Skip to main content

Advertisement

SpringerLink
Log in

Hidden diversity in two species complexes of munnopsid isopods (Crustacea) at the transition between the northernmost North Atlantic and the Nordic Seas

  • Biodiversity of Icelandic Waters
  • Published:
Marine Biodiversity Aims and scope Submit manuscript

Abstract

Eurycope producta Sars, 1868 and Eurycope inermis Hansen, 1916 are two widely distributed and highly abundant isopod species complexes within Icelandic waters, a region known for its highly variable environment. The two species complexes have bathymetric depth ranges from 103 to 2029 m (E. producta) and from 302 to 2113 m (E. inermis). Molecular evidence was used for species delimitation within these species complexes by analyzing nuclear (18S rDNA, H3) and mitochondrial (16S rDNA, COI) sequence data. Tree-based methods (BI and ML) and four species delimitation methods (ABGD, GMYC, NDT, PTP) were applied, in order to disentangle the two species complexes. A total of eight and four species clades could be identified within samples of the E. producta and E. inermis complexes and respectively included the closely related species E. dahli Svavarsson, 1987; E. hanseni Ohlin, 1901; and E. cornuta Sars, 1864. The morphological findings coincide with the observed molecular species clades. The elucidated species clades were geographically and bathymetrically much more restricted than previously assumed. Eight species clades featured depth spans of less than 400 m and only four species clades featured depth spans of 1000 to 1500 m. Only two species clades (E. producta sensu stricto and E. inermis sensu stricto) were found on both sides of the Greenland-Scotland Ridge. Further, species distribution maps were generated using random forest, to predict potential distributional patterns for the resolved species clades of the two species complexes. We present the first attempt of combining morphological, molecular, and species distribution models in marine isopods thus far.

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
Fig. 10
Fig. 11

Similar content being viewed by others

Abbreviations

ABGD:

Automated Barcoding Gap Discovery

AWTY:

Are We There Yet

BI:

Bayesian inference

DZMB:

German Centre for Marine Biodiversity Research

GMYC:

Generalized mixed Yule coalescent

GSR:

Greenland-Scotland Ridge

IFR:

Iceland-Faroe Ridge

ML:

Maximum likelihood

NDT:

Nucleotide divergence threshold

OOB:

Out-of-the-box error

PCR:

Polymerase chain reactions

PTP:

Poisson tree process

RF:

Random forest

SDM:

Species distribution modeling

SQ:

Sequencing

ZMH:

Zoological Museum of Hamburg

References

  • Altabet MA, Deuser WG, Honjo S, Stienen C (1991) Seasonal and depth-related changes in the source of sinking particles in the North Atlantic. Nature 354:136–139. https://doi.org/10.1038/354136a0

    Article  Google Scholar 

  • Altschul S, Gish W, Miller W, Myers E, Lipman D (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    Article  PubMed  CAS  Google Scholar 

  • Baird HP, Miller KJ, Stark JS (2011) Evidence of hidden biodiversity, ongoing speciation and diverse patterns of genetic structure in giant Antarctic amphipods. Mol Ecol 20:3439–3454

    Article  PubMed  Google Scholar 

  • Barnard KH (1920) Contributions to the crustacean fauna of South Africa. 6. Further additions to the list of marine isopods. Ann S Afr Mus 17:319–438

    Google Scholar 

  • Barrowclough GF, Zink RM (2009) Funds enough, and time: mtDNA, nuDNA and the discovery of divergence. Mol Ecol 18(14):2934–2936. https://doi.org/10.1111/j.1365-294X.2009.04271.x

    Article  CAS  Google Scholar 

  • Bik HM, Thomas WK, Lunt DH, Lambshead PJ (2010) Low endemism, continued deep-shallow interchanges, and evidence for cosmopolitan distributions in free-living marine nematodes (order Enoplida). BMC Evol Biol 10:389. https://doi.org/10.1186/1471-2148-10-389

    Article  PubMed  PubMed Central  Google Scholar 

  • Birky CW Jr, Wolf C, Maughan H, Herbertson L, Henry E (2005) Speciation and selection without sex. Hydrobiologia 546:29–45. https://doi.org/10.1007/1-4020-4408-9_3

    Article  CAS  Google Scholar 

  • Birstein JA (1971) Additions to the fauna of isopods (Crustacea, Isopoda) of the Kurile-Kamtchatka Trench. Part II. Asellota 2. J Inst Oceanol Russ Acad Sci 92:162–198

    Google Scholar 

  • Bober S, Brix S, Riehl T, Schwentner M, Brandt A (2018) Does the Mid-Atlantic Ridge affect the distribution of abyssal benthic crustaceans across the Atlantic Ocean? Deep Sea Res PT II. https://doi.org/10.1016/j.dsr2.2018.02.007

  • Bonnier J (1896) Edriophthalmes. In: Koehler R (ed) Résultats Scientifiques de la Campagne du “Caudan” dans le Golfe de Gascogne: Annelides, Poissons, Edriophthalmes, Diatomees, Debris Vegetaux et Roches, Liste des especes recueillies. Annales de l’Université de Lyon, pp 527–689

  • Brandt A (1992) Origin of Antarctic Isopoda (Crustacea, Malacostraca). Mar Biol 113(3):415–423. https://doi.org/10.1007/bf00349167

    Article  Google Scholar 

  • Brandt A, Gooday AJ, Brandao SN, Brix S, Brökeland W, Cedhagen T, Choudhury M, Cornelius N, Danis B, De Mesel I, Diaz RJ, Gillan DC, Ebbe B, Howe JA, Janussen D, Kaiser S, Linse K, Malyutina M, Pawlowski J, Raupach M, Vanreusel A (2007) First insights into the biodiversity and biogeography of the Southern Ocean deep sea. Nature 447(7142):307–311 http://www.nature.com/nature/journal/v447/n7142/suppinfo/nature05827_S1.html

