Skip to main content Skip to main navigation menu Skip to site footer
Type: Article
Published: 2021-08-31
Page range: 374–389
Abstract views: 1445
PDF downloaded: 31

Further evidence of Cretaceous termitophily: Description of new termite hosts of the trichopseniine Cretotrichopsenius (Coleoptera: Staphylinidae), with emendations to the classification of lower termites (Isoptera)

College of Marine Science and Biological Engineering, Qingdao University of Science and Technology, Qingdao, China
College of Marine Science and Biological Engineering, Qingdao University of Science and Technology, Qingdao, China
Kansas Department of Agriculture, Kansas, USA, Division of Entomology, Natural History Museum, University of Kansas, Lawrence, Kansas, USA
College of Marine Science and Biological Engineering, Qingdao University of Science and Technology, Qingdao, China
State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology, and Centre for Excellence in Life and Paleoenvironment, Chinese Academy of Sciences, Nanjing, China
School of Earth Sciences, University of Bristol, Bristol, UK
State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology, and Centre for Excellence in Life and Paleoenvironment, Chinese Academy of Sciences, Nanjing, China
College of Marine Science and Biological Engineering, Qingdao University of Science and Technology, Qingdao, China
Division of Entomology, Natural History Museum, University of Kansas, Lawrence, Kansas, USA, Department of Ecology & Evolutionary Biology, University of Kansas, Lawrence, Kansas, USA
State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology, and Centre for Excellence in Life and Paleoenvironment, Chinese Academy of Sciences, Nanjing, China, School of Earth Sciences, University of Bristol, Bristol, UK
Termites Rove beetles Symbionts Myanmar amber Trichopseniini Coleoptera Staphylinidae

Abstract

Termites (Isoptera) are among the most ecologically ubiquitous of terrestrial eusocial insects and provide an attractive environment for symbionts, which have evolved numerous times independently, and in lineages as diverse as millipedes and beetles. Previous studies reported the discovery of unequivocal termitophily in mid-Cretaceous amber from northern Myanmar, providing evidence that pushed the origin of termitophily back into the Mesozoic. Here we report the discovery of two more pieces of Cretaceous amber containing individuals of the trichopseniine rove beetle Cretotrichopsenius burmiticus Cai et al., 2017 (Staphylinidae: Aleocharinae: Trichopseniini) preserved together with their potential host termites, providing further evidence regarding the association between these two insect lineages. Two new termite species and genera are described as putative hosts for C. burmiticus: Arceotermes hospitis Engel & Jiang, gen. et sp. nov. and Tanytermitalis philetaerus Engel & Cai, gen. et sp. nov. Each is included in a new family, Arceotermitidae Engel, fam. nov. (type genus: Arceotermes Engel & Jiang, gen. nov.), and Tanytermitidae Engel, fam. nov. (type genus: Tanytermes Engel et al., 2007). In order to better characterize these two families the classification of lower Isoptera and clade Xylophagodea (= Cryptocercidae + Isoptera) is emended with the following new taxa: Idanotermitinae Engel, subfam. nov.; Melqartitermitidae Engel, fam. nov.; Mylacrotermitidae Engel, fam. nov.; Krishnatermitidae Engel, fam. nov.; Cosmotermitinae Engel, subfam. nov.; Hodotermopsinae Engel, subfam. nov.; Artisoptera Engel, minord. nov.; Cryptocercaptera Engel, infraord. nov. Lower termites were remarkably diverse during the mid-Cretaceous but declined in diversity considerably by the Palaeogene. The fossil rove beetle Cretotrichopsenius Cai et al., 2017 currently provides the earliest definitive evidence of termitophily and the complex association between rove beetles and termites.

References

  1. Ahmad, M. (1950) The phylogeny of termite genera based on imago-worker mandibles. Bulletin of the American Museum of Natural History, 95 (2), 37–86.
