Phylogenetic relationship within Cumacea (Crustacea: Peracarida) and genetic variability of two Antarctic species of the family Leuconidae

Peter Rehm; Sven Thatje; Florian Leese; Christoph Held

doi:10.3989/scimar.05053.17A

Authors

Peter Rehm Functional Ecology, Alfred-Wegener-Institut, Helmholtz-Zentrum für Polar- und Meeresforschung (AWI) https://orcid.org/0000-0002-9646-0807
Sven Thatje National Oceanography Centre, School of Ocean and Earth Science, University of Southampton https://orcid.org/0000-0001-8727-0115
Florian Leese Aquatic Ecosystem Research, University of Duisburg-Essen https://orcid.org/0000-0002-5465-913X
Christoph Held Functional Ecology, Alfred-Wegener-Institut, Helmholtz-Zentrum für Polar- und Meeresforschung (AWI) https://orcid.org/0000-0001-8854-3234

DOI:

https://doi.org/10.3989/scimar.05053.17A

Keywords:

16S rDNA, biogeography, cryptic speciation, cryptic species, mitochondrial DNA, molecular phylogeny

Abstract

Phylogenetic hypotheses for the peracarid order Cumacea are scarce and have not provided a solution to the full extent. In the present study, a fragment of the mitochondrial 16S rDNA was used to erect a phylogenetic hypothesis for three cumacean families, Diastylidae, Bodotriidae and Leuconidae, along with intra-family relationships of the latter. The Cumacea resolved monophyletic with tanaids and isopods as outgroup taxa. The Diastylidae were the only family with good support for monophyly. The genus Leucon resolved paraphyletic, whereas the subgenus Crymoleucon was monophyletic. Furthermore, the genetic structure was analysed for two leuconid species, Leucon antarcticus Zimmer, 1907 and L. intermedius Mühlenhardt-Siegel, 1996, from the Weddell Sea and the Ross Sea. The two species showed different patterns of intraspecific genetic variability. In contrast to L. intermedius, a bimodal distribution of pairwise genetic distances was observed for L. antarcticus, which is correlated with geographical and depth distributions between the Ross Sea and the Weddell Sea. Although a clear evaluation of cryptic speciation in these species requires additional work on more specimens from more geographic regions and broader depth ranges, differences shown in the sequences of 16S rDNA can only be explained by genetic separation of populations between the Weddell Sea and the Ross Sea for an extended period of time.

Downloads

Download data is not yet available.

References

Allcock A.L., Brierley A.S., Thorpe J.P., et al. 1997. Restricted gene flow and evolutionary divergence between geographically separated populations of the Antarctic octopus Pareledone turqueti. Mar. Biol. 129: 97-102. https://doi.org/10.1007/s002270050150

Arango C.P., Soler-Membrives A., Miller K.J. 2011. Genetic differentiation in the circum-Antarctic sea spider Nymphon australe (Pycnogonida; Nymphonidae). Deep-Sea Res. II 58: 212-219. https://doi.org/10.1016/j.dsr2.2010.05.019

Băcescu M., Muradian Z. 1974. Campylaspenis, Styoptocuma, Atlantocuma, new genera of Cumacea from the deep waters of the Atlantic. Rev. Roum. Biol. 19: 71-78.

Băcescu M., Petrescu I. 1999. Ordre des Cumacés (Cumacea Krøyer, 1846). Mém. Inst. Océanogr. (Monaco) 19: 391-428.

Baird H.P., Miller K.J., Stark J.S. 2011. Evidence of hidden biodiversity, ongoing speciation and diverse patterns of genetic structure in giant Antarctic amphipods. Mol. Ecol. 20: 3439-3454. https://doi.org/10.1111/j.1365-294X.2011.05173.x PMid:21733028

Beermann J., Westbury M.V., Hofreiter M., et al. 2018. Cryptic species in a well-known habitat: applying taxonomics to the amphipod genus Epimeria (Crustacea, Peracarida). Sci. Rep. 8: 6893. https://doi.org/10.1038/s41598-018-25225-x PMid:29720606 PMCid:PMC5931980

Błażewicz M., Heard W.H. 1999. First record of the family Gynodiastylidae Stebbing, 1912 (Crustacea: Malacostraca: Cumacea) from Antarctic waters with the description of Gynodiastylis jazdzewskii, a new species. Proc. Biol. Soc. Wash. 112: 362-367.

