Advertisement

Marine Biology

, Volume 156, Issue 6, pp 1265–1275 | Cite as

A tropical/subtropical biogeographic disjunction in southeastern Africa separates two Evolutionarily Significant Units of an estuarine prawn

  • P. R. Teske
  • H. Winker
  • C. D. McQuaid
  • N. P. Barker
Original Paper

Abstract

Recent phylogeographic research has indicated that biodiversity in the sea may be considerably greater than previously thought. However, the majority of phylogeographic studies on marine invertebrates have exclusively used a single locus (mitochondrial DNA), and it is questionable whether the phylogroups identified can be considered distinct species. We tested whether the mtDNA phylogroups of the southern African sandprawn Callianassa kraussi Stebbing (Decapoda: Thalassinidea) are also recovered using nuclear sequence data. Four mtDNA phylogroups were recovered that were each associated with one of South Africa’s four major biogeographic provinces. Three of these were poorly differentiated, but the fourth (tropical) group was highly distinct. The nuclear phylogeny recovered two major clades, one present in the tropical region and the other in the remainder of South Africa. Congruence between mitochondrial and nuclear DNA indicates that the species comprises two Evolutionarily Significant Units sensu Moritz (1994). In conjunction with physiological data from C. kraussi and morphological, ecological and physiological data from other species, this result supports the notion that at least some of the mtDNA phylogroups of coastal invertebrates whose distributions are limited by biogeographic disjunctions can indeed be considered to be cryptic species.

Keywords

Phylogeographic Pattern Restricted Gene Flow Biogeographic Province Phylogeographic Break High Dispersal Potential 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

This is a contribution from the African Coelacanth Ecosystem Programme (ACEP). We are grateful to Brent Newman, Paul Cowley and Isabelle Papadopoulos for providing samples, to Joanne Palmer for generating COI sequences for the isolation-by-distance analysis and to George Branch for information concerning the distribution range of Callianassa kraussi. Three anonymous referees are thanked for comments that considerably improved the quality of this manuscript. This study was supported by postdoctoral research fellowships from the Claude Harris Leon Foundation and the NRF awarded to PRT, an overseas study grant from the Ernest Oppenheimer Memorial Trust awarded to PRT, the National Research Foundation (GUN 2069119 to NPB) and Rhodes University.

