Skip to main content
SpringerLink
Log in

Distinct phylogeographic patterns in populations of two oribatid mite species from the genus Pantelozetes (Acari, Oribatida, Thyrisomidae) in Central Europe

  • Published:
Experimental and Applied Acarology Aims and scope Submit manuscript

Abstract

Oribatid mites are important decomposers of dead organic matter in soils across the world. Their origin dates back at least 380 Mya. Multiple severe climatic changes during Late Pliocene and Pleistocene shaped the migration patterns of these organisms and should be reflected in the genetic variability of their current populations. In this study, we examined the genetic diversity and phylogeographic structure as well as the evolutionary history of populations of two ecologically different oribatid mite species. Pantelozetes cavaticus is a troglophile oribatid mite known mainly from Central European caves, whereas Pantelozetes paolii is a common surface eurytopic species with Holarctic distribution. We used two molecular markers—mitochondrial cytochrome c oxidase subunit I (COI) and the nuclear D3 region of the 28S rDNA gene—to reveal phylogenetic relationships between contemporary populations. Whereas the D3 region showed minimal or no variability within populations, COI appeared to be a relevant marker for population studies. Phylogeographic analysis based on COI detected two lineages of P. cavaticus (‘Czech’ and ‘Slovak’), which separated during the Late Pliocene (2.9 Mya) and revealed the existence of one new species. In contrast, three identified genetic lineages of P. paolii (radiation time 2.9 and 1.2 Mya, respectively) uncovered in this study were found to coexist in the distant sampling localities, suggesting a connection between populations even over long distances.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Data availability

All the sequences obtained for this study are publicly available from the GenBank (accession numbers are listed in Table 1). The datasets (alignments) generated and analyzed during the current study are available from the corresponding author on reasonable request.

References

  • Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25(17):3389–3402

    CAS  PubMed  PubMed Central  Google Scholar 

  • Avise JC (1994) Molecular markers, natural history and evolution. Chapman & Hall, New York

    Google Scholar 

  • Bas C (1995) Ecological structures: expansion and replacement. Sci Mar 59:373–380

    Google Scholar 

  • Beebee T, Row G (2008) An introduction to molecular ecology, 3rd edn. Oxford University Press, Oxford

    Google Scholar 

  • Beheregaray LB (2008) Twenty years of phylogeography: the state of the field and the challenges of the southern hemisphere. Mol Ecol 17(17):3754–3774

    PubMed  Google Scholar 

  • Bouckaert R, Vaughan TG, Barido-Sottani J, Duchêne S, Fourment M, Gavryushkina A et al (2019) BEAST 2.5: an advanced software platform for Bayesian evolutionary analysis. PLoS Comput Biol 15(4):e1006650

    CAS  PubMed  PubMed Central  Google Scholar 

  • Brower AVZ (1994) Rapid morphological radiation and convergence among races of the butterfly Heliconius erato inferred from patterns of mitochondrial DNA evolution. PNAS USA 91:6491–6495

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bruckner A (1995) Cave-dwelling oribatid mites (Acarina, Cryptostigmata) from East Austria. Verh Zool-Bot Ges Österr 132:81–107

    Google Scholar 

  • Colborn J, Crabtree RE, Shaklee JB, Pfeiler E, Bowen BW (2001) The evolutionary enigma of bonefishes (Albulaspp.): cryptic species and ancient separations in a globally distributed shorefish. Evolution 55(4):807–820

    CAS  PubMed  Google Scholar 

  • Excoffier LG, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50

    CAS  Google Scholar 

  • Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome C oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3(5):294–299

    CAS  PubMed  Google Scholar 

  • Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147(2):915–925

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hall TA (1999) BioEdit: A User-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acid Symp Ser 41:95–98

    CAS  Google Scholar 

  • Hebert PDN, Cywinska A, Ball SL, de Waard JR (2003) Biological identifications through DNA barcodes. Proc R Soc B 270(1512):313–321

    CAS  PubMed  PubMed Central  Google Scholar 

  • Heethoff M, Domes K, Laumann M, Maraun M, Norton RA, Scheu S (2007) High genetic divergences indicate ancient separation of parthenogenetic lineages of the oribatid mite Platynothrus peltifer (Acari, Oribatida). J Evol Biol 20:392–402

    CAS  PubMed  Google Scholar 

  • Hewitt GM (2004) Genetic consequences of climatic oscillations in the Quaternary. Philos Trans R Soc Lond B Biol Sci 359(1442):183–195

