Skip to main content Skip to main navigation menu Skip to site footer
Type: Monograph
Published: 2024-12-16
Page range: 1-78
Abstract views: 149
PDF downloaded: 9

Seven new species from Eocene Baltic amber reveal surprising diversity and suggest possible speciation scenarios in the relictual family Collohmanniidae (Acari: Oribatida)

Papanin Institute for Biology of Inland Waters; Russian Academy of Sciences; 152742 Borok; Yaroslavl Province; Russia; Institute of Environmental and Agricultural Biology (X-BIO); Tyumen State University; 625003 Tyumen; Russia
Koltzov Institute of Developmental Biology; Russian Academy of Sciences; 119334 Moscow; Russia; Borissiak Paleontological Institute; Russian Academy of Sciences; 117647 Moscow; Russia
Borissiak Paleontological Institute; Russian Academy of Sciences; 117647 Moscow; Russia
Acari oribatid mites biodiversity sexual dimorphism sympatric allopatric paleodiversity new species biogeography female choice

Abstract

This study provides a comprehensive morphological analysis of ten fossil specimens from the genus Collohmannia, found in Eocene Baltic amber, with nine representing different species. Collohmanniidae, a unique monogeneric family of oribatid mites are among the largest oribatids. They feed on leaf litter and present significant sexual dimorphism and courtship behavior, which includes the transfer of nuptial food from male to female. Extant Collohmannia species inhabit isolated mountain forest areas. A fragmentation hypothesis has been proposed to account for their highly disjunctive distribution, suggesting that climate change divided a large forest area previously occupied by a parent species, leading to the allopatric evolution of several species of Collohmannia. However, with the discovery of a significant number of fossil species in Eocene Baltic amber we propose an alternate hypothesis with the Baltic amber forest serving as an arena for speciation of Collohmanniidae. According to it, the driving force of speciation was dietary and was based on gut microbiome specificity, reinforced by the female choice during the courtship ritual. In this paper we describe seven new fossil species of Collohmannia (C. sellnicki sp. nov., C. albertii sp. nov., C. nortoni sp. nov., C. groehni sp. nov., C. kerneggeri sp. nov., C. weiterschani sp. nov., C. clavata sp. nov.), re-describe C. schusteri based on study of the holotype, synonymize Embolacarus with Collohmannia, propose and describe the neotype of C. pergrata comb. nov., and provide a key to all described Collohmanniidae. Together with the hypotheses of speciation we propose verification experiments to be performed on extant Collohmannia mites.

 

References

  1. Alberti, G. & Schuster, R. (2005) Behavioural and ultrastructural peculiarities of reproduction in Collohmannia gigantea (Oribatida: Mixonomata). In: Weigmann, G., Alberti, G., Wohltmann, A. & Ragusa, A. (Eds.), Acarine Biodiversity in the Natural and Human Sphere. Proceedings of the V Symposium of the European Association of Acarologists (Berlin 2004). Phytophaga, Palermo, 14, pp. 129–140.
  2. Behan-Pelletier, V.M. & Eamer, B. (2010) The first sexually dimorphic species of Oribatella (Acari, Oribatida, Oribatellidae) and a review of sexual dimorphism in the Brachypylina. Zootaxa, 2332 (1), 1–20. https://doi.org/10.11646/zootaxa.2332.1.1
  3. Brucker, R.M. & Bordenstein, S.R. (2012) Speciation by symbiosis. Trends in Ecology & Evolution, 27 (8), 443–451. https://doi.org/10.1016/j.tree.2012.03.011
  4. Brucker, R.M. & Bordenstein, S.R. (2013) The hologenomic basis of speciation: gut bacteria cause hybrid lethality in the genus Nasonia. Science, 341 (6146), 667–669. https://doi.org/10.1126/science.1240659
  5. Bukejs, A., Alekseev, V.I. & Pollock, D.A. (2019) Waidelotinae, a new subfamily of Pyrochroidae (Coleoptera: Tenebrionoidea) from Baltic amber of the Sambian peninsula and the interpretation of Sambian amber stratigraphy, age and location. Zootaxa, 4664 (2), 261–273. https://doi.org/10.11646/zootaxa.4664.2.8
  6. Chao, A. & Chiu, C.-H. (2016) Species richness: estimation and comparison. In: Wiley StatsRef: Statistics Reference Online. John Wiley & Sons, Ltd., Chichester, pp. 1–26. https://doi.org/10.1002/9781118445112.stat03432.pub2
  7. Christov, V.V. (1970) New species of the oribatid mites in the soils of Tadzikistan. In: Bulanova-Zakhvatkina, E.M., Gilyarov, M.S., Krivolutsky, D.A., Petrova-Nikitina, A.D., Eitminavičiũtė, I.S. & Aukshtikalnene, A.M. (Eds.), Oribatei and their role in the process of the soil formation. Academy of Sciences of the Lithuanian SSR, Vilnius, pp. 155–160.
