Skip to main content Skip to main navigation menu Skip to site footer
Article
Published: 2021-07-29

The hidden diversity of the genus Lyurella Derzhavin, 1939 (Crustacea: Amphipoda: Crangonyctidae): four new species from the subterranean habitats of the northwestern Caucasus, Russia

A.N. Severtsov Institute of Ecology and Evolution of RAS, Moscow 119071, Russia.
A.N. Severtsov Institute of Ecology and Evolution of RAS, Moscow 119071, Russia.
diversity stygobiotic Russia Caucasus

Abstract

Four new species of the Palaearctic crangonyctid amphipod genus Lyurella Derzhavin, 1939 (Crustacea: Amphipoda: Crangonyctidae), L. mikhailovi sp. n., L. fanagorica sp. n., L. fontinalis sp. n. and L. asheensis sp. n., are described based on an integrative approach from the subterranean habitats of the southwestern foothills of the Greater Caucasian Ridge (the north-eastern Black Sea coast). Despite the relative proximity of the habitats, the interspecific genetic divergence (by COI mtDNA gene marker) between the newly outlined Caucasian species of the genus varied from 11 to 21%, demonstrating a long-term isolation and lack of gene flow for at least 3–7Mya, starting from the Pliocene. The lowest genetic divergence between L. shepsiensis Sidorov, 2015 and L. asheensis sp. n., estimated as 4%, is also considered species-specific due to the presence of distinct morphological differences. We discuss the phylogeny, morphology, and distribution and provide a key for all known species of Lyurella. DNA barcoding data for all species, including the type species of the genus, Lyurella hyrcana Derzhavin, 1939, are presented for the first time.

References

  1. Aliev, R.A. (2000) Fauna bokoplavov (Crustacea, Amphipoda) presnyh vodoemov Azerbaidzhana. Elm, Baku, 516 pp. [In Russian]

  2. Arbačiauskas, K. (2008) Synurella ambulans (F. Müller, 1846), A new native amphipod species of Lithuanian waters. Acta Zoologica Lituanica, 18 (1), 66–68.  https://doi.org/10.2478/v10043-008-0006-z

    DOI: https://doi.org/10.2478/v10043-008-0006-z
  3. Avise, J.C. (1993) Perspective: The evolutionary biology of aging, sexual reproduction, and DNA repair. Evolution, 47 (5), 1293–1301.  https://doi.org/10.1111/j.1558-5646.1993.tb02155.x

    DOI: https://doi.org/10.1111/j.1558-5646.1993.tb02155.x
  4. Bouckaert, R., Heled, J., Kühnert, D., Vaughan, T., Wu, Ch., Xie, D., Suchard, M.A., Rambaut, A. & Drummond, A.J. (2014) Beast 2: a software platform for Bayesian evolutionary analysis. PLoS Computational Biology, 10, e1003537.  https://doi.org/10.1371/journal.pcbi.1003537

    DOI: https://doi.org/10.1371/journal.pcbi.1003537
  5. Bouckaert, R., Vaughan, T.G., Barido-Sottani, J., Duchêne, S., Fourment, M., Gavryushkina, A., Heled, J., Jones, G., Kühnert, D., De Maio, N., Matschiner, M., Mendes, F.K., Müller, N.F., Ogilvie, H.A., du Plessis, L., Popinga, A., Rambaut, A., Rasmussen, D., Siveroni, I., Suchard, M.A., Wu, Ch., Xie, D., Zhang, C., Stadler, T. & Drummond, A.J. (2019) BEAST 2.5: An advanced software platform for Bayesian evolutionary analysis. PLoS Computational Biology, 15 (4), e1006650.  https://doi.org/10.1371/journal.pcbi.1006650

    DOI: https://doi.org/10.1101/474296
  6. Copilaş‐Ciocianu, D. & Petrusek, A. (2015) The southwestern Carpathians as an ancient centre of diversity of freshwater gammarid amphipods: insights from the Gammarus fossarum species complex. Molecular Ecology, 24 (15), 3980–3992.  https://doi.org/10.1111/mec.13286

    DOI: https://doi.org/10.1111/mec.13286
  7. Copilaș-Ciocianu, D., Sidorov, D. & Gontcharov, A. (2019) Adrift across tectonic plates: molecular phylogenetics supports the ancient Laurasian origin of old limnic crangonyctid amphipods. Organisms Diversity & Evolution, 19, 191–207.  https://doi.org/10.1007/s13127-019-00401-7