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hoang DT, Chernomor O, von Haeseler A, Minh BQ, Vinh LS (2018) UFBoot2: improving the ultrafast bootstrap approximation. Mol Biol Evol 35(2):518–522

    CAS  PubMed  Google Scholar 

  • Kalyaanamoorthy S, Minh BQ, Wong TKW, von Haeseler A, Jermiin LS (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods 14:587–589

    CAS  PubMed  PubMed Central  Google Scholar 

  • Korstian KM, Hale AM, Williams DA (2015) Genetic diversity, historic population size, and population structure in 2 North American tree bats. J Mamm 96(5):972–980

    Google Scholar 

  • Kováč Ľ, Parimuchová A, Miklisová D (2016) Distributional patterns of cave Collembola (Hexapoda) in association with habitat conditions, geography and subterranean refugia in the Western Carpathians. Biol J Linn Soc 119(3):571–592

    Google Scholar 

  • Kreipe V, Corral-Hernández E, Scheu S, Schaefer I, Maraum M (2015) Phylogeny and species delineation in European species of the genus Steganacarus (Acari, Oribatida) using mitochondrial and nuclear markers. Exp Appl Acarol 66(2):173–186

    PubMed  Google Scholar 

  • Krivolutsky DA, Lebedeva NV (2004) Oribatid mites (Oribatei, Acariformes) in bird feathers: non-passerines. Acta Zool Litu 14(1):26–45

    Google Scholar 

  • Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35(6):1547–1549

    CAS  PubMed  PubMed Central  Google Scholar 

  • Laumann M, Norton RA, Weigmann G, Scheu S, Maraun M, Heethoff M (2007) Speciation in the parthenogenetic oribatid mite genus Tectocepheus (Acari, Oribatida) as indicated by molecular phylogeny. Pedobiologia 51(2):111–122

    CAS  Google Scholar 

  • Lebedeva NV, Krivolutsky DA (2003) Birds spread soil microarthropods to arctic islands. Dokl Biol Sci 391:329–332

    CAS  PubMed  Google Scholar 

  • Lehmitz R, Decker P (2017) The nuclear 28S gene fragment D3 as species marker in oribatid mites (Acari, Oribatida) from German peatlands. Exp Appl Acarol 71(3):259–276

    CAS  PubMed  Google Scholar 

  • Lehmitz R, Russel D, Hohberg K, Christian A (2011) Wind dispersal of oribatid mites as mode of migration. Pedobiologia 54(3):201–207

    Google Scholar 

  • Lehmitz R, Russell D, Hohberg K, Christian A, Xylander WER (2012) Active dispersal of oribatid mites into young soils. Appl Soil Ecol 55:10–19

    Google Scholar 

  • Leigh JW, Bryant D (2015) PopART: full-feature software for haplotype network construction. Methods Ecol Evol 6(9):1110–1116

    Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    CAS  PubMed  Google Scholar 

  • Ľuptáčik P (2004) Príspevok k rozšíreniu Gemmazetes cavaticus (Kunst, 1962) (Acarina, Oribatida, Thyrisomidae) v Európe so zameraním na územie Slovenska. Book of Abstracts Zoologické dny. Brno, Brno

    Google Scholar 

  • Ľuptáčik P, Miko L (2003) Oribatid mites (Acarina, Oribatida) of Slovak caves. Subterr Biol 1:25–29

    Google Scholar 

  • Luxton M (1972) Studies on the oribatid mites of a Danish beech wood soil. I. Nutritional biology. Pedobiologia 12(3):434–463

    Google Scholar 

  • Maraun M, Scheu S (2000) The structure of oribatid mite communities (Acari, Oribatida): patterns, mechanisms and implications for future research. Ecography 23:374–383

    Google Scholar 

  • Maraun M, Heethoff M, Scheu S, Norton RA, Weigmann G, Thomas RH (2003) Radiation in sexual and parthenogenetic oribatid mites (Oribatida, Acari) as indicated by genetic divergence of closely related species. Exp Appl Acarol 29(3–4):265–277

    PubMed  Google Scholar 

  • Marshall VG (1972) Comparison of two methods of estimating efficiency of funnel extractors for soil microarthropods. Soil Biol Biochem 4:417–426

    Google Scholar 

  • Nguyen LT, Schmidt HA, von Haeseler A, Bui QM (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 32(4):268–274

    CAS  PubMed  Google Scholar 

  • Norton RA, Bonamo PM, Grierson JD, Shears WA (1988) Oribatid mite fossils from a terrestrial Devonian deposit near Gilboa, New York. J Paleontol 62:259–269