    Article  PubMed  CAS  Google Scholar 

  • Brandt A, Elsner N, Brenke N, Golovan OA, Riehl T, Schwabe E, Würzberg L (2013) Epifauna of the Sea of Japan collected via a new epibenthic sledge equipped with camera and environmental sensor systems. Deep Sea Res PT II 86-87:43–55

    Article  Google Scholar 

  • Brandt A, Brix S, Held C, Kihara TC (2014) Molecular differentiation in sympatry despite morphological stasis: deep-sea Atlantoserolis Wägele, 1994 and Glabroserolis Menzies, 1962 from the south-west Atlantic (Crustacea: Isopoda: Serolidae). Zool J Linnean Soc 172(2):318–359. https://doi.org/10.1111/zoj.12178

    Article  Google Scholar 

  • Breiman L (2001) Random forests. Mach Learn 45:5–32

    Article  Google Scholar 

  • Brenke N (2005) An epibenthic sledge for operations on marine soft bottom and bedrock. Mar Technol Soc J 39(2):10–19

    Article  Google Scholar 

  • Brix S, Svavarsson J (2010) Distribution and diversity of desmosomatid and nannoniscid isopods (Crustacea) on the Greenland–Iceland–Faeroe Ridge. Polar Biol 33(4):515–530. https://doi.org/10.1007/s00300-009-0729-8

    Article  Google Scholar 

  • Brix S, Riehl T, Leese F (2011) First genetic data for species of the genus Haploniscus Richardson, 1908 (Isopoda: Asellota: Haploniscidae) from neighbouring deep-sea basins. Zootaxa 2838:79–84

    Google Scholar 

  • Brix S, Leese F, Riehl T, Kihara T (2014a) A new genus and new species of Desmosomatidae Sars, 1897 (Isopoda) from the eastern South Atlantic abyss described by means of integrative taxonomy. Mar Biodiv:1–55. doi: 10.1007/s12526-014-0218-3

  • Brix S, Svavarsson J, Leese F (2014b) A multi-gene analysis reveals multiple highly divergent lineages of the isopod Chelator insignis (Hansen, 1916) south of Iceland. Pol Polar Res 35(2):225–242

    Article  Google Scholar 

  • Brix S, Bober S, Tschesche C, Kihara T-C, Driskell A, Jennings RM (2018) Molecular species delimitation and its implications for species descriptions using desmosomatid and nannoniscid isopods from the VEMA fracture zone as example taxa. Deep-Sea Res PT II. https://doi.org/10.1016/j.dsr2.2018.02.004

  • Brökeland W, Raupach MJ (2008) A species complex within the isopod genus Haploniscus (Crustacea: Malacostraca: Peracarida) from the Southern Ocean deep sea: a morphological and molecular approach. Zool J Linnean Soc 152(4):655–706. https://doi.org/10.1111/j.1096-3642.2008.00362.x

    Article  Google Scholar 

  • Buhay JE (2009) “COI-like” sequences are becoming problematic in molecular systematic and DNA barcoding studies. J Crustacean Biol 29:96–110

    Article  Google Scholar 

  • Carvalho GR, Piertney SB (1997) Interspecific comparisons of genetic population structure in members of the Jaera albifrons species complex. J Mar Biol Ass UK 77:77–93

    Article  Google Scholar 

  • Claridge MF, Dawah HA, Wilson MR (1997) Species: the units of biodiversity. Chapman & Hall, London

    Google Scholar 

  • Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659

    Article  PubMed  CAS  Google Scholar 

  • Coleman CO (2003) “Digital inking”: how to make perfect line drawings on computers. Org Divers Evol 3(4):303–304. https://doi.org/10.1078/1439-6092-00081

    Article  Google Scholar 

  • Coleman CO (2009) Drawing setae the digital way. Zoosyst Evol 85(2):305–310. https://doi.org/10.1002/zoos.200900008

    Article  Google Scholar 

  • Colgan DJ, McLauchlan A, Wilson GDF, Livingston SP, Edgecombe GD, Macaranas J, Cassis G, Gray MR (1998) Histone H3 and U2 snRNA DNA sequences and arthropod molecular evolution. Aus J Zool 46(5):419–437. https://doi.org/10.1071/ZO98048

    Article  Google Scholar 

  • Dauvin J-C, Alizier S, Weppe A, Guðmundsson G (2012) Diversity and zoogeography of Icelandic deep-sea Ampeliscidae (Crustacea: Amphipoda). Deep Sea Res PT I 68:12–23. https://doi.org/10.1016/j.dsr.2012.04.013

    Article  Google Scholar 

  • Dayrat B (2005) Towards integrative taxonomy. Biol J Linn Soc 85(3):407–415. https://doi.org/10.1111/j.1095-8312.2005.00503.x

    Article  Google Scholar 

  • Degraer S, Verfaillie E, Willems W, Adriaens E, Vincx M, Van Lancker V (2008) Habitat suitability modelling as a mapping tool for macrobenthic communities: an example from the Belgian part of the North Sea. Cont Shelf Res 28(3):369–379. https://doi.org/10.1016/j.csr.2007.09.001

    Article  Google Scholar 

  • Dijkstra HH, Warén A, Gudmundsson G (2009) Pectinoidea (Mollusca: Bivalvia) from Iceland. Mar Biol Res 5:207–243

