Skip to main content
Log in

Bathynomus giganteus (Isopoda: Cirolanidae) and the canyon: a population genetics assessment of De Soto Canyon as a glacial refugium for the giant deep-sea isopod

  • CRUSTACEAN GENOMICS
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

Population genetics has gained popularity as a method to discover glacial refugia in terrestrial species, but has only recently been applied to the marine realm. The last glacial maxima occurred 20,000 years ago, decreasing sea levels by 120 m and exposing much of the continental shelf in the northern Gulf of Mexico, with the exception of De Soto Canyon (2100 m depth). The goal of this study was to determine whether population dynamics of the giant deep-sea isopod, Bathynomus giganteus, were better explained by habitat diversity or by the past presence of a marine glacial refugium in De Soto Canyon. To accomplish this we (1) measured genetic diversity in De Soto Canyon and adjacent regions, (2) characterized gene flow and connectivity between these regions, and (3) investigated historical changes to population size. We sequenced three mitochondrial loci (12S, 16S, and COI) from 212 individuals and also performed a next-generation sequencing pilot study using double digest Restriction site-Associated DNA sequencing. We found high genetic diversity and connectivity throughout the study regions, migration between all three regions, low population differentiation, and evidence of population expansion. This study suggests that habitat heterogeneity, rather than the presence of a glacial refugium, has had an historical effect on the population dynamics of B. giganteus.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Allendorf, F. W. & G. Luikart, 2009. Conservation and the genetics of populations. Wiley, New York.

    Google Scholar 

  • Atkinson, T., K. Briffa & G. Coope, 1987. Seasonal temperatures in Britain during the past 22,000 years, reconstructed using beetle remains. Nature 325: 587–592.

    Google Scholar 

  • Avise, J. C., 1992. Molecular population structure and the biogeographic history of a regional fauna: a case history with lessons for conservation biology. Oikos 63: 62–76.

    CAS  Google Scholar 

  • Barradas-Ortiz, C., P. Briones-Fourzán & E. Lozano-Álvarez, 2003. Seasonal reproduction and feeding ecology of giant isopods Bathynomus giganteus from the continental slope of the Yucatán peninsula. Deep Sea Res Part I 50: 495–513.

    Google Scholar 

  • Beck, J. B., H. Schmuths & B. A. Schaal, 2008. Native range genetic variation in Arabidopsis thaliana is strongly geographically structured and reflects Pleistocene glacial dynamics. Mol Ecol 17: 902–915.

    CAS  PubMed  Google Scholar 

  • Beerli, P. & M. Palczewski, 2010. Unified framework to evaluate panmixia and migration direction among multiple sampling locations. Genetics 185: 313–326.

    PubMed  PubMed Central  Google Scholar 

  • Bernatchez, L. & J. J. Dodson, 1991. Phylogeographic structure in mitochondrial DNA of the Lake Whitefish (Coregonus clupeaformis) and its relation to Pleistocene glaciations. Evolution 45: 1016–1035.

    PubMed  Google Scholar 

  • Bernatchez, L. & C. C. Wilson, 1998. Comparative phylogeography of Nearctic and Paleartic fishes. Mol Ecol 7: 431–452.

    Google Scholar 

  • Bouckaert, R., J. Heled, D. Kühnert, T. Vaughan, C. H. Wu, D. Xie, M. Suchard, A. Rambaut & A. J. Drummond, 2014. BEAST 2: a software platform for Bayesian evolutionary analysis. PLoS Comput Biol 10: 1–6.

    Google Scholar 

  • Briggs, J. C., 1974. Marine Zoogeography. McGraw-Hill, New York.

    Google Scholar 

  • Briones-Fourzan, P. & E. Lozano-Alvarez, 1991. Aspects of the biology of the giant isopod Bathynomus giganteus A. Milne Edwards, 1879 (Flabellifera: Cirolanidae), off the Yucatan Peninsula. J Crustac Biol 11: 375–385.

