Between the current and the coast: genetic connectivity in the spiny lobster Panulirus homarus rubellus, despite potential barriers to gene flow
The spiny lobster Panulirus homarus rubellus is endemic to the Southwest Indian Ocean, where it inhabits a narrow continental shelf between an exposed coast and the upper reaches of the strong western-boundary Agulhas Current. Long-lived phyllosoma larvae released in this dynamic ocean environment have an uncertain fate—they can be retained over the shelf by sub-mesoscale processes, dispersed downstream along the coast or across the Mozambique Channel, or become entrained in the Agulhas Current, and presumably lost. To assess gene flow and population genetic structure, we analyzed mitochondrial cytochrome oxidase subunit 1 and hypervariable control region sequences, and 19 nuclear microsatellite loci obtained from lobsters collected at nine sites in eastern South Africa, Mozambique and southeast Madagascar. Clustering analyses confirmed genetic connectivity among all populations, and gene flow patterns supported the hypothesis that nearshore processes, such as lee eddies and counter currents, retain some phyllosomas over the shelf; whereas, net gene flow direction was moderate towards the southwest. The Mozambique Channel did not impede contemporary gene flow from Madagascar to the African shelf, but return gene flow was rare. Different marker types showed contrasting gene flow patterns during contemporary and evolutionary periods, when Pleistocene glacial/interglacial cycles would have affected sea level, ocean currents and dispersal patterns. Despite genetic connectivity and the importance of local recruitment, recent gene flow suggests an ancillary source/sink dynamic concordant with the prevailing southwesterly direction of boundary currents at the shelf-edge—a factor to consider in regional fisheries and conservation strategies.
We thank Lourenzo Zacarias (Instituto Nacional de Investigaҫӑo Pesqueira, Maputo Mozambique), and the African Coelecanth Ecosystems Project (ACEP, Suitcase Project) for providing tissue samples.
The study received funding support from the South West Indian Ocean Fisheries Project (SWIOFP) and the first author obtained a PhD grant through the Professional Development Programme (PDP) of the National Research Foundation in South Africa.
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflict of interest.
All applicable institutional and/or national guidelines for the care and use of animals were followed. Samples were collected under permits from the Department of Environmental Affairs in South Africa (Permit numbers RES2012/35, RES2013/65, RES2014/48, RES2015/36 and RES2016/14).
- Abel G (2012) Migest: useful R code for the estimation of migration. The CRAN Project. Retrieved Jan 2018Google Scholar
- Babbucci M, Buccoli S, Cau A, Cannas R, Goñi R, Díaz D, Marcato S, Zane L, Patarnello T (2010) Population structure, demographic history, and selective processes: contrasting evidences from mitochondrial and nuclear markers in the European spiny lobster Palinurus elephas (Fabricius, 1787). Mol Phylogenet Evol 56:1040–1050PubMedCrossRefPubMedCentralGoogle Scholar
- Berry PF (1978) Reproduction, growth and production in the mussel Perna perna (Linnaeus) on the east coast of South Africa. Investigational Report No. 48. Durban, South Africa: Oceanographic Research InstituteGoogle Scholar
- Berry PF, Heydorn AEF (1970) A comparison of the spermatophoric masses and mechanisms of fertilization in Southern African spiny lobsters (Palinuridae). Investigational Report No. 25. Durban, South Africa: Oceanographic Research InstituteGoogle Scholar
- Dao HT, Smith-Keune C, Wolanski E, Jones CM, Jerry DR, Suzuki N (2015) Oceanographic currents and local ecological knowledge indicate, and genetics does not refute, a contemporary pattern of larval dispersal for the ornate spiny lobster, Panulirus ornatus in the South-East Asian Archipelago. PLoS One. https://doi.org/10.1371/journal.pone.0124568 CrossRefPubMedPubMedCentralGoogle Scholar
- Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome C oxidase subunit I from metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299Google Scholar
- Francis CM (2014) Systematics of the Laurencia complex (Rhodomelaceae, Rhodophyta) in southern Africa. PhD Thesis, Department of Biological Sciences, University of Cape Town, South Africa, xii + 199Google Scholar
- Hall T (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98Google Scholar
- Halo I, Malauene B, Ostrowski M (2017) Physical oceanography. In: Groeneveld JC, Koranteng KA (eds) The RV Dr Fridtjof Nansen in the Western Indian Ocean: voyages of marine research and capacity development. FAO, Rome, pp 37–50Google Scholar
- Lavery SD, Farhadi A, Farahmand H, Chan TY, Azhdehakoshpour A, Thakur V, Jeffs AG (2014) Evolutionary divergence of geographic subspecies within the scalloped spiny lobster Panulirus homarus (Linnaeus 1758). PLoS One. https://doi.org/10.1371/journal.pone.0097247 CrossRefPubMedPubMedCentralGoogle Scholar
- Lutjeharms JRE (2006) The agulhas current. Springer, Heidelberg, p 329Google Scholar
- Planes S, Jones GP, Thorrold SR (2009) Larval dispersal connects fish populations in a network of marine protected areas. Proc Natl Acad Sci 106:5693–5697Google Scholar
- Pollock DE (1990) Palaeoceanography and speciation in the spiny lobster genus Jasus. Bull Mar Sci 46:387–405Google Scholar
- Pollock DE (1992) Palaeoceanography and speciation in the spiny lobster genus Panulirus in the Indo-Pacific. Bull Mar Sci 51:135–146Google Scholar
- Pritchard JK, Wen X, Falush D (2009) Documentation for structure software: Version 2.3Google Scholar
- R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/
- Rambaut A, Drummond AJ (2007) Tracer v. 1.6. http://tree.bio.ed.ac.uk/software/tracer/
- Randall JE, King DR (2009) Parupeneus fraserorum, a new species of goatfish (Perciformes: Mullidae) from South Africa and Madagascar. Smithiana Bull 10:31–35Google Scholar
- Senevirathna JDM, Munasinghe DHN, Mather PB (2016) Assessment of genetic structure in wild populations of Panulirus homarus (Linnaeus, 1758) across the South Coast of Sri Lanka inferred from mitochondrial DNA sequences. Int J Mar Sci 6:1–9Google Scholar
- Singh SP, Groeneveld JC, Hart-Davis MG, Backeberg BC, Willows-Munro S (2018) Seascape genetics of the spiny lobster Panulirus homarus in the Western Indian Ocean: understanding how oceanographic features shape the genetic structure of species with high larval dispersal potential. Ecol Evol 8:12221–12237. https://doi.org/10.1002/ece3.4684 CrossRefPubMedPubMedCentralGoogle Scholar
- 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 8:341PubMedPubMedCentralCrossRefGoogle Scholar
- Tsang LM, Achituv Y, Chu KH, Chan BKK (2012) Zoogeography of intertidal communities in the West Indian Ocean as determined by ocean circulation systems: patterns from the Tetraclita barnacles. PLoS One 7(9):e45120. https://doi.org/10.1371/journal.pone.0045120 CrossRefPubMedPubMedCentralGoogle Scholar
- Waples RS (1991) Genetic methods for estimating the effective size of cetacean populations. Rep Int Whal Comm Spec Issue 13:279–300Google Scholar
- Wickham H, Francois R (2015) Dplyr: a grammar of data manipulation. R Package Version 0.4.3. http://CRAN.R-project.org/package=dplyr
- Yellapu B, Jeffs A, Battaglene S, Lavery SD (2016) Population subdivision in the tropical spiny lobster Panulirus ornatus throughout its Indo-West Pacific distribution. ICES J Mar Sci 74:759–768Google Scholar