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Biologia

, Volume 74, Issue 1, pp 65–89 | Cite as

Parasitic cockroaches indicate complex states of earliest proved ants

  • Peter VršanskýEmail author
  • Lucia Šmídová
  • Hemen Sendi
  • Peter Barna
  • Patrick Müller
  • Sieghard Ellenberger
  • Hao Wu
  • Xiaoyin Ren
  • Xiaojie Lei
  • Dany Azar
  • Juraj Šurka
  • Tao Su
  • Weiyudong Deng
  • Xianhui Shen
  • Jun Lv
  • Tong Bao
  • Günter Bechly
Original Article

Abstract

Myrmecophilous and termitophilous interactions likely contributed to the competitive advantage and evolutionary success of eusocial insects, but how these commensal and parasitic relationships originated is unclear due to absence of fossil records. New extinct cockroaches of the still living family Blattidae are reported here from the Cretaceous Myanmar amber (99 Ma) and are the earliest known inhabitants of complex ant nests, demonstrating that this specialised myrmecophily originated shortly after ant eusociality and appeared in the fossil record. Cretaceous stem aposematic Blattidae are known from the amber of Myanmar and Lebanon and we report them here also from the Syrian amber. Concurrent evolution suggests that the collective internal defence of early ants was weak and allowed infiltrations by numerous unrelated organisms, At the same time, the contemporary presence of ant mimicking myrmecomorphs suggests a need for strong external protection against visually hunting predators. Myrmecophily is supported by morphological adaptations (lack of wide fat body and feeding of adult male; short, fossorial legs; shortened cerci; oligomerised antenna; hairy surface structures) and camouflage behaviour, documented by sediment and own feces covering. Moreover the same piece of amber contains ants, ant mimics and other undescribed ant nest-visiting insects as syninclusions. Another species preserved along with two termites is a putative termitophile. Abundant comparatively large parasitic cockroaches influenced Mesozoic tropical forest ecosystems by affecting the early evolution of complex nests of eusocial insects. Rainforest rudiments in South Yunnan yielded observation of analogical still living, formally undescribed species.

Keywords

Fossil insect Mesozoic Cretaceous amber Myanmar Syria New genera New species 

Notes

Acknowledgments

We thank Ing. Robert Oružinský, Dr. Mária Kazimírová, Dr. Ľubomír Vidlička, Martin Styan (Bratislava), Prof. Bo Wang (Nanjing) and Dr. Karin Wolfschwenninger (Stuttgart) for technical help and linguistic revision. This work was supported by the Slovak Research and Development Agency under the contract no. APVV-0436-12, and by UNESCO-Amba/ MVTS supporting grant of Presidium of the Slovak Academy of Sciences; VEGA 0012-14, 2/0042/18; Literary Fund. This research was supported by the Strategic Priority Research Program (B) of the Chinese Academy of Sciences (XDB26000000) and the National Natural Science Foundation of China (41572010, 41622201, 41688103).