    Google Scholar 

  • Brooke, S. & W. W. Schroeder, 2007. State of deep coral ecosystems in the Gulf of Mexico region: Texas to the Florida Straits. State Deep Coral Ecosyst USA 59: 271–306.

    Google Scholar 

  • Buhay, J. E., G. Moni, N. Mann & K. A. Crandall, 2007. Molecular taxonomy in the dark: evolutionary history, phylogeography, and diversity of cave crayfish in the subgenus Aviticambarus, genus Cambarus. Mol Phylogenetics Evol 42: 435–448.

    CAS  Google Scholar 

  • Campbell, J. W. & T. Aarup, 1992. New production in the North Atlantic derived from seasonal patterns of surface chlorophyll. Deep Sea Research Part A. Oceanogr Res Papers 39: 1669–1694.

    CAS  Google Scholar 

  • Campo, D., J. Molares, L. Garcia, P. Fernandez-Rueda, C. Garcia-Gonzalez & E. Garcia-Vazquez, 2009. Phylogeography of the European stalked barnacle (Pollicipes pollicipes): identification of glacial refugia. Mar Biol 157: 147–156.

    Google Scholar 

  • Carnaval, A. C., M. J. Hickerson, C. F. B. Haddad, M. T. Rodrigues & C. Moritz, 2009. Stability predicts genetic diversity in the Brazilian Atlantic forest hotspot. Science 323: 785–789.

    CAS  PubMed  Google Scholar 

  • Chamberlain, S. C., V. B. Meyer-Rochow & W. P. Dossert, 1986. Morphology of the compound eye of the giant deep-sea isopod Bathynomus giganteus. J Morphol 189: 145–156.

    CAS  PubMed  Google Scholar 

  • Coleman FC, Chanton JP, Chassinger EP (2014). Ecological connectivity in northeastern Gulf of Mexico – The Deep-C Initiative. Proceedings of the International Oil Spill Conference: pp. 1972–1984

  • Cowen, R. K. & S. Sponaugle, 2009. Larval dispersal and marine population connectivity. Ann Rev Mar Sci 1: 443–466.

    PubMed  Google Scholar 

  • Crandall, K. A. & J. F. Fitzpatrick, 1996. Crayfish molecular systematics: using a combination of procedures to estimate phylogeny. Syst Biol 45: 1–26.

    Google Scholar 

  • Dömel, J. S., P. Convey & F. Leese, 2015. Genetic data support independent glacial refugia and open ocean barriers to dispersal for the Southern Ocean sea spider Austropallene cornigera (Möbius, 1902). J Crustac Biol 35: 480–490.

    Google Scholar 

  • Doyle, R. W., 1972. Genetic variation in Ophiomusium lymani (Echinodermata) populations in the deep sea. Deep Sea Res Oceanogr Abstr 19: 661–664.

    CAS  Google Scholar 

  • Etter, R. J. & F. Grassle, 1992. Patterns of species diversity in the deep sea as a function of sediment particle size diversity. Nature 360: 576–578.

    Google Scholar 

  • Etter, R. J. & M. A. Rex, 1990. Population differentiation decreases with depth in deep-sea gastropods. Deep Sea Research Part A. Oceanogr Res Papers 37: 1251–1261.

    Google Scholar 

  • Etter, R. J., M. A. Rex, M. R. Chase & J. M. Quattro, 2005. Population differentiation decreases with depth in deep-sea bivalves. Evolution 59: 1479–1491.

    PubMed  Google Scholar 

  • Excoffier, L. & H. E. L. Lischer, 2010. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10: 564–567.

    PubMed  Google Scholar 

  • Folmer, O., W. R. Hoeh, M. B. Black & R. C. Vrijenhoek, 1994. Conserved primers for PCR amplification of mitochondrial DNA from different invertebrate phyla. Mol Mar Biol Biotechnol 3: 294–299.