    DOI: https://doi.org/10.1007/s13127-019-00401-7
  8. Derzhavin, A.N. (1939) The freshwater Peracarida of the Talysh. Trudy Zoologicheskogo Instituta Azerbaijanskogo filiala AN, Baku, 10, 43–58. [in Russian]

  9. Drummond, A.J. & Bouckaert, R.R. (2015) Bayesian evolutionary analysis with BEAST. Cambridge University Press, Cambridge, 249 pp. https://doi.org/10.1017/CBO9781139095112

    DOI: https://doi.org/10.1017/CBO9781139095112
  10. Drummond, A.J., Suchard, M.A., Xie, D. & Rambaut, A. (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution, 29, 1969–73.  http://doi.org/10.1093/molbev/mss075

    DOI: https://doi.org/10.1093/molbev/mss075
  11. Eme, D., Zagmajster, M., Delić, T., Fišer, C., Flot, J.-F., Konecny-Dupré, L., Pálsson, S., Stoch, F., Zakšek, V., Douady, C.J. & Malard, F. (2017) Do cryptic species matter in macroecology? Sequencing European groundwater crustaceans yields smaller ranges but does not challenge biodiversity determinants. Ecography, 41, 424–436.  https://doi.org/10.1111/ecog.02683

    DOI: https://doi.org/10.1111/ecog.02683
  12. Fišer, C., Sket, B. & Stoch, F. (2006) Distribution of four narrowly endemic Niphargus species (Crustacea: Amphipoda) in the western Dinaric region with description of a new species. Zoologischer Anzeiger, 245, 77–94.  https://doi.org/10.1016/j.jcz.2006.05.003

    DOI: https://doi.org/10.1016/j.jcz.2006.05.003
  13. 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. Molecular Marine Biology and Biotechnology, 3, 294–299.

  14. Guindon, S., Dufayard, J.F., Lefort, V., Anisimova, M., Hordijk, W. & Gascuel, O. (2010) New Algorithms and Methods to Estimate Maximum–Likelihood Phylogenies: Assessing the Performance of PhyML 3.0. Systematic, 59 (3), 307–321.  https://doi.org/10.1093/sysbio/syq010

    DOI: https://doi.org/10.1093/sysbio/syq010
  15. Guy-Haim, T., Simon-Blecher, N., Frumkin, A., Naaman, I. & Achituv, Y. (2018) Multiple transgressions and slow evolution shape the phylogeographic pattern of the blind cave-dwelling shrimp Typhlocaris. PeerJ, 6, e5268.  https://doi.org/10.7717/peerj.5268

    DOI: https://doi.org/10.7717/peerj.5268
  16. Holsinger, J.R. (1977) A review of the systematics of the Holarctic amphipod family Crangonyctidae. Crustaceana, Supplement, 4, 244–281.

  17. Holsinger, J.R. (1994) Pattern and process in the biogeography of subterranean amphipods. Hydrobiologia, 287 (1), 131–145.  https://doi.org/10.1007/BF00006902

    DOI: https://doi.org/10.1007/BF00006902
  18. Karaman, G.S. (1974) 59. Contribution to the knowledge of the Amphipoda. Revision of the genus Stygobromus Cope 1872 (Fam. Gammaridae) from North America. Glasnik Republickog Zavoda za Zastitu Prirode, 7, 97–125.

  19. Kimura, M. (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution, 16 (2), 111–120.  https://doi.org/10.1007/BF01731581

    DOI: https://doi.org/10.1007/BF01731581
  20. Kornobis, E., Pálsson, S., Sidorov, D.A., Holsinger, J.R. & Kristjánsson, B.K. (2011) Molecular taxonomy and phylogenetic affinities of two groundwater amphipods, Crangonyx islandicus and Crymostygius thingvallensis, endemic to Iceland. Molecular Phylogenetics and Evolution, 58 (3), 527–539.  https://doi.org/10.1016/j.ympev.2010.12.010

    DOI: https://doi.org/10.1016/j.ympev.2010.12.010
  21. Kristjánsson, B.K. & Svavarsson, J. (2004) Crymostygidae, a new family of subterranean freshwater gammaridean amphipods (Crustacea) recorded from subarctic Europe. Journal of Natural History, 38, 1881–1894.  https://doi.org/10.1080/00222930310001597295

