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Implications of life history for genetic structure and migration rates of southern African coastal invertebrates: planktonic, abbreviated and direct development

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Abstract

The amount of genetic structure in marine invertebrates is often thought to be negatively correlated with larval duration. However, larval retention may increase genetic structure in species with long-lived planktonic larvae, and rafting provides a means of dispersal for species that lack a larval dispersal phase. We compared genetic structure, demographic histories and levels of gene flow of regional lineages (in most cases defined by biogeographic region) of five southern African coastal invertebrates with three main types of larval development: (1) dispersal by long-lived planktonic larvae (mudprawn Upogebia africana and brown mussel Perna perna), (2) abbreviated larval development (crown crab Hymenosoma orbiculare) and (3) direct development (estuarine isopod Exosphaeroma hylecoetes and estuarine cumacean Iphinoe truncata). We hypothesized that H. orbiculare, having abbreviated larval development, would employ a strategy of larval retention, resulting in genetic structure comparable to that of the direct developers rather than the planktonic dispersers. However, regional population structure was significantly lower in all species with planktonic larvae, including H. orbiculare, than in the direct developers. Moreover, nested clade analysis identified demographic histories resulting from low levels of gene flow (isolation by distance and allopatric fragmentation) in the direct developers only, and migration rates were significantly higher in all three species having planktonic larvae than in the direct developers. We conclude that the amount of genetic structure within marine biogeographic regions strongly depends on the presence or absence of free-swimming larvae. Whether such larvae are primarily exported or retained, whether they have long or short larval duration, and whether or not they are capable of active dispersal seems to have little effect on connectivity among populations.

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References

  • Anger K (2001) The biology of decapod crustacean larvae. In: Vonk R (ed) Crustacean issues, vol. 14. AA Balkema, Tokyo, pp 263–318

    Google Scholar 

  • Audzijonyte A, Dabneliya ME, Väinölä R (2006) Comparative phylogeography of Ponto-Caspian mysid crustaceans: isolation and exchange among dynamic inland sea basis. Mol Ecol 15:2969–2984

    Article  CAS  PubMed  Google Scholar 

  • Barber PH, Palumbi SR, Erdmann MV, Moosa MK (2000) Biogeography—a marine Wallace’s line? Nature 406:692

    Article  CAS  PubMed  Google Scholar 

  • Bayne BL (1965) Growth and the delay of metamorphosis of the larvae of Mytilus edulis L. (Mollusca) Ophelia 2:1–47

    Article  Google Scholar 

  • Boström C, Mattila J (1999) The relative importance of food and shelter for seagrass-associated invertebrates: a latitudinal comparison of habitat choice by isopod grazers. Oecologia 120:162–170

    Article  PubMed  Google Scholar 

  • Broekhuysen GJ (1955) The breeding and growth of Hymenosoma orbiculare Desm. Ann S Afr Mus 41: 313–343

    Google Scholar 

  • Caley MJ, Carr MH, Hixon MA, Hughes TP, Jones GP, Menge BA (1996) Recruitment and the local dynamics of open marine populations. Ann Rev Ecol Syst 27:477–500

    Article  Google Scholar 

  • Castelloe J, Templeton AR (1994) Root probabilities for intraspecific gene trees under neutral coalescent theory. Mol Phylogen Evol 3:102–113

    Article  CAS  Google Scholar 

  • Cavalcanti MJ (2005) MANTEL for Windows version 1.16—test for association between two symmetric distance matrices with permuation iterations. Departemento de Vertebrados, Museum Nacional de Rio de Janeiro, Brasil. Software available at http://www.life.bio.sunysb.edu/morph/

  • Clement M, Posada D, Crandall KA (2000) tcs: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1660

    Article  CAS  PubMed  Google Scholar 

  • Crandall KA, Templeton AR (1993) Empirical tests of some predictions from coalescent theory with applications to intraspecific phylogeny reconstruction. Genetics 134:959–969

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dornelas M, Paula J, Macia A (2003) The larval development of Hymenosoma orbiculare Desmarest, 1825 (Crustacea: Decapoda: Brachyura: Hymenosomatidae). J Nat Hist 37:2579–2597

    Article  Google Scholar 

  • Eckert GL (2003) Effects of the planktonic period on marine population fluctuations. Ecology 84:372–383

    Article  Google Scholar 

  • Edkins MT, Teske PR, Papaopoulos I, Griffiths CL (2007) Morphological and genetic analyses suggest that southern African crown crabs, Hymenosoma orbiculare, represent five distinct species. Crustaceana (In press)

