstructions require biological evidence to test evolutionary hypotheses: a case study examining the evolution of reproductive mode in squamate reptiles. J Exp Zool (Mol Dev Evol) 324B:493–503CrossRefGoogle Scholar
  37. Grimaldi DA, Ross AJ (2004) Raphidiomimula, and enigmatic new cockroach in cretaceous amber from Myanmar (Burma) (insecta: Blattodea: Raphidiomimidae). J Syst Palaeontol 2:101–104CrossRefGoogle Scholar
  38. Gullan PJ, Cranston PS (2005) The insects—an outline of entomology. Blackwell publishingGoogle Scholar
  39. Hagan HR (1951) Embryology of the viviparous insects. The Ronald Press Co., New YorkGoogle Scholar
  40. Handlirsch A (1925) Ordnung: Blattariae Latr. (Schaben). In: Schröder C (ed) Handbuch der Entomologie 3. Verlag von Gustav Fischer, Jena, pp. 481–493Google Scholar
  41. Hanitsch R (1925) On a collection of Blattidae from northern Sarawak, chiefly Mt. Murud and Mt. Dulit. Sarawak Museum Journal 3:75–106Google Scholar
  42. Hara A, Niino-DuPonte R (2015) Hawai‘i landscape plant pest guide: chewing insects. Insect Pests, IP37.Google Scholar
  43. Holbrook GL, Schal C (1998) Social influences on nymphal development in the cockroach, Diploptera punctata. Physiol Entomol 23:121–130CrossRefGoogle Scholar
  44. Holbrook GL, Schal C (2004) Maternal investment affects offspring phenotypic plasticity in a viviparous cockroach. Proc Natl Adad Sci USA 101:5595–5597CrossRefGoogle Scholar
  45. Hörnig MK, Sombke A, Haug C, Harzsch S, Haug JT (2016) What nymphal morphology can tell us about parental investment—a group of cockroach hatchlings in Baltic amber documented by a multi-method approach. Paleontol electron AN 19(1):6AGoogle Scholar
  46. Iwan D (2000) Ovoviviparity in tenebrionid beetles of the melanocratoid Platynotina (Coleoptera: Tenebrionidae: Platynotini) from Madagascar, with notes on the viviparous beetles. Ann Zool 50:15–25Google Scholar
  47. Kathirithamby J (2009) Host-parasitoid associations in Strepsiptera. Annu Rev Entomol 54:227–249CrossRefPubMedGoogle Scholar
  48. Kirby WF (1903) Notes on Blattidae, with descriptions of new genera and species in the collection of the British museum, South Kensington. Ann Mag Nat Hist 7:404–415CrossRefGoogle Scholar
  49. Kurahashi H (1971) The tribe Calliphorini from Australian and oriental regions, II. Calliphora-group (Diptera: Calliphoridae). Pacific Insects 13:141–204Google Scholar
  50. Latreille PA (1810) Considérations générales sur l’ordre naturel des animaux composant les classes des Crustacés, des Arachniddes et des Insectes avec un tableau methodique de leurs genres disposés en familles. Schoell, ParisGoogle Scholar
  51. Lee S (2014) New lower cretaceous basal mantodean (insecta) from the Crato formation (NE Brazil). Geol Carpath 65:285–292CrossRefGoogle Scholar
  52. Lee S (2016) Revision reveals low diversity of Blattaria (Insecta) from the Aptian Crato Formation, NE Brazil. Geol Carpath 67:in pressGoogle Scholar
  53. Li X, Wang Z (2015) A taxonomic study of the beetle cockroaches (Diploptera Saussure) from China, with notes on the genus and species worldwide (Blattodea: Blaberidae: Diplopterinae). Zootaxa 4018:35–56CrossRefPubMedGoogle Scholar
  54. Li L, Shih C, Ren D (2014) Revision of Anomopterella Rasnitsyn, 1975 (insecta, hymenoptera, Anomopterellidae) with two new middle Jurassic species from northeastern China. Geol Carpath 65:365–374CrossRefGoogle Scholar
  55. Liebherr JK, Kavanaugh DH (1985) Ovoviviparity in carabid beetles of the genus Pseudomorpha (insecta: Coleoptera). J Nat Hist 19:1079–1086CrossRefGoogle Scholar
  56. Long AJ, Trinajstic K, Johanson Z (2009) Devonian arthrodire embryos and the origin of internal fertilization in vertebrates. Nature 457:1124–1127CrossRefPubMedGoogle Scholar