  2. Banks, N. (1906) Two new termites. Entomological News, 17 (9), 336–337.
  3. Barden, P. & Engel, M.S. (2021) Fossil social insects. In: Starr, C.K. (Ed.), Encyclopedia of social insects. Springer Nature, Cham, pp. 384–403. https://doi.org/10.1007/978-3-319-90306-4_45-1
  4. Bourguignon, T., Lo, N., Cameron, S.L., Šobotník, J., Hayashi, Y., Shigenobu, S., Watanabe, D., Roisin, Y., Miura, T. & Evans, T.A. (2015) The evolutionary history of termites as inferred from 66 mitochondrial genomes. Molecular Biology and Evolution, 32 (2), 406–421. https://doi.org/10.1093/molbev/msu308
  5. Brullé, G.A. (1832) Expédition scientifique de Morée. Section des Sciences Physiques. Tome III. Partie 1. Zoologie. Deuxième Section—Des Animaux Articulés. Levrault, Paris & Strasbourg, York, pp. 1–240.
  6. Buček, A., Šobotník, J., He, S., Shi, M., McMahon, D.P., Holmes, E.C., Roisin, Y., Lo, N. & Bourguignon, T. (2019) Evolution of termite symbiosis informed by transcriptome-based phylogenies. Current Biology, 29 (21), 3278–3734. https://doi.org/10.1016/j.cub.2019.08.076
  7. Cai, C.Y., Huang, D.Y., Newton, A.F., Eldredge, K.T. & Engel, M.S. (2017a) Early evolution of specialized termitophily in Cretaceous rove beetles. Current Biology, 27 (8), 1229– 1235. https://doi.org/10.1016/j.cub.2017.03.009
  8. Cai, C.Y., Huang, D.Y., Newton, A.F., Eldredge, K.T. & Engel, M.S. (2017b) Response to “evidence from amber for the origins of termitophily”. Current Biology, 27 (16), R794–R795. https://doi.org/10.1016/j.cub.2017.06.083
  9. Chouvenc, T., Šobotník, J., Engel, M.S. & Bourguignon, T. (2021) Termite evolution: mutualistic associations, key innovations, and the rise of Termitidae. Cellular Molecular Life Sciences, 78 (6), 2749–2769. https://doi.org/10.1007/s00018-020-03728-z
  10. Cruickshank, R.D. & Ko, K. (2003) Geology of an amber locality in the Hukawng Valley, northern Myanmar. Journal of Asian Earth Sciences, 21 (5), 441–455. https://doi.org/10.1016/S1367-9120(02)00044-5
  11. Desneux, J. (1904a) A propos de la phylogénie des Termitides. Annales de la Société Entomologique de Belgique, 48 (8), 278–286.
  12. Desneux, J. (1904b) A new termite from India. Journal of the Bombay Natural History Society, 15, 445–446.
  13. Emerson, A.E. (1933) A revision of the genera of fossil and Recent Termopsinae (Isoptera). University of California Publications in Entomology, 6 (6), 165–196.
  14. Engel, M.S. (2008) Two new termites in Baltic amber (Isoptera). Journal of the Kansas Entomological Society, 81 (3), 194–203. https://doi.org/10.2317/JKES-0802.01.1
  15. Engel, M.S. (2014) A termite (Isoptera) in Late Cretaceous amber from Vendée, northwestern France. Paleontological Contributions, 10E, 21–24. https://doi.org/10.17161/PC.1808.15985
  16. Engel, M.S. (2020) Myanmar: palaeontologists must stop buying conflict amber. Nature, 584 (7822), 525. https://doi.org/10.1038/d41586-020-02432-z
  17. Engel, M.S. & Delclòs, X. (2010) Primitive termites in Cretaceous amber from Spain and Canada (Isoptera). Journal of the Kansas Entomological Society, 83 (2), 111–128. https://doi.org/10.2317/JKES0908.06.1
  18. Engel, M.S., Grimaldi, D.A. & Krishna, K. (2007) Primitive termites from the Early Cretaceous of Asia (Isoptera). Stuttgarter Beiträge zur Naturkunde, Serie B, Geologie und Paläontologie, 371, 1–32.
  19. Engel, M.S., Grimaldi, D.A. & Krishna, K. (2009) Termites (Isoptera): their phylogeny, classification, and rise to ecological dominance. American Museum Novitates, 3650, 1–27. https://doi.org/10.1206/651.1
  20. Engel, M.S., Nel, A., Azar, D., Soriano, C., Tafforeau, P., Néraudeau, D., Colin, J.-P. & Perrichot, V. (2011) New, primitive termites (Isoptera) from Early Cretaceous ambers of France and Lebanon. Palaeodiversity, 4, 39–49.
