Skip to main content
SpringerLink
Log in

Molecular evidence for species separation in the water mite Hygrobates nigromaculatus Lebert, 1879 (Acari, Hydrachnidia): evolutionary consequences of the loss of larval parasitism

  • Research Article
  • Published:
Aquatic Sciences Aims and scope Submit manuscript

Abstract

In the present study, we used mitochondrial cytochrome oxidase subunit I (COI) and nuclear D2 region of 28S rDNA sequence data to examine the taxonomic status of the water mite species Hygrobates nigromaculatus from two types of freshwater habitats: lentic (lakes) and lotic (streams). Previous hypotheses about (sub)species status of populations inhabiting lakes and streams based on differences in morphometric data and life-cycle strategy (parasitic vs. non-parasitic larvae) were strongly supported by molecular data. Levels of COI and D2 28S rDNA differentiation between lake and stream populations were much higher (ca. 18 and 7.5%, respectively) than those typically observed for populations of a single species. Both lake and stream populations showed similar high levels of gene diversity (Hd = 0.894 and 0.836, respectively). However, nucleotide within-population polymorphism was more than twice as high in lake populations as that in stream populations (π = 1.33 and 0.60%, respectively). We hypothesize that the ancestral lake-dwelling population originated from a stream form with parasitic larvae (here: H. setosus nov. stat.). For the observed populations, H. nigromaculatus individuals could be separated from H. setosus by distinct morphometric characters. The loss of phoretic parasitic larvae greatly decreased dispersal ability of lake-dwelling mites and consequently also the gene flow between lake populations. Thus, relatively more differentiated genetic structure in lake populations probably results from a stronger isolation between particular lake habitats, but this hypothesis needs further extensive studies.

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
Fig. 4

Similar content being viewed by others

References

  • Abascal F, Zardoya R, Posada D (2005) ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21(9):2104–2105

    Article  PubMed  CAS  Google Scholar 

  • Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48

    PubMed  CAS  Google Scholar 

  • Bert W, Messiaen M, Manhout J, Houthoofd W, Borgonie G (2006) Evolutionary loss of parasitism by nematodes? Discovery of a free-living filaroid nematode. J Parasitol 92(3):645–647

    Article  PubMed  Google Scholar 

  • Besseling AJ (1942) Nederlandsche Hydrachnidae. Genus Hygrobates. Entomol Ber 11(243):2–6

    Google Scholar 

  • Biesiadka E, Kowalik W (1979) A new species of Mideopsis Neumann (Hydrachnellae, Acari) from Poland. Bull Acad Pol Sci Sér Sci Biol Cl II 26:695–702

    Google Scholar 

  • Bohonak AJ (1999a) Dispersal, gene flow, and population structure. Q Rev Biol 74:21–45

    Article  PubMed  CAS  Google Scholar 

  • Bohonak AJ (1999b) Effect of insect-mediated dispersal on the genetic structure of postglacial water mite populations. Heredity 82:451–461

    Article  PubMed  Google Scholar 

  • Bohonak AJ, Jenkins DG (2003) Ecological and evolutionary significance of dispersal by freshwater invertebrates. Ecol Lett 6:783–796

    Article  Google Scholar 

  • Bohonak AJ, Smith BP, Thornton M (2004) Distributional, morphological and genetic consequences of dispersal for temporary pond water mites. Freshw Biol 49:170–180

    Article  Google Scholar 

  • Borda E, Siddall ME (2004) Arhynchobdellida (Annelida: Oligochaeta: Hirudinida): phylogenetic relationships and evolution. Mol Phylogenet Evol 30:213–225

    Article  PubMed  CAS  Google Scholar 

  • Brunke M (2004) Stream typology and lake outlets—a perspective towards validation and assessment from northern Germany (Schleswig-Holstein). Limnologica 34:460–478

    Google Scholar 

  • Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9(10):1657–1660

    Article  PubMed  CAS  Google Scholar 

  • Cruickshank RH, Paterson AM (2006) The great escape: do parasites break Dollo’s law? Trends Parasitol 22(11):509–515

