Skip to main content
SpringerLink
Log in

Five subspecies of the Dorogostaiskia parasitica complex (Dybowsky) (Crustacea: Amphipoda: Acanthogammaridae), epibionts of sponges in Lake Baikal

  • SPECIATION IN ANCIENT LAKES 6
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

Based on morphological and molecular characters, the gammaroid amphipod Dorogostaiskia parasitica, living as an epibiont on sponges in Lake Baikal, Siberia, is here split into five parapatrically or allopatrically distributed subspecies: D. p. parasitica (Dybowsky, Horae Societatis Entomologicae Rossicae 10(Beiheft):1–218, 1874), D. p. kamaltynovi subsp. nov., D. p. hanajevi subsp. nov., D. p. ushkaniensis subsp. nov., and D. p. stenocephala subsp. nov. Diagnostic differences are described in the shape of dorsal keels, shape of head, length of antenna 1, number of segments of accessory flagellum, shape and armature of coxal plates, relative lengths of pereopod segments, and body coloration. Each subspecies is characterized by a distinct mitochondrial lineage, differing from others by 5–11% in the sequence of the COI gene, while they do not differ in nuclear 28S rRNA gene sequence. The question of taxonomic ranks for members of intralacustrine species complexes is considered and an argument is presented for a use of the subspecies rank for parapatrically distributed population segments that are distinguished by multiple independent geographically congruent character differences. This usage sorts out a pattern of systematic diversity lower than one based on documented reproductive isolation (e.g., sympatry) of full species but stronger than that based on single-gene genealogies alone.

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
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Aljanabi, S. M. & I. Martinez, 1997. Universal and rapid salt-extraction of high quality genomic DNA for PCR-based techniques. Nucleic Acids Research 25: 4692–4693.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Andres, H. G. & N. Lott, 1977. Verzeichnis der Typen aus der Sammlung Crustacea des Zoologishen Instituts und Zoologicshen Museums der Universität Hamburg. Mitteilungen aus dem Hamburgischen Zoologischen Museum und Institut 74: 53–64.

    Google Scholar 

  • Audzijonyte, A. & R. Väinölä, 2005. Diversity and distributions of circumpolar fresh- and brackish-water Mysis (Crustacea: Mysida): descriptions of M. relicta Lovén, 1862, M. salemaai n. sp., M. segerstralei n. sp. and M. diluviana n. sp., based on molecular and morphological characters. Hydrobiologia 544: 89–141.

  • Audzijonyte, A., J. Damgaard, S.-L. Varvio, J. K. Vainio & R. Väinölä, 2005. Phylogeny of Mysis (Crustacea, Mysida): history of continental invasions inferred from molecular and morphological data. Cladistics 21: 575–596.

    Article  Google Scholar 

  • Barnard, J. L. & C. M. Barnard, 1983. Freshwater Amphipoda of the World. Vol. I and II. Hayfield Associates, Mt. Vernon, VA.

  • Bazikalova, A. Ya., 1945. Amfipody ozera Baikal. Trudy Baikalskoi Limnologicheskoi Stantsii AN SSSR 11: 1–440.

    Google Scholar 

  • Bazikalova, A. Ya., 1948. Zametki ob amfipodakh ozera Baikal. Trudy Baikalskoi Limnologicheskoi Stantsii AN SSSR 12: 20–32.

    Google Scholar 

  • Bazikalova, A. Ya., 1962. Sistematika, ekologiya i rasprostranenie rodov Micruropus Stebbing i Pseudomicruropus nov. gen. (Amphipoda, Gammaridae). Ch. 1. Trudy Limnologicheskogo Instituta Sibirskogo Otdeleniya AN SSSR 2: 3–140.

    Google Scholar 

  • Bousfield, E. L., 1977. A new look at the systematics of gammaroidean amphipods of the world. Crustaceana 4(Supplement): 282–318.

    Google Scholar 

  • Braby, J. F., R. Eastwood & N. Murray, 2012. The subspecies concept in butterflies: has its application in taxonomy and conservation biology outlived its usefulness? Biological Journal of the Linnean Society 106: 699–716.

    Article  Google Scholar 

  • Daneliya, M. E., R. M. Kamaltynov, T. Kontula & R. Väinölä, 2009. Systematics of the Baikalian Babr (Crustacea: Amphipoda: Pallaseidae). Zootaxa 2276: 49–68.