  8. Colwell, R.K. (2013) EstimateS: statistical estimation of species richness and shared species from samples. Version 9. User’s Guide and application published at: https://www.robertkcolwell.org/pages/estimates (accessed 21 August 2024)
  9. Colwell, R.K. & Elsensohn, J.E. (2014) EstimateS turns 20: statistical estimation of species richness and shared species from samples, with non-parametric extrapolation. Ecography, 37 (6), 609–613. https://doi.org/10.1111/ecog.00814
  10. Colwell, R.K., Mao, C.X. & Chang, J. (2004) Interpolating, extrapolating, and comparing incidence-based species accumulation curves. Ecology, 85 (10), 2717–2727. https://doi.org/10.1890/03-0557
  11. Damián Chávez, M. de J., Villegas Guzmán, G.A. & Lozano Román, L.F. (2019) Ácaros asociados a nidos de águila real (Aquila chrysaetos canadensis) (Falconiformes: Accipitridae) en México. Acta zoológica mexicana 35. https://doi.org/10.21829/azm.2019.3502196
  12. Díaz-Sánchez, S., Estrada-Peña, A. & Cabezas-Cruz, A. & de la Fuente J. (2019) Evolutionary insights into the tick hologenome. Trends in Parasitology, 35 (9), 725–737. https://doi.org/10.1016/j.pt.2019.06.014
  13. Gafarova, E., Kuracji, D., Sogomonyan, K., Gorokhov, I., Polev, D., Zubova, E., Golikova, E., Granovitch, A. & Maltseva, A. (2023) Gut bacteriomes and ecological niche divergence: an example of two cryptic gastropod species. Biology, 12 (12), 1521. https://doi.org/10.3390/biology12121521
  14. Gong, X., Chen, T.-W., Zieger, S.L., Bluhm, C., Heidemann, K., Schaefer, I., Maraun, M., Liu, M. & Scheu, S. (2018) Phylogenetic and trophic determinants of gut microbiota in soil oribatid mites. Soil Biology and Biochemistry, 123, 155–164. https://doi.org/10.1016/j.soilbio.2018.05.011
  15. Grandjean, F. (1966) Collohmannia gigantea Selln. (Oribate). Première partie. Acarologia, 8 (2), 328–357.
  16. Grandjean, F. (1969) Considérations sur le classement des Oribates. Leur division en 6 groupes majeurs. Acarologia, 11, 127–153.
  17. Hoffeins, C. & Hoffeins, H.W. (2003) Untersuchungen über die Häufigkeit von Inklusen in Baltischem und Bitterfelder Bernstein (Tertiär, Eozän) aus unselektierten Aufsammlungen unter besonderer Berücksichtigung der Ordnung Diptera. Studia dipterologica, 10 (2), 381–392. [in German]
  18. International Commission on Zoological Nomenclature (2018) Opinion 2419 (Case 3674) Collohmannia Sellnick, 1922 (Arachnida, Acari, Oribatida): conditional precedence granted over Embolacarus Sellnick, 1919. Bulletin of Zoological Nomenclature, 75, 264–266. https://doi.org/10.21805/bzn.v75.a056
  19. Jackson, R., Patapiou, P.A., Golding, G., Helanterä, H., Economou, C.K., Chapuisat, M. & Henry, L.M. (2023) Evidence of phylosymbiosis in Formica ants. Frontiers in Microbiology, 14, 1044286. https://doi.org/10.3389/fmicb.2023.1044286
  20. Kohl, K.D., Varner, J., Wilkening, J.L. & Dearing, M.D. (2018) Gut microbial communities of American pikas (Ochotona princeps): Evidence for phylosymbiosis and adaptations to novel diets. Journal of Animal Ecology, 87 (2), 323–330. https://doi.org/10.1111/1365-2656.12692
  21. Lienhard, A. & Krisper, G. (2021) Hidden biodiversity in microarthropods (Acari, Oribatida, Eremaeoidea, Caleremaeus). Scientific Reports, 11 (1), 23123. https://doi.org/10.1038/s41598-021-02602-7
  22. Li, J., Wei, X., Huang, D. & Xiao, J. (2022) The phylosymbiosis pattern between the fig wasps of the same genus and their associated microbiota. Frontiers in Microbiology, 12, 800190. https://doi.org/10.3389/fmicb.2021.800190
  23. Mänd, K., Muehlenbachs, K., McKellar, R.C., Wolfe, A.P. & Konhauser, K.O. (2018) Distinct origins for Rovno and Baltic ambers: Evidence from carbon and hydrogen stable isotopes. Palaeogeography, Palaeoclimatology, Palaeoecology, 505, 265–273. https://doi.org/10.1016/j.palaeo.2018.06.004
  24. Norton, R.A. (2006) First record of Collohmannia (C. schusteri n. sp.) and Hermannia (H. sellnicki n. sp.) from Baltic amber, with notes on Sellnick’s genera of fossil oribatid mites (Acari: Oribatida). Acarologia, 46 (1–2), 111–125.