Author’s contribution

We collected the material (S.E., P.M., D.A., L.J., W.H., B.T.); took the photographs (S.E., P.M., P.B., L.Š., P.V., X.R., X.L.), produced drawings (L.Š., P.B., P.V.), CT (P.B., L.Š., H.S.), descriptions and comparison (P.V., L.Š., P.B., H.S.); observations in the living ecosystem (P.V., T.S., W.D., T.B., X.S.); designed research (P.V.), wrote and edited the paper (P. V., G.B., D.A.) with contributions from all authors.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Anisyutkin LN, Gorochov AV (2008) A new genus and species of the cockroach family Blattulidae from Lebanese Amber (Dictyoptera, Blattina). Paleontol J 42:43–46.  https://doi.org/10.1007/s11492-008-1006-y CrossRefGoogle Scholar
  2. Bai M, Beutel RG, Klass K-D, Zhang WW, Yang WK, Wipfler B (2016) †Alienoptera — a new insect order in the roach–mantodean twilight zone. Gondwana Res 39:317–326.  https://doi.org/10.1016/j.gr.2016.02.002 CrossRefGoogle Scholar
  3. Bai M, Beutel RG, Zhang WW et al (2018) A new cretaceous insect with a unique cephalothoracic scissor device. Curr Biol 28:438–443.  https://doi.org/10.1016/j.cub.2017.12.031 CrossRefPubMedGoogle Scholar
  4. Barden P (2017) Fossil ants (Hymenoptera: Formicidae): ancient diversity and the rise of modem lineages. Myrmecol News 24:1–30Google Scholar
  5. Barden P, Grimaldi DA (2016) Adaptive radiation in socially advanced stem-group ants from the Cretaceous. Curr Biol 26:515–521.  https://doi.org/10.1016/j.cub.2015.12.060 CrossRefPubMedGoogle Scholar
  6. Baum E, Dressler C, Beutel RG (2007) Head structures of Karoophasma sp. (Hexapoda, Mantophasmatodea) with phylogenetic implications. J Zool Syst Evol Res 45:104–119.  https://doi.org/10.1111/j.1439-0469.2006.00380.x CrossRefGoogle Scholar
  7. Behie SW, Zelisko PM, Bidochka MJ (2012) Endophytic insect-parasitic fungi translocate nitrogen directly from insects to plants. Science 336:1576–1577.  https://doi.org/10.1126/science.1222289 CrossRefPubMedGoogle Scholar
  8. Bell WJ, Roth LM, Nalepa CA (2007) Cockroaches - ecology, behavior, and natural history. The Johns Hopkins University Press, BaltimoreGoogle Scholar
  9. Beutel RG, Gorb SN (2006) A revised interpretation of the evolution of attachment structures in Hexapoda with special emphasis on Mantophasmatodea. Arthropod Syst Phylogeny 61:3–35Google Scholar
  10. Beutel RG, Gorb SN (2008) Evolutionary scenarios for unusual attachment devices of Phasmatodea and Mantophasmatodea (Insecta). Syst Entomol 33:501–510.  https://doi.org/10.1111/j.1365-3113.2008.00428.x CrossRefGoogle Scholar
  11. Beutel RG, Friedrich F, Ge SG, Yang XK (2014) Insect morphology and phylogeny. Walter De Gruyter, BerlinGoogle Scholar
  12. Blanke A, Wipfler B, Letsch H, Koch M, Beckman F, Beutel R, Misof B (2012) Revival of Palaeoptera—head characters support a monophyletic origin of Odonata and Ephemeroptera (Insecta). Cladistics 28:560–581.  https://doi.org/10.1111/j.1096-0031.2012.00405.x CrossRefGoogle Scholar
  13. Bolívar I (1905) Les blattes myrmecophiles. Mitt Schweiz Entomol Ges 11:134–141Google Scholar
  14. Bradler S (2003) Lehrbuch der Speziellen Zoologie, Band 1: Wirbellose Tiere, 2nd edn. Spektrum Akademischer Verlag, Berlin, pp 251–261Google Scholar
  15. Brady SG, Fisher BL, Schultz TR, Ward PS (2014) The rise of army ants and their relatives: diversification of specialized predatory doryline ants. BMC Evol Biol 14:2–14.  https://doi.org/10.1186/1471-2148-14-93 CrossRefGoogle Scholar
  16. Brunner von Wattenwyl C (1882) Prodromus der Europäischen Orthopteren. Wilhelm Engelmann, LeipzigGoogle Scholar
  17. Cai CY, Huang DY, Newton AF, Eldredge KT, Engel, MS (2017a) Evidence from amber for the origins of termitophily. Curr Biol 27(16):R794-R795.  https://doi.org/10.1016/j.cub.2017.06.083
  18. Cai CY, Huang DY, Newton AF, Eldredge KT, Engel MS (2017b) Early Evolution of Specialized Termitophily in Cretaceous Rove Beetles. Curr Biol 27(8):1229–1235.  https://doi.org/10.1016/j.cub.2017.03.009
  19. Capinera JL (2008) Encyclopedia of entomology. Kluwer, DodrechtCrossRefGoogle Scholar
