Polar Biology

, Volume 30, Issue 4, pp 513–521 | Cite as

The utility of fast evolving molecular markers for studying speciation in the Antarctic benthos

Original Paper

Abstract

The Southern Ocean is surprisingly rich in species that coexist in one of the most extreme environments on Earth yet the processes leading to speciation in this ecosystem are not well understood. To remedy this, tools that measure the genetic connectedness within a species are needed. Although useful for phylogenetic purposes, the readily available mitochondrial markers (e.g. 16S, COI) suffer from numerous shortcomings for population genetics. Therefore, molecular markers are needed that are sufficiently variable, unlinked, biparentally inherited, and distributed over the whole genome. We argue that microsatellites are suitable markers that have not been widely used in exploratory studies due to their difficult initial set-up. Working with the Ceratoserolis trilobitoides species complex (Isopoda), we demonstrate that using a novel protocol many microsatellites can be identified quickly. An increased availability of these highly sensitive markers will be useful for studies addressing the origin of species in the Southern Ocean and their response to future climate change.

Keywords

Antarctic benthos Population genetics Phylogeography Microsatellites Speciation 

References

  1. Abajian C (1994) Sputnik beta version 29 July 1994. http://www.espressosoftware.com/pages/sputnik.jsp
  2. Aronson RB, Blake DB (2001) Global climate change and the origin of modern benthic communities in Antarctica. Am Zool 41:27–39CrossRefGoogle Scholar
  3. Avise JC (2000) Phylogeography. The history and formation of species. Harvard University Press, CambridgeGoogle Scholar
  4. Ballard JW, Whitlock MC (2004) The incomplete natural history of mitochondria. Mol Ecol 13:729–744PubMedCrossRefGoogle Scholar
  5. Baltzer C, Held C, Waegele J-W (2000) Furcarcturus polarsterni gen. nov., sp. nov., a large deep-sea arcturid isopod from the Drake Passage, with a preliminary molecular characterization. Polar Biol 23:833–839CrossRefGoogle Scholar
  6. Bargelloni L, Zane L, Derome N, Lecointre G, Patarnello T (2000) Molecular zoogeography of Antarctic euphausiids and notothenioids: from species phylogenies to intraspecific patterns of genetic variation. Antarct Sci 12:259–268Google Scholar
  7. Bensch S, Akesson M (2005) Ten years of AFLP in ecology and evolution: why so few animals? Mol Ecol 14:2899–2914PubMedCrossRefGoogle Scholar
  8. Bernardi G, Goswami U (1997) Molecular evidence for cryptic species among the Antarctic fish Trematomus bernachii and Trematomus hansoni. Antarct Sci 9:381–385Google Scholar
  9. Chambers GK, MacAvoy ES (2000) Microsatellites: consensus and controversy. Comp Biochem Physiol B: Biochem Mol Biol 126:455–476CrossRefGoogle Scholar
  10. Clarke A (1983) Life in cold water: the physiological ecology of polar marine ectotherms. Oceanogr Mar Biol, Annu Rev 21:241–453Google Scholar
  11. Clarke A, Aronson RB, Crame JA, Gil JM, Blake DB (2004) Evolution and diversity of the benthic fauna of the Southern Ocean continental shelf. Antarct Sci 16:559–568CrossRefGoogle Scholar
  12. Coyne JA, Orr HA (1998) The evolutionary genetics of speciation. Philos Trans R Soc Lond B Biol Sci 353:287–305PubMedCrossRefGoogle Scholar
  13. Ellegren H (2004) Microsatellites: simple sequences with complex evolution. Nat Rev Genet 5:435–445PubMedCrossRefGoogle Scholar
  14. Ellsworth LE, Rittenhouse KD, Honeycutt RL (1993) Artifactual variation in randomly amplified polymorphic DNA banding patterns. BioTechniques 14:214–217PubMedGoogle Scholar
  15. Gaffney PM (2000) Molecular tools for understanding population structure in Antarctic species. Antarct Sci 12:288–296Google Scholar
  16. Gray JS (2001) Antarctic marine benthic biodiversity in a world-wide latitudinal context. Polar Biol 24:633–641CrossRefGoogle Scholar
  17. Gutt J, Sirenko BI, Smirnov IS, Arntz WE (2004) How many macrozoobenthic species might inhabit the Antarctic shelf? Antarct Sci 16:11–16CrossRefGoogle Scholar
  18. Hebert PDN, Ratnasingham S, deWaard JR (2003) Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proc R Soc Lond B Biol Sci 270:S96–S99CrossRefGoogle Scholar