    CAS  PubMed  Google Scholar 

  • France, S. C. & T. D. Kocher, 1996. Geographic and bathymetric patterns of mitochondrial 16S rRNA sequence divergence among deep-sea amphipods, Eurythenes gryllus. Mar Biol 126: 633–643.

    CAS  Google Scholar 

  • Gaines, S., B. Gaylord, L. Gerber, A. Hastings & B. Kinlan, 2007. Connecting places: the ecological consequences of dispersal in the sea. Oceanography 20: 90–99.

    Google Scholar 

  • García-Merchán, V. H., A. Robainas-Barcia, P. Abelló, E. Macpherson, F. Palero, M. García-Rodríguez, L. G. de Sola & M. Pascual, 2012. Phylogeographic patterns of decapod crustaceans at the Atlantic-Mediterranean transition. Mol Phylogenetics Evol 62: 664–672.

    Google Scholar 

  • Goodall-Copestake, W. P., G. A. Tarling & E. J. Murphy, 2012. On the comparison of population-level estimates of haplotype and nucleotide diversity: a case study using the gene cox1 in animals. Heredity 109: 50–56.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gore, R. H., 1992. The Gulf of Mexico. Pineapple Press Inc, Sarasota.

    Google Scholar 

  • Grassle, J. F. & N. J. Maciolek, 1992. Deep-sea species richness: regional and local diversity estimates from quantitative bottom samples. Am Nat 139: 313–341.

    Google Scholar 

  • GRIP Project Members, 1993. Climate instability during the last inter-glacial period recorded in the GRIP ice core. Nature 364: 203–207.

    Google Scholar 

  • Grosberg, R. & C. W. Cunningham, 2001. Genetic structure in the sea: from populations to communities. Mar Commun Ecol 2001: 61–84.

    Google Scholar 

  • Hartl, D. L. & A. G. Clark, 1997. Principles of Population Genetics. Sinauer Associates, Sunderland.

    Google Scholar 

  • Havermans, C., G. Sonet, C. d’Udekem d’Acoz, Z. T. Nagy, P. Martin, S. Brix, T. Riehl, S. Agrawal & C. Held, 2013. Genetic and morphological divergences in the cosmopolitan deep-sea amphipod Eurythenes gryllus reveal a diverse abyss and a bipolar species. PLoS ONE 8: e74218.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hewitt, G. M., 1996. Some genetic consequences of ice ages, and their role in divergence and speciation. Biol J Linn Soc 58: 247–276.

    Google Scholar 

  • Hewitt, G. M., 2004. Genetic consequences of climatic oscillations in the Quaternary. Philosophical Transactions of the Royal Society of London. Series B 359: 183–195.

    CAS  Google Scholar 

  • Katoh, K. & D. M. Standley, 2013. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30: 772–780.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kearse, M., R. Moir, A. Wilson, S. Stones-Havas, M. Cheung, S. Sturrock, S. Buxton, A. Cooper, S. Markowitz, C. Duran, T. Thierer, B. Ashton, P. Mantjies & A. Drummond, 2012. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28: 1647–1649.

    PubMed  PubMed Central  Google Scholar 

  • Knowles, L., 2001. Did the Pleistocene glaciations promote divergence? Tests of explicit refugial models in montane grasshoppers. Mol Ecol 10: 691–701.

    CAS  PubMed  Google Scholar 

  • Leese, F., S. Agrawal & C. Held, 2010. Long-distance island hopping without dispersal stages: transportation across major zoogeographic barriers in a Southern Ocean isopod. Naturwissenschaften 97: 583–594.

    CAS  PubMed  Google Scholar 

  • Levin, L. A., R. J. Etter, M. A. Rex, A. J. Gooday, C. R. Smith, J. Pineda, C. T. Stuart, R. R. Hessler & D. Pawson, 2001. Environmental influences on regional deep-sea species diversity. Ann Rev Ecol Syst 32: 51–93.

