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Parasitic cockroaches indicate complex states of earliest proved ants

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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.

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References

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Barden P (2017) Fossil ants (Hymenoptera: Formicidae): ancient diversity and the rise of modem lineages. Myrmecol News 24:1–30

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Bell WJ, Roth LM, Nalepa CA (2007) Cockroaches - ecology, behavior, and natural history. The Johns Hopkins University Press, Baltimore

    Google Scholar 

  • Beutel RG, Gorb SN (2006) A revised interpretation of the evolution of attachment structures in Hexapoda with special emphasis on Mantophasmatodea. Arthropod Syst Phylogeny 61:3–35

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Beutel RG, Friedrich F, Ge SG, Yang XK (2014) Insect morphology and phylogeny. Walter De Gruyter, Berlin

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Bolívar I (1905) Les blattes myrmecophiles. Mitt Schweiz Entomol Ges 11:134–141

    Google Scholar 

  • Bradler S (2003) Lehrbuch der Speziellen Zoologie, Band 1: Wirbellose Tiere, 2nd edn. Spektrum Akademischer Verlag, Berlin, pp 251–261

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Brunner von Wattenwyl C (1882) Prodromus der Europäischen Orthopteren. Wilhelm Engelmann, Leipzig

    Google Scholar 

  • 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

  • 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

  • Capinera JL (2008) Encyclopedia of entomology. Kluwer, Dodrecht

    Book  Google Scholar 

  • Chopard L (1924) Description d'un Blattide myrmécophile nouveau [Orth.]. Bull Soc Entomol Fra 11-12:131–132

    Google Scholar 

  • Choufani J, Halabi WE, Azar D, Nel A (2015) First fossil insect from lower cretaceous Lebanese amber in Syria (Diptera: Ceratopogonidae). Cretac Res 54:106–116

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Eisner T (1958) Spray mechanism of the cockroach Diploptera punctata. Science 128:148–149

    Article  CAS  PubMed  Google Scholar 

  • 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 20:20.3.1FC

  • 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

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Giles ET (1963) The comparative external morphology and affinities of the Dermaptera. Ecol Entomol 115:95–164

    Google Scholar 

  • Grimaldi DA (2003) A revision of Cretaceous mantises and their relationships, including new taxa (Insecta : Dictyoptera : Mantodea). Am Mus Novit 3412:1–47

    Article  Google Scholar 

  • Grimaldi DA, Engel MS (2005) Evolution of the insects. Cambridge University Press, Cambridge

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Gurney AB (1937) Studies in certain genera of American Blattidae (Orthoptera). Proc Entomol Soc Wash 39:101–112

    Google Scholar 

  • Haas F (2006) Evidence from folding and functional lines of wings on inter-ordinal relationships in Pterygota. Arthropod Syst Phylogeny 64:149–158

    Google Scholar 

  • Hölldobler B, Wilson EO (1990) The ants. Belknap Press of Harvard University Press, Cambridge

    Book  Google Scholar 

  • Hörnig MK, Haug C, Haug JT (2013) New details of Santanmantis axelrodi and the evolution of the mantodean morphotype. Palaeodiversity 6:157–168

    Google Scholar 

  • 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

  • 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 206–223

    Google Scholar 

  • Hudson GB (1945) A study of the tentorium in some orthopteroid Hexapoda. J Entomol Soc S Africa 8:71–90

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Klass KD, Ehrmann R (2003) Lehrbuch der Speziellen Zoologie, Band 1: Wirbellose Tiere, 2nd edn. Spektrum Akademischer Verlag, Berlin, pp 182–197

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Klass KD, Eulitz U, Schmidt C, Barton A (2009) The tibiotarsal articulation and antertibiotarsal leg sclerite in Dictyoptera (Insecta). Ins Syst Evol 40(4):361–387

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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, Paris

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leverault P (1936) The morphology of the Carolina mantis. Univ Kans Sci Bull 24:206–259

    Google Scholar 

  • 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

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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 211–234

  • 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, Stockholm

    Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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 3:85–105

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

  • 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

    Article  PubMed  Google Scholar 

  • Moser JC (1964) Inquiline roach respond to trail-marking substance of leaf-cutting ants. Science 143:1048–1049