  19. Held C (2000) Phylogeny and biogeography of serolid isopods (Crustacea, Isopoda, Serolidae) and the use of ribosomal expansion segments in molecular systematics. Mol Phylogenet Evol 15:165–178PubMedCrossRefGoogle Scholar
  20. Held C (2001) No evidence for slow-down of molecular substitution rates at subzero temperatures in Antarctic serolid isopods (Crustacea, Isopoda, Serolidae). Polar Biol 24:497–501CrossRefGoogle Scholar
  21. Held C (2003) Molecular evidence for cryptic speciation within the widespread Antarctic crustacean Ceratoserolis trilobitoides (Crustacea, Isopoda). In: Huiskes AHL, Gieskes WWC, Rozema J, Schorno RML, van der Vies SM, Wolff WJ (eds) Antarctic biology in a global context. Backhuys, Leiden, pp 135–139Google Scholar
  22. Held C, Wägele J-W (2005) Cryptic speciation in the giant Antarctic isopod Glyptonotus antarcticus (Isopoda: Valvifera: Chaetiliidae). Sci Mar 69:175–181CrossRefGoogle Scholar
  23. Hoelzel AR, Natoli A, Dahlheim ME, Olavarria C, Baird RW, Black NA (2002) Low worldwide genetic diversity in the killer whale (Orcinus orca): implications for demographic history. Proc R Soc Lond B Biol Sci 269:1467–1473CrossRefGoogle Scholar
  24. Jarman SN (2001) The evolutionary history of krill inferred from nuclear large subunit rDNA sequence analysis. Biol J Linn Soc 73:199–212CrossRefGoogle Scholar
  25. Jarman SN, Elliott NG, Nicol S, McMinn A (2000) Molecular phylogenetics of circumglobal Euphausia species (Euphausiacea: Crustacea). Can J Fish Aquat Sci 57:51–58CrossRefGoogle Scholar
  26. Jarman SN, Elliott NG, Nicol S, McMinn A (2002) Genetic differentiation in the Antarctic coastal krill Euphausia crystallorophias. Heredity 88:280–287PubMedCrossRefGoogle Scholar
  27. Kashi Y, Soller M (1999) Functional role of microsatellites and minisatellites. In: Goldstein DB, Schlötterer C (eds) Microsatellites. Evolution and applications. Oxford University Press, New York, pp 10–23Google Scholar
  28. Lecointre G, Bonillo C, Ozouf-Costaz C, Hureau J-C (1997) Molecular evidence for the origins of Antarctic fishes: paraphyly of the Bovichtidae and no indication for the monophyly of the Notothenioidei (Teleostei). Polar Biol 18:193–208CrossRefGoogle Scholar
  29. Lee YH, Song M, Lee S, Leon R, Godoy SO, Canete I (2004) Molecular phylogeny and divergence time of the Antarctic sea urchin (Sterechinus neumayeri) in relation to the South American sea urchins. Antarct Sci 16:29–36CrossRefGoogle Scholar
  30. Li YC, Korol AB, Fahima T, Beiles A, Nevo E (2002) Microsatellites: genomic distribution, putative functions and mutational mechanisms: a review. Mol Ecol 11:2453–2465PubMedCrossRefGoogle Scholar
  31. Loerz AN, Held C (2004) A preliminary molecular and morphological phylogeny of the Antarctic Epimeriidae and Iphimediidae (Crustacea, Amphipoda). Mol Phylogenet Evol 31:4–15CrossRefGoogle Scholar
  32. Lunt DH, Hutchinson WF, Carvalho GR (1999) An efficient method for PCR-based isolation of microsatellite arrays (PIMA). Mol Ecol 8:891–893CrossRefGoogle Scholar
  33. Near TJ (2004) Estimating divergence times of notothenioid fishes using a fossil-calibrated molecular clock. Antarct Sci 16:37–44CrossRefGoogle Scholar
  34. Near TJ, Pesavento JJ, Cheng CHC (2003) Mitochondrial DNA, morphology, and the phylogenetic relationships of Antarctic icefishes (Notothenioidei: Channichthyidae). Mol Phylogenet Evol 28:87–98PubMedCrossRefGoogle Scholar
  35. Near TJ, Pesavento JJ, Cheng CHC (2004) Phylogenetic investigations of Antarctic notothenioid fishes (Perciformes: Notothenioidei) using complete gene sequences of the mitochondrial encoded 16S rRNA. Mol Phylogenet Evol 32:881–891PubMedCrossRefGoogle Scholar
  36. Nolte AW, Stemshorn KC, Tautz D (2005) Direct cloning of microsatellite loci from Cottus gobio through a simplified enrichment procedure. Mol Ecol Notes 5:628–636Google Scholar
  37. Page TJ, Linse K (2002) More evidence of speciation and dispersal across the Antarctic Polar Front through molecular systematics of Southern Ocean Limatula (Bivalvia: Limidae). Polar Biol 25:818–826Google Scholar
  38. Patarnello T, Bargelloni L, Varotto V, Battaglia B (1996) Krill evolution and the Antarctic ocean currents: evidence of vicariant speciation as inferred by molecular data. Mar Biol 126:603–608CrossRefGoogle Scholar