    Google Scholar 

  • Lewis, P. O. & D. J. Crawford, 1995. Pleistocene refugium endemics exhibit greater allozymic diversity than widespread congeners in the genus Polygonella (Polygonaceae). Am J Bot 82: 141–149.

    Google Scholar 

  • Librado, P. & J. Rozas, 2009. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25: 1451–1452.

    CAS  PubMed  Google Scholar 

  • Maggs, C. A., R. Castilho, D. Foltz, C. Henzler, M. T. Jolly, J. Kelly, J. Olsen, K. E. Perez, W. Stam, R. Väinölä, F. Viard & J. Wares, 2008. Evaluating signatures of glacial refugia for North Atlantic benthic marine taxa. Ecology 89: S108–S122.

    PubMed  Google Scholar 

  • Mäkinen, H. S. & J. Merilä, 2008. Mitochondrial DNA phylogeography of the three-spined stickleback (Gasterosteus aculeatus) in Europe - Evidence for multiple glacial refugia. Mol Phylogenetics Evol 46: 167–182.

    Google Scholar 

  • Marko, P. B., 2004. “What”s larvae got to do with it?’ Disparate patterns of post-glacial population structure in two benthic marine gastropods with identical dispersal potential. Mol Ecol 13: 597–611.

    CAS  PubMed  Google Scholar 

  • Médail, F. & K. Diadema, 2009. Glacial refugia influence plant diversity patterns in the Mediterranean Basin. J Biogeogr 36: 1333–1345.

    Google Scholar 

  • Mokady, O., S. Rozenblatt, D. Graur & Y. Loya, 1994. Coral-host specificity of Red Sea Lithophaga bivalves: interspecific and intraspecific variation in 12S mitochondrial ribosomal RNA. Mol Mar Biol Biotechnol 3: 158–164.

    CAS  PubMed  Google Scholar 

  • Nei, M., 1987. Molecular Evolutionary Genetics. Columbia University Press, New York.

    Google Scholar 

  • Nei, M. & W.-H. Li, 1979. Mathematical model for studying genetic variation in terms of restriction endonucleases. Proc Nat Acad Sci USA 76: 5269–5273.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nesbø, C. L., T. Fossheim, L. A. Vøllestad & K. S. Jakobsen, 1999. Genetic divergence and phylogeographic relationships among European perch (Perca fluviatilis) populations reflect glacial refugia and postglacial colonization. Mol Ecol 8: 1387–1404.

    PubMed  Google Scholar 

  • Nguyen, T. T., 2014. Variability of cross-slope flow in the De Soto Canyon region. Florida State University, Tallahassee.

    Google Scholar 

  • Nowlin, W. D., 1971. Water masses and general circulation of the Gulf of Mexico. Oceanology 6: 28–33.

    Google Scholar 

  • Palero, F., P. Abelló, E. Macpherson, M. Gristina & M. Pascual, 2008. Phylogeography of the European spiny lobster (Palinurus elephas): influence of current oceanographical features and historical processes. Mol Phylogenetics Evol 48: 708–717.

    CAS  Google Scholar 

  • Palumbi, S. R., A. Martin, S. Romano, W. O. McMillan, L. Stice & G. Grabowski, 2002. The simple fool’s guide to PCR version 2. University of Hawaii, Honolulu.

    Google Scholar 

  • Peterson, B. K., J. N. Weber, E. H. Kay, H. S. Fisher & H. E. Hoekstra, 2012. Double digest RADseq: an inexpensive method for de novo SNP discovery and genotyping in model and non-model species. PloS One 7: e37135.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Petit, R. J., 2003. Glacial refugia: hot spots but not melting pots of genetic diversity. Science 300: 1563–1565.

    CAS  PubMed  Google Scholar 

  • Poore, G. C. B. & N. L. Bruce, 2012. Global diversity of marine isopods (except Asellota and crustacean symbionts). PLoS ONE 7: e43529.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Provan, J. & K. D. Bennett, 2008. Phylogeographic insights into cryptic glacial refugia. Trends Ecol Evol 23: 564–571.