  25. Norton, R.A. (2007) Holistic acarology and ultimate causes: examples from the oribatid mites. In: Morales-Malacara, J.B., Behan-Pelletier, V., Ueckermann, E., Pérez, T.M., Estrada-Venegas, E.G. & Badii, M. (Eds.), Acarology XI: Proceedings of the International Congress, Universidad Nacional Autónoma de México, Sociedad Latinoamericana de Acarología, Mexico, pp. 3–20.
  26. Norton, R.A. & Alberti, G. (1997) Porose integumental organs of oribatid mites (Acari, Oribatida). 3. Evolutionary and ecological aspects. Zoologica, 146, 115–143.
  27. Norton, R.A. & Behan-Pelletier, V.M. (2009) Chapter 15, Oribatida. In: Krantz, G.W. & Walter, D.E. (Eds.), A Manual of Acarology. Texas Tech University Press. Lubbock, Texas, pp. 430–564.
  28. Norton, R.A. & Fuangarworn, M. (2015) Nanohystricidae n. fam., an unusual, plesiomorphic enarthronote mite family endemic to New Zealand (Acari, Oribatida). Zootaxa, 4027 (2), 151–204. https://doi.org/10.11646/zootaxa.4027.2.1
  29. Norton, R.A., Kethley, J., Johnston, D.E. & OConnor, B.M. (1993) Phylogenetic perspectives on genetic systems and reproductive modes of mites. In: Wrensch, D.L. & Ebbert, M.A. (Eds.), Evolution and Diversity of Sex Ratio in Insects and Mites. Chapman & Hall, New York and London, pp. 8–99.
  30. Norton, R.A. & Sidorchuk, E.A. (2014) Collohmannia johnstoni n. sp. (Acari, Oribatida) from West Virginia (U.S.A.), including description of ontogeny, setal variation, notes on biology and systematics of Collohmanniidae. Acarologia, 54 (3), 271–334. https://doi.org/10.1051/acarologia/20142134
  31. Norton, R.A. & Sidorchuk, E.A. (2015) Case 3674 Collohmannia Sellnick, 1922 (Arachnida, Acari, Oribatida): proposed conservation by giving it precedence over the senior subjective synonym Embolacarus Sellnick, 1919. Bulletin of Zoological Nomenclature, 72 (1), 33–40. https://doi.org/10.21805/bzn.v72i1.a9
  32. Oliveira, A.R., Norton, R.A., de Moraes, G.J. & Faccini, J.L.H. (2007) Preliminary observations on courtship behaviour in Mochloribatula (Oribatida: Mochlozetidae). In: Morales-Malacara, J.B., Behan-Pelletier, V., Ueckermann, E., Pérez, T.M., Estrada-Venegas, E.G. & Badii, M. (Eds.), Acarology XI: Proceedings of the International Congress. Universidad Nacional Autónoma de México, Sociedad Latinoamericana de Acarología, Mexico City, pp. 715–718
  33. Penney, D. & Preziosi, R.F. (2013) Estimating fossil ant species richness in Eocene Baltic amber. Acta Palaeontologica Polonica, 59 (4), 927–929. https://doi.org/10.4202/app.00097.2014
  34. Pfingstl T. (2013) Habitat use, feeding and reproductive traits of rocky-shore intertidal mites from Bermuda (Oribatida: Fortuyniidae and Selenoribatidae). Acarologia, 53(4), 369–382. https://doi.org/10.1051/acarologia/20132101
  35. Pfingstl, T. & Kerschbaumer, M. (2022) Sexually dimorphic claws predict courtship and mating sequence in the intertidal oribatid mite Fortuynia atlantica (Acari, Oribatida). Acarologia, 62 (3), 666–671. https://doi.org/10.24349/55m8-v2ub
  36. Pfingstl, T., Krisper, G. & Schuster, R. (2005) Morphological analysis of the nymphal stages of Collohmannia gigantea Sellnick (Acari: Oribatida, Collohmanniidae). International Journal of Acarology, 31 (4), 367–374. https://doi.org/10.1080/01647950508683677
  37. Pfingstl, T., Lienhard, A. & Baumann, J. (2019a) New and cryptic species of intertidal mites (Acari, Oribatida) from the Western Caribbean – an integrative approach. International Journal of Acarology, 45, 10–25. https://doi.org/10.1080/01647954.2018.1532458