References

  1. Avise JC, Arnold J, Ball RM Jr, Bermingham E, Lamb T, Neigel JE, Reed CA, Saunders NC (1987) Intraspecific phylogeography: the mitochondrial DNA bridge between population genetics and systematics. Annu Rev Ecol Syst 18:489–522CrossRefGoogle Scholar
  2. Banks S, Piggott M, Williamson J, Bove U, Holbrook N, Beheregaray LB (2007) Oceanic variability and coastal topography shape local genetic structure in a long-dispersing marine invertebrate. Ecology 88:3055–3064. doi: https://doi.org/10.1890/07-0091.1 CrossRefGoogle Scholar
  3. Barber PH, Erdmann MV, Palumbi SR (2006) Comparative phylogeography of three codistributed stomatopods: origins and timing of regional lineage diversification in the coral triangle. Evolution 60:1825–1839CrossRefGoogle Scholar
  4. Beheregaray LB (2008) Twenty years of phylogeography: the state of the field and the challenges for the Southern Hemisphere. Mol Ecol 17:3754–3774PubMedGoogle Scholar
  5. Beheregaray LB, Caccone A (2007) Cryptic biodiversity in a changing world. J Biol 6:1–5. doi: https://doi.org/10.1186/jbiol60 CrossRefGoogle Scholar
  6. Bolton JJ, Coppejans E, Anderson RJ, De Clerck O, Samyn Y, Leliaert F, Thandar AS (2001) Biodiversity of seaweeds and echinoderms in the western Indian Ocean: workshop report. S Afr J Sci 97:453–454Google Scholar
  7. Bolton JJ, Leliaert F, De Clerck O, Anderson RJ, Stegenga H, Engledow HE, Coppejans E (2004) Where is the western limit of the tropical Indian Ocean seaweed flora? An analysis of intertidal seaweed biogeography on the east coast of South Africa. Mar Biol 144:51–59. doi: https://doi.org/10.1007/s00227-003-1182-9 CrossRefGoogle Scholar
  8. Bruton MN (1980) An outline of the ecology of the Mgobezeleni lake system at Sodwana, with emphasis on the mangrove community. In: Bruton MN, Cooper KH (eds) Studies in the ecology of Maputaland. Rhodes University and The Natal Branch of The Wildlife Society of Southern Africa, Durban, pp 408–426Google Scholar
  9. Cerff EC (1986) Salinity and temperature responses in Callianassa kraussi (Crustacea: Decapoda: Thalassinidea). M.Sc. thesis, University of Natal, Durban, South AfricaGoogle Scholar
  10. Clement M, Posada D, Crandall KA (2000) tcs: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1660. doi: https://doi.org/10.1046/j.1365-294x.2000.01020.x CrossRefGoogle Scholar
  11. Dawson MN, Jacobs DK (2001) Molecular evidence for cryptic species of Aurelia aurita (Cnidaria, Scyphozoa). Biol Bull 200:92–96. doi: https://doi.org/10.2307/1543089 CrossRefGoogle Scholar
  12. Day JH (1981) Fauna. In: Day JH (ed) Estuarine ecology with particular reference to southern Africa. Balkema, Cape Town, pp 147–178Google Scholar
  13. Diekmann U, Doebeli M, Metz JAJ, Tautz D (2004) Adaptive speciation. Cambridge University Press, Cambridge, UKCrossRefGoogle Scholar
  14. Dizon AE, Lockyer C, Perrin WF, Demasters DP, Sisson J (1992) Rethinking the stock concept: a phylogeographic approach. Conserv Biol 6:24–36. doi: https://doi.org/10.1046/j.1523-1739.1992.610024.x CrossRefGoogle Scholar
  15. Edkins MT, Teske PR, Papadopoulos I, Griffiths CL (2007) Morphological and genetic data suggest that southern African crown crabs, Hymenosoma orbiculare, represent five distinct species. Crustaceana 80:667–683. doi: https://doi.org/10.1163/156854007781360694 CrossRefGoogle Scholar
  16. Evans BS, Sweijd NA, Bowie RCK, Cook PA, Elliott NG (2004) Population genetic structure of the perlemoen, Haliotis midae in South Africa: evidence of range expansion and founder events. Mar Ecol Prog Ser 270:163–172. doi: https://doi.org/10.3354/meps270163 CrossRefGoogle Scholar
  17. Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: An integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50CrossRefGoogle Scholar