  21. Engel, M.S., Barden, P., Riccio, M.L. & Grimaldi, D.A. (2016) Morphologically specialized termite castes and advanced sociality in the Early Cretaceous. Current Biology, 26 (4), 522–530. https://doi.org/10.1016/j.cub.2015.12.061
  22. Froggatt, W.W. (1897) Australian Termitidae, Part II. Proceedings of the Linnean Society of New South Wales, 21 (4), 510–552, + pls. xxxv–xxxvi. https://doi.org/10.5962/bhl.part.8483
  23. Froggatt, W.W. (1898) Australian Termitidae, Part III. Proceedings of the Linnean Society of New South Wales, 22 (4), 721–758, + pls. xxxiv–xxxv. https://doi.org/10.5962/bhl.part.12741
  24. Goloboff, P.A. & Catalano, S.A. (2016) TNT version 1.5, including a full implementation of phylogenetic morphometrics. Cladistics, 32 (3), 221–238. https://doi.org/10.1111/cla.12160
  25. Grimaldi, D.A., Engel, M.S. & Nascimbene, P.C. (2002) Fossiliferous Cretaceous amber from Myanmar (Burma): its rediscovery, biotic diversity, and paleontological significance. American Museum Novitates, 3361, 1–72. https://doi.org/10.1206/0003-0082(2002)361<0001:FCAFMB>2.0.CO;2
  26. Hagen, H. (1858) Monographie der Termiten. Linnaea Entomologica, 12, 1–342.
  27. Hill, G.F. (1927) Termites from the Australian region—Part I. Memoirs of the National Museum, Melbourne, 7 (1), 5–120, + 9 pls. https://doi.org/10.24199/j.mmv.1927.7.01
  28. Holmgren, N. (1911) Termitenstudien: 2. Systematik der Termiten. Die Familien Protermitidae und Mesotermitidae. Kungliga Svenska Vetenskapsakademiens Handlingar, 46 (6), 1–86.
  29. Horn, G.H. (1877) Synopsis of the genera and species of the staphylinide tribe Tachyporini of the United States. Transactions of the American Entomological Society, 6, 81– 128, + 1 pl. https://doi.org/10.2307/25076320
  30. ICZN [International Commission on Zoological Nomenclature]. (1999) International Code of Zoological Nomenclature (4th ed.). (London: International Trust for Zoological Nomenclature).
  31. Jouault, C., Legendre, F., Grandcolas, P. & Nel, A. (2021) Revising dating estimates and the antiquity of eusociality in termites using the fossilized birth-death process. Systematic Entomology, 46 (3), 592–610. https://doi.org/10.1111/syen.12477
  32. Kistner, D.H. (1969) The biology of termitophiles. In: Krishna, K. & Weesner, F.M. (Eds), Biology of termites. Academic Press, New York, pp. 525–557. https://doi.org/10.1016/B978-0-12-395529-6.50021-0
  33. Kistner, D.H. (1982) The social insects’ bestiary. In: Hermann, H.R. (Ed.), Social insects. Volume 3. Academic Press, New York, pp. 1–244. https://doi.org/10.1016/B978-0-12-342203-3.50008-4
  34. Kistner, D.H. (1998) New species of termitophilous Trichopseniinae (Coleoptera: Staphylinidae) found with Mastotermes darwiniensis in Australia and in Dominican amber. Sociobiology, 31, 51–76.
  35. Krishna, K., Grimaldi, D.A., Krishna, V. & Engel, M.S. (2013) Treatise on the Isoptera of the world. Bulletin of the American Museum Natural History, 377, 1–2704. https://doi.org/10.1206/377.1
  36. LeConte, J.L. (1863) New species of North American Coleoptera. Part I. Smithsonian Miscellaneous Collections, 6 (167), 1–86. https://doi.org/10.5962/bhl.title.51303
  37. LeConte, J.L. (1880) Short studies of North American Coleoptera. Transactions of the American Entomological Society, 8, 163–218. https://doi.org/10.2307/25076392
  38. Legendre, F., Nel, A., Svenson, G.J., 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 (7), e0130127. https://doi.org/10.1371/journal.pone.0130127
  39. Maddison, W.P. & Maddison, D.R. (2019) Mesquite: a modular system for evolutionary analysis. Version 3.61 [http://www.mesquiteproject.org]
  40. Pasteels, J.M. & Kistner, D.H. (1971) Revision of the termitophilous subfamily Trichopseniinae (Coleoptera: Staphylinidae). II. The remainder of the genera with a representative study of the gland systems and a discussion of their relationships. Miscellaneous publications of the Entomological Society of America, 7, 351–399.