  20. Chopard L (1924) Description d'un Blattide myrmécophile nouveau [Orth.]. Bull Soc Entomol Fra 11-12:131–132Google Scholar
  21. Choufani J, Halabi WE, Azar D, Nel A (2015) First fossil insect from lower cretaceous Lebanese amber in Syria (Diptera: Ceratopogonidae). Cretac Res 54:106–116CrossRefGoogle Scholar
  22. Delclós X, Penalver E, Arillo A, Engel MS, N el A, Azar D, Ross A (2016) New mantises (Insecta: Mantodea) in cretaceous ambers from Lebanon, Spain, and Myanmar. Cretac Res 60:91–108.  https://doi.org/10.1016/j.cretres.2015.11.001 CrossRefGoogle Scholar
  23. Eisner T (1958) Spray mechanism of the cockroach Diploptera punctata. Science 128:148–149CrossRefPubMedGoogle Scholar
  24. Evangelista D, Djernæs M, Kohli MK (2017) Fossil calibrations for the cockroach phylogeny (Insecta, Dictyoptera, Blattodea), comments on the use of wings for their identification, and a redescription of the oldest Blaberidae. Palaeontol Electronica 20:20.3.1FCGoogle Scholar
  25. Gao TP, Shih CG, Labandeira CC, Liu X, Wang ZQ, Che YL, Yin XC, Ren D (2018) Maternal care by early cretaceous cockroaches. J Syst Palaeontol.  https://doi.org/10.1080/14772019.2018.1426059
  26. Gasmi L, Boulain H, Gauthier J, Hua-Van A, Musset K, Jakubowska AK, Aury JM, Volkoff AN, Huguet E, Herrero S, Drezen JM (2015) Recurrent domestication by Lepidoptera of genes from their parasites mediated by Bracoviruses. PLoS Genet 11:e1005470.  https://doi.org/10.1371/journal.pgen.1005470 CrossRefPubMedPubMedCentralGoogle Scholar
  27. Giles ET (1963) The comparative external morphology and affinities of the Dermaptera. Ecol Entomol 115:95–164Google Scholar
  28. Grimaldi DA (2003) A revision of Cretaceous mantises and their relationships, including new taxa (Insecta : Dictyoptera : Mantodea). Am Mus Novit 3412:1–47CrossRefGoogle Scholar
  29. Grimaldi DA, Engel MS (2005) Evolution of the insects. Cambridge University Press, CambridgeGoogle Scholar
  30. Grimaldi DA, Ross AJ (2004) Raphidiomimula, an enigmatic new cockroach in Cretaceous amber from Myanmar (Burma) (Insecta: Blattodea: Raphidiomimidae). J Syst Palaeontol 2(2):101–104.  https://doi.org/10.1017/S1477201904001142 CrossRefGoogle Scholar
  31. Gurney AB (1937) Studies in certain genera of American Blattidae (Orthoptera). Proc Entomol Soc Wash 39:101–112Google Scholar
  32. Haas F (2006) Evidence from folding and functional lines of wings on inter-ordinal relationships in Pterygota. Arthropod Syst Phylogeny 64:149–158Google Scholar
  33. Hölldobler B, Wilson EO (1990) The ants. Belknap Press of Harvard University Press, CambridgeCrossRefGoogle Scholar
  34. Hörnig MK, Haug C, Haug JT (2013) New details of Santanmantis axelrodi and the evolution of the mantodean morphotype. Palaeodiversity 6:157–168Google Scholar
  35. Hörnig MK, Haug JT, Haug C (2017) An exceptionally preserved 110 million years old praying mantis provides new insights into the predatory behaviour of early mantodeans. PeerJ 5:AN e3605.  https://doi.org/10.7717/peerj.3605
  36. Huber P, McDonald NG, Olsen PE (2003) Early Jurassic insects from the Newark Supergroup, Northeastern United States. In: PM LT, Olsen PE (eds) The great rift valleys of Pangea in Eastern North America, volume 2: Sedimentology, stratigraphy, and paleontology, pp 206–223Google Scholar
  37. Hudson GB (1945) A study of the tentorium in some orthopteroid Hexapoda. J Entomol Soc S Africa 8:71–90Google Scholar
  38. Inui Y, Tanaka H, Hyodo F, Itioka T (2009) Within-nest abundance of a tropical cockroach Pseudoanaplectinia yumotoi associated with Crematogaster ants inhabiting epiphytic ferndomatia in a Bornean dipterocarp forest. J Nat Hist 43:1139–1145.  https://doi.org/10.1080/00222930902807734 CrossRefGoogle Scholar
  39. Kania I, Wang B, Szwedo J (2015) Dicranoptycha Osten Sacken, 1860 (Diptera, Limoniidae) from the earliest upper Cretaceous Burmese amber. Cretac Res 52:522–530.  https://doi.org/10.1016/j.cretres.2014.03.002 CrossRefGoogle Scholar