    Article  Google Scholar 

  • Divins DL (2003) Total sediment thickness of the world’s oceans & marginal seas. Ver 1. World Data Service for Geophysics. http://www.ngdc.noaa.gov/mgg/sedthick/sedthick.html

  • Dreyer H, Wägele JW (2001) Parasites of crustaceans (Isopoda: Bopyridae) evolved from fish parasites: molecular and morphological evidence. Zool 103:157–178

    CAS  Google Scholar 

  • Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 29(8):1969–1973. https://doi.org/10.1093/molbev/mss075

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Edzard T, Fujisawa T, Barraclough TG (2009) SPLITS: SPecies’ LImits by Threshold Statistics. R package version 1.0-18/r45

  • Elith J, Graham CH (2009) Do they? How do they? Why do they differ? On finding reasons for differing performances of species distribution models. Ecography 32(1):66–77. https://doi.org/10.1111/j.1600-0587.2008.05505.x

    Article  Google Scholar 

  • ETOPO2v2 (2006) 2-minute gridded global relief data ETOPO2v2. U.S. Department of Commerce. doi: 10.7289/V5J1012Q

  • Etter RJ, Rex MA, Chase MC, Quattro JM (1999) A genetic dimension to deep-sea biodiversity. Deep Sea Res PT I 46(6):1095–1099. https://doi.org/10.1016/S0967-0637(98)00100-9

    Article  Google Scholar 

  • Etter RJ, Boyle EE, Glazier A, Jennings RM, Dutra E, Chase MR (2011) Phylogeography of a pan-Atlantic abyssal protobranch bivalve: implications for evolution in the Deep Atlantic. Mol Ecol 20(4):829–843. https://doi.org/10.1111/j.1365-294X.2010.04978.x

    Article  PubMed  Google Scholar 

  • Eustace RM, Ritchie H, Kilgallen NM, Piertney SB, Jamieson AJ (2016) Morphological and ontogenetic stratification of abyssal and hadal Eurythenes gryllus sensu lato (Amphipoda: Lysianassoidea) from the Peru–Chile Trench. Deep Sea Res PT I 109(Supplement C):91–98. https://doi.org/10.1016/j.dsr.2015.11.005

    Article  Google Scholar 

  • Eytan RI, Hayes M, Arbour-Reily P, Miller M, Hellberg ME (2009) Nuclear sequences reveal mid-range isolation of an imperilled deep-water coral population. Mol Ecol 18(11):2375–2389. https://doi.org/10.1111/j.1365-294X.2009.04202.x

    Article  PubMed  CAS  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39(4):783–791. https://doi.org/10.2307/2408678

    Article  PubMed  Google Scholar 

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

    Google Scholar 

  • France SC, Kocher TD (1996) Geographic and bathymetric patterns of mitochondrial 16S rRNA sequence divergence among deep-sea amphipods, Eurythenes gryllus. Mar Biol 126(4):633–643. https://doi.org/10.1007/bf00351330

    Article  CAS  Google Scholar 

  • Fujita MK, Leaché AD, Burbrink FT, McGuire JA, Moritz C (2012) Coalescent-based species delimitation in an integrative taxonomy. Trends Ecol Evol 27(9):480–488

    Article  PubMed  Google Scholar 

  • Galtier N, Nabholz B, Glemin S, Hurst GD (2009) Mitochondrial DNA as a marker of molecular diversity: a reappraisal. Mol Ecol 18(22):4541–4550. https://doi.org/10.1111/j.1365-294X.2009.04380.x

    Article  PubMed  CAS  Google Scholar 

  • Gogina M, Zettler ML (2010) Diversity and distribution of benthic macrofauna in the Baltic Sea: data inventory and its use for species distribution modelling and prediction. J Sea Res 64(3):313–321. https://doi.org/10.1016/j.seares.2010.04.005

    Article  Google Scholar 

  • Hansen HJ (1916) Crustacea Malacostraca: the Order Isopoda. Dan Ingolf-Exp 3:1–262

    Google Scholar 

  • Hansen B, Østerhus S (2000) North Atlantic-Nordic Seas exchanges. Prog Oceanogr 45(2):109–208

    Article  Google Scholar 

  • Hare MP (2001) Prospects for nuclear gene phylogeography. Trends Ecol Evol 16(12):700–706. https://doi.org/10.1016/S0169-5347(01)02326-6

    Article  Google Scholar 

  • Harrison RG (1998) Linking evolutinary pattern and process. The relevance of species concepts fo the study of speciation. In: Howard DJ, Berlocher S (eds) Endless forms: species and speciation. Oxford University Press, New York, pp 19–31

    Google Scholar 

  • Hart MW, Sunday J (2007) Things fall apart: biolgical species from unconnected parsimony networks. Biol Lett 3:509–512

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Havermans C, Sonet G, d’Udekem d’Acoz C, Nagy ZT, Martin P, Brix S, Riehl T, Agrawal S, Held C (2013) Genetic and morphological divergences in the cosmopolitan deep-sea amphipod Eurythenes gryllus reveal a diverse abyss and a bipolar species. PLoS One 8(9):e74218. https://doi.org/10.1371/journal.pone.0074218

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hebert PDN, Ratnasingham S, deWaard JR (2003) Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. P Roy Soc B Biol Sci 270(Suppl 1):S96–S99. https://doi.org/10.1098/rsbl.2003.0025

    Article  CAS  Google Scholar 

  • Held C (2003) Molecular evidence for cryptic speciation within the widespread Antarctic crustacean Ceratoserolis trilobitoides (Crustacea, Isopoda). In: Antarctic biology in a global context. pp 135–139

  • Held C, Wägele J-W (2005) Cryptic speciation in the giant Antarctic isopod Glyptonotus antarcticus (Isopoda, Valvifera, Chaetiliidae). Sci Mar 69:175–181