  57. Lü J, Kobayashi Y, Deeming DC,Liu Y (2014) Post-natal parental care in a Cretaceous diapsid from northeastern China. Geosci J:1–8. DOI  10.1007/s12303-014-0047-1
  58. Mi S, Lee X, Li X, Veldman GM, Finnerty H, Racie L, et al. (2000) Syncytin is a captive retroviral envelope protein involved in human placental morphogenesis. Nature 403:785–789CrossRefPubMedGoogle Scholar
  59. Mikó I, Copeland RS, Balhoff JP, Yoder MJ, Deans AR (2014) Folding wings like a cockroach: a review of transverse wing folding ensign wasps (hymenoptera: Evaniidae: Afrevania and Trissevania). PLoS One 9:e94056CrossRefPubMedPubMedCentralGoogle Scholar
  60. Miller D (1921) Sheep maggot-flies and their allies. New Zeal J Agric 22:321–334Google Scholar
  61. Miller SC, Omura TH, Smith LJ (1985) Changes in dentin appositional rates during pregnancy and lactation in rats. J Dent Res 64:1062–1064CrossRefPubMedGoogle Scholar
  62. Motani R, Jiang D, Tintori A, Rieppel O (2014) Terrestrial origin of viviparity in Mesozoic marine reptiles indicated by early Triassic embryonic fossils. PLoS One 9(2):e88640CrossRefPubMedPubMedCentralGoogle Scholar
  63. Nalepa C (2009) Altricial development in subsocial cockroach ancestors: foundation for the evolution of phenotypic plasticity in termites. Evol Dev 12:95–105CrossRefGoogle Scholar
  64. Nalepa CA, Bell WJ (1997) Postovulation parental investment and parental care in cockroaches. In: Jae CC, Crespi BJ (eds). The Evolution of Social Behavior in Insects and Arachnids. Cambridge University Press, pp 26–51Google Scholar
  65. O’Keefe FR, Chiappe LN (2011) Viviparity and K-selected life history in a Mesozoic marine plesiosaur (Reptilia, Sauropterygia). Science 333:870–873CrossRefPubMedGoogle Scholar
  66. Packard GC (1966) The influence of ambient temperature and aridity on modes of reproduction and excretion of amniote vertebrates. Am Nat 100:667–682CrossRefGoogle Scholar
  67. Piñeiro G, Ferigolo J, Ramos A, Laurin M (2012) Cranial morphology of the early Permian mesosaurid Mesosaurus tenuidens and the evolution of the lower temporal fenestration reassessed. Compt Rend Palevol 11:379–391CrossRefGoogle Scholar
  68. Princis K (1950) Indomalaiische und australische Blattarien aus dem Entomologischen Museum der Universität in Lund. Opuscula Entomologica 15:161–188Google Scholar
  69. Princis K (1954) Kleine Beiträge zur Kenntnis der Blattarien und ihrer Verbreitung. VI. Entomologisk Tidskrift 74:203–213Google Scholar
  70. Princis K (1963) Blattariae: Suborde [sic] Polyphagoidea: Fam.: Homoeogamiidae, Euthyrrhaphidae, Latindiidae, Anacompsidae, Atticolidae, Attaphilidae. Subordo Blaberoidea: Fam. Blaberidae In Beier (ed) Orthopterorum Catalogus, W. Junk, s’GravenhageGoogle Scholar
  71. Princis K (1965) Blattariae: Subordo Blaberoidea: Fam.: Oxyhaloidae, Panesthiidae, Cryptocercidae, Chorisoneuridae, Oulopterigidae, Diplopteridae, Anaplectidae, Archiblattidae, Nothoblattidae. pp. 283–400. In: Beier M (ed.) Orthopterorum Catalogus 7. Dr. W. Junk, ´s-GravenhageGoogle Scholar
  72. Pyron RA, Burbrink FT (2013) Phylogenetic estimates of speciation and extinction rates for testing ecological and evolutionary hypotheses. Trends Ecol Evol 28(12):729–736Google Scholar
  73. Pyron RA, Burbrink FT (2014) Early origin of viviparity and mulitple reversions to oviparity in squamate reptiles. Ecol Lett 17:13–21CrossRefPubMedGoogle Scholar
  74. Rao TA, Suresh PV, Sherief AN (1986) Multiple viviparity in a few taxa of mangroves. Curr Sci 55:259–261Google Scholar
  75. Roth LM, Willis ER (1960) The biotic associations of cockroach. Smith Misc Coll 141:1–470Google Scholar
  76. Saussure H d (1862) Orthoptera Nova Americana (diagnoses praeliminares)-III. Rev mag zool 2(163–171):227–234Google Scholar