Calman W.T. 1907. Crustacea. II. Cumacea. National Antarctic Expedition 1901-1904. Brit. Mus. Nat. Hist. Rep. Zool. 2: 1-6.

Cartes J.E. 1993. Diets of two deep-sea decapods: Nematocarcinus exilis (Caridea: Nematocarcinidae) and Munida tenuimana (Anomura: Galatheidae) on the Western Mediterranean slope. Ophelia 37: 213-229. https://doi.org/10.1080/00785326.1993.10429919

Clarke A., Crame J.A. 1989. The origin of the Southern Ocean marine fauna. In: Crame J.A. (ed.) Origins and evolution of the Antarctic biota. Geol. Soc. Lond. Spec. Publ. 47: 253-268. https://doi.org/10.1144/GSL.SP.1989.047.01.19

Dornburg A., Federman S., Eytan R.I., et al. 2016. Cryptic species diversity in sub-Antarctic islands: A case study of Lepidonotothen. Mol. Phyl. Evol. 194: 32-43. https://doi.org/10.1016/j.ympev.2016.07.013 PMid:27421566

Fraser C.I., Zuccarello G.C., Spencer H.G., et al. 2013. Genetic affinities between trans-oceanic populations of non-buoyant macroalgae in the high latitudes of the Southern Hemisphere. PLoS ONE 8: e69138. https://doi.org/10.1371/journal.pone.0069138 PMid:23894421 PMCid:PMC3718832

Gutell R.R., Gray M.W., Schnare M.N. 1993. A compilation of large subunit (23S and 23S-like) ribosomal RNA structures: 1993. Nucleic Acids Res. 21: 3055-3074. https://doi.org/10.1093/nar/21.13.3055 PMid:8332527 PMCid:PMC309733

Hall T.A. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41: 95-98.

Haye P.A. 2002. Systematics of the Cumacea (Crustacea). PhD Thesis, University of Maine, 266 pp.

Haye P.A. 2007. Systematics of the genera of Bodotriidae (Crustacea: Cumacea). Zool. J. Linn. Soc. 151: 1-58. https://doi.org/10.1111/j.1096-3642.2007.00322.x

Haye P.A., Kornfield I., Watling L. 2004. Molecular insights into Cumacean family relationships (Crustacea, Cumacea). Mol. Phyl. Evol. 30: 798-809. https://doi.org/10.1016/j.ympev.2003.08.003 PMid:15012957

Held C. 2000. Speziation im Südpolarmeer - Systematik und Biogeographie der Serolidae und Arcturidae (Crustacea, Isopoda). PhD Thesis, University of Bielefeld, 144 pp.

Held C. 2003. Molecular evidence for cryptic speciation within the widespread Antarctic crustacean Ceratoserolis trilobitoides (Crustacea, Isopoda). In: Huiskes A.H., Geiskes W.W., et al. (eds), Antarctic biology in a global context. Backhuys Publishers, Leiden, 135-139.

Held C., Wägele J.W. 2005. Cryptic speciation in the giant Antarctic isopod Glyptonotus antarcticus (Isopoda: Valvifera: Chaertiliidae). Sci. Mar. 69: 175-181. https://doi.org/10.3989/scimar.2005.69s2175

Hessler R.R. 1983. A defense of the caridoid facies: wherein the early evolution of the Eumalacostraca is discussed. In: Schram F.R, (ed.) Crustacean Phylogeny, Crustacean Issues, A.A. Balkema, Rotterdam, pp. 145-164.

Hillis D.M., Moritz C., Mable B.K. (eds). 1996. Molecular Systematics, 2nd ed., Palgrave Macmillan, 655 pp. https://doi.org/10.2307/1447682

Huelsenbeck J.P., Ronquist F.R. 2001. MrBayes: Bayesian inference of phylogeny. Biometrics 17: 754-755. https://doi.org/10.1093/bioinformatics/17.8.754 PMid:11524383

Jones N.S. 1984. The family Nannastacidae (Crustacea: Cumacea) from the deep Atlantic. Bull. Brit. Mus. Nat. Hist. Zool. 46: 207-289. https://doi.org/10.5962/bhl.part.15965

Kalendar R. 2003. FastPCR: A Program for fast design PCR Primer, DNA and Protein manipulation. (2.5.59).