    Article  Google Scholar 

  • Hessler RR (1970) The Desmosomatidae (Isopoda, Asellota) of the gay head-bermuda transect. Bull Scripps Inst Oceanogr 15:1–185

  • Hessler RR (1981) Evolution of Arthropod locomotion: a crustacean model. In: Herraid CF, Fourtner CR (eds) Locomotion and exercise in arthropods. Plenum, New York, pp 9–29

    Chapter  Google Scholar 

  • Hessler RR, Strömberg JO (1989) Behavior of janiroidean isopods (Asellota), with special reference to deep-sea genera. Sarsia 74:145–159

    Article  Google Scholar 

  • Iverson LR, Prasad AM, Matthews SN, Peters M (2008) Estimating potential habitat for 134 eastern US tree species under six climate scenarios. For Ecol Manag 254(3):390–406. https://doi.org/10.1016/j.foreco.2007.07.023

    Article  Google Scholar 

  • Jennings RM, Etter RJ, Ficarra L (2013) Population differentiation and species formation in the deep sea: the potential role of environmental gradients and depth. PLoS One 8(10):e77594. https://doi.org/10.1371/journal.pone.0077594

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jochumsen K, Schnurr SM, Quadfasel D (2016) Bottom temperature and salinity distribution and its variability around Iceland. Deep Sea Res PT I 111:79–90. https://doi.org/10.1016/j.dsr.2016.02.009

    Article  Google Scholar 

  • Johnson NK, Cicero C (2002) The role of ecologic diversification in sibling speciation of Empidonax flycatchers (Tyrannidae): multigene evidence from mt DNA. Mol Ecol 11:2065–2081

    Article  PubMed  CAS  Google Scholar 

  • Johnson SB, Young CR, Jones WJ, Warén A, Vrijenhoek RC (2006) Migration, isolation, and speciation of hydrothermal vent limpets (Gastropoda; Lepetodrilidae) across the Blanco Transform Fault. Biol Bull 210(2):140–157

    Article  PubMed  Google Scholar 

  • Just J, Wilson GDF (2004) Revision of the Paramunna complex (Isopoda: Asellota: Paramunnidae). Invertebr Syst 18(4):377–466. https://doi.org/10.1071/IS03027

    Article  Google Scholar 

  • Kaiser S, Brix S, Kihara TC, Janssen A, Jennings RM (2017) Integrative species delimitation in the deep-sea genus Thaumastosoma Hessler, 1970 (Isopoda, Asellota, Nannoniscidae) reveals a new genus and species from the Atlantic and central Pacific abyss. Deep Sea Res PT II. https://doi.org/10.1016/j.dsr2.2017.05.006

  • Katoh K, Misawa K, Kuma K-i, Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 30(14):3059–3066

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kunz W (2001) Taking more care in using different species concepts—an opinion. Parasitol Res 87(5):413–416. https://doi.org/10.1007/s004360000372

    Article  PubMed  CAS  Google Scholar 

  • Kussakin OG (2003) Marine and brackishwater like-footed Crustacea (Isopoda) from the cold and temperate waters of the Northern hemisphere. III. Suborder Asellota. Part 3. Family Munnopsidae. Opredeliteli po faune, izdavaemie Zoologicheskim Institutom Rossiyskoy Academii Nauk

  • Leaché AD, Koo MS, Spencer CL, Papenfuss TJ, Fisher RN, McGuire JA (2009) Quantifying ecological, morphological, and genetic variation to delimit species in the coast horned lizard species complex (Phrynosoma). Proc Natl Acad Sci 106(30):12418–12423. https://doi.org/10.1073/pnas.0906380106

    Article  PubMed  PubMed Central  Google Scholar 

  • Leese F, Kop A, Wägele J-W, Held C (2008) Cryptic speciation in a benthic isopod from Patagonian and Falkland Island waters and the impact of glaciations on its population structure. Front Zool 5(1):19

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Liaw A, Wiener M (2002) Classification and regression by randomForest. R News 2(3):18–22

    Google Scholar 

  • Lilljeborg W (1864) Bidrag till Kannedomen om de inom Sverige och Norrige frekommende Crustaceen af Isopodernas underordning och Tanaidernas familj. Inbjudningsskrift till hrande af de Offentliga Frelsninger 1:1–32

    Google Scholar 

  • Lörz A-N, Smith P, Linse K, Steinke D (2012) High genetic diversity within Epimeria georgiana (Amphipoda) from the southern Scotia Arc. Mar Biodivers 42(2):137–159. https://doi.org/10.1007/s12526-011-0098-8

    Article  Google Scholar 

  • Lutz MJ, Caldeira K, Dunbar RB, Behrenfeld MJ (2007) Seasonal rhythms of net primary production and particulate organic carbon flux to depth describe the efficiency of biological pump in the global ocean. J Geophys Res 112(C10):C10011. https://doi.org/10.1029/2006jc003706

    Article  Google Scholar 

  • Malyutina M, Brandt A (2006) A revaluation of the Eurycopinae (Crustacea, Isopoda, Munnopsidae) with a description of Dubinectes gen. nov. from the southern Atlantic deep sea. Zootaxa 1272:1–44

    Google Scholar 

  • Marlétaz F, Le Parco Y, Liu S, Peijnenburg KTCA (2017) Extreme mitogenomic variation in natural populations of chaetognaths. GBE 9(6):1374–1384. https://doi.org/10.1093/gbe/evx090

    Article  PubMed  PubMed Central  Google Scholar 

  • Marshall N, Diebel C (1995) Deep-sea spiders’ that walk through the water. J Exp Biol 198(Pt 6):1371–1379