  • Edmands S (2001) Phylogeography of the intertidal copepod Tigriopus californicus reveals substantially reduced population differentiation at northern latitudes. Mol Ecol 10:1743–1750

    Article  CAS  PubMed  Google Scholar 

  • Evans PR, Ward RM, Bone M, Leakey M (1998) Creation of temperate-climate intertidal mudflats: factors affecting colonization and use by benthic invertebrates and their bird predators. Mar Poll Bull 37:535–545

    Article  CAS  Google Scholar 

  • Evans BP, 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

    Article  Google Scholar 

  • Excoffier L, Laval G, Schneider S (2005) arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50

    Article  CAS  Google Scholar 

  • 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 Biotech 3:294–299

    CAS  Google Scholar 

  • Gore RH (1985) Molting and growth in decapod larvae. In: Wenner AM (eds) Crustacean issues 2: larval growth. Balkema, Rotterdam, pp 1–65

    Google Scholar 

  • Guinot D, Richer de Forges B (1997) Affinités entre les Hymenosomatidae MacLeay, 1838 et les Inachoididae Dana, 1851 (Crustacea, Decapoda, Brachyura). Zoosystema 19:453–502

    Google Scholar 

  • Harding RM (1996) New phylogenies: an introductory look at the coalescent. In: Harvey PH et al. (eds) New uses for new phylogenies. Oxford University Press, New York, pp 15–22

    Google Scholar 

  • Hasegawa M, Kishino K, Yano T (1985) Dating the human–ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 22:160–174

    Article  CAS  PubMed  Google Scholar 

  • Hellberg ME (1994) Relationships between inferred levels of gene flow and geographic distance in a philopatric coral, Balanophyllia elegans. Evolution 48:1829–1854

    Article  PubMed  Google Scholar 

  • Hellberg ME, Burton RS, Neigel JE, Palumbi SR (2002) Genetic assessment of connectivity among marine populations. Bull Mar Sci 70:S273–S290

    Google Scholar 

  • Hey J, Nielsen R (2004) Multilocus methods for estimating population sizes, migration rates and divergence time, with applications to the divergence of Drosophila pseudoobscura and D. persimilis. Genetics 167:747–760

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hicks DW, Tunnell JW Jr (1995) Ecological notes and patterns of dispersal in the recently introduced mussel, Perna perna (Linne, 1758), in the Gulf of Mexico. Am Malacol Bull 11:203–206

    Google Scholar 

  • Hindell JS, Jenkins GP, Keough MJ (2000) Evaluating the impact of predation by fish on the assemblage structure of fishes associated with seagrass (Heterozostera tasmanica) (Martens ex Ascherson) den Hartog, and unvegetated sand habitats. J Exp Mar Biol Ecol 255:153–174

    Article  CAS  PubMed  Google Scholar 

  • Hood GM (2004) poptools 2.6.2. Available online at http://www.cse.csiro.au/poptools

  • Hudson RR (1990) Gene genealogies and the coalescent process. Oxf Surv Evol Biol 7:1–44

    Google Scholar 

  • Jiang L, Wu WL, Huang PC 1995. The mitochondrial DNA of Taiwan abalone Haliotis diversicolor Reeve, 1846 (Gastropoda: Archaeogastropoda: Haliotidae). Mol Mar Biol Biotech 4:353–364

    CAS  Google Scholar 

  • Johannesson K 1988. The paradox of Rockall: why is a brooding gastropod (Littorina saxatilis) more widespread than one having a planktonic larval dispersal stage (L. littorea)? Mar Biol 99:507–513

    Article  Google Scholar 

  • Kingman JFC (1982) The coalescent. Stochastic Process Appl 13:235–248

    Article  Google Scholar 

  • Kinlan BP, Gaines SD (2003) Propagule dispersal in marine and terrestrial environments: a community perspective. Ecology 84:2007–2020

    Article  Google Scholar 

  • Levin LA, Bridges TS (1995) Pattern and diversity in reproduction and development. In: McEdward L (eds) Ecology of marine invertebrate larvae. CRC Press, Boca Raton pp 1–48

    Google Scholar 

  • Lewontin RC (1974) The genetic basis of evolutionary change. Columbia University Press, NY

    Google Scholar 

  • Lockyear JF, Hecht T, Kaiser H, Teske PR (2006) The distribution and abundance of the endangered Knysna seahorse, Hippocampus capensis (Pisces: Syngnathidae), in South African estuaries. Afr J Aquati Sci 31:275–283