    Article  PubMed  Google Scholar 

  • Dabert J (2005) Feather mites (Astigmata; Pterolichoidea; Analgoidea) and birds as models for cophylogenetic studies. Phytophaga 14:409–424

    Google Scholar 

  • Dabert J, Ehrnsberger R, Dabert M (2008) Glaucalges tytonis sp. n. (Analgoidea, Xolalgidae) from the barn owl Tyto alba (Strigiformes, Tytonidae): compiling morphology with DNA barcode data for taxon descriptions in mites (Acari). Zootaxa 1719:41–52

    Google Scholar 

  • Dabert M, Witalinski W, Kazmierski A, Olszanowski Z, Dabert J (2010) Molecular phylogeny of acariform mites (Acari, Arachnida): strong conflict between phylogenetic signal and long‐branch attraction artifacts. Mol Phylogenet Evol. doi:10.1016/j.ympev.2009.12.020

  • Davids C (1997) A new water mite (Acari, Hydrachnidia: Limnesiidae) split off from Limnesia undulata. Entomol Ber 57:157–160

    Google Scholar 

  • Davids C, Heijnis CF, Weekenstroo JE (1981) Habitat differentiation and feeding strategies in water mites in Lake Maarsseveen I. Aquat Ecol 15(1–2):87–91

    Google Scholar 

  • Davids C, Di Sabatino A, Gerecke R, Gledhill T, Smit H (2007) Acari, Hydrachnidia I. In: Gerecke R (ed) Süßwasserfauna von Mitteleuropa, vol. 7, 2–1, Chelicerata: Araneae, Acari I. Spektrum Elsevier, München, pp 241–388

    Google Scholar 

  • Dorris M, Viney ME, Blaxter ML (2002) Molecular phylogenetic analysis of the genus Strongyloides and related nematodes. Int J Parasitol 32:1507–1517

    Article  PubMed  CAS  Google Scholar 

  • Ehlers J, Eissmann L, Lippstreu L, Stephan H-J, Wansa S (2004) Pleistocene glaciations of North Germany. In: Ehlers J, Gibbard PL (eds) Quaternal glaciations - Extent and chronology, Part 1: Europe. Elsevier B.V., Amsterdam, pp 135–146

    Chapter  Google Scholar 

  • Ernsting BR, Edwards DD, Vidrine MF, Cun H (2008) Genetic differences among sibling species of the subgenus Dimockatax (Acari: Unionicolidae: Unionicola): Heterogeneity in DNA sequence data supports morphological differentiation. Int J Acarol 34:403–407

    Article  Google Scholar 

  • Ernsting BR, Edwards DD, Aldred KJ, Fites JS, Neff CR (2009) Mitochondrial genome sequence of Unionicola foili (Acari: Unionicolidae): a unique gene order with implications for phylogenetic inference. Exp Appl Acarol 49(4):305–316

    Article  PubMed  CAS  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  Google Scholar 

  • Fittkau EJ, Reiss F (1978) Chironomidae. In: Illies J (ed) Limnofauna Europaea, 2nd edn. Gustav Fischer, Stuttgart, pp 404–440

    Google Scholar 

  • Gerecke R (2002) The water mites (Acari, Hydrachnidia) of a little disturbed forest stream in southwest Germany—a study on seasonality and habitat preference, with remarks on diversity patterns in different geographical areas. In: Bernini F, Nannelli G, Nuzzaci G, de Lillo E (eds) Acarid phylogeny and evolution. Adaptation in mites and ticks. Kluwer Academic, Dordrecht, pp 69–89

    Google Scholar 

  • Gledhill T, Sutcliffe DW, Williams WD (1993) British freshwater Crustacea. Malacostraca. A key with ecological notes. Freshw Biol Assoc Sci Publ 52:173

    Google Scholar 

  • Hassanin A (2006) Phylogeny of Arthropoda inferred from mitochondrial sequences: strategies for limiting the misleading effects of multiple changes in pattern and rates of substitution. Mol Phylogenet Evol 38:100–116