    PubMed  CAS  Google Scholar 

  • McCallum KP, Guerin GR, Breed MF, Lowe AJ (2014) Combining population genetics, species distribution modelling and field assessments to understand a species vulnerability to climate change. Austral Ecol 39(1):17–28. https://doi.org/10.1111/aec.12041

    Article  Google Scholar 

  • McClain CR, Hardy SM (2010) The dynamics of biogeographic ranges in the deep sea. P Roy Soc B Biol Sci 277:3533–3546

  • Meier R, Kwong S, Vaidya G, Ng PKL (2006) DNA barcoding and taxonomy in Diptera: a tale of high intraspecific variability and low identification success. Syst Biol 55:715–728

    Article  PubMed  Google Scholar 

  • Meißner K, Darr A, Rachor E (2008) Development of habitat models for Nephtys species (Polychaeta: Nephtyidae) in the German Bight (North Sea). J Sea Res 60(4):276–291. https://doi.org/10.1016/j.seares.2008.08.001

    Article  Google Scholar 

  • Meißner K, Fiorentino D, Schnurr S, Martinez Arbizu P, Huettmann F, Holst S, Brix S, Svavarsson J (2014) Distribution of benthic marine invertebrates at northern latitudes―an evaluation applying multi-algorithm species distribution models. J Sea Res 85:241–254. https://doi.org/10.1016/j.seares.2013.05.007

    Article  Google Scholar 

  • Menzel L, George KH, Arbizu PM (2011) Submarine ridges do not prevent large-scale dispersal of abyssal fauna: a case study of Mesocletodes (Crustacea, Copepoda, Harpacticoida). Deep Sea Res PT I 58(8):839–864. https://doi.org/10.1016/j.dsr.2011.05.008

    Article  Google Scholar 

  • Menzies RJ (1962) The isopods of the abyssal depths in the Atlantic Ocean. Vema Res Ser 1:79-206

    Google Scholar 

  • Monaghan MT, Wild R, Elliot M, Fujisawa T, Balke M, Inward DJG, Lees DC, Ranaivosolo R, Eggleton P, Barraclough TGB, Vogler AP (2009) Accelerated species inventory on Madagascar using coalescent-based models of species delineation. Syst Biol 58(3):298–311

    Article  PubMed  CAS  Google Scholar 

  • Nilsen J, Hátún H, Mork K, Valdimarsson H (2008) The NISE dataset. Technical Report 08-07. Tórshavn, Faroe Islands

  • Nylander JAA (2004) MrAIC.pl. Program distributed by the author. Evolutionary Biology Centre, Uppsala University, Uppsala

  • Ohlin A (1901) Arctic Crustacea collected during the Swedish Arctic Expeditions 1898 and 1899 under the Direction of Professor A G Nathorst. Leptostraca, Isopoda, Cumacea. Bihang till Kungliga Svenska Vetenskaps-Akademiens Handlingar 26:1–54

    Google Scholar 

  • Osborn KJ (2009) Relationships within the Munnopsidae (Crustacea, Isopoda, Asellota) based on three genes. Zool Scr 38(6):617–635. https://doi.org/10.1111/j.1463-6409.2009.00394.x

    Article  Google Scholar 

  • Padial JM, Miralles A, DeLaRiva I, Vences M (2010) The integrative future of taxonomy. Front Zool 7(1):16. https://doi.org/10.1186/1742-9994-7-16

    Article  PubMed  PubMed Central  Google Scholar 

  • Palumbi SR, Martin A, Romanos S, McMillan WO, Stice L (1991) The simple fool’s guide to PCR. Version 2. University of Hawaii Press, Hawaii, Honolulu

    Google Scholar 

  • Petit RJ, Excoffier L (2009) Gene flow and species delimitation. Trends Ecol Evol 24(7):386–393. https://doi.org/10.1016/j.tree.2009.02.011

    Article  PubMed  Google Scholar 

  • Pons J, Barraclough TG, Gomez-Zurita J, Cardoso A, Duran DP, Hazell S, Kamoun S, Sumlin WD, Vogler AP (2006) Sequence-based species delimitation for the DNA taxonomy of undescribed insects. Syst Biol 55(4):595–609

    Article  PubMed  Google Scholar 

  • Puillandre N, Lambert A, Brouillet S, Achaz G (2012) ABGD, Automatic Barcode Gap Discovery for primary species delimitation. Mol Ecol 21(8):1864–1877. https://doi.org/10.1111/j.1365-294X.2011.05239.x

    Article  PubMed  CAS  Google Scholar 

  • Radulovici AE, Sainte-Marie B, Dufresne F (2009) DNA barcoding of marine crustaceans from the Estuary and Gulf of St Lawrence: a regional-scale approach. Mol Ecol Resour 9(Suppl s1):181–187. https://doi.org/10.1111/j.1755-0998.2009.02643.x

    Article  PubMed  CAS  Google Scholar 

  • Rambaut A, Drummond AJ (2007) Tracer v1.5.0

  • Raupach MJ, Wägele JW (2006) Distinguishing cryptic species in Antarctic Asellota (Crustacea: Isopoda)—a preliminary study of mitochondrial DNA in Acanthaspidia drygalskii. Antarct Sci 18:191–198. https://doi.org/10.1017/S0954102006000228

    Article  Google Scholar 

  • Raupach MJ, Malyutina M, Brandt A, Wägele J-W (2007) Molecular data reveal a highly diverse species flock within the munnopsoid deep-sea isopod Betamorpha fusiformis (Barnard, 1920) (Crustacea: Isopoda: Asellota) in the Southern Ocean. Deep-Sea Res PT II 54(16–17):1820–1830