  38. Pfingstl, T., Baumann, J. & Lienhard, A. (2019b) The Caribbean enigma: the presence of unusual cryptic diversity in intertidal mites (Arachnida, Acari, Oribatida). Organisms Diversity & Evolution, 19, 609–623. https://doi.org/10.1007/s13127-019-00416-0
  39. Pfingstl, T., Lienhard, A., Baumann, J. & Koblmüller, S. (2021) A taxonomist‘s nightmare – Cryptic diversity in Caribbean intertidal arthropods (Arachnida, Acari, Oribatida). Molecular Phylogenetics and Evolution, 163, 107–240. https://doi.org/10.1016/j.ympev.2021.107240
  40. Pfingstl, T., Bardel‐Kahr, I. & Schäffer, S. (2023) The Caribbean intertidal mite Alismobates inexpectatus (Acari, Oribatida), an unexpected case of cryptic diversity? Organisms Diversity & Evolution, 23, 811–832. https://doi.org/10.1007/s13127-023-00624-9
  41. Raspotnig, G. (2006) Chemical alarm and defence in the oribatid mite Collohmannia gigantea (Acari: Oribatida). Experimental and Applied Acarology, 39 (3), 177–194. https://doi.org/10.1007/s10493-006-9015-4
  42. Raspotnig, G., Schuster, R. & Krisper, G. (2003) Functional anatomy of oil glands in Collohmannia gigantea (Acari, Oribatida). Zoomorphology, 122 (3), 105–112. https://doi.org/10.1007/s00435-003-0075-2
  43. Raspotnig, G., Schuster, R., Krisper, G., Fauler, G. & Leis, H.-J. (2001) Chemistry of the oil gland secretion of Collohmannia gigantea (Acari: Oribatida). Experimental and Applied Acarology, 25 (12), 933–946. https://doi.org/10.1023/A:1020634215709
  44. Reeves, R.M. (1998) Biogeography of Carabodidae (Acari: Oribatida) in North America. Applied Soil Ecology, 9 (1–3), 59–62. https://doi.org/10.1016/S0929-1393(98)00054-7
  45. Rudman, S.M., Greenblum, S., Hughes, R.C., Rajpurohit, S., Kiratli, O., Lowder, D.B., Lemmon, S.G., Petrov, D.A., Chaston, J.M. & Schmidt, P. (2019) Microbiome composition shapes rapid genomic adaptation of Drosophila melanogaster. Proceedings of the National Academy of Sciences, 116 (40), 20025–20032. https://doi.org/10.1073/pnas.1907787116
  46. Sadowski, E.-M., Schmidt, A., Seyfullah, L. & Kunzmann, L. (2017) Conifers of the ‘Baltic Amber Forest’ and their palaeoecological significance. Stapfia, 106, 1–73.
  47. Sadowski, E.-M., Schmidt, A.R. & Denk, T. (2020) Staminate inflorescences with in situ pollen from Eocene Baltic amber reveal high diversity in Fagaceae (oak family). Willdenowia, 50 (3), 405–517. https://doi.org/10.3372/wi.50.50303
  48. Schatz, H., Behan-Pelletier, V.M., OConnor, B.M. & Norton, R.A. (2011) Suborder Oribatida van der Hammen, 1968. In: Zhang, Z.-Q. (Ed.), Animal biodiversity: An outline of higher-level classification and survey of taxonomic richness. Zootaxa, 3148 (1), 141–148. https://doi.org/10.11646/zootaxa.3148.1.26
  49. Schäffer, S., Kerschbaumer, M. & Koblmüller, S. (2019) Multiple new species: Cryptic diversity in the widespread mite species Cymbaeremaeus cymba (Oribatida, Cymbaeremaeidae). Molecular Phylogenetics and Evolution, 135, 185–192. https://doi.org/10.1016/j.ympev.2019.03.008
  50. Schuster, R. (1962) Nachweis eines Paarungszeremoniells bei den Hornmilben (Oribatei, Acari). Naturwissenschaften, 49 (21), 502. https://doi.org/10.1007/BF00637051
  51. Sellnick, M. (1919) Die Oribatiden der Bernsteinsammlung der Universität Königsberg in Preussen. Schriften der Physikalisch-ökonomischen Gesellschaft zu Königsberg in Preussen, 18 (1918), 21–42.