    Article  PubMed  CAS  Google Scholar 

  • Hebert PDN, Penton EH, Burns JM, Janzen DH, Hallwachs W (2004) Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator. Proc Natl Acad Sci USA 101(41):14812–14817

    Article  PubMed  CAS  Google Scholar 

  • Hof C, Brändle M, Brandl R (2008) Latitudinal variation of diversity in European freshwater animals is not concordant across habitat types. Global Ecol Biogeogr 17:539–546

    Article  Google Scholar 

  • Huyse T, Poulin R, Théron A (2005) Speciation in parasites: a population genetics approach. Trends Parasitol 21(10):469–475

    Article  PubMed  Google Scholar 

  • Jobb G (2008) TREEFINDER version of October 2008. Munich, Germany. Distributed by the author at http://www.treefinder.de

  • Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16(2):111–120

    Article  PubMed  CAS  Google Scholar 

  • Klimov PB, OConnor BM (2008) Morphology, evolution and host associations of bee associated mites of the family Chaetodactylidae (Acari: Astigmata), with monographic revision of North American taxa. Museum of Zoology, University of Michigan, Ann Arbor, 243 pp

  • Kohler SL (2008) The ecology of host–parasite interactions in aquatic insects. In: Lancaster J, Briers RA (eds) Aquatic insects: challenges to populations, CABI, pp 55–80

  • Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948

    Article  PubMed  CAS  Google Scholar 

  • Lebert H (1879) Description de quelques espèces nouvelles d’Hydrachnides du Lac Léman. - Mémoire posthume. B Soc Vaudoise sciences naturelles 16:327–377

    Google Scholar 

  • Lundblad O (1968) Die Hydracarinen Schwedens. III. Ark Zool 21:1–633

    Google Scholar 

  • Marten A, Brändle M, Brandl R (2006) Habitat type predicts genetic population differentiation in freshwater invertebrates. Mol Ecol 15:2643–2651

    Article  PubMed  CAS  Google Scholar 

  • Martin P (1996) Faunistisch-ökologische Benthosstudien an den Wassermilben (Hydrachnidia, Acari) zweier Bäche des Norddeutschen Tieflandes (Ostholsteinisches Hügelland, Schleswig-Holstein). Faun-Ökol Mitteil 7:153–167

    Google Scholar 

  • Martin P (2000) Larval morphology and host-parasite associations of some stream living water mites (Hydrachnidia, Acari). Arch Hydrobiol Suppl 121/3-4, Monogr Stud 269–320

  • Martin P, Davids C (2002) Life history strategies of Hygrobates nigromaculatus, a widespread palaearctic water mite (Acari, Hydrachnidia, Hygrobatidae). In: Bernini F, Nannelli G, Nuzzaci G, de Lillo E (eds) Acarid phylogeny and evolution. Adaptation in mites and ticks. Kluwer Academic, Dordrecht, pp 101–110

    Google Scholar 

  • Martin P, Stur E (2006) Parasite–host associations and life cycles of spring-living water mites (Hydrachnidia, Acari) from Luxembourg. Hydrobiologia 573:17–37

    Article  Google Scholar 

  • Masta SE, Longhorn SJ, Boore JL (2009) Arachnid relationships based on mitochondrial genomes: asymmetric nucleotide and amino acid bias affects phylogenetic analyses. Mol Phylogenet Evol 50(1):117–128

    Article  PubMed  CAS  Google Scholar 

  • Meyer E (1986) Die Wassermilben (Hydrachnellae, Acari) in den Fließgewässern um Freiburg i. Br. Mitteil bad Landesverein Naturk Naturschutz N F 14:147–206

    Google Scholar 

  • Nicholas KB, Nicholas HB Jr (1997) GeneDoc: a tool for editing and annotating multiple sequence alignments. Pittsburgh Supercomputing Center’s National Resource for Biomedical Supercomputing. http://www.nrbsc.org/downloads/. Accessed 2 March 2007

  • Nilsson AN (1986) Life cycles and habitats of the northern European Agabini (Coleoptera: Dytiscidae). Entomol basil 11:391–417