    Article  Google Scholar 

  • Raupach MJ, Mayer C, Malyutina M, Wägele JW (2009) Multiple origins of deep-sea Asellota (Crustacea: Isopoda) from shallow waters revealed by molecular data. Proc Biol Sci 276(1658):799–808

    Article  PubMed  CAS  Google Scholar 

  • Reiss H, Cunze S, König K, Neumann H, Kröncke I (2011) Species distribution modelling of marine benthos: a North Sea case study. Mar Ecol Prog Ser 442:71–86

    Article  Google Scholar 

  • Reveillaud J, Remerie T, van Soest R, Erpenbeck D, Càrdenas P, Derycke S, Xavier JR, Rigaux A, Vanreusel A (2010) Species boundaries and phylogenetic relationships between Atlanto-Mediterranean shallow-water and deep-sea coral associated Hexadella species (Porifera, Ianthellidae). Mol Phylogenet Evol 56:104–114

    Article  PubMed  Google Scholar 

  • Rex MA, Etter RJ (2010) Deep-sea biodiversity: pattern and scale. Harvard University Press, Cambridge

    Google Scholar 

  • Riehl T, Brand A (2013) Southern Ocean Macrostylidae reviewed with a key to the species and new descriptions from Maud Rise. Zootaxa 3692(1):160–203. https://doi.org/10.11646/zootaxa.3692.1.10

    Article  Google Scholar 

  • Riehl T, Kaiser S (2012) Conquered from the deep sea? A new deep-sea isopod species from the Antarctic shelf shows pattern of recent colonization. PLoS One 7(11):e49354. https://doi.org/10.1371/journal.pone.0049354

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Riehl T, Brenke N, Driskell A, Kaiser S, Brand A (2014) Field and laboratory methods for DNA studies on deep-sea isopod crustaceans. Pol Polar Res 35(2):203–224

    Article  Google Scholar 

  • Riehl T, Lins L, Brandt A (2017) The effects of depth, distance, and the Mid-Atlantic Ridge on genetic differentiation of abyssal and hadal isopods (Macrostylidae). Deep Sea Res PT II. https://doi.org/10.1016/j.dsr2.2017.10.005

  • Rogers AD (2003) Molecular ecology and evolution of slope species. In: Wefer G, Billett D, Hebbeln D, Jørgensen B, Schlüter M, van Weering TE (eds) Ocean margin systems. Springer, Berlin, pp 323–337. https://doi.org/10.1007/978-3-662-05127-6_20

    Chapter  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. https://doi.org/10.1093/sysbio/sys029

  • Rothlisberg PC, Pearcy WG (1977) An epibenthic sampler used to study the ontogeny of vertical migration of Pandalus jordani (Decapoda, Caridea). Fish Bull 74:994–997

    Google Scholar 

  • Rubinoff D, Holland BS (2005) Between two extremes: mitochondrial DNA is neither the panacea nor the nemesis of phylogenetic and taxonomic inference. Syst Biol 54(6):952–961. https://doi.org/10.1080/10635150500234674

    Article  PubMed  Google Scholar 

  • Sanders HL, Hessler RR (1969) Ecology of the deep-sea benthos. Science 163(3874):1419–1424

    Article  PubMed  CAS  Google Scholar 

  • Sanders HL, Hessler RR, Hampson GR (1965) An introduction to the study of deep-sea benthic faunal assemblages along the Gay Head-Bermuda transect. Deep Sea Res Oceanogr Abstr 12(6):845–867

    Article  Google Scholar 

  • Sars GO (1864) On en anomal Gruppe af Isopoder. Forh Vidensk Selsk Kristiania 1863:1–16

    Google Scholar 

  • Sars GO Beretning om en i Sommeren 1865 foretagan zoologisk Reise ved Kysterne af Christianias og Christiansands Stifter-Crustaceer. Forh Vidensk Selsk Kristiania 1868, 1868:1–47

  • Schnurr S, Malyutina M (2014) Two new species of the genus Eurycope (Isopoda, Munnopsidae) from Icelandic waters. Pol Polar Res 35(2):361–388

    Article  Google Scholar 

  • Schnurr S, Brandt A, Brix S, Fiorentino D, Malyutina M, Svavarsson J (2014) Composition and distribution of selected munnopsid genera (Crustacea, Isopoda, Asellota) in Icelandic waters. Deep Sea Res PT I 84:142–155. https://doi.org/10.1016/j.dsr.2013.11.004

    Article  Google Scholar 

  • Schüller M (2011) Evidence for a role of bathymetry and emergence in speciation in the genus Glycera (Glyceridae, Polychaeta) from the deep Eastern Weddell Sea. Polar Biol 34(4):549–564. https://doi.org/10.1007/s00300-010-0913-x

    Article  Google Scholar 

  • Schüller M, Hutchings PA (2012) New species of Terebellides (Polychaeta: Trichobranchidae) indicate long-distance dispersal between western South Atlantic deep-sea basins. Zootaxa 3254:1–31

    Google Scholar 

  • Schwentner M, Timms BV, Richter S (2011) An integrative approach to species delineation incorporating different species concepts: a case study of Limnadopsis (Branchiopoda: Spinicaudata). Biol J Linn Soc 104(3):575–599. https://doi.org/10.1111/j.1095-8312.2011.01746.x

    Article  Google Scholar 

  • Seiter K, Hensen C, Zabel M (2005) Benthic carbon mineralization on a global scale. Glob Biogeochem Cy 19(1):GB1010. https://doi.org/10.1029/2004gb002225