  18. Flemming BW, Hay ER (1988) Sediment distribution and dynamics on the Natal continental shelf. In: Schumann EH (ed) Coastal ocean studies off Natal, South Africa. Springer, New YorkGoogle Scholar
  19. Forbes AT (1973) An unusual abbreviated larval life in the estuarine burrowing prawn Callianassa kraussi (Crustacea:Decapoda:Thalassinidea). Mar Biol 22:361–365. doi: https://doi.org/10.1007/BF00391395 CrossRefGoogle Scholar
  20. Forbes AT (1974) Osmotic and ionic regulation in Callianassa kraussi Stebbing (Crustacea: Decapoda: Thalassinidea). J Exp Mar Biol Ecol 16:301–311CrossRefGoogle Scholar
  21. Forbes AT (1978) Maintenance of non-breeding populations of the estuarine prawn Callianassa kraussi (Crustacea, Anomura, Thalassinidea). Zool Afr 13:33–40CrossRefGoogle Scholar
  22. Garrick RC, Dyer RJ, Beheregaray LB, Sunnucks P (2008) Babies and bathwater: a comment on the premature obituary for nested clade phylogeographical analysis. Mol Ecol 17:1401–1403. doi: https://doi.org/10.1111/j.1365-294X.2008.03675.x CrossRefGoogle Scholar
  23. Gopal K, Tolley KA, Groeneveld JC, Matthee CA (2006) Mitochondrial DNA variation in spiny lobster Palinurus delagoae suggests genetically structured populations in the southwestern Indican Ocean. Mar Ecol Prog Ser 319:191–198. doi: https://doi.org/10.3354/meps319191 CrossRefGoogle Scholar
  24. Hart MN (1980) An outline of the ecology of Lake Sibaya, with emphasis on the vertebrate communities. In: Bruton MN, Cooper KH (eds) Studies in the ecology of Maputaland. Rhodes University and The Natal Branch of The Wildlife Society of Southern Africa, Durban, pp 382–407Google Scholar
  25. Harrison TD (2004) Physiochemical characteristics of South African estuaries in relation to the zoogeography of the region. Estuar Coast Shelf Sci 61:73–87CrossRefGoogle Scholar
  26. Higgins D, Thompson J, Gibson T, Thompson JD, Higgins DG, Gibson TJ (1994) clustalw: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680. doi: https://doi.org/10.1093/nar/22.22.4673 CrossRefGoogle Scholar
  27. Irwin DE (2002) Phylogeographic breaks without geographic barriers to gene flow. Evolution 56:2383–2394CrossRefGoogle Scholar
  28. Jackson LF (1976) Aspects of the intertidal ecology of the east coast of South Africa. Invest Rep Oceangr Res Inst 46:1–72Google Scholar
  29. Jensen JL, Bohonak AJ, Kelley ST (2005) Isolation by distance, web service. BMC Genet 6:13. doi: https://doi.org/10.1186/1471-2156-6-13 CrossRefGoogle Scholar
  30. Kuo C-H, Avise JC (2005) Phylogeographic breaks in low-dispersal species: the emergence of concordance across gene trees. Genetica 124:179–186. doi: https://doi.org/10.1007/s10709-005-2095-y CrossRefGoogle Scholar
  31. Machordom A, Macpherson E (2004) Rapid radiation and cryptic speciation in squat lobsters of the genus Munida (Crustacea, Decapoda) and related genera in the South West Pacific: molecular and morphological evidence. Mol Phylogenet Evol 33:259–279. doi: https://doi.org/10.1016/j.ympev.2004.06.001 CrossRefGoogle Scholar
  32. Mantel N (1967) The detection of disease clustering and generalized regression approach. Cancer Res 27:209–220Google Scholar
  33. Matthee CA, Cockcroft AC, Gopal K, von der Heyden S (2007) Mitochondrial DNA variation of the west-coast rock lobster, Jasus lalandii: marked genetic diversity differences among sampling sites. Mar Freshw Res 58:1130–1135. doi: https://doi.org/10.1071/MF07138 CrossRefGoogle Scholar
  34. Moritz C (1994) Applications of mitochondrial DNA analysis in conservation: a critical review. Mol Ecol 3:401–411. doi: https://doi.org/10.1111/j.1365-294X.1994.tb00080.x CrossRefGoogle Scholar
  35. Morrison CL, Harvey AW, Lavery S, Tieu K, Huang Y, Cunningham CW (2002) Mitochondrial gene rearrangements confirm parallel evolution of the crab-like form. Proc R Soc Lond B Biol Sci 269:345–350. doi: https://doi.org/10.1098/rspb.2001.1886 CrossRefGoogle Scholar