  39. Peck LS (2002) Ecophysiology of Antarctic marine ectotherms: limits to life. Polar Biol 25:31–40CrossRefGoogle Scholar
  40. Perez T, Albornoz J, Dominguez A (1998) An evaluation of RAPD fragment reproducibility and nature. Mol Ecol 7:1347–1357PubMedCrossRefGoogle Scholar
  41. Raupach MJ, Wägele JW (2006) Distinguishing cryptic species in Antarctic Asellota (Crustacea: Isopoda)—a preliminary study of mitochondrial DNA in Acanthaspidia drygalskii. Antarct Sci 18:191–198CrossRefGoogle Scholar
  42. Raupach MJ, Held C, Wagele JW (2004) Multiple colonization of the deep sea by the Asellota (Crustacea: Peracarida: Isopoda). Deep-Sea Res (2 Top Stud Oceanogr) 51:1787–1795CrossRefGoogle Scholar
  43. Reilly A, Ward RD (1999) Microsatellite loci to determine population structure of the Patagonian toothfish Dissostichus eleginoides. Mol Ecol 8:1753–1754PubMedCrossRefGoogle Scholar
  44. Ritchie PA, Bargelloni L, Meyer A, Taylor JA, MacDonald JA, Lambert DM (1996) Mitochondrial phylogeny of trematomid fishes (Nototheniidae, Perciformes) and the evolution of Antarctic fish. Mol Phylogenet Evol 5:383–390PubMedCrossRefGoogle Scholar
  45. Ritchie PA, Lavoue S, Lecointre G (1997) Molecular phylogenetics and the evolution of Antarctic Notothenioid fishes. Comp Biochem Physiol A: Physiol 118:1009–1025CrossRefGoogle Scholar
  46. Roeder AD, Marshall RK, Mitchelson AJ, Visagathilagar T, Ritchie PA, Love DR, Pakai TJ, McPartlan HC, Murray ND, Robinson NA, Kerry KR, Lambert DM (2001) Gene flow on the ice: genetic differentiation among Adelie penguin colonies around Antarctica. Mol Ecol 10:1645–1656PubMedCrossRefGoogle Scholar
  47. Roman J, Palumbi SR (2004) A global invader at home: population structure of the green crab, Carcinus maenas, in Europe. Mol Ecol 13:2891–2898PubMedCrossRefGoogle Scholar
  48. Schlötterer C (2004) The evolution of molecular markers—just a matter of fashion? Nat Rev Genet 5:63–69PubMedCrossRefGoogle Scholar
  49. Shaw PW, Arkhipkin AI, Al Khairulla H (2004) Genetic structuring of Patagonian toothfish populations in the Southwest Atlantic Ocean: the effect of the Antarctic Polar Front and deep-water troughs as barriers to genetic exchange. Mol Ecol 13:3293–3303PubMedCrossRefGoogle Scholar
  50. Simon C, Frati F, Beckenbach A, Crespi B, Liu H, Flook P (1994) Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Ann Entomol Soc Am 87:651–701Google Scholar
  51. Stankovic A, Spalik K, Kamler E, Borsuk P, Weglenski P (2002) Recent origin of sub-Antarctic notothenioids. Polar Biol 25:203–205Google Scholar
  52. Tautz D, Arctander P, Minelli A, Thomas RH, Vogler AP (2003) A plea for DNA taxonomy. Trends Ecol Evol 18:70–74CrossRefGoogle Scholar
  53. Thatje S, Hillenbrand CD, Larter R (2005) On the origin of Antarctic marine benthic community structure. Trends Ecol Evol 20:534–540PubMedCrossRefGoogle Scholar
  54. Valsecchi E, Palsboll P, Hale P, Glockner-Ferrari D, Ferrari M, Larsen F, Mattila D, Sears R, Sigurjonsson J, Brown M, Corkeron P, Amos B (1997) Microsatellite genetic distances between oceanic populations of the humpback whale (Megaptera novaeangliae). Mol Biol Evol 14:355–362PubMedGoogle Scholar
  55. Waples RS, Gaggiotti O (2006) What is a population? An empirical evaluation of some genetic methods for identifying the number of gene pools and their degree of connectivity. Mol Ecol 15:1419–1439PubMedCrossRefGoogle Scholar
  56. Zane L, Patarnello T (2000) Krill: a possible model for investigating the effects of ocean currents on the genetic structure of a pelagic invertebrate. Can J Fish Aquat Sci 57:16–23CrossRefGoogle Scholar
  57. Zane L, Ostellari L, Maccatrozzo L, Bargelloni L, Battaglia B, Patarnello T (1998) Molecular evidence for genetic subdivision of Antarctic krill (Euphausia superba Dana) populations. Proc R Soc Lond B Biol Sci 265:2387–2391CrossRefGoogle Scholar
  58. Zane L, Bargelloni L, Patarnello T (2002) Strategies for microsatellite isolation: a review. Mol Ecol 11:1–16PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  1. 1.Alfred Wegener Institute for Polar and Marine ResearchBremerhavenGermany
  2. 2.Lehrstuhl für Spezielle ZoologieRuhr-University of BochumBochumGermany

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