    DOI: https://doi.org/10.1080/00222930310001597295
  22. Lefébure, T., Douady, C.J., Gouy, M., Trontelj, P., Briolay, J. & Gibert, J. (2006) Phylogeography of a subterranean amphipod reveals cryptic diversity and dynamic evolution in extreme environments. Molecular Ecology, 15, 1797–1806.  https://doi.org/10. 1111/j.1365-294X.2006.02888.x

    DOI: https://doi.org/10.1111/j.1365-294X.2006.02888.x
  23. Lefébure, T., Douady, C.J., Malard, F. & Gibert, J. (2007) Testing dispersal and cryptic diversity in a widely distributed groundwater amphipod (Niphargus rhenorhodanensis). Molecular Phylogenetics and Evolution, 42, 676–686.  https://doi.org/10.1016/j.ympev.2006.08.020

    DOI: https://doi.org/10.1016/j.ympev.2006.08.020
  24. Marin, I.N. (2019) Crustacean “cave fishes” from the Arabika karst massif (Abkhazia, Western Caucasus): new species of stygobiotic crustacean genera Xiphocaridinella and Niphargus from the Gegskaya Cave and adjacent area. Arthropoda Selecta, 28 (2), 225–245.  https://doi.org/10.15298/arthsel.28.2.05

    DOI: https://doi.org/10.15298/arthsel.28.2.05
  25. Marin, I.N. (2020) The Quaternary speciation in the Caucasus: a new cryptic species of stygobiotic amphipod of the genus Niphargus (Crustacea: Amphipoda: Niphargidae) from the Kumistavi (Prometheus) Cave, Western Georgia. Arthropoda Selecta, 29 (4), 419–432.  https://doi.org/10.15298/arthsel.29.4.04

    DOI: https://doi.org/10.15298/arthsel.29.4.04
  26. Marin, I., Krylenko, S. & Palatov, D. (2021) The Caucasian relicts: a new species of the genus Niphargus (Crustacea: Amphipoda: Niphargidae) from the Gelendzhik–Tuapse area of the Russian southwestern Caucasus. Zootaxa, 4963 (3), 483–504.  https://doi.org/10.11646/zootaxa.4963.3.5

    DOI: https://doi.org/10.11646/zootaxa.4963.3.5
  27. Marin, I. & Palatov, D. (2019) A new species of the genus Niphargus (Crustacea: Amphipoda: Niphargidae) from the south-western part of the North Caucasus. Zoology in the Middle East, 65 (4), 336–346.  https://doi.org/10.1080/09397140.2019.1663907

  28. Marin, I. & Palatov, D. (2021a) Volgonyx gen.n. and Pontonyx gen.n., two new genera of the family Crangonyctidae (Crustacea: Amphipoda) from the southeastern Europe. Arthropoda Selecta, 30 (1), 43–61.  https://doi.org/10.15298/arthsel.30.1.05

    DOI: https://doi.org/10.15298/arthsel.30.1.05
  29. Marin, I. & Palatov, D. (2021b) Cryptic refugee on the northern slope of the Greater Caucasian Ridge: Discovery of Niphargus (Crustacea: Amphipoda: Niphargidae) in the North Ossetia–Alania, North Caucasus, separated from its relatives in the late Miocene. Zoologischer Anzeiger, 292, 163–183.  https://doi.org/10.1016/j.jcz.2021.03.002

    DOI: https://doi.org/10.1016/j.jcz.2021.03.002
  30. McInerney, C.E., Maurice, L., Robertson, A.L., Knight, L.R.F.D., Arnscheidt, J., Venditti, C., Dooley, J.S.G., Mathers, T., Matthijs, S., Eriksson, K., Proudlove, G.S. & Hänfling, B. (2014) The ancient Britons: groundwater fauna survived extreme climate change over tens of millions of years across NW Europe. Molecular Ecology, 23, 1153–1166.  https://doi.org/10.1111/mec.12664

    DOI: https://doi.org/10.1111/mec.12664
  31. Ruffo, S. (1974) Studi sui Crostacei Anfipodi. 75. Il genere Synurella Wrzesn. in Anatolia, descrizione di una nuova specie e considerazioni su Lyurella hyrcana Dersh. (Crustacea, Amphipoda, Gammaridea). Memorie del Museo Civico di Storia Naturale, Verona, 20, 389–404.