  40. Klass KD, Ehrmann R (2003) Lehrbuch der Speziellen Zoologie, Band 1: Wirbellose Tiere, 2nd edn. Spektrum Akademischer Verlag, Berlin, pp 182–197Google Scholar
  41. Klass K, Eulitz U (2007) The tentorium and anterior head sulci in Dictyoptera and Mantophasmatodea (Insecta). Zool Anz 246:205–234.  https://doi.org/10.1016/j.jcz.2007.06.001 CrossRefGoogle Scholar
  42. Klass KD, Eulitz U, Schmidt C, Barton A (2009) The tibiotarsal articulation and antertibiotarsal leg sclerite in Dictyoptera (Insecta). Ins Syst Evol 40(4):361–387CrossRefGoogle Scholar
  43. Lachaud G, Bartolo-Reyes JC, Quiroa-Montalván CM, Cruz-López L, Lenoir A, Lachaud JP (2015) How to escape from the host nest: imperfect chemical mimicry in eucharitid parasitoids and exploitation of the ants’ hygienic behavior. J Insect Physiol 75:63–72.  https://doi.org/10.1016/j.jinsphys.2015.03.003 CrossRefPubMedGoogle Scholar
  44. Latreille PA (1810) Considerations generales sur l'ordre naturel des animaux composant les classes des crustaces, des arachnides, et des insectes; avec un tableau methodique de leurs genres, disposes en familles. Schoell, ParisGoogle Scholar
  45. Lee SW (2016) Taxonomic diversity of cockroach assemblages (Blattaria, Insecta) of the Aptian Crato formation (Cretaceous, NE Brazil). Geol Carpath 67:433–450.  https://doi.org/10.1515/geoca-2016-0027 CrossRefGoogle Scholar
  46. Legendre F, Nel A, Svenson GJ, Robillard T, Pellens R, Grandcolas P (2015) Phylogeny of Dictyoptera: dating the origin of cockroaches, praying mantises and termites with molecular data and controlled fossil evidence. PLoS ONE 10:e0130127.  https://doi.org/10.1371/journal.pone.0130127 CrossRefPubMedPubMedCentralGoogle Scholar
  47. Leverault P (1936) The morphology of the Carolina mantis. Univ Kans Sci Bull 24:206–259Google Scholar
  48. Li XR, Huang D (2018a) A new cretaceous cockroach with heterogeneous tarsi preserved in Burmese amber (Dictyoptera, Blattodea, Corydiidae). Cretac Res 92:12–17.  https://doi.org/10.1016/j.cretres.2018.07.017
  49. Li XR, Huang D (2018b) A new praying mantis from middle cretaceous Burmese amber exhibits bilateral asymmetry of forefemoral spination (Insecta: Dictyoptera). Cretac Res 91:269–273.  https://doi.org/10.1016/j.cretres.2018.06.019 CrossRefGoogle Scholar
  50. Liang JH, Shih CK, Ren D (2018) New Jurassic predatory cockroaches (Blattaria: Raphidiomimidae) from Daohugou, China and Karatau, Kazakhstan. Alcheringa 42(1):101–109.  https://doi.org/10.1080/03115518.2017.1374460 CrossRefGoogle Scholar
  51. Lin QB (1980) Mesozoic insects from Zhejian and Anhui Provinces. Division and Correlation of the Mesozoic Volcano-Sedimentary Strata in Zhejiang and Anhui Provinces, pp 211–234Google Scholar
  52. Linnæus C (1758) Systema naturæ per regna tria naturæ, secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis, locis, vol 1, 10th edn. Holmiæ Salvius, StockholmGoogle Scholar
  53. Lo N, Beninati T, Stone F, Walker J, Sacchi L (2007) Cockroaches that lack Blattabacterium endosymbionts: the phylogenetically divergent genus Nocticola. Biol Lett 3:327–300.  https://doi.org/10.1098/rsbl.2006.0614 CrossRefPubMedPubMedCentralGoogle Scholar
  54. Mashimo Y, Beutel RG, Dallai R, Lee CY, Machida R (2014) Embryonic development of Zoraptera with special reference to external morphology, and its phylogenetic implications (Insecta). J Morphol 275:295–312.  https://doi.org/10.1002/jmor.20215 CrossRefPubMedGoogle Scholar
  55. Matsumura Y, Wipfler B, Pohl H et al (2015) Cephalic anatomy of Zorotypus weidneri New, 1978: new evidence for a placement of Zoraptera. Arthropod Syst Phylogeny 3:85–105Google Scholar
  56. McIver JD, Stonedahl G (1993) Myrmecomorphy: morphological and behavioral mimicry of ants. Annu Rev Entomol 38:351–377.  https://doi.org/10.1146/annurev.en.38.010193.002031 CrossRefGoogle Scholar
  57. Mlynský T, Wu H, Koubová I (2018) Dominant Burmite cockroach Jantaropterix ellenbergeri sp.n. might laid isolated eggs together. Paleontographica Abt A.  https://doi.org/10.1127/pala/2019/0091