  36. Nicastro KR, Zardi GI, McQuaid CD, Teske PR, Barker NP (2008) Coastal topography drives genetic structure in marine mussels. Mar Ecol Prog Ser 368:189–195. doi: https://doi.org/10.3354/meps07607 CrossRefGoogle Scholar
  37. Palumbi SR (1996) Nucleic acids II: the polymerase chain reaction. In: Hillis DM, Moritz C, Mable BK (eds) Molecular systematics. Sinauer Associates, Sunderland, pp 205–247Google Scholar
  38. Panchal M (2007) The automation of nested clade phylogeographic analysis. Bioinformatics 23:509–510. doi: https://doi.org/10.1093/bioinformatics/btl614 CrossRefGoogle Scholar
  39. Panchal M, Beaumont MA (2007) The automation and evaluation of nested clade phylogeographic analysis. Evolution 61:1466–1480. doi: https://doi.org/10.1111/j.1558-5646.2007.00124.x CrossRefGoogle Scholar
  40. Porter ML, Perez-Losada M, Crandall KA (2005) Model-based multi-locus estimation of decapod phylogeny and divergente times. Mol Phylogenet Evol 37:355–369. doi: https://doi.org/10.1016/j.ympev.2005.06.021 CrossRefGoogle Scholar
  41. Posada D, Crandall KA, Templeton AR (2000) GeoDis: A program for the cladistic nested analysis of the geographical distribution of genetic haplotypes. Mol Ecol 9:487–488. doi: https://doi.org/10.1046/j.1365-294x.2000.00887.x CrossRefGoogle Scholar
  42. Ridgway TM, Stewart BA, Branch GM, Hodgson AM (1998) Morphological and genetic differentiation of Patella granularis (Gastropoda: Patellidae) along the coast of South Africa. J Zool (Lond) 245:317–333. doi: https://doi.org/10.1111/j.1469-7998.1998.tb00107.x CrossRefGoogle Scholar
  43. Rocha LA, Robertson DS, Roman J, Bowen BW (2005) Ecological speciation in tropical reef fishes. Proc R Soc Lond B Biol Sci 272:573–579CrossRefGoogle Scholar
  44. Rundle HD, Nosil P (2005) Ecological speciation. Ecol Lett 8:336–352. doi: https://doi.org/10.1111/j.1461-0248.2004.00715.x CrossRefGoogle Scholar
  45. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425Google Scholar
  46. Samraoui B, Weekers PHH, Dumont HJ (2003) Two taxa within the North African Lestes virens complex (Odonata, Zygoptera). Odonatologica 32:131–142Google Scholar
  47. Schumann EH (1988) Physical oceanography off Natal. In: Schuman EH, coastal ocean studies off Natal, South Africa. Lecture Notes on Coastal and Estuarine Studies vol 26, pp 1–271Google Scholar
  48. Sink KJ, Branch GM, Harris JM (2005) Biogeographic patterns in rocky intertidal communities in KwaZulu-Natal, South Africa. Afr J Mar Sci 27:81–96CrossRefGoogle Scholar
  49. Slatkin M (1995) A measure of population subdivision based on microsatellite allele frequencies. Genetics 139:457–462PubMedPubMedCentralGoogle Scholar
  50. Stefanni S, Thorley JL (2003) Mitochondrial DNA phylogeography reveals the existence of an evolutionarily significant unit of the sand goby Pomatoschistus minutus in the Adriatic (Eastern Mediterranean). Mol Phylogenet Evol 28:601–609. doi: https://doi.org/10.1016/S1055-7903(03)00054-X CrossRefGoogle Scholar
  51. Stuckenberg BR (1969) Effective temperature as an ecological factor in southern Africa. Zool Afr 4:145–197CrossRefGoogle Scholar
  52. Tamura K, Nei M (1993) Estimations of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526Google Scholar
  53. Tamura K, Nei M, Kumar S (2004) Prospects for inferring very large phylogenies by using the neighbour-joining method. Proc Natl Acad Sci USA 101:11030–11035. doi: https://doi.org/10.1073/pnas.0404206101 CrossRefGoogle Scholar
  54. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599. doi: https://doi.org/10.1093/molbev/msm092 CrossRefGoogle Scholar
  55. Templeton AR, Sing CF (1993) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping. IV. Nested analyses with cladogram uncertainty and recombination. Genetics 134:659–669PubMedPubMedCentralGoogle Scholar