    PubMed  Google Scholar 

  • Provan, J., R. A. Wattier & C. A. Maggs, 2005. Phylogeographic analysis of the red seaweed Palmaria palmata reveals a Pleistocene marine glacial refugium in the English Channel. Mol Ecol 14: 793–803.

    CAS  PubMed  Google Scholar 

  • Raupach, M. J., M. Malyutina, A. Brandt & J. W. Wägele, 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 Part II 54: 1820–1830.

    Google Scholar 

  • Rex, M. A., 1983. Geographic patterns of species diversity in deep-sea benthos. In Rowe, G. T. (ed.), Deep-Sea Biology. Wiley, New York: 453–472.

    Google Scholar 

  • Rex, M. A., C. T. Stuart, R. R. Hessler, J. A. Allen, H. L. Sanders & G. D. F. Wilson, 1993. Global-scale latitudinal patterns of species diversity in the deep-sea benthos. Nature 365: 636–639.

    Google Scholar 

  • Richmond, G. M. & D. S. Fullerton, 1986. Summation of Quaternary glaciations in the United States of America. Quat Sci Rev 5: 183–196.

    Google Scholar 

  • Rowe, G. T., 1983. Biomass and Production of the Deep-Sea Macrobenthos. In Rowe, G. T. (ed.), Deep-Sea Biology. Wiley, New York: 97–121.

    Google Scholar 

  • Sager, W. W., W. W. Schroeder, J. S. Laswell, K. S. Davis, R. Rezak & S. R. Gittings, 1992. Mississippi-Alabama outer continental shelf topographic features formed during the late Pleistocene-Holocene transgression. Geo-Mar Lett 12: 41–48.

    Google Scholar 

  • Sibuet, M., C. E. Lambert, R. Chesselet & L. Laubier, 1989. Density of the major size groups of benthic fauna and trophic input in deep basins of the Atlantic Ocean. J Mar Res 47: 851–867.

    CAS  Google Scholar 

  • Siebenaller, J. F., 1978. Genetic variation in deep-sea invertebrate populations: the bathyal gastropod Bathybembix bairdii. Mar Biol 47: 265–275.

    CAS  Google Scholar 

  • Stamatis, C., A. Triantafyllidis, K. A. Moutou & Z. Mamuris, 2004. Mitochondrial DNA variation in Northeast Atlantic and Mediterranean populations of Norway lobster, Nephrops norvegicus. Mol Ecol 13: 1377–1390.

    CAS  PubMed  Google Scholar 

  • Taberlet, P., 1998. Biodiversity at the intraspecific level: the comparative phylogeographic approach. J Biotechnol 64: 91–100.

    CAS  Google Scholar 

  • Taberlet, P., L. Fumagalli, A.-G. Wust-Saucy & J.-F. Cossons, 1998. Comparative phylogeography and postglacial colonization. Mol Ecol 7: 453–464.

    CAS  PubMed  Google Scholar 

  • Tajima, F., 1983. Evolutionary relationship of DNA sequences in finite populations. Genetics 105: 437–460.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Taylor, M. L. & C. N. Roterman, 2017. Invertebrate population genetics across Earth’s largest habitat: the deep-sea floor. Mol Ecol 26: 4872–4896.

    CAS  PubMed  Google Scholar 

  • Thatje, S., C.-D. Hillenbrand & R. Larter, 2005. On the origin of Antarctic marine benthic community structure. Trends Ecol Evol 20: 534–540.

    PubMed  Google Scholar 

  • Timm, L. E., B. Moahamed & H. D. Bracken-Grissom, 2018. DEEPEND: Mitochondrial DNA sequence alignments and raw fastq files for the population genetic analysis of the deep-sea isopod, Bathynomus giganteus. Distributed by: Gulf of Mexico Research Initiative Information and Data Cooperative (GRIIDC), Harte Research Institute, Texas A&M University – Corpus Christi.