    Google Scholar 

  • Ojala R, Huhta V (2001) Dispersal of microarthropods in forest soil. Pedobiologia 45:443–450

    Google Scholar 

  • Pachl P, Lindl AC, Krause A, Scheu S, Schaefer I, Maraun M (2017) The tropics as an ancient cradle of oribatid mite diversity. Acarologia 57(2):309–322

    Google Scholar 

  • Papadopoulou A, Anastasiou I, Keskin B, Vogler AP (2009) Comparative phylogeography of tenebrionid beetles in the Aegean archipelago: the effect of dispersal ability and habitat preference. Mol Ecol 18(11):2503–2517

    CAS  PubMed  Google Scholar 

  • Parimuchová A, Kováč Ľ, Žurovcová M, Miklisová D, Paučulová L (2017) A glacial relict in the Carpathian caves—population variability or a species complex? Arthropod Syst Phylo 75(3):351–362

    Google Scholar 

  • Pfingstl T, Baumann J, Lienhard A (2019) The Caribbean enigma: the presence of unusual cryptic diversity in intertidal mites (Arachnida, Acari, Oribatida). Org Divers Evol 19(4):609–623

    PubMed  PubMed Central  Google Scholar 

  • Rambaut A, Drummond AJ, Xie D, Baele G, Suchard MA (2018) Posterior summarisation in Bayesian phylogenetics using tracer 1.7. Syst Biol 67(5):901–904

    CAS  PubMed  PubMed Central  Google Scholar 

  • Retallack GJ (2001) Cenozoic expansion of grasslands and climatic cooling. J Geol 109(4):407–426

    CAS  Google Scholar 

  • Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MRBAYES 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61(3):539–542

    PubMed  PubMed Central  Google Scholar 

  • Rosenberger MJ (2010) Phylogeography in sexual and parthenogenetic European Oribatida. Dissertation, Göttingen Centre for Biodiversity and Ecology

  • Rosenberger MJ, Maraun M, Scheu S, Schaefer I (2013) Pre- and post-glacial diversifications shape genetic complexity of soil-living microarthropod species. Pedobiologia 56:79–87

    Google Scholar 

  • Schaefer I, Norton RA, Scheu S, Maraun M (2010) Arthropod colonization of land-linking molecules and fossils in oribatid mites (Acari, Oribatida). Mol Phylogenet Evol 55:113–121

    Google Scholar 

  • Schäffer S, Pfingstl T, Koblmüller S, Winkler KA, Sturmbauer Ch, Krisper G (2010) Phylogenetic analysis of European Scutovertex mites (Acari, Oribatida, Scutoverticidae) reveals paraphyly and cryptic diversity: a molecular genetics and morphological approach. Mol Phyl Evol 55:677–688

    Google Scholar 

  • Schäffer S, Kerschbaumer M, Koblmüller S (2019) Multiple new species: cryptic diversity in the widespread mite species Cymberemaeus cymba (Oribatida, Cymbaeremaeidae). Mol Phylogenet Evol 135:185–192

    PubMed  Google Scholar 

  • Schuppenhauer MM, Lehmitz R, Xylander WER (2019) Slow-moving soil organisms on a water highway: aquatic dispersal and survival potential of Oribatida and Collembola in running water. Mov Ecol. https://doi.org/10.1186/s40462-019-0165-5

    Article  PubMed  PubMed Central  Google Scholar 

  • Skoracka A, Magalhães S, Rector BG, Kuczyński L (2015) Cryptic speciation in the Acari: a function of species lifestyles or our ability to separate species? Exp Appl Acarol 67(2):165–182

    PubMed  PubMed Central  Google Scholar 

  • Starý J (2008) Diversity and distribution of oribatid mites (Acari: Oribatida) in caves of Czech Republic. Acta Carsol Slovaka 46(1):185–197

    Google Scholar 

  • Subías LS (2020) Listado sistemático, sinonímico y biogeográfico de los Ácaros Oribátidos (Acariformes: Oribatida) del mundo (excepto fósiles), 15a actualización. http://bba.bioucm.es/cont/docs/RO_1.pdf. Accessed June 2020

  • Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. G3 (Bethesda) 123:585–595

    CAS  Google Scholar 

  • Villesen P (2007) FaBox: an online toolbox for fasta sequences. Mol Ecol Notes 7(6):965–968

    CAS  Google Scholar 

  • von Saltzwedel H, Mark M, Scheu S, Schaefer I (2014) Evidence for frozen niche variation in a cosmopolitan parthenogenetic soil mite species (Acari, Oribatida). PLoS ONE 9(11):e113268