  52. Sellnick, M. (1922) Milben der Sammlung des Deutschen Entomologischen Instituts. I. Oribatidae. Entomologische Mittelungen, 11 (1), 18–20. https://doi.org/10.5962/bhl.part.3330
  53. Sellnick, M. (1932) Oribatiden aus dem Karst. Zoologische Jahrbücher, Abteilung für Systematik, 63, 701–714.
  54. Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B., Tinevez, J.-Y., White, D.J., Hartenstein, V., Eliceiri, K., Tomancak, P. & Cardona, A. (2012) Fiji: an open-source platform for biological-image analysis. Nature Methods, 9 (7), 676–682. https://doi.org/10.1038/nmeth.2019
  55. Sidorchuk, E.A. (2013) A new technique for preparation of small-sized amber samples with application to mites. In: Azar, D., Engel, M., Jarzembowski, E., Krogmann, L. & Santiago-Blay, J. (Eds.), Insect Evolution in an Amberiferous and Stone Alphabet. Brill, Leiden, The Netherlands, pp. 187–201. https://doi.org/10.1163/9789004210714_014
  56. Sidorchuk, E. (2016) Collohmanniidae (Oribatida: Mixonomata) – diverse family with a rich fossil record? 8th Symposium of the European Association of Acarologists, Valencia, Spain, 2016, abstracts, 34.
  57. Sidorchuk, E. (2018) A family story told by amber inclusions (Acari: Collohmanniidae). Amberif 2018. International Fair of Amber, Jewellery and Gemstones: International Symposium “Amber. Science and Art”, Gdańsk, Poland, 2018, abstracts, 21.
  58. Sidorchuk, E.A. & Norton, R.A. (2016) The identity and type specimens of Collohmannia asiatica (Acari, Oribatida, Collohmanniidae). Acarina, 24 (1), 5–16. https://doi.org/10.21684/0132-8077.2016.24.1.5.16
  59. Sidorchuk, E.A. & Vorontsov, D.D. (2018) Preparation of small-sized 3D amber samples: state of the technique. Palaeoentomology, 1 (1), 80–90. https://doi.org/10.11646/palaeoentomology.1.1.10
  60. Štorkán, J. (1925) Prispevky ku znamostem o ceskych Oribatidech (Acarina) [Additions to the knowledge of Czech oribatids (Acarina)]. Spisy vydávané Přírodovědeckou fakultou Karlovy University, 42, 1–40. [in Czech]
  61. Tinker, K.A. & Ottesen, E.A. (2021) Differences in gut microbiome composition between sympatric wild and allopatric laboratory populations of omnivorous cockroaches. Frontiers in Microbiology, 12. https://doi.org/10.3389/fmicb.2021.703785
  62. Travé, J. & Vachon, M. (1975) François Grandjean 1882–1975 (Notice biographique et bibliographique). Acarologia, 17, 1–19.
  63. Vorontsov, D.D., Kolesnikov, V.B., Voronezhskaya, E.E., Perkovsky, E.E., Berto, M.M., Mowery, J., Ochoa, R. & Klimov, P.B. (2023) Beyond the limits of light: An application of super-resolution confocal microscopy (sCLSM) to investigate Eocene amber microfossils. Life, 13 (4), 865. https://doi.org/10.3390/life13040865
  64. Weigmann, G. (2006) Hornmilben (Oribatida). Die Tierwelt Deutschlands. 76. Teil. Goecke & Evers, Keltern, 520 pp.
  65. Wolfe, A.P., McKellar, R.C., Tappert, R., Sodhi, R.N. & Muehlenbachs, K. (2016) Bitterfeld amber is not Baltic amber: Three geochemical tests and further constraints on the botanical affinities of succinite. Review of Palaeobotany and Palynology, 225, 21–32. https://doi.org/10.1016/j.revpalbo.2015.11.002
  66. Wolfe, A.P., Tappert, R., Muehlenbachs, K., Boudreau, M., McKellar, R.C., Basinger, J.F. & Garrett, A. (2009) A new proposal concerning the botanical origin of Baltic amber. Proceedings of the Royal Society B: Biological Sciences, 276 (1672), 3403–3412. https://doi.org/10.1098/rspb.2009.0806
  67. Zilber-Rosenberg, I. & Rosenberg, E. (2008) Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution. FEMS Microbiology Reviews, 32 (5), 723–735. https://doi.org/10.1111/j.1574-6976.2008.00123.x