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Marine Biodiversity

, Volume 46, Issue 2, pp 465–471 | Cite as

No divergent evolution, despite restricted connectivity, between Atlantic and Indian Ocean goby populations

  • Eduard Drost
  • Tirupathi Rao Golla
  • Sophie von der Heyden
  • Peter R. Teske
Original Paper

Abstract

Southern Africa is a marine biodiversity hotspot that not only comprises faunal elements from the Atlantic and Indian Oceans, but also large numbers of endemic species. Using mitochondrial and nuclear DNA sequence data, we explored whether genetic structure in the endemic coastal goby Psammogobius knysnaensis, a species whose range straddles both biomes, is linked to the boundary between the two oceans. Subtle genetic structure was identified between Atlantic and Indian Ocean populations, with genetic diversity being lower in the Atlantic, and particularly on the west coast. Our results point to partial isolation between the populations associated with each biome that is most likely driven by the region’s oceanography, but unlike in other species, there is no evidence for distinct regional evolutionary lineages that are likely adapted to the environmental conditions prevalent in each region. The exclusive presence of P. knysnaensis in sheltered habitats (estuaries and lagoons) may protect this species from the severe impacts of cold water upwelling on the west coast.

Keywords

Cryptic biodiversity Genetic structure Mitochondrial DNA COI gene Nuclear DNA S72 intron Psammogobius knysnaensis 

Notes

Acknowledgments

We are grateful to Nadine Strydom for providing information on the life history of Psammogobius knysnaensis. This study was funded by the PADI Foundation (Grant No. 10981, awarded to P. Teske) and the University of Johannesburg. T.R. Golla gratefully acknowledges the National Research Foundation and the University of Johannesburg for financial support.