  77. Saussure H d (1864a) Blattarum novarum species aliquot. Revue et Magasin de Zoologie Pure et Appliquée 16(305–326):341–355Google Scholar
  78. Saussure H d (1864b) Orthoptères de l’Amérique Moyenne. I. Famille des Blattes. Mémoires pour servir a L’Histoire Naturelle du Mexique, des Antilles et des États-Unis. Quartrième mémoire. Geneve 1:1–279Google Scholar
  79. Sayer D, Dickinson SD (2013) Reconsidering obstetric death and female fertility in Anglo-Saxon England. World Archaeology 45:285–297CrossRefGoogle Scholar
  80. Schal C, Gautier JY, Bell WJ (1984) Behavioural ecology of cockroaches. Biol Rev 59:209–254CrossRefGoogle Scholar
  81. Serville JGA (1838) Histoire naturelle des insectes, Orthoptères. Librairie encyclopédique de Roret, Paris, xvii + 777 pp.Google Scholar
  82. Serville JGA (1839) Histoire naturelle des Insectes. Orthoptères. Librairie Encyclopédique de Roret, ParisGoogle Scholar
  83. Shelford R (1907) On some new species of Blattidae in the Oxford and Paris museums. Ann Mag Nat Hist 7:25–49CrossRefGoogle Scholar
  84. Shelford R (1908) New species of Blattidae in the collection of the deutsche Entomologische National-Museum (Orthopt.). Dtsch Entomol Z 1908:115–131Google Scholar
  85. Shine R (2014) Evolution of an evolutionary hypothesis: a history of changing ideas about the adaptive significance of viviparity in reptiles. J Herpetol 48:147–161CrossRefGoogle Scholar
  86. Shiraki T (1931) Orthoptera of the Japanese empire. II. Blattidae. Insecta Matsumurana 5:171–209Google Scholar
  87. Sites JW, Reeder TW, Wiens JJ (2011) Phylogenetic insights on evolutionary novelties in lizards and snakes: sex, birth, bodies, niches, and venom. Annu Rev Ecol Evol Syst 42:227–244CrossRefGoogle Scholar
  88. Stay, B. & Roth, L. M., 1958: The reproductive behavior of Diploptera punctata (Blattaria; Diplopteridae) Proceedings X International Congress of Entomology 547–552.Google Scholar
  89. Sulikowska-Drozd A, Walczak M, Binkowski M (2014) Evolution of shell apertural barriers in viviparous land snails (Gastropoda: Pulmonata: Clausiliidae). Can J Zool 92:205–213CrossRefGoogle Scholar
  90. Swofford DL (2003) PAUP*. Phylogenetic analysis using parsimony (*and other methods). Sinauer Associates, Sunderland, MassachusettsGoogle Scholar
  91. Thompson MB, Speake BK (2006) A review of the evolution of viviparity in lizards: structure, function and physiology of the placenta. J Comp Physiol B 176:179–189CrossRefPubMedGoogle Scholar
  92. Tinkle DW, Gibbons JW (1977) The distribution and evolution of viviparity in reptiles. Misc Publ Mus Zool Univ Mich 154:1–47Google Scholar
  93. Tworzydlo W, Kisiel E, Bilinski SM (2013) Embryos of the viviparous Dermapteran, Arixenia esau develop sequentially in two compartments: terminal ovarian follicles and the uterus. PLoS One 8:e64087. doi: 10.1371/journal.pone.0064087 CrossRefPubMedPubMedCentralGoogle Scholar
  94. Vidlička Ľ (2001) Fauna Slovenska Blattaria – šváby, Mantodea - modlivky (insecta: Orthopteroidea). Veda, BratislavaGoogle Scholar
  95. Vršanský P (1999) Lower Cretaceous Blattaria. In: Vršanský P (ed) Proc1st Internat Palaeoentomol Conf, Moscow 1998, Amba projekty, BratislavaGoogle Scholar
  96. Vršanský P (2003) Umenocoleoidea—an amazing lineage of aberrant insects (insecta, Blattaria). Amba projekty 7:1–32Google Scholar
  97. Vršanský P (2005) Mass mutations of insects at the Jurassic/cretaceous boundary? Geol Carpath 56:473–781Google Scholar
  98. Vršanský P (2010) Cockroach as the earliest eusocial animal. Acta Geol Sin-Engl Ed 84:793–808CrossRefGoogle Scholar