    Article  CAS  PubMed  Google Scholar 

  • 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

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

  • 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

    Article  Google Scholar 

  • 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

  • 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

    Article  Google Scholar 

  • Rähle W (1970) Untersuchungen an Kopf und Prothorax von Embia ramburi Rimsky-Korsakow, 1906 (Embioptera, Embiidae). Zool Jahrb Abt Anat Ontog Tiere 87:248–330

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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 17:219–225

    Google Scholar 

  • 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 208–235

    Google Scholar 

  • Roth LM (1995) Pseudoanaplectina yumotoi, a new ovoviviparous myrmecophilous cockroach genus and species from Sarawak (Blattaria: Blattellidae; Blattellinae). Psyche 102:79–87

    Article  Google Scholar 

  • Roth LM (2003) Systematics and phylogeny of cockroaches (Dictyoptera: Blattaria). Orient Insects 37:1–186. https://doi.org/10.1080/00305316.2003.10417344

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Scudder SH (1862) Materials for a monograph of the North American Orthoptera. H. O. Houghton, Cambridge

    Book  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Silvestri F (1946) Descrizione di due specie neotropicali di Zorotypus (Insecta, Zoraptera). Boll Lab Entomol Agrar Portici 7:1–12

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Song XB, Li LZ (2014) Three new species of the myrmecophilous genus Doryloxenus from China (Coleoptera, Staphylinidae, Aleocharinae). Zookeys 456:75–83

    Article  Google Scholar 

  • Tang JW, Zhang JH, Song QS, Feng ZY (1999) Community analysis on secondary tropical vegetations in Xishuangbanna. Chin J Appl Ecol 10:135–139

    Google Scholar 

  • 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 64–77

  • Vršanský P (1999) Lower Cretaceous Blattodea. In: Vršanský P (Ed) Proc. 1st Intern. Paleoentomol. Conf. Moscow 1998. Amba projekty Bratislava, pp 167–176

  • Vršanský P (2002) Origin and the early evolution of mantises. Amba projekty 6:1–16

    Google Scholar 

  • Vršanský P (2003) Umenocoleoidea – an amazing lineage of aberrant insects (Insecta, Blattaria). Amba projekty 7:1–32

    Google Scholar 

  • Vršanský P (2008) Central ocellus of extinct cockroaches (Blattida: Caloblattinidae). Zootaxa 1958:41–50

    Article  Google Scholar 

  • Vršanský P (2009) Albian cockroaches (Insecta, Blattida) from French amber of Archingeay. Geodiversitas 31:73–98

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

  • 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

  • Walker EM (1931) On the Anatomy of Grylloblatta campodeiformis Walker. 1. Exoskeleton and musculature of the head. Ann Entomol Soc Am 24:519–536

    Article  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

  • Ward PS (2007) Phylogeny, classification, and species-level taxonomy of ants (Hymenoptera: Formicidae). Zootaxa 1668:549–563

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Wheeler WM (1900) A new myrmecophile from the mushroom gardens of the Texan leaf-cutting ant. Am Nat 34:851–862

    Article  Google Scholar 

  • Wieland F (2006) The cervical sclerites of Mantodea discussed in the context of dictyopteran phylogeny (Insecta: Dictyoptera). Entomol Abh 63:51–76

    Google Scholar 

  • Wieland F (2013) The phylogenetic system of Mantodea (Insecta: Dictyoptera). Spec Phylog Evol 3:3–222

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Wipfler B, Wieland F, DeCarlo F, Hörnschemeyer T (2012) Cephalic morphology of Hymenopus coronatus (Insecta: Mantodea) and its phylogenetic implications. Arthrop Struct Dev 41:87–100

    Article  CAS  Google Scholar 

  • 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 49:301–305

    Article  Google Scholar 

  • 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 76:1477–1486

    Article  Google Scholar 

  • Xia FY, Yang GD, Zhang QQ, Shi GG, Wang B (2015) Amber: life through time and space. Science Press, Nanjing

    Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

  • 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

    Article  Google Scholar 

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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).

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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.

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Correspondence to Peter Vršanský.

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Vršanský, P., Šmídová, L., Sendi, H. et al. Parasitic cockroaches indicate complex states of earliest proved ants. Biologia 74, 65–89 (2019). https://doi.org/10.2478/s11756-018-0146-y

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