    Google Scholar 

  • Daneliya, M. E., R. M. Kamaltynov & R. Väinölä, 2011. Phylogeography and systematics of Acanthogammarus s. str., giant amphipod crustaceans from Lake Baikal. Zoologica Scripta 40: 623–637.

    Article  Google Scholar 

  • de Queiroz, K., 2007. Species concepts and species delimitation. Systematic Biology 56: 879–886.

    Article  PubMed  Google Scholar 

  • Dorogostaisky, V. Ch, 1922. Materialy dlya kartsinologicheskoi fauny ozera Baikala. Trudy Komissii po Izucheniyu Ozera Baikala 1: 105–153.

    Google Scholar 

  • Dorogostaisky, V. Ch, 1930. Novye materialy dlya kartsinologicheskoi fauny ozera Baikala. Trudy Komissii po Izucheniyu Ozera Baikala 3: 49–76.

    Google Scholar 

  • Dybowsky, B. N., 1874. Beiträge zur näheren Kenntniss der in dem Baikal-See vorkommenden niederen Krebse aus der Gruppe der Gammariden. Horae Societatis Entomologicae Rossicae 10(Beiheft): 1–218.

    Google Scholar 

  • Flot, J.-F., G. Wörheide & S. Dattagupta, 2010. Unsuspected diversity of Niphargus amphipods in the chemoautotrophic cave ecosystem of Frasassi, central Italy. BMC Evolutionary Biology 10: 171.

    Article  PubMed  PubMed Central  Google Scholar 

  • Funk, D. J. & K. E. Omland, 2003. Species-level paraphyly and polyphyly: frequency, causes, and consequences, with insights from animal mitochondrial DNA. Annual Review of Ecology, Evolution and Systematics 34: 397–423.

    Article  Google Scholar 

  • Garjajeff, V. P., 1901. Gammaridy ozera Baikala. Chast I: Acanthogammarinae. Trudy Obshchestva Estestvoispytatelei pri Imperatorskom Kazanskom Universitete 35: 1–62.

    Google Scholar 

  • Gomanenko, G. V., R. M. Kamaltynov, Zh. V. Kuzmenkova, K. Bêrênos & D. Yu. Scherbakov, 2005. Population structure of the Baikalian amphipod Gmelinoides fasciatus (Stebbing). Russian Journal of Genetics 41: 1108–1114.

    Article  CAS  Google Scholar 

  • Hebert, P. D. N., S. Ratnasingham & J. R. de Waard, 2003. Barcoding animal life: cytochrome c oxidase subunit I divergences among closely related species. Proceedings of the Royal Society of London, Series B – Biological Sciences 270(Supplement): 96–99.

    Article  Google Scholar 

  • Herder, F., A. W. Nolte, J. Pfaender, J. Schwarer, R. K. Hadiaty & U. K. Schliewen, 2006. Adaptive radiation and hybridization in Wallace’s Dreamponds: evidence from sailfin silversides in the Malili Lakes of Sulawesi. Proceedings of the Royal Society of London, Series B – Biological Sciences 273: 2209–2217.

  • Hou, Z. & S. Li, 2010. Intraspecific or interspecific variation: delimitation of species boundaries within the genus Gammarus (Crustacea, Amphipoda, Gammaridae), with description of four new species. Zoological Journal of the Linnean Society 160: 215–253.

    Article  Google Scholar 

  • Hou, Z., J. Fu & S. Li, 2007. A molecular phylogeny of the genus Gammarus (Crustacea: Amphipoda) based on mithochondrial and nuclear gene sequences. Molecular Phylogenetics and Evolution 45: 596–611.

    Article  PubMed  CAS  Google Scholar 

  • Hou, Z., Z. Li & S. Li, 2009. Identifying Chinese species of Gammarus (Crustacea: Amphipoda) using DNA barcoding. Current Zoology 55: 158–164.

    CAS  Google Scholar 

  • ICZN (International Commission on Zoological Nomenclature). 1999. International Code of Zoological Nomenclature. The International Trust for Zoological Nomenclature, London. (http://www.nhm.ac.uk/hosted-sites/iczn/code/).

  • Jörger, K. M., J. L. Norenburg, N. G. Wilson & M. Schrödl, 2012. Barcoding against a paradox? Combined molecular species delineations reveal multiple cryptic lineages in elusive meiofaunal sea slugs. BMC Evolutionary Biology 12: 245.