    Article  Google Scholar 

  • Marko PB (1998) Historical allopatry and the biogeography of speciation in the prosobranch snail genus Nucella. Evolution 52:757–774

    Article  PubMed  Google Scholar 

  • McQuaid CD, Phillips TE (2000) Limited wind-driven dispersal of the intertidal mussel larvae: in situ evidence from the plankton and the spread of the invasive species Mytilus galloprovincialis in South Africa. Mar Ecol Prog Ser 201:211–220

    Article  Google Scholar 

  • Mills LS, Allendorf FW (1996) The one-migrant-per-generation rule in conservation and management. Conserv Biol 10:1509–1518

    Article  Google Scholar 

  • Morgan SG (1995) The timing of larval release. In: McEdward L (eds) Ecology of marine invertebrate larvae. CRC Press, Boca Raton, pp 157–191

    Google Scholar 

  • Moy LD, Levin LA (1991) Are Spartina marshes a replaceable resource? A functional approach to evaluation of marsh creation efforts. Estuaries 14:1–16

    Article  Google Scholar 

  • Newman BK, Papadopoulos I, Vorsatz J, Wooldridge TH (2006) Influence of temperature on the larval development of Upogebia africana and Upogebia capensis (Decapoda: Thalassinidea: Upogebiidae) in the laboratory. Mar Ecol Prog Ser 325:165–180

    Article  Google Scholar 

  • Palmer AR, Strathmann RR (1981) Scale of dispersal in varying environments and its implications for life histories of marine invertebrates. Oecologia 48:308–318

    Article  CAS  PubMed  Google Scholar 

  • Palumbi SR (1994) Genetic divergence, reproductive isolation and marine speciation. Annu Rev Ecol Syst 25:547–572

    Article  Google Scholar 

  • Palumbi SR (2003) Population genetics, demographic connectivity, and the design of marine reserves. Ecol Appl 13:S146–S158

    Article  Google Scholar 

  • Papadopoulos I, Wooldridge TH, Newman BK (2002) Larval life history strategies of sub-tropical Southern African estuarine brachyuran crabs and implications for tidal inlet management. Wetlands Ecol Management 10:249–256

    Article  Google Scholar 

  • Papadopoulos I, Newman BK, Schoeman DS, Wooldridge TH (2006) Influence of salinity and temperature on the larval development of the crown crab, Hymenosoma orbiculare (Crustacea, Brachyura, Hymenosomatidae). Afr J Aquat Sci 31:43–52

    Article  Google Scholar 

  • Paula J, Mendes RN, Paci S, McLaughlin P, Gherardi F, Emmerson W (2001) Combined effects of temperature and salinity on the larval development of the estuarine mud prawn Upogebia africana (Crustacea, Thalassinidea). Hydrobiologia 449:141–148

    Article  Google Scholar 

  • Paulay G, Meyer C (2002) Diversification in the tropical Pacific: comparisons between marine and terrestrial systems and the importance of founder speciation. Integr Comp Biol 42:922–934

    Article  PubMed  Google Scholar 

  • Perissinotto R, Nozias C, Kibirige I (2002) Spatio-temporal dynamics of phytoplankton and microphytobenthos in a South African temporarily open/closed estuary. Estuar Coast Shelf Sci 55:47–58

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Rabalais NN, Gore RH (1985) Abbreviated development in decapods. In: Wenner AM (eds) Crustacean issues 2: larval growth. Balkema, Rotterdam, pp 67–126

    Google Scholar 

  • Ridgway TM, Stewart BA, Branch GM (1999) Morphological and genetic differentiation of Patella granularis (Gastropoda: Patellidae): recognition of two sibling species along the coast of southern Africa. J Zool London 245:317–333

    Article  Google Scholar 

  • Robertson AI (1984) Trophic interactions between the fish fauna and macrobenthos of an eelgrass community in Western Port, Australia. Aquat Bot 18:135–153

    Article  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbour Press, Plainview

    Google Scholar 

  • Scheltema RS (1975) Relationship of larval dispersal, gene-flow and natural selection to geographic variation of invertebrates in estuaries and along coastal regions. Estuar Res 1:372–391

    Google Scholar 

  • Shanks AL (1995) Mechanisms of cross-shelf dispersal of larval invertebrates and fish. In: McEdward L (ed) Ecology of marine invertebrate larvae. CRC Press, Boca Raton, pp 157–