  99. Vršanský P, Bechly GN (2015) New predatory cockroaches (insecta: Blattaria: Manipulatoridae fam.N.) from the upper cretaceous Myanmar amber. Geol Carpath 66(2):133–138. doi: 10.1515/geoca-2015-0015 Google Scholar
  100. Vršanský P, Vidlička Ľ, Čiampor F Jr, Marsh F (2012) Derived, still living cockroach genus Cariblattoides (Blattida: Blattellidae) from the Eocene sediments of Green River in Colorado. USA Insect Sci 19:143–152CrossRefGoogle Scholar
  101. Vršanský P, Vidlička Ľ, Barna P, Bugdaeva E, Markevich V (2013) Paleocene origin of the cockroach families Blaberidae and Corydiidae: evidence from Amur River region of Russia. Zootaxa 3635:117–126CrossRefPubMedGoogle Scholar
  102. Vršanský P, Oružinský R, Barna P, Vidlička L, Labandeira CC (2014) Native Ectobius (Blattaria: Ectobiidae) from the early Eocene Green River formation of Colorado and its reintroduction to North America 49 million years later. Ann Entomol Soc Am 107:28–36CrossRefGoogle Scholar
  103. Vrsansky P, Lis JA, Schloegl J, Guldan M, Mlynsky T, Barna P, Stys P (2015) Partially disarticulated new Miocene burrower bug (Hemiptera: Heteroptera: Cydnidae) from Cerova (Slovakia) documents occasional preservation of terrestrial arthropods in deep-marine sediments. Eur J Entomol 112:844–854Google Scholar
  104. Vršanský P, Aristov D, Wei DD, Vidlička Ľ, Ren D (2016) Deleterious mass mutations relate to originations of cockroach families. Biologia, in pressGoogle Scholar
  105. Walker F (1868) Catalogue of the specimens of Blattariae in the collection of the British museum. British Museum (Natural History), London, pp. 1–239Google Scholar
  106. Walker F (1869) Supplement to the catalogue of Blattariae (included in the catalogue of the specimens of Dermaptera Saltatoria and supplement to the Blattariae in the collection of the British museum, by the same author. British Museum (Natural History), London, pp. 119–156Google Scholar
  107. Wang Y, Evans SE (2011) A gravid lizard from the cretaceous of China and the early history of squamate viviparity. Naturwissenschaften 98:735–743Google Scholar
  108. Wang B et al. (2015) Brood care in a 100-million-year-old scale insect. eLife 4:e05447. doi: 10.7554/eLife.05447 PubMedCentralGoogle Scholar
  109. Weitschat W, Wichard W (2010) Baltic Amber. In Penney D (ed) Biodiversity of fossils in amber. Siri Scientific Press: pp 80–115Google Scholar
  110. Williford B, Keppler C, Bhattacharya D (2004) Evolution of a novel function: nutritive milk in the viviparous cockroach, Diploptera punctata. Evol Dev 6:67–77CrossRefPubMedGoogle Scholar
  111. Wyttenbach R, Eisner T (2001) Use of defensive glands during mating in a cockroach (Diploptera punctata). Chemoecology 11:25–28CrossRefGoogle Scholar
  112. Zherikhin VV, Ponomarenko AG, Rasnitsyn AP (2008) Introduction to the paleoentomology. KMK, MoscowGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Peter V. Vršanský
    • 1
    • 2
    • 3
  • Lucia Šmídová
    • 4
  • Daniel Valaška
    • 5
  • Peter Barna
    • 3
  • Ľubomír Vidlička
    • 1
  • Peter Takáč
    • 1
  • Lubomir Pavlik
    • 6
    • 7
  • Tatiana Kúdelová
    • 4
  • Talia S. Karim
    • 8
  • David Zelagin
    • 8
  • Dena Smith
    • 8
  1. 1.Institute of ZoologySlovak Academy of SciencesBratislavaSlovakia
  2. 2.Paleontological InstituteRussian Academy of SciencesMoscowRussia
  3. 3.Earth Science InstituteSlovak Academy of SciencesBratislavaSlovakia
  4. 4.Faculty of Natural SciencesComenius UniversityBratislavaSlovakia
  5. 5.BratislavaSlovakia
  6. 6.Faculty of Materials and TechnologySlovak Technical University BratislavaTrnavaSlovakia
  7. 7.Institute of Materials and Machine MechanicsSlovak Academy of SciencesBratislavaSlovakia
  8. 8.CU Museum of Natural HistoryUniversity of ColoradoBoulderUSA

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