  32. Palatov, D.M. & Marin, I.N. (2020) A new genus of the family Crangonyctidae (Crustacea, Amphipoda) from the Palaearctic, with descriptions of two new species from the foothills of the Altai Mountains. Zoologicheskii Zhurnal, 99 (10), 1160–1186.  https://doi.org/10.31857/S004451342010013X

    DOI: https://doi.org/10.31857/S004451342010013X
  33. Pons, J., Barraclough, T.G., Gomez-Zurita, J., Cardoso, A., Duran, D.P., Hazell, S., Kamoun, S., Sumlin, W.D. & Vogler, A.P. (2006) Sequencebased species delimitation for the DNA taxonomy of undescribed insects. Systematic Biology, 55, 595–609.  https://doi.org/10.1080/10635150600852011

    DOI: https://doi.org/10.1080/10635150600852011
  34. Puillandre, N., Lambert, A., Brouillet, S. & Achaz, G. (2011) ABGD, Automatic Barcode Gap Discovery for primary species delimitation. Molecular Ecology, 21 (8) 1864–1877.  https://doi.org/10.1111/j.1365-294X.2011.05239.x

    DOI: https://doi.org/10.1111/j.1365-294X.2011.05239.x
  35. Reid, N.M. & Carstens, B.C. (2012) Phylogenetic estimation error can decrease the accuracy of species delimitation: A Bayesian implementation of the general mixed Yule-coalescent model. BMC Evolutionary Biology, 12 (1), 196.  https://doi.org/10.1186/1471-2148-12-196

    DOI: https://doi.org/10.1186/1471-2148-12-196
  36. Sidorov, D. (2015) The spring-dwelling amphipod genus Lyurella (Peracarida, Amphipoda): systematics, distribution, and affinity, with description of the second representative from the Black Sea coast region. Crustaceana, 88, 27–50.  https://doi.org/10.1163/15685403-00003392

    DOI: https://doi.org/10.1163/15685403-00003392
  37. Sidorov, D.A. & Holsinger, J.R. (2007) Amurocrangonyx, a new genus of subterranean amphipod (Crangonyctidae) from the Russian Far East, with a redescription of the poorly known Crangonyx arsenjevi and comments on biogeographic relationships. Journal of Crustacean Biology, 27, 660–669.  https://doi.org/10.1651/S-2817R.1

    DOI: https://doi.org/10.1651/S-2817R.1
  38. Sidorov, D.A. & Gontcharov, A.A. (2015) Preliminary analysis of phylogenetic relationships of the Asian-Pacific endemial subterranean amphipod genus Pseudocrangonyx among families and genera of crangonyctoidean amphipods inferred by partial LSU rDNA gene sequences. Zoological Science, 32, 178–182.  https://doi.org/10. 2108/zs140129

    DOI: https://doi.org/10.2108/zs140129
  39. Svavarsson, J. & Kristjánsson, B.K. (2006) Crangonyx islandicus sp. nov., a subterranean freshwater amphipod (Crustacea, Amphipoda, Crangonyctidae) from springs in lava fields in Iceland. Zootaxa, 1365, 1–17.  https://doi.org/10.11646/zootaxa.1365.1.1

    DOI: https://doi.org/10.11646/zootaxa.1365.1.1
  40. Zhang, J. & Holsinger, J.R. (2003) Systematics of the freshwater amphipod genus Crangonyx (Crangonyctidae) in North America. Virginia Museum of Natural History Memoir, 6, 1–274.  https://doi.org/10.1163/156854008X354894

  41. Zhang, J., Kapli, P., Pavlidis, P. & Stamatakis, A. (2013) A general species delimitation method with applications to phylogenetic placements. Bioinformatics, 29, 2869–2876.  https://doi.org/10.1093/bioinformatics/btt499

    DOI: https://doi.org/10.1093/bioinformatics/btt499

How to Cite

MARIN, I. N., & PALATOV, D. M. (2021). The hidden diversity of the genus <em>Lyurella</em> Derzhavin, 1939 (Crustacea: Amphipoda: Crangonyctidae): four new species from the subterranean habitats of the northwestern Caucasus, Russia. Zootaxa, 5006(1), 127–168. https://doi.org/10.11646/zootaxa.5006.1.17