    Article  Google Scholar 

  • Shaw KL (2002) Conflict between nuclear and mitochondrial DNA phylogenies of a recent species radiation: what mtDNA reveals and conceals about modes of speciation in Hawaiian crickets. Proc Natl Acad Sci 99(25):16122–16127. https://doi.org/10.1073/pnas.242585899

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sites JW, Marshall JC (2004) Operational criteria for delimiting species. Annu Rev Ecol Syst 35:199–227. https://doi.org/10.2307/30034115

    Article  Google Scholar 

  • Somero GN (1992) Adaptations to high hydrostatic pressure. Annu Rev Physiol 54:557–577

    Article  PubMed  CAS  Google Scholar 

  • Song H, Buhay JE, Whiting MF, Crandall KA (2008) Many species in one: DNA barcoding overestimates the number of species when nuclear mitochondrial pseudogenes are coamplified. Proc Natl Acad Sci 105(36):13486–13491. https://doi.org/10.1073/pnas.0803076105

    Article  PubMed  PubMed Central  Google Scholar 

  • Stamatakis A, Hoover P, Rougemont J (2008) A rapid bootstrap algorithm for the RAxML Web servers. Syst Biol 57(5):758–771. https://doi.org/10.1080/10635150802429642

    Article  PubMed  Google Scholar 

  • Svavarsson J (1987) Eurycopidae (Isopoda, Asellota) from bathyal and abyssal depths in the Norwegian, Greenland, and North Polar Seas. Sarsia 72:183–196

    Article  Google Scholar 

  • Svavarsson J (1997) Diversity of isopods (Crustacea): new data from the Arctic and Atlantic Oceans. Biodivers Conserv 6:1571–1579

    Article  Google Scholar 

  • Svavarsson J, Brattegard T, Strömberg JO (1990) Distribution and diversity patterns of asellote isopods (Crustacea) in the deep Norwegian and Greenland Seas. Prog Oceanogr 24:297–310

    Article  Google Scholar 

  • Svavarsson J, Strömberg JO, Brattegard T (1993) The deep-sea asellote (Isopoda, Crustacea) fauna of the Northern Seas: species composition, distributional patterns and origin. J Biogeogr 20(5):537–555

    Article  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tang CQ, Leasi F, Obertegger U, Kieneke A, Barraclough TG, Fontaneto D (2012) The widely used small subunit 18S rDNA molecule greatly underestimates true diversity in biodiversity surveys of the meiofauna. Proc Natl Acad Sci 109(40):16208–16212. https://doi.org/10.1073/pnas.1209160109

    Article  PubMed  PubMed Central  Google Scholar 

  • Templeton AR (2001) Using phylogeographic analyses of gene trees to test species status and processes. Mol Ecol 10(3):779–791. https://doi.org/10.1046/j.1365-294x.2001.01199.x

    Article  PubMed  CAS  Google Scholar 

  • Teske PR, Papadopoulos I, Zardi GI, McQuaid CD, Edkins MT, Griffiths CL, Barker NP (2007) Implications of life history for genetic structure and migration rates of southern African coastal invertebrates: planktonic, abbreviated and direct development. Mar Biol 152(3):697–711. https://doi.org/10.1007/s00227-007-0724-y

    Article  Google Scholar 

  • Tsang LM, Chan BKK, Shih F-L, Chu KH, Allen Chen C (2009) Host-associated speciation in the coral barnacle Wanella milleporae (Cirripedia: Pyrgomatidae) inhabiting the Millepora coral. Mol Ecol 18(7):1463–1475. https://doi.org/10.1111/j.1365-294X.2009.04090.x

    Article  PubMed  Google Scholar 

  • Vrijenhoek RC (2009) Cryptic species, phenotypic plasticity, and complex life histories: assessing deep-sea faunal diversity with molecular markers. Deep Sea Res PT II 56(19–20):1713–1723. https://doi.org/10.1016/j.dsr2.2009.05.016

    Article  CAS  Google Scholar 

  • Watling L, Guinotte J, Clark MR, Smith CR (2013) A proposed biogeography of the deep ocean floor. Prog Oceanogr 111:91–112. https://doi.org/10.1016/j.pocean.2012.11.003

    Article  Google Scholar 

  • Whittaker JM, Muller RD, Roest WR, Wessel P, Smith WHF (2008) How supercontinents and superoceans affect seafloor roughness. Nature 456 (7224):938–941. doi:http://www.nature.com/nature/journal/v456/n7224/suppinfo/nature07573_S1.html

  • Wilgenbusch JC, Warren DL, Swofford DL (2004) AWTY: a system for graphical exploration of MCMC convergence in Bayesian phylogenetic inference. http://ceb.csit.fsu.edu/awty

  • Wilson GDF (1982) Systematics of a species complex in the deep-sea genus Eurycope, with a revision of six previously described species (Crustacea, Isopoda, Eurycopidae). Bull Scripps Inst Oceanogr 25:1–64

    Google Scholar 

  • Wilson GDF (1983a) An unusual species complex in the genus Eurycope (Crustacea: Isopoda: Asellota) from the deep north Atlantic Ocean. P Biol Soc Wash 96(3):452–467

    Google Scholar 

  • Wilson GDF (1983b) Variation in the deep-sea isopod Eurycope iphthima (Asellota, Eurycopidae): depth related clines in rostral morphology and in populations structure. J Crustacean Biol 3(1):127–140

    Article  Google Scholar 

  • Wilson GDF (1985) The distribution of eurycopid species complexes (Crustacea: Isopoda: Asellota). In: Laubier L, Monniot C (eds) Peuplements profonds du Golfe de Gascogne. Brest, pp 630–468