  58. Moreau CS, Bell CD (2013) Testing the museum versus cradle tropical biological diversity hypothesis: phylogeny, diversification, and ancestral biogeographic range evolution of the ants. Evolution 67:2240–2257.  https://doi.org/10.1111/evo.12105 CrossRefPubMedGoogle Scholar
  59. Moser JC (1964) Inquiline roach respond to trail-marking substance of leaf-cutting ants. Science 143:1048–1049CrossRefPubMedGoogle Scholar
  60. Nehring V, Francesca R, Dani FR, Calamai L, Turillazzi S, Bohn H, Klass KD, d’Ettorre P (2016) Chemical disguise of myrmecophilous cockroaches and its implications for understanding nestmate recognition mechanisms in leaf-cutting ants. BMC Ecol 16(35).  https://doi.org/10.1186/s12898-016-0089-5
  61. Orivel J, Servigne P, Cerdan P, Dejean A, Corbara B (2004) The ladybird Thalassa saginata, an obligatory myrmecophile of Dolichoderus bidens ant colonies. Sci Nat 91:97–100.  https://doi.org/10.1007/s00114-003-0499-z CrossRefGoogle Scholar
  62. Perrichot V, Wang B, Engel MS (2016) Extreme morphogenesis and ecological specialization among cretaceous basal ants. Curr Biol 26:1468–1472.  https://doi.org/10.1016/j.cub.2016.03.075 CrossRefPubMedGoogle Scholar
  63. Pierce NE, Braby MF, Heath A, Lohman DJ, Mathew J, Rand DB, Travassos MA (2002) The ecology and evolution of ant association in the Lycaenidae (Lepidoptera). Annu Rev Entomol 47:733–771.  https://doi.org/10.1146/annurev.ento.47.091201.145257 CrossRefPubMedGoogle Scholar
  64. Podstrelená L, Sendi H (2018) Cratovitisma Bechly, 2007 (Blattaria: Umenocoleidae) recorded in Lebanese and Myanmar ambers. Paleontographica Abt A 310:212–219.  https://doi.org/10.1127/pala/2018/0076 CrossRefGoogle Scholar
  65. Poinar GO (1999) Paleochordodes protus n.g., n.sp. (Nematomorpha, Chordodidae), parasites of a fossil cockroach, with a critical examination of other fossil hairworms and helminths of extant cockroaches (Insecta: Blattaria). Invertebr Biol 118:109–115.  https://doi.org/10.2307/3227053 CrossRefGoogle Scholar
  66. Poinar GO Jr (2009a) Description of an early Cretaceous termite (Isoptera: Kalotermitidae) and its associated intestinal protozoa, with comments on their co-evolution. Parasit Vectors 2:12.  https://doi.org/10.1186/1756-3305-2-12
  67. Poinar GO (2009b) Early Cretaceous protist flagellates (Parabasalia: Hypermastigia: Oxymonada) of cockroaches (Insecta: Blattaria) in Burmese amber. Cretac Res 30(5):1066–1072.  https://doi.org/10.1016/j.cretres.2009.03.008 CrossRefGoogle Scholar
  68. Poinar G, Fanti F, (2016) New Fossil Soldier Beetles ( ) in Burmese, Baltic and Dominican Amber. Palaeodiversity 9(1):1–7.  https://doi.org/10.18476/pale.v9.a1
  69. Poinar GO, Brown AE (2017) An exotic insect Aethiocarenus burmanicus gen. et sp. nov. (Aethiocarenodea ord. nov., Aethiocarenidae fam. nov.) from mid-Cretaceous Myanmar amber. Cretac Res 72:100–104.  https://doi.org/10.1016/j.cretres.2016.12.011 CrossRefGoogle Scholar
  70. Rähle W (1970) Untersuchungen an Kopf und Prothorax von Embia ramburi Rimsky-Korsakow, 1906 (Embioptera, Embiidae). Zool Jahrb Abt Anat Ontog Tiere 87:248–330Google Scholar
  71. Rettenmeyer CW, Rettenmeyer ME, Joseph J, Berghoff SM (2011) The largest animal association centered on one species: the army ant Eciton burchellii and its more than 300 associates. Insect Soc 58:281–292.  https://doi.org/10.1007/s00040-010-0128-8 CrossRefGoogle Scholar
  72. Rodríguez J, Montoya-Lerma J, Calle Z (2013) First record of Attaphila fungicola (Blattaria: Polyphagidae) in Atta cephalotes nests (Hymenoptera: Myrmicinae) in Colombia. Bol Cient Mus Hist Nat Univ de Caldas 17:219–225Google Scholar
  73. Ross A, Mellish C, York P, Crighton B (2010) In: Penney D (ed) Biodiversity of fossils in amber from the major world deposits. Siri Scientific Press, Manchester, pp 208–235Google Scholar
  74. Roth LM (1995) Pseudoanaplectina yumotoi, a new ovoviviparous myrmecophilous cockroach genus and species from Sarawak (Blattaria: Blattellidae; Blattellinae). Psyche 102:79–87CrossRefGoogle Scholar
  75. Roth LM (2003) Systematics and phylogeny of cockroaches (Dictyoptera: Blattaria). Orient Insects 37:1–186.  https://doi.org/10.1080/00305316.2003.10417344 CrossRefGoogle Scholar