  • Trewick, S. A. & G. P. Wallis, 2001. Bridging the “beech-gap”: new Zealand invertebrate phylogeography implicates Pleistocene glaciation and Pliocene isolation. Evolution 55: 2170–2180.

    CAS  PubMed  Google Scholar 

  • Vanreusel, A., G. Fonseca, R. Danovaro, M. C. Da Silva, A. M. Esteves, T. Ferrero, G. Gad, V. Galtsova, C. Gambi, V. Da Fonsêca Genevois, J. Ingels, B. Ingole, N. Lampadariou, B. Merckx, D. Miljutin, M. Miljutina, M. Raes, A. Tchesunov, J. Vanaverbeke, S. Van Gaever, V. Venekey, T. N. Bezerra, H. Flint, J. Copley, E. Pape, D. Zeppilli, P. A. Martinez & J. Galeron, 2010. The contribution of deep-sea macrohabitat heterogeneity to global nematode diversity. Mar Ecol 31: 6–20.

    Google Scholar 

  • Venables, W. N. & B. D. Ripley, 2002. Modern Applied Statistics with S (Fourth). Springer, New York.

    Google Scholar 

  • Wilson, G. D. F., 1983. Variation in the deep-sea isopod Eurycope iphthima (Asellota, Eurycopidae): depth related clines in rostral morphology and in population. J Crustac Biol 3: 127–140.

    Google Scholar 

  • Zardus, J. D., R. J. Etter, M. R. Chase, M. A. Rex & E. E. Boyle, 2006. Bathymetric and geographic population structure in the pan-Atlantic deep-sea bivalve Deminucula atacellana (Schenck, 1939). Mol Ecol 15: 639–651.

    CAS  PubMed  Google Scholar 

  • Zemlak, T. S., E. M. Habit, S. J. Walde, M. A. Battini, E. D. M. Adams & D. E. Ruzzante, 2008. Across the southern Andes on fin: glacial refugia, drainage reversals and a secondary contact zone revealed by the phylogeographical signal of Galaxias platei in Patagonia. Mol Ecol 17: 5049–5061.

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This research was made possible in part by a grant from The Gulf of Mexico Research Initiative through the Florida Institute of Oceanography, a Grant to the Deep-C Consortium, and a Grant to the Deep Pelagic Nekton Dynamics of the Gulf of Mexico (DEEPEND) Consortium. Funding was also provided by the Florida International University (FIU) Presidential Fellowship and the FIU Doctoral Evidence Acquisition Fellowship. All data are publicly available through the Gulf of Mexico Research Initiative Information & Data Cooperative (GRIIDC) at https://data.gulfresearchinitiative.org (https://doi.org/10.7266/N7VX0F19). The authors would like to specially thank Dr. Mike Heithaus and Dr. Dean Grubbs for their support in sample collection. The authors also thank L. E. Timm’s PhD committee: Dr. José Eirin-Lopez, Dr. Mauricio Rodriguez-Lanetty, Dr. Eric von Wettberg, and Dr. Wensong Wu; as well as Ms. Emily Warschefsky, Mr. Joseph Ahrens, and Dr. Danielle DeLeo for additional comments and suggestions. Finally, the authors thank the anonymous reviewers for feedback on earlier versions of this manuscript. This is contribution #84 from the Center for Coastal Oceans Research in the Institute of Water and Environment at Florida International University.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to L. E. Timm.

Additional information

Guest editors: Guiomar Rotllant, Ferran Palero, Peter Mather, Heather Bracken-Grissom & Begoña Santos / Crustacean Genomics

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Timm, L.E., Moahamed, B., Churchill, D.A. et al. Bathynomus giganteus (Isopoda: Cirolanidae) and the canyon: a population genetics assessment of De Soto Canyon as a glacial refugium for the giant deep-sea isopod. Hydrobiologia 825, 211–225 (2018). https://doi.org/10.1007/s10750-018-3563-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-018-3563-6

Keywords

Navigation