References

  1. Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48CrossRefPubMedGoogle Scholar
  2. Beckley LE (1985) Tidal exchange of ichthyoplankton in the Swartkops estuary mouth, South Africa. S Afr J Zool 20:15–20CrossRefGoogle Scholar
  3. Beldade R, Pedro T, Goncalves EJ (2007) Pelagic larval duration of 10 temperate cryptobenthic fishes. J Fish Biol 71:376–382CrossRefGoogle Scholar
  4. Benjamini Y, Yekutieli D (2001) The control of false discovery rate under dependency. Ann Stat 29:1165–1188CrossRefGoogle Scholar
  5. Branch GM, Griffiths CL, Branch ML, Beckley LE (2010) Two Oceans. A guide to the marine life of southern Africa. David Philip Publishers, Cape Town, South AfricaGoogle Scholar
  6. Brown L, du Preez J, Smit N, van As J (2012) The story of life and the environment, an African perspective. Struik Nature Publishers, Cape TownGoogle Scholar
  7. Chow S, Hazama K (1998) Universal PCR primers for S7 ribosomal protein gene introns in fish. Mol Ecol 7:1255–6PubMedGoogle Scholar
  8. Dawson MN (2012) Parallel phylogeographic structure in ecologically similar sympatric sister taxa. Mol Ecol 21:987–1004CrossRefPubMedGoogle Scholar
  9. Dawson J, Griffiths CL (2012) Revision of the crown crabs, genus Hymenosoma (Crustacea: Hymenosomatidae), of South Africa. Afr Nat Hist 8:16–29Google Scholar
  10. Ducombe Rae CM (1991) Agulhas retroflection rings in the South Atlantic Ocean: an overview. S Afr J Mar Sci 11:327–344Google Scholar
  11. Dufois F, Rouault M (2012) Sea surface temperature in False Bay (South Africa): towards a better understanding of its seasonal and inter-annual variability. Cont Shelf Res 43:24–35Google Scholar
  12. Excoffier L, Lischer HE (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under linux and windows. Mol Ecol Resour 10:564–567CrossRefPubMedGoogle Scholar
  13. Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491PubMedPubMedCentralGoogle Scholar
  14. Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–9PubMedGoogle Scholar
  15. Griffiths CL, Robinson TB, Lange L, Mead A (2010) Marine biodiversity in South Africa: an evaluation of current states of knowledge. PLoS One 5, e12008CrossRefPubMedPubMedCentralGoogle Scholar
  16. Kalinowski ST (2005) HP-Rare 1.0: A computer program for performing rarefaction on measures of allelic richness. Mol Ecol Notes 5:187–189CrossRefGoogle Scholar
  17. Lutjeharms JRE (2006) The Agulhas current. Springer, New YorkGoogle Scholar
  18. Lutjeharms JRE, Meeuwis JM (1987) The extent and variability of south-east Atlantic upwelling. Afr J Marine Sci 5:51–62CrossRefGoogle Scholar
  19. Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220PubMedGoogle Scholar
  20. Meadows ME (1985) Biogeography and ecosystems of South Africa. Juta, Cape TownGoogle Scholar
  21. Mmonwa KL, Teske PR, McQuaid CD, Barker NP (2015) Phylogeography and demographic history of multiple southern African patellid limpets: congruence of Pleistocene spatial expansion, but not phylogeography. Afr J Mar Sci 37:11–20CrossRefGoogle Scholar
  22. Muller CM, Svd H, Bowie RCK, Matthee CA (2012) Linking oceanic circulation, local upwelling and palaeoclimatic changes to the phylogeography of larval dispersal in the southern African Cape sea urchin, Parechinus angulosus. Mar Ecol Prog Ser 468:203–215CrossRefGoogle Scholar
  23. Muteveri T, Matthee CA, Bowie RCK, Svd H (2015) High population connectivity and Pleistocene range expansion in the direct-developing plough shell Bullia rhodostoma along the South African coast. Afr J Marine Sci 37:21–31CrossRefGoogle Scholar
  24. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New YorkGoogle Scholar
  25. Papadopoulos I, Teske PR (2014) Larval development reflects biogeography in two formerly synonymised southern African coastal crabs. Afr J Aquat Sci 39:347–350CrossRefGoogle Scholar
  26. Qhaji Y, Papadopoulos I, Jansen van Vuuren B, McQuaid CD, Teske PR (2015) A comparison of genetic structure in two low-dispersal crabs from the Wild Coast, South Africa. Afr J Marine Sci, in pressGoogle Scholar
  27. Reynolds TV, Matthee CA, von der Heyden S (2014) The influence of Pleistocene climatic changes and ocean currents on the phylogeography of the southern African barnacle, Tetraclita serrata (Thoracica; Cirripedia). PLoS One 9, e102115CrossRefPubMedPubMedCentralGoogle Scholar
  28. Roy C, Weeks S, Rouault M, Nelson G, Barlow R, van der Lingen C (2001) Extreme oceanographic events recorded in the southern benguela during the 1999–2000 summer season. S Afr J Sci 97:465–471Google Scholar
  29. Shannon LV, Chapman P (1983) Suggested mechanism for the chronic pollution by oil of beaches east of Cape Agulhas, South Africa. Afr J Marine Sci 1:231–244CrossRefGoogle Scholar
  30. Slatkin M (1995) A measure of population subdivision based on microsatellite allele frequencies. Genetics 139:457–462PubMedPubMedCentralGoogle Scholar
  31. Smith AJ, Robets M, Anderson RJ et al (2013) A coastal seawater temperature dataset for biogeographical studies: large biases between in situ and remotely-sensed data sets around the coast of South Africa. PLoS One 8, e81944CrossRefGoogle Scholar
  32. Stephens M, Smith NJ, Donnelly P (2001) A new statistical method for haplotype reconstruction from population data. Am J Human Genet 68:978–989CrossRefGoogle Scholar
  33. Strydom N (2015) Patterns in larval fish diversity, abundance, and distribution in temperate South African estuaries. Estuar Coast 38:268–284CrossRefGoogle Scholar
  34. Sutherland K, Strydom NA, Wooldridge TH (2012) Composition, abundance, distribution and seasonality of larval fishes in the Sundays Estuary, South Africa. Afr Zool 47:229–244CrossRefGoogle Scholar
  35. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729CrossRefPubMedPubMedCentralGoogle Scholar
  36. Teske PR, McQuaid CD, Froneman P, Barker NP (2006) Impacts of marine biogeographic boundaries on phylogeographic patterns of three South African estuarine crustaceans. Mar Ecol Prog Ser 314:283–293CrossRefGoogle Scholar
  37. 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 prawns. BMC Evol Biol 8:341CrossRefPubMedPubMedCentralGoogle Scholar
  38. Teske PR, McLay JSC, Papadopoulos I et al (2009) Tri-locus sequence data reject a “Gondwanan origin hypothesis” for the African/South Pacific crab genus Hymenosoma. Mol Phylogenet Evol 53:23–33CrossRefPubMedGoogle Scholar
  39. Teske PR, von der Heyden S, McQuaid CD, Barker NP (2011) A review of marine phylogeography in southern Africa. S Afr J Sci 107:43–53CrossRefGoogle Scholar
  40. Teske PR, Zardi GI, McQuaid CD, Nicastro K (2013) Two sides of the same coin: extinctions and originations across the Atlantic/Indian Ocean boundary as consequences of the same climate oscillation. Front Biogeogr 5:48–59Google Scholar
  41. Teske PR, Papadopoulos I, Barker NP, McQuaid CD, Beheregaray LB (2014) Mitonuclear discordance in genetic structure across the Atlantic/Indian Ocean biogeographical transition zone. J Biogeogr 41:392–401CrossRefGoogle Scholar
  42. Turpie JK, Beckley LE, Katua SM (2000) Biogeography and the selection of priority areas for conservation of South African coastal fishes. Biol Conserv 92:59–72CrossRefGoogle Scholar
  43. von der Heyden S, Prochazka K, Bowie RCK (2008) Significant population structure amidst expanding populations of Clinus cottoides (Perciformes, Clinidae): application of molecular tools to marine conservation planning in South Africa. Mol Ecol 17:4812–4826CrossRefPubMedGoogle Scholar
  44. von der Heyden S, Bowie RCK, Prochazka K, Bloomer P, Crane NL, Bernardi G (2011) Phylogeographic patterns and cryptic speciation across oceanographic barriers in South African intertidal fishes. J Evol Biol 24:2505–2519Google Scholar
  45. Whitfield AK (1989) Ichthyoplankton in a southern African surf zone: nursery area for the postlarvae of estuarine associated fish species? Estuar Coast Shelf Sci 29:533–547CrossRefGoogle Scholar
  46. Wright S (1950) The genetical structure of populations. Nature 166:247–249CrossRefPubMedGoogle Scholar
  47. Wright D, Bishop JM, Matthee CA, von der Heyden S (2015) Genetic isolation by distance reveals restricted dispersal across a range of life-histories: implications for biodiversity conservation planning across highly variable marine environments. Divers Distrib 21:698–710CrossRefGoogle Scholar
  48. Zeugin JA, Hartley JL (1985) Ethanol precipitation of DNA. Focus 7:1–2Google Scholar

Copyright information

© Senckenberg Gesellschaft für Naturforschung and Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Eduard Drost
    • 1
  • Tirupathi Rao Golla
    • 1
  • Sophie von der Heyden
    • 2
  • Peter R. Teske
    • 1
  1. 1.Molecular Zoology Lab, Department of ZoologyUniversity of JohannesburgAuckland ParkSouth Africa
  2. 2.Evolutionary Genomics Group, Department of Botany and ZoologyStellenbosch UniversityMatielandSouth Africa

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