  41. Sánchez-García, A., Peñalver, E., Delclòs, X. & Engel, M.S. (2020) Early Cretaceous termites in amber from northern Spain (Isoptera). Cretaceous Research, 110, 1–10. https://doi.org/10.1016/j.cretres.2020.104385
  42. Seevers, C.H. (1945) New genera and species of Trichopseniinae from American and Australian termite nests (Coleoptera, Staphylinidae). Pan-Pacific Entomologist, 21 (2), 63–72.
  43. Seevers, C.H. (1957) A monograph on the termitophilous Staphylinidae (Coleoptera). Fieldiana Zoology, 40, 1–334. https://doi.org/10.5962/bhl.title.3797
  44. Shi, C., Cai, H.H., Jiang, R.X., Wang, S., Engel, M.S., Yuan, J., Bai, M., Yang, D., Long, C.L., Zhao, Z.T., Zhang, D.X., Zhang, X.C., Peng, H., Wang, Y.D. & Spicer, R.A. (2021) Balance scientific and ethical concerns to achieve a nuanced perspective on ‘blood amber’. Nature Ecology & Evolution, 5 (6), 705–706. https://doi.org/10.1038/s41559-021-01479-z
  45. Shi, G., Grimaldi, D.A., Harlow, G.E., Wang, J., Wang, J., Yang, M., Lei, W., Li, Q. & Li, X. (2012) Age constraint on Burmese amber based on U-Pb dating of zircons. Cretaceous Research, 37, 155–163. https://doi.org/10.1016/j.cretres.2012.03.014
  46. Sokal, R.R. & Sneath, P.H.A. (1963) Principles of numerical taxonomy. Freeman and Co., San Francisco, pp. 1–573.
  47. Sjöstedt, Y. (1926) Revision der Termiten Afrikas: 3. Monographie. Kungliga Svenska Vetenskapsakademiens Handlingar, 3 (3), 1–419.
  48. Szwedo, J., Wang, B., Soszyńska-Maj, A., Azar, D. & Ross, A.J. (2020) International Palaeoentomological Society statement. Palaeoentomology, 3 (3), 221–222. https://doi.org/10.11646/palaeoentomology.3.3.1
  49. Ware, J.L., Grimaldi, D.A. & Engel, M.S. (2010) The effects of fossil placement and calibration on divergence times and rates: an example from the termites (Insecta: Isoptera). Arthropod Structure and Development, 39 (2–3), 204–219. https://doi.org/10.1016/j.asd.2009.11.003
  50. Wilson, E.O. (1971) The insect societies. Harvard University Press, Cambridge, pp. 1–548.
  51. Yamamoto, S., Maruyama, M. & Parker, J. (2016) Evidence for social parasitism of early insect societies by Cretaceous rove beetles. Nature Communications, 7, 13658. https://doi.org/10.1038/ncomms13658
  52. Yamamoto, S., Maruyama, M. & Parker, J. (2017) Evidence from amber for the origins of termitophily. Current Biology, 27 (16), R792–R794. https://doi.org/10.1016/j.cub.2017.06.078
  53. Yu, T.T., Kelly, R., Mu, L., Ross, A., Kennedy, J., Broly, P., Xia, F.Y., Zhang, H.C., Wang, B. & Dilcher, D. (2019) An ammonite trapped in Burmese amber. Proceedings of the National Academy of Sciences of the United States of America, 116 (23), 11345–11350. https://doi.org/10.1073/pnas.1821292116
  54. Zhao, Z.P., Eggleton, P., Yin, X.C., Gao, T.P., Shih, C.K. & Ren, D. (2019) The oldest known mastotermitids (Blattodea: Termitoidae) and phylogeny of basal termites. Systematic Entomology, 44 (3), 612–623. https://doi.org/10.1111/syen.12344
  55. Zhao, Z.P., Yin, X.C., Shih, C.K., Gao, T.P. & Ren, D. (2020) Termite colonies from mid-Cretaceous Myanmar demonstrate their early eusocial lifestyle in damp wood. National Science Review, 7 (2), 381–390. https://doi.org/10.1093/nsr/nwz141