    Google Scholar 

  • von Saltzwedel H, Scheu S, Schaefer I (2016) Founder events and pre-glacial divergences shape the genetic structure of European Collembola species. BMC Evol Biol 16:148. https://doi.org/10.1186/s12862-016-0719-8

    Article  CAS  Google Scholar 

  • von Saltzwedel H, Scheu S, Schaefer I (2017) Genetic structure and distribution of Parisotoma notabilis (Collembola) in Europe: cryptic diversity, split of lineages and colonization patterns. PLoS ONE 12(2):e0170909

    Google Scholar 

  • Waters JM, Fraser CI, Hewitt GM (2013) Founder takes all: density-dependent processes structure biodiversity. Trends Ecol Evol 28(2):78–85

    PubMed  Google Scholar 

  • Weigmann G (2006) Die Tierwelt Deutschlands, Teil 76: Hornmilben (Oribatida). Goecke and Evers, Keltern

    Google Scholar 

  • Xia X (2017) DAMBE6: new tools for microbial genomics, phylogenetics and molecular evolution. J Hered 108:431–437

    CAS  PubMed  PubMed Central  Google Scholar 

  • Xia X, Xie Z, Salemi M, Chen L, Wang Y (2003) An index of substitution saturation and its application. Mol Phylogenet Evol 26:1–7

    CAS  PubMed  Google Scholar 

  • Yosii R (1956) Monographie zur Höhlencollembolen Japans, vol 3. Biological Laboratory, Kyoto University, Kyoto, p 1

    Google Scholar 

  • Żbikowska-Zdun K, Piksa K, Smaczyńska A (2009) Variation of selected morphological characters of the cave mite Oribella cavatica Kunst, 1962 (Acari, Oribatida). Biol Lett 46(2):123–127

    Google Scholar 

Download references

Acknowledgements

The research was supported by the Czech Academy of Sciences (under Research Plan No. AV0Z606960521), by two grant projects of the Czech Science Foundation (projects No. P504/12/1218 and No. 14-09231S) and one project of the Slovak Research and Development Agency (APVV-17-0477). The research in Czech caves was undertaken in the collaboration with the Cave Administration of Czech Republic. We want to thank to Dr. Koudelka (Head of the Javoříčské Caves) for cooperation and enabling the access to the Javoříčské Caves; Dr. Štefka (Head of the Moravian Karst PLA), Dr. Tůma and Dr. Kovařík for cooperation and help with the field sampling in Sloupsko-šošůvské Caves and Amatérská Cave. We thank also to the Slovak Caves Administration and to the Administrations of Šumava NP, Wigry NP, Tatranský NP and Slovenský kras NP for their permission to conduct the study in the national parks.

Funding

This study was supported by the Academy of Sciences of the Czech Republic (under Research Plan No. AV0Z606960521), by two grant projects of the Czech Science Foundation (projects No. P504/12/1218 and No.14-09231S) and by one project of the Slovak Research and Development Agency (APVV-17-0477).

Author information

Authors and Affiliations

  1. Department of Ecosystem Biology, Faculty of Science, University of South Bohemia in České Budějovice, České Budějovice, Czech Republic

    Petra Kokořová

  2. Biology Centre, Institute of Soil Biology, Czech Academy of Sciences, České Budějovice, Czech Republic

    Petra Kokořová & Josef Starý

  3. Biology Centre, Institute of Entomology, Czech Academy of Sciences, České Budějovice, Czech Republic

    Petra Kokořová & Martina Žurovcová

  4. Faculty of Sciences, Institute of Biology and Ecology, Pavol Josef Šafárik University in Košice, Košice, Slovakia

    Peter Ľuptáčik

Authors
  1. Petra Kokořová
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Martina Žurovcová
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Peter Ľuptáčik
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Josef Starý
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Petra Kokořová.

Ethics declarations

Conflicts of interest

The authors have no conflict of interest to declare that are relevant to the content of this article.

Ethics approval

No approval of research ethics committees was required to accomplish the goals of this study because experimental work was conducted with an unregulated invertebrate species.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kokořová, P., Žurovcová, M., Ľuptáčik, P. et al. Distinct phylogeographic patterns in populations of two oribatid mite species from the genus Pantelozetes (Acari, Oribatida, Thyrisomidae) in Central Europe. Exp Appl Acarol 83, 493–511 (2021). https://doi.org/10.1007/s10493-021-00605-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10493-021-00605-7

Keywords

Search

Navigation