    Google Scholar 

  • Polzin T, Daneschmand SV (2003) On Steiner trees and minimum spanning trees in hypergraphs. Oper Res Lett 31:12–20

    Article  Google Scholar 

  • Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818

    Article  PubMed  CAS  Google Scholar 

  • Poulin R (1999) The functional importance of parasites in animal communities: many roles at many levels? Int J Parasitol 29:903–914

    Article  PubMed  CAS  Google Scholar 

  • Poulin R (2007) Evolutionary ecology of parasites. Princeton University Press, Princeton

    Google Scholar 

  • Radovsky FJ, Krantz GW (1998) A new genus and species of predaceous mite in the parasitic family Macronyssidae (Acari: Mesostigmata). J Med Entomol 35:527–537

    PubMed  CAS  Google Scholar 

  • R Development Core Team (2008) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org

  • Reice SR (1991) Effects of experimental spates on benthic community structure in New Hope Creek, North Carolina, USA. Verh Int Ver Theor Angew Limnol 24(3):1691–1693

    Google Scholar 

  • Ribera I, Barraclough TG, Vogler AP (2001) The effect of habitat type on speciation rates and range movements in aquatic beetles: inferences from species-level phylogenies. Mol Ecol 10:721–735

    Article  PubMed  CAS  Google Scholar 

  • Rozas J, Sánchez-DelBarrio JC, Messegyer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497

    Article  PubMed  CAS  Google Scholar 

  • Salewski V (2003) Satellite species in lampreys: a worldwide trend for ecological speciation in sympatry? J Fish Biol 63(2):267–279

    Article  Google Scholar 

  • Schneider S, Roessli D, Excoffier L (2000) Arlequin: a software for population genetics data analysis. Ver 2.000. Genetics and Biometry Laboratory, Department of Anthropology, University of Geneva

  • Shao R, Mitani H, Barker SC, Takahashi M, Fukunaga M (2005) Novel mitochondrial gene content and gene arrangement indicate illegitimate inter-mtDNA recombination in the chigger mite, Leptotrombidium pallidum. J Mol Evol 60(6):764–773

    Article  PubMed  CAS  Google Scholar 

  • Siddall ME, Brooks DR, Desser SS (1993) Phylogeny and the reversibility of parasitism. Evolution 47:308–313

    Article  Google Scholar 

  • Skoracka A, Dabert M (2010) The cereal rust mite Abacarus hystrix (Acari: Eriophyoidea) is a complex of species: evidence from mitochondrial and nuclear DNA sequences. B Entomol Res. doi:10.1017/S0007485309990216

  • Smith BP (1998) Loss of larval parasitism in parasitengonine mites. Exp Appl Acarol 22:187–200

    Article  Google Scholar 

  • Smith IM, Oliver DR (1986) Review of parasitic associations of larval water mites (Acari: Parasitengona: Hydrachnida) with insect hosts. Can Entomol 118:407–472

    Article  Google Scholar 

  • Smith IM, Cook DR, Smith BP (2001) Water mites (Hydrachnida) and other arachnids. In: Thorp JH, Covich AP (eds) Ecology and classification of North American freshwater invertebrates. Academic Press, San Diego, pp 551–659

    Chapter  Google Scholar 

  • Sonnenberg R, Nolte AW, Tautz D (2007) An evaluation of LSU rDNA D1–D2 sequences for their use in species identification. Front Zool 4:6. doi:10.1186/1742-9994-4-6

    Article  PubMed  CAS  Google Scholar 

  • Strathmann RR (1978) The evolution and loss of feeding larval stages of marine invertebrates. Evolution 32:894–906

    Article  Google Scholar 

  • Strathmann RR (1985) Feeding and nonfeeding larval development and life-history evolution in marine invertebrates. Ann Rev Ecol Syst 16:339–361

    Article  Google Scholar 

  • Swofford DL (2002) PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4. Sinauer Associates, Sunderland

    Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  PubMed  CAS  Google Scholar 

  • Templeton AR, Crandall KA, Sing CF (1992) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. Genetics 132:619–633