  • Wilson GDF (1989) A systematic revision of the deep-sea subfamily Lipomerinae of the isopod crustacean family Munnopsidae. Bull Scripps Inst Oceanogr 27:1–138

    Google Scholar 

  • Wilson GDF (2008) A review of taxonomic concepts in the Nannoniscidae (Isopoda, Asellota), with a key to the genera and a description of Nannoniscus oblongus Sars. Zootaxa 1680:1–24

    Google Scholar 

  • Wilson GDF, Hessler RR (1981) A revision of the genus Eurycope (Isopoda, Asellota) with descriptions of three new genera. J Crustacean Biol 1(3):401–423

    Article  Google Scholar 

  • Wilson GDF, Hessler RR (1987) Speciation in the deep sea. Annu Rev Ecol Syst 18:185–207

    Article  CAS  Google Scholar 

  • Wilson GDF, Schotte M (2017) Munnopsidae Lilljeborg, 1864. http://www.marinespecies.org/aphia.php?p=taxdetails&id=118264. Accessed 2017-12-14 2017

  • Wilson AC, Cann RL, Carr SM, George M, Gyllensten UB, Helm-Bychowski KM, Higuchi RG, Palumbi SR, Prager EM, Sage RD, Stoneking M (1985) Mitochondrial DNA and two perspectives on evolutionary genetics. Biol J Linn Soc 26(4):375–400. https://doi.org/10.1111/j.1095-8312.1985.tb02048.x

    Article  Google Scholar 

  • Wolff T (1962) The systematics and biology of bathyal and abyssal Isopoda Asellota. Galathea Rep 6:1–320

    Google Scholar 

  • Zardus JD, Etter RJ, Chase MR, Rex MA, Boyle EE (2006) Bathymetric and geographic population structure in the pan-Atlantic deep-sea bivalve Deminucula atacellana (Schenck, 1939). Mol Ecol 15(3):639–651. https://doi.org/10.1111/j.1365-294X.2005.02832.x

    Article  PubMed  CAS  Google Scholar 

  • Zhang J, Kapli P, Pavlidis P, Stamatakis A (2013) A general species delimitation method with applications to phylogenetic placements. Bioinformatics 29(22):2869–2876. https://doi.org/10.1093/bioinformatics/btt499

    Article  PubMed  PubMed Central  CAS  Google Scholar 

Download references

Acknowledgements

We would like to thank the crew and participants of the IceAGE expeditions, as well as all pickers and sorters at the DZMB in Hamburg, Germany, and the Nature Centre in Sandgerði, Iceland. Special thanks go to Dr. Herman Wirshing for his help during S. Schnurr’s stays at the facilities of the Laboratories of Analytical Biology (LAB) at the Smithonian National Museum of Natural History, Washington, DC. We thank Karen Jeskulke for introducing lab workflow, Lukas Rischke for solving hardware problems, and Falk Huettmann for his introduction to random forest models.

Funding

S. Schnurr was partly funded by the German Science Foundation (DFG) under contract 2843/4-1 and BR3843/6-1, as well as by the Census of the Diversity of Abyssal Marine Life (CeDAMar), the Smithsonian’s Rathbun Fund for Crustacean Research, and the Annette Barthelt Stiftung. The IceAGE cruises were funded by the DFG contract BR3843/3-1 (IceAGE1) and 4-1 (IceAGE2).

Author information

Authors and Affiliations

  1. Senckenberg am Meer, German Centre for Marine Biodiversity Research (DZMB), c/o CeNak, Biocenter Grindel, Martin-Luther-King-Platz 3, 20146, Hamburg, Germany

    Sarah Schnurr & Saskia Brix

  2. Smithsonian National Museum of Natural History, Washington, DC, 20013, USA

    Karen J. Osborn & Amy Driskell

  3. A.V. Zhirmunsky Institute of Marine Biology, National Scientific Center of Marine Biology, FEB RAS, Palchevsky Str, 17, 690041, Vladivostok, Russia

    Marina Malyutina

  4. Far Eastern Federal University, Ajax St., Russky Island, 690600, Vladivostok, Russia

    Marina Malyutina

  5. Biology Department, Temple University, 1900 North 12th Street, Philadelphia, PA, 19122, USA

    Robert Jennings

  6. Institute of Biology, University of Iceland, Sturlugata 7, 101, Reykjavik, Iceland

    Jörundur Svavarsson

  7. Senckenberg am Meer, German Centre for Marine Biodiversity Research (DZMB), Südstrand 44, 26382, Wilhelmshaven, Germany

    Pedro Martinez Arbizu

Authors
  1. Sarah Schnurr
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Karen J. Osborn
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Marina Malyutina
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Robert Jennings
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Saskia Brix
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Amy Driskell
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Jörundur Svavarsson
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Pedro Martinez Arbizu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sarah Schnurr.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed by the authors.

Sampling and field studies

All necessary permits for sampling and observational field studies have been obtained by the authors from the competent authorities and are mentioned in the acknowledgements, if applicable.

Additional information

Communicated by K. Halanych

Electronic supplementary material

Online Resource 1

Uncorrected pairwise p-distances for the 16S gene of all evaluated E. producta complex specimens. (XLSX 26.8 kb)

Online Resource 2

Uncorrected pairwise p-distances for the 16S gene of all evaluated E. inermis complex specimens. (XLSX 33.7 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Schnurr, S., Osborn, K.J., Malyutina, M. et al. Hidden diversity in two species complexes of munnopsid isopods (Crustacea) at the transition between the northernmost North Atlantic and the Nordic Seas. Mar Biodiv 48, 813–843 (2018). https://doi.org/10.1007/s12526-018-0877-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12526-018-0877-6

Keywords

Search

Navigation