  56. Templeton AR, Crandall KA, Sing CF (1992) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. Genetics 132:619–633PubMedPubMedCentralGoogle Scholar
  57. Teske PR, McQuaid CD, Froneman PW, Barker NP (2006) Impacts of marine biogeographic boundaries on phylogeographic patterns of three South African estuarine crustaceans. Mar Ecol Prog Ser 314:283–293. doi: https://doi.org/10.3354/meps314283 CrossRefGoogle Scholar
  58. Teske PR, Papadopulos I, Zardi GI, McQuaid CD, Griffiths CL, Edkins MT, Barker NP (2007a) Implications of life history for genetic structure and migration rates of five southern African coastal invertebrates: planktonic, abbreviated and direct development. Mar Biol 152:697–711. doi: https://doi.org/10.1007/s00227-007-0724-y CrossRefGoogle Scholar
  59. Teske PR, Froneman PW, McQuaid CD, Barker NP (2007b) Phylogeographic structure of the caridean shrimp Palaemon peringueyi in South Africa: further evidence for intraspecific genetic units associated with marine biogeographic provinces. Afr J Mar Sci 29:253–258. doi: https://doi.org/10.2989/AJMS.2007.29.2.9.192 CrossRefGoogle Scholar
  60. Teske PR, McQuaid CD, Barker NP (2007c) Lack of genetic differentiation among four southeast African intertidal limpets (Siphonariidae): phenotypic plasticity in a single species? J Moll Stud 73:223–228. doi: https://doi.org/10.1093/mollus/eym012 CrossRefGoogle Scholar
  61. Teske PR, Papadopoulos I, Newman BK, Dworschak PC, McQuaid CD, Barker NP (2008) Oceanic dispersal barriers, adaptation and larval retention: an interdisciplinary assessment of potential factors maintaining a phylogeographic break between sister lineages of an African prawn. BMC Evol Biol 8:341. doi: https://doi.org/10.1186/1471-2148-8-341 CrossRefGoogle Scholar
  62. von der Heyden S, Prochazka K, Bowie RCK (2008) Significant population structure and asymmetric gene flow patterns amidst expanding populations of Clinus cottoides (Perciformes, Clinidae): application of molecular data to marine conservation planning in South Africa. Mol Ecol 17:4812–4826. doi: https://doi.org/10.1111/j.1365-294X.2008.03959.x CrossRefGoogle Scholar
  63. Vorsatz J (2000) Life history strategies of the estuarine sandprawn Callianassa kraussi. PhD thesis, University of Port ElizabethGoogle Scholar
  64. Walsh PS, Metzger DA, Higuchi R (1991) Chelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Biotechniques 10:506–513Google Scholar
  65. Weekers PHH, Gast RJ, Fuerst PA, Byers TJ (1994) Sequence variations in small-subunit ribosoma RNAs of Hartmanella vermiformis and their phylogenetic implications. Mol Biol Evol 11:684–690PubMedGoogle Scholar
  66. York KL, Blacket MJ, Appleton BR (2008) The Bassian Isthmus and the major ocean currents of southeast Australia influence the phylogeography and population structure of a southern Australian intertidal barnacle Catomerus polymerus (Darwin). Mol Ecol 17:1948–1961. doi: https://doi.org/10.1111/j.1365-294X.2008.03735.x CrossRefGoogle Scholar
  67. Zardi GI, McQuaid CD, Teske PR, Barker NP (2007) Unexpected population structure in indigenous (Perna perna) and invasive (Mytilus galloprovincialis) mussel populations in South Africa. Mar Ecol Prog Ser 337:135–144. doi: https://doi.org/10.3354/meps337135 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • P. R. Teske
    • 1
    • 2
    • 4
  • H. Winker
    • 3
  • C. D. McQuaid
    • 4
  • N. P. Barker
    • 1
  1. 1.Molecular Ecology and Systematics Group, Department of BotanyRhodes UniversityGrahamstownSouth Africa
  2. 2.Molecular Ecology Laboratory, Department of Biological SciencesMacquarie UniversitySydneyAustralia
  3. 3.Department of Ichthyology and Fisheries ScienceRhodes UniversityGrahamstownSouth Africa
  4. 4.Department of Zoology and EntomologyRhodes UniversityGrahamstownSouth Africa

Personalised recommendations