    PubMed  CAS  Google Scholar 

  • Van Haaren T, Tempelman D (2009) The Dutch species of Limnesia, with ecological and biological notes (Acari: Hydrachnidia: Limnesiidae). Nederl Faunist Mededel 30:53–74

    Google Scholar 

  • Van Hezewijk MJ, Davids C (1985) The larvae of three water mite species of the genus Hygrobates and their development (Acari, Hydrachnellae). B Zool Mus Univ Amsterdam 10:97–105

    Google Scholar 

  • Viets K (1924) Die Hydracarinen der norddeutschen, besonders der holsteinischen Seen. Arch Hydrobiol Suppl 4:71–179

    Google Scholar 

  • Viets K (1936) Wassermilben oder Hydracarina (Hydrachnellae und Halacaridae). In: Dahl F (ed) Die Tierwelt Deutschlands und der angrenzenden Meeresteile nach ihren Merkmalen und ihrer Lebensweise. Gustav Fischer, Jena

    Google Scholar 

  • Viets KO (1960) Über Hygrobates nigromaculatus Lebert 1879 (Hydrachnellae, Acari). Mitteil Zool Mus Berlin 36:445–461

    Google Scholar 

  • Viets KO (1978) Hydracarina. In: Illies J (ed) Limnofauna Europaea, 2nd edn. Gustav Fischer, Stuttgart, pp 154–181

    Google Scholar 

  • Walter DE, Proctor HC (1999) Mites: ecology, evolution, and behaviour. University of New South Wales Press, Sydney

    Google Scholar 

  • Wharton GW (1976) House dust mites. J Med Entomol 12(6):577–621

    PubMed  CAS  Google Scholar 

  • Wiggins GB, Mackay RJ, Smith IM (1980) Evolutionary and ecological strategies of animals in annual temporary pools. Arch Hydrobiol Suppl 58:97–206

    Google Scholar 

  • Wohltmann A (1999) Life-history evolution in Parasitengonae (Acari: Prostigmata): constrains on number and size of offspring. In: Bernini F, Nannelli G, Nuzzaci G, de Lillo E (eds) Acarid phylogeny and evolution. Adaptation in mites and ticks. Kluwer Academic, Dordrecht, pp 137–148

    Google Scholar 

  • Wohltmann A (2001) The evolution of life histories in Parasitengonae (Acari; Prostigmata). Acarologia 41:145–204

    Google Scholar 

  • Zwickl DJ (2006) Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. Dissertation, University of Texas

Download references

Acknowledgments

The authors thank Dr. Reinhard Gerecke, Tübingen, Germany, for checking some doubtful specimens for their species identity. Thanks also to the late Dr. Cornelis Davids (1931–2004), Amsterdam, The Netherlands, for his interest in the topic and the loan of specimens from The Netherlands. Dr. Heather C. Proctor, Edmonton, Canada, gave us valuable comments on a former version of this paper. Parts of the study were financially supported by bilateral partnership contract of the Christian-Albrechts-Universität zu Kiel (Germany) and Adam Mickiewicz University in Poznan (Poland).

Author information

Authors and Affiliations

  1. Zoological Institute, Christian-Albrechts-Universität zu Kiel, Olshausenstr. 40, 24098, Kiel, Germany

    Peter Martin

  2. Molecular Biology Techniques Laboratory, Faculty of Biology, Adam Mickiewicz University, Umultowska 89, 61-614, Poznan, Poland

    M. Dabert

  3. Department of Animal Morphology, Institute of Environmental Biology, Faculty of Biology, Adam Mickiewicz University, Umultowska 89, 61-614, Poznan, Poland

    J. Dabert

Authors
  1. Peter Martin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. Dabert
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. J. Dabert
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Peter Martin.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Martin, P., Dabert, M. & Dabert, J. Molecular evidence for species separation in the water mite Hygrobates nigromaculatus Lebert, 1879 (Acari, Hydrachnidia): evolutionary consequences of the loss of larval parasitism. Aquat. Sci. 72, 347–360 (2010). https://doi.org/10.1007/s00027-010-0135-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00027-010-0135-x

Keywords

Search

Navigation