Karaman S. 1953. Über subterrane Isopoden und Amphipoden des Karstes von Dubrovnik und seines Hinterlandes. Acta Musei Macedonici Sci. Nat. 1(7): 137-167.

Leese F., Agrawal S., Held C. 2010. Long-distance island hopping without dispersal stages: transportation across major zoogeographic barriers in a Southern Ocean isopod. Naturwissenschaften, 97: 583-594. https://doi.org/10.1007/s00114-010-0674-y PMid:20454771

Ledoyer M. 1993. Cumacea (Crustacea) de la campagne EPOS 3 du R.V. Polarstern en mare de Weddell (est Antarctique). J. Nat. Hist. 27: 1041-1096. https://doi.org/10.1080/00222939300770661

Linse K., Cope T., Lörz A.N., et al. 2007. Is the Scotia Sea a centre of Antarctic marine diversification? Some evidence of cryptic speciation in the circum-Antarctic bivalve Lissarca notorcadensis (Arcoidea: Philobryidae). Polar Biol. 30: 1059-1068. https://doi.org/10.1007/s00300-007-0265-3

Lomakina M. 1968. Stroenie pecenocinih diverticul u cumovih rakov (Cumacea) i ego filogeneticeskoe znancenie. Zool. J. 47: 60-72.

Löytynoja A., Milinkovitch M.C. 2003. ProAlign, a probabilistic multiple alignment program (version 0.5a0). Bioinformatics 19: 1505-1513. https://doi.org/10.1093/bioinformatics/btg193 PMid:12912831

Martin J.W., Davis G.E. 2001. An updated classification of the recent Crustacea. Nat. Hist. Mus. Los Ang. Count., Sci. Ser. 39: 124 pp.

Mühlenhardt-Siegel U. 1999. On the biogeography of Cumacea (Crustacea, Malacostraca). A comparison between South America, the Subantarctic Islands, and Antarctica: present state of the art. Sci. Mar. 63(Suppl. 1): 295-302. https://doi.org/10.3989/scimar.1999.63s1295

Pabis K., Błażewicz-Paszkowycz M. 2011. Distribution and diversity of cumacean assemblages in Admiralty Bay, King George Island. Polish Polar Res. 32: 341-354. https://doi.org/10.2478/v10183-011-0024-6

Palumbi S.R., Martin A., Romano S., et al. 1991. The Simple Fool's Guide to PCR, version 2. University of Hawaii Press, Honolulu, 43 pp.

Posada D., Crandall K.A. 1998. Modeltest: testing the model of DNA substitution. Bioinformatics 14: 817-818. https://doi.org/10.1093/bioinformatics/14.9.817 PMid:9918953

Raupach M.J., Wägele J.W. 2006. Distinguishing cryptic species in Antarctic Asellota (Crustacea: Isopoda)-a preliminary study of mitochondrial DNA in Acanthaspidia drygalskii. Ant. Sci. 18: 191-198. https://doi.org/10.1017/S0954102006000228

Rehm P., Heard R. 2008. Leucon (Crymoleucon) rossi, a new species (Crustacea: Cumacea: Leuconidae) from the shelf waters of the Ross Sea (Antarctica), with a key to the genus Leucon south of 60°S. Sci. Mar. 72: 683-691. https://doi.org/10.3989/scimar.2008.72n4683

Rehm P., Thatje S., Mühlenhardt-Siegel U., et al. 2007. Composition and distribution of the peracarid crustacean fauna along a latitudinal transect off Victoria Land (Ross Sea, Antarctica) with special emphasis on the Cumacea. Polar Biol. 30: 871-881. https://doi.org/10.1007/s00300-006-0247-x

Richter S., Scholz G.S. 2001. Phylogenetic analysis of the Malacostraca (Crustacea). J. Zool. Syst. Evo. Res. 39: 113-136. https://doi.org/10.1046/j.1439-0469.2001.00164.x

San Vicente C., Ramos A., Jimeno A., et al. 1997. Suprabenthic assemblages from South Shetland Islands and Bransfield Strait (Antarctica): preliminary observations on faunistical composition, bathymetric and near-bottom distribution. Polar Biol. 18: 415-422. https://doi.org/10.1007/s003000050208

Sars G.O. 1873. Beskrivelse af syv nye Cumaceer fravestindien og det syd-Atlantiske Ocean. Kongl Svenska Vetenskaps-Akademiens Handlingar 11: 3-30.