  76. Santos PP, Vasconcellos A, Jahyny B, Delabie JHC (2010) Ant fauna (Hymenoptera, Formicidae) associated to arboreal nests of Nasutitermes spp: (Isoptera, Termitidae) in a cacao plantation in southeastern Bahia, Brazil. Rev Bras Entomol 54:450–454.  https://doi.org/10.1590/S0085-56262010000300016 CrossRefGoogle Scholar
  77. Scudder SH (1862) Materials for a monograph of the North American Orthoptera. H. O. Houghton, CambridgeCrossRefGoogle Scholar
  78. Sendi H, Azar D (2017) New aposematic and presumably repellent bark cockroach from Lebanese amber. Cretac Res 72:13–17.  https://doi.org/10.1016/j.cretres.2016.11.013 CrossRefGoogle Scholar
  79. Shi G, Grimaldi DA, Harlow GE, Wang J, Wang J, Yanga M, Lei W, Li Q, Li X (2012) Age constraint on Burmese amber based on U-Pb dating of zircons. Cretac Res 37:155–163.  https://doi.org/10.1016/j.cretres.2012.03.014 CrossRefGoogle Scholar
  80. Silvestri F (1946) Descrizione di due specie neotropicali di Zorotypus (Insecta, Zoraptera). Boll Lab Entomol Agrar Portici 7:1–12Google Scholar
  81. Šmídová L, Lei X (2017) The earliest amber-recorded type cockroach family was aposematic (Blattaria: Blattidae). Cretac Res 72:189–199.  https://doi.org/10.1016/j.cretres.2017.01.008 CrossRefGoogle Scholar
  82. Smrž J, Kováč Ľ, Mikeš J, Lukešová A (2013) Microwhip scorpions (Palpigradi) feed on heterotrophic cyanobacteria in Slovak caves - a curiosity among Arachnida. PLoS ONE 8:e75989  https://doi.org/10.1371/journal.pone.0075989 CrossRefPubMedPubMedCentralGoogle Scholar
  83. Song XB, Li LZ (2014) Three new species of the myrmecophilous genus Doryloxenus from China (Coleoptera, Staphylinidae, Aleocharinae). Zookeys 456:75–83CrossRefGoogle Scholar
  84. Tang JW, Zhang JH, Song QS, Feng ZY (1999) Community analysis on secondary tropical vegetations in Xishuangbanna. Chin J Appl Ecol 10:135–139Google Scholar
  85. Vishniakova VN (1973) New cockroaches (Insecta: Blattodea) from the Upper Jurassic of Karatau mountains. Lectures at the XXIV Annual Readings in the Memory of NA Kholodkovsky (1–2 April, 1971), pp 64–77Google Scholar
  86. Vršanský P (1999) Lower Cretaceous Blattodea. In: Vršanský P (Ed) Proc. 1st Intern. Paleoentomol. Conf. Moscow 1998. Amba projekty Bratislava, pp 167–176Google Scholar
  87. Vršanský P (2002) Origin and the early evolution of mantises. Amba projekty 6:1–16Google Scholar
  88. Vršanský P (2003) Umenocoleoidea – an amazing lineage of aberrant insects (Insecta, Blattaria). Amba projekty 7:1–32Google Scholar
  89. Vršanský P (2008) Central ocellus of extinct cockroaches (Blattida: Caloblattinidae). Zootaxa 1958:41–50CrossRefGoogle Scholar
  90. Vršanský P (2009) Albian cockroaches (Insecta, Blattida) from French amber of Archingeay. Geodiversitas 31:73–98CrossRefGoogle Scholar
  91. Vršanský P, Bechly G (2015) New predatory cockroaches (Insecta: Blattaria: Manipulatoridae fam.n.) from the Upper Cretaceous Myanmar amber. Geol Carpath 66:133–138.  https://doi.org/10.1515/geoca-2015-0015 CrossRefGoogle Scholar
  92. Vršanský P, Wang B (2017) A new cockroach, with bipectinate antennae, (Blattaria: Olidae fam. nov.) further highlights the differences between the Burmite and other faunas. Biologia 72(11):1327–1333.  https://doi.org/10.1515/biolog-2017-0144 CrossRefGoogle Scholar
  93. Vršanský P, Storozhenko SY, Labandeira CC, Ihringova P (2001) Galloisiana olgae sp. nov. (Grylloblattodea: Grylloblattidae) and the paleobiology of a relict order of insects. Ann Entomol Soc Am 94:179–184.  https://doi.org/10.1603/0013-8746 CrossRefGoogle Scholar
  94. Vršanský P, Vidlička L, Barna P, Bugdaeva E, Markevich V (2013) Paleocene origin of the cockroach families Blaberidae and Corydiidae: evidence from Amur River region of Russia. Zootaxa 3635:117–126.  https://doi.org/10.11646/zootaxa.3625.2.2 CrossRefPubMedGoogle Scholar
  95. Vršanský PV, Šmídová L, Valaška D, Barna P, Vidlička L, Takáč P, Pavlik L, Kúdelová T, Karim TS, Zelagin D, Smith D (2016) Origin of origami cockroach reveals long-lasting (11 Ma) phenotype instability following viviparity. Sci Nat 103:78.  https://doi.org/10.1007/s00114-016-1398-4 CrossRefGoogle Scholar