    Article  PubMed  PubMed Central  Google Scholar 

  • Joyce, D. A., D. H. Lunt, M. J. Genner, G. F. Turner, R. Bills & O. Seehausen, 2011. Repeated colonization and hybridization in Lake Malawi cichlids. Current Biology 21: R108–R109.

    Article  PubMed  CAS  Google Scholar 

  • Kamaltynov, R. M., 1992. O sovremennom sostoyanii sistematiki Baikalskikh amfipod. Zoologicheskii Zhurnal 71: 24–31.

    Google Scholar 

  • Kamaltynov, R. M., 1999. On the higher classification of Lake Baikal amphipods. Crustaceana 72: 933–944.

    Article  Google Scholar 

  • Kamaltynov, R. M., 2001 [printing date 2002]. Amfipody (Amphipoda: Gammaroidea). In Timoshkin, O. A. (ed.), Index of Animal Species Inhabiting Lake Baikal and its Catchment Area, 1(1). Nauka, Novosibirsk: 572–831.

  • Kamaltynov, R. M., 2009. Vyshie rakoobraznye (Amphipoda: Gammaroidea) Angary i Eniseya. In Timoshkin, O. A. (ed.), Index of Animal Species Inhabiting Lake Baikal and its Catchment Area, 2(1). Nauka, Novosibirsk: 297–329.

    Google Scholar 

  • Kamaltynov, R. M., V. I. Chernykh, Z. V. Slugina & E. B. Karabanov, 1993. The consortium of the sponge Lubomirskia baicalensis in Lake Baikal, East Siberia. Hydrobiologia 271: 179–189.

    Google Scholar 

  • Koblmüller, S., N. Duftner, K. M. Sefc, et al., 2007. Reticulate phylogeny of gastropod-shell-breeding cichlids from Lake Tanganyika – the result of repeated introgressive hybridization. BMC Evolutionary Biology 7: 7.

    Article  PubMed  PubMed Central  Google Scholar 

  • Kroll, O., R. Hershler, C. Albrecht, et al., 2012. The endemic gastropod fauna of Lake Titicaca: correlation between molecular evolution and hydrographic history. Ecology and Evolution. doi:10.1002/ece3.280.

    PubMed  PubMed Central  Google Scholar 

  • Lefébure, T., C. J. Douady, M. Gouy & J. Gibert, 2006. Relationship between morphological taxonomy and molecular divergence within Crustacea: proposal of a molecular threshold to help species delimitation. Molecular Phylogenetics and Evolution 40: 435–447.

    Article  PubMed  Google Scholar 

  • Macdonald, K. S., L. Yampolsky & J. E. Duffy, 2005. Molecular and morphological evolution of the amphipod radiation of Lake Baikal. Molecular Phylogenetics and Evolution 35: 323–343.

    Article  PubMed  CAS  Google Scholar 

  • Mayr, E., 1963. Animal Species and Evolution. Belknap Press, Cambridge, Mass.

    Book  Google Scholar 

  • Mekhanikova, I. V., 2010. Morphology of mandible and lateralia in six endemic amphipods (Amphipoda, Gammaridae) from Lake Baikal in relation to feeding. Crustaceana 83: 865–887.

    Article  Google Scholar 

  • Mekhanikova, I. V., T. Ya. Sitnikova, V. V. Petryashev, M. M. Penzina & O. A. Timoshkin, 2010. Catalogue of amphipod collection (including type speciemens), stored in the Limnological Institute SB RAS (Irkutsk). In Timoshkin, O. A. & T. Ya. Sitnikova (eds), Index of Animal Species Inhabiting Lake Baikal and its Catchment Area 2(2), Nauka, Novosibirsk: 1270–1325.

  • Schön, I., R. L. Pinto, S. Halse, A. J. Smith, K. Martens & C. W. Birky Jr., 2012. Cryptic species in putative ancient asexual darwinulids (Crustacea, Ostracoda). PLoS One 7(7): e39844.

    Article  PubMed  PubMed Central  Google Scholar 

  • Schreiber, K., T. Hauffe, C. Albrecht & T. Wilke, 2008. The role of barriers and gradients in differentiation processes of pyrgulinid microgastropods of Lake Ohrid. Hydrobiologia 682: 61–73.

    Article  Google Scholar 

  • Sowinsky, V. K., 1915. Amphipoda ozera Baikala (Sem. Gammaridae). Zoologicheskieya izsledovaniya ozera Baikala 9. Kiev.