Sars G.O. 1887. Report on the Cumacea collected by H.M.S Challenger during the years 1873-1876. Rep. Sci. Res. Voy. HMS Chall. Zool. 19: 1-78. https://doi.org/10.5962/bhl.title.10403

Schlacher T.A, Wooldridge T.H. 1996. Patterns of selective predation by juvenile, benthivorous fish on estuarine macrofauna. Mar. Biol. 125: 241-247. https://doi.org/10.1007/BF00346304

Schram F.R. 1986. Crustacea. Oxford University Press, New York, 606 pp.

Schram F.R., Hof C.H.J. 1998. Fossils and the interrelationships of major Crustacean groups. In: Edgecombe G.D. (ed.), Arthropod Fossils and Phylogeny. New York, Columbia University Press: pp. 233-302.

Schubart C.D, Koller P. 2005. Genetic diversity of freshwater crabs (Brachyura: Sesarmidae) from central Jamaica with description of a new species. J. Nat. Hist. 39: 469-481. https://doi.org/10.1080/00222930410001671291

Siewing R. 1963. Studies in malacostracan morphology: results and problems. In: Whittington H.B., Rolfe W.D.I. (eds), Phylogeny and Evolution of Crustacea. Mus. Comp. Zool. Spec. Publ. 13: 85-103.

Staden R., Beal K.F., Bornefield J.K. 1989. The Staden package, 1989. Methods Mol. Biol. 132: 115-130. https://doi.org/10.1385/1-59259-192-2:115 PMid:10547834

Stamatakis A. 2006. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688-2690. https://doi.org/10.1093/bioinformatics/btl446 PMid:16928733

Swofford D.L. 2003. PAUP*. Phylogenetic analysis using parsimony (*and other methods). Version 4. Sinauer Associates, Sunderland, Massachusetts.

Thatje S. 2012. Effects of capability for dispersal on the evolution of diversity in Antarctic benthos. Int. Comp. Biol. 52: 470-482. https://doi.org/10.1093/icb/ics105 PMid:22821584

Thatje S., Hillenbrand C.D., Larter R. 2005. On the origin of Antarctic marine benthic community structure. Trends Ecol. Evol. 20: 534-540. https://doi.org/10.1016/j.tree.2005.07.010 PMid:16701431

Thatje S, Hillenbrand C.D, Mackensen A., et al. 2008. Life hung by a thread: endurance of Antarctic fauna in glacial periods. Ecology 89: 682-692. https://doi.org/10.1890/07-0498.1 PMid:18459332

Watling L. 1991. Revision of the cumacean family Leuconidae. J. Crust. Biol. 11: 569-582. https://doi.org/10.2307/1548527

Watling L. 1999. Towards understanding the relationships of the peracaridan orders: the necessity of determining exact homologies. In: Schram F.R., von Vaupel Klein J.C., (eds), Crustaceans and the Biodiversity Crisis. Proc. Fourth Int. Crust. Congr. Vol. I, Amsterdam, Netherlands, pp. 73-89.

Wills M.A. 1998. A phylogeny of recent and fossil Crustacea derived from morphological characters. In: Fortey R.A., Thomas R.H. (eds), Arthropod Relationships. Syst. Ass. Spec. Vol. Ser. 55, Chapman & Hal, London, pp. 189-209. https://doi.org/10.1007/978-94-011-4904-4_15

Wilson N.G., Hunter R.L., Lockhart S.J., et al. 2007. Multiple lineages and absence of panmixia in the "circumpolar" crinoid Promachocrinus kerguelensis from the Atlantic sector of Antarctica. Mar. Biol. 152: 895-904. https://doi.org/10.1007/s00227-007-0742-9

Zimmer C. 1907. Neue Cumaceen aus den Familien Diastylidae und Leuconidae von der Deutschen und Schwedischen Südpolar- Expedition. Zoologischer Anzeiger 31: 220-229.

Zimmer C. 1913. Die Cumaceen der Deutschen Südpolar-Expedition 1901-1903. Zoologie 6: 437-492.

Zimmer C. 1941. Cumacea. Dr. H.G. Bronns Klassen und Ordnungen des Tierreichs 5: 222 pp.