  96. Vršanský P, Oružinský R, Aristov D, Wei DD, Vidlička L, Ren D (2017) Temporary deleterious mass mutations relate to originations of cockroach families. Biologia 72(8):886–912.  https://doi.org/10.1515/biolog-2017-0096 CrossRefGoogle Scholar
  97. Vršanský P, Bechly G, Zhang QQ, Jarzembowski J et al (2018a) Batesian insect-insect mimicry-related explosive radiation of ancient alienopterid cockroaches. Biologia 73:987–1006.  https://doi.org/10.2478/s11756-018-0117-3
  98. Vršanský P, Vršanská L, Beňo M et al. (2018b) Pathogenic DWV infection symptoms in a Cretaceous cockroach. Palaeontographica Abt A.  https://doi.org/10.1127/0375-0442/2018/0000/008
  99. Walker EM (1931) On the Anatomy of Grylloblatta campodeiformis Walker. 1. Exoskeleton and musculature of the head. Ann Entomol Soc Am 24:519–536CrossRefGoogle Scholar
  100. Wang B, Xia F, Engel MS, Perrichot V, Shi G, Zhang H, Chen J, Jarzembowski EA, Wappler T, Rust J (2016) Debris-carrying camouflage among diverse lineages of Cretaceous insects. Sci Adv 2:e1501918.  https://doi.org/10.1126/sciadv.1501918 CrossRefPubMedPubMedCentralGoogle Scholar
  101. Wang ZQ, Shi Y, Qiu ZW, Che YL, Lo N (2017) Reconstructing the phylogeny of Blattodea: robust support for interfamilial relationships and major clades. Sci Rep 7(3903)  https://doi.org/10.1038/s41598-017-04243-1
  102. Ward PS (2007) Phylogeny, classification, and species-level taxonomy of ants (Hymenoptera: Formicidae). Zootaxa 1668:549–563Google Scholar
  103. Wei D, Ren D (2013) Completely preserved cockroaches of the family Mesoblattinidae from the Upper Jurassic—lower cretaceous Yixian Formation (Liaoning Province, NE China). Geol Carpath 64:291–304.  https://doi.org/10.2478/geoca-2013-0021 CrossRefGoogle Scholar
  104. Wheeler WM (1900) A new myrmecophile from the mushroom gardens of the Texan leaf-cutting ant. Am Nat 34:851–862CrossRefGoogle Scholar
  105. Wieland F (2006) The cervical sclerites of Mantodea discussed in the context of dictyopteran phylogeny (Insecta: Dictyoptera). Entomol Abh 63:51–76Google Scholar
  106. Wieland F (2013) The phylogenetic system of Mantodea (Insecta: Dictyoptera). Spec Phylog Evol 3:3–222Google Scholar
  107. Wipfler B, Machida R, Mueller B, Beutel RG (2011) On the head morphology of Grylloblattodea (Insecta) and the systematic position of the order, with a new nomenclature for the head muscles of Dicondylia. Syst Entomol 36:241–266.  https://doi.org/10.1111/j.1365-3113.2010.00556.x CrossRefGoogle Scholar
  108. Wipfler B, Wieland F, DeCarlo F, Hörnschemeyer T (2012) Cephalic morphology of Hymenopus coronatus (Insecta: Mantodea) and its phylogenetic implications. Arthrop Struct Dev 41:87–100CrossRefGoogle Scholar
  109. Witte V, Janssen R, Eppenstein A, Maschwitz U (2002) Allopeas myrmekophilos (Gastropoda, Pulmonata), the first myrmecophilous mollusc living in colonies of the ponerine army ant Leptogenys distinguenda (Formicidae, Ponerinae). Insect Soc 49:301–305CrossRefGoogle Scholar
  110. Witte V, Leinggärtner A, Sabaß L, Hashim R, Foitzik S (2008) Symbiont microcosm in an ant society and the diversity of interspecific interactions. Anim Behav 76:1477–1486CrossRefGoogle Scholar
  111. Xia FY, Yang GD, Zhang QQ, Shi GG, Wang B (2015) Amber: life through time and space. Science Press, NanjingGoogle Scholar
  112. Yamamoto S, Maruyama M, Parker J (2016) Evidence for social parasitism of early insect societies by cretaceous rove beetles. Nat Commun 7:13658.  https://doi.org/10.1038/ncomms13658 CrossRefPubMedPubMedCentralGoogle Scholar
  113. Yamamoto S, Maruyama M, Parker J (2017) Evidence from amber for the origins of termitophily. Current Biology 27:R792–R794.  https://doi.org/10.1016/j.cub.2017.06.078
  114. Yin ZW (2018) Loeblibatrus Yin, a new genus of Myrmecophilous Pselaphinae (Coleoptera: Staphylinidae) from Southern China. Coleopt Bull 72(2):233–240.  https://doi.org/10.1649/0010-065X-72.2.233 CrossRefGoogle Scholar