  • Stebbing, T. R. R., 1899. Amphipoda from the Copenhagen Museum and other sources. Part 2. Transaction of the Linnean Society of London, 2nd series. Zoology 7: 395–432.

    Google Scholar 

  • Stebbing, T. R. R., 1906. Amphipoda. I. Gammaridea. Das Tierreich 21: 1–806.

    Google Scholar 

  • Sturmbauer, C., S. Baric, W. Salzburger, L. Rüber & E. Verheyen, 2001. Lake level fluctuations synchronize genetic divergence of cichlid fishes in African lakes. Molecular Biology and Evolution 18: 144–154.

    Article  PubMed  CAS  Google Scholar 

  • Takhteev, V. V., 2000. Ocherki o bokoplavakh ozera Baikal (sistematika, sravnitelnaya ekologiya, evolyutsiya). Izdadelstvo Irkutskogo Universiteta, Irkutsk.

    Google Scholar 

  • Takhteev, V. V. & A. M. Levashkevich, 2006. K sistematike roda Garjajewia (Crustacea, Amphipoda) iz ozera Baikal s opisaniem novogo podvida. Zoologicheskii Zhurnal 85: 1422–1432.

    Google Scholar 

  • Tamura, K., D. Peterson, N. Peterson, G. Stecher, M. Nei & S. Kumar, 2011. MEGA 5: molecular evolution genetic analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28: 2439–2442.

    Article  Google Scholar 

  • Väinölä, R. & R. M. Kamaltynov, 1999. Species diversity and speciation in the endemic amphipods of Lake Baikal: molecular evidence. Crustaceana 72: 945–956.

    Article  Google Scholar 

  • Verovnik, R., B. Sket & P. Trontelj, 2005. The colonization of Europe by the freshwater crustacean Asellus aquaticus (Crustacea: Isopoda) proceeded from ancient refugia and was directed by habitat connectivity. Molecular Ecology 14: 4355–4369.

    Article  PubMed  CAS  Google Scholar 

  • Yampolsky, L Yu, R. M. Kamaltynov, D. Ebert, D. A. Filatov & V. I. Chernykh, 1994. Variation of allozyme loci in endemic gammarids of Lake Baikal. Biological Journal of the Linnean Society 53: 309–323.

    Article  Google Scholar 

Download references

Acknowledgments

We thank the crews of r/v “Titov” and r/v “Vereshchagin” and the expedition and project leaders I. V. Khanaev, S. V. Kirilchik, D. Yu. Sherbakov and E. Verheyen for enabling the fieldwork, and V. V. Petryashev (ZIN), K. Philipps-Bussau, P. Wagner and A. Brandt (ZMH), and C. O. Coleman (ZMB) for the access to museum specimens. We are grateful to Igor V. Khanaev and his diving team, who collected most of the material, and to Qui Yang, who kindly sent us DNA samples and voucher specimens from two localities. We thank Ravil M. Kamaltynov, who shared his information about variability of Dorogostaiskia, which directed our initial sampling, and his notes on color variation in his own material. We also thank Vadim V. Takhteev for discussion that clarified the nomenclature of the group and Koen Martens for valuable comments on the manuscript, and acknowledge the help of the MES laboratory staff at UH. Our work has been supported by grants from the Academy of Finland, partly in connection with the ESF EuroDiversity project MOLARCH (AF Grant 112001), from the Finnish Cultural Foundation and the Ella and Georg Ehrnrooth Foundation.

Author information

Authors and Affiliations

  1. Finnish Museum of Natural History, University of Helsinki, P.O. Box 17, 00014, Helsinki, Finland

    Mikhail E. Daneliya & Risto Väinölä

Authors
  1. Mikhail E. Daneliya
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Risto Väinölä
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mikhail E. Daneliya.

Additional information

Guest editors: T. von Rintelen, R. M. Marwoto, G. D. Haffner & F. Herder / Speciation in Ancient Lakes – Classic Concepts and New Approaches

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 1360 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Daneliya, M.E., Väinölä, R. Five subspecies of the Dorogostaiskia parasitica complex (Dybowsky) (Crustacea: Amphipoda: Acanthogammaridae), epibionts of sponges in Lake Baikal. Hydrobiologia 739, 95–117 (2014). https://doi.org/10.1007/s10750-013-1671-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-013-1671-x

Keywords

Search

Navigation