Copyright information

© Institute of Zoology, Slovak Academy of Sciences 2018

Authors and Affiliations

  • Peter Vršanský
    • 1
    • 2
    • 3
    • 4
    • 5
    Email author
  • Lucia Šmídová
    • 6
  • Hemen Sendi
    • 7
  • Peter Barna
    • 3
  • Patrick Müller
    • 8
  • Sieghard Ellenberger
    • 9
  • Hao Wu
    • 10
  • Xiaoyin Ren
    • 5
  • Xiaojie Lei
    • 5
  • Dany Azar
    • 5
    • 11
  • Juraj Šurka
    • 12
  • Tao Su
    • 13
  • Weiyudong Deng
    • 13
  • Xianhui Shen
    • 13
  • Jun Lv
    • 14
  • Tong Bao
    • 5
    • 15
  • Günter Bechly
    • 16
  1. 1.Institute of ZoologySlovak Academy of SciencesBratislavaSlovakia
  2. 2.Institute of Physics, Research Centre of Quantum InformaticsSlovak Academy of SciencesBratislavaSlovakia
  3. 3.Earth Science InstituteSlovak Academy of SciencesBratislavaSlovakia
  4. 4.Palaeontological InstituteRussian Academy of SciencesMoscowRussia
  5. 5.State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and PalaeontologyChinese Academy of SciencesNanjingChina
  6. 6.Institute of Geology and Palaeontology, Faculty of ScienceCharles University in PraguePrague 2Czech Republic
  7. 7.Faculty of Natural SciencesComenius UniversityBratislavaSlovakia
  8. 8.KäshofenGermany
  9. 9.KasselGermany
  10. 10.Zhejiang Museum of Natural HistoryHangzhouChina
  11. 11.Natural Sciences Department, Faculty of Science II, FanarLebanese UniversityFanar – MatnLebanon
  12. 12.Earth Science InstituteSlovak Academy of SciencesBanská BystricaSlovakia
  13. 13.Paleoecology Research Group, CAS MenglunXishuangbanna Tropical Botanical GardenMenglaChina
  14. 14.Dian Jiang Collection, Zhao Jia Yue TaiBaoshanChina
  15. 15.Steinmann-InstitutAbteilung PaläontologieBonnGermany
  16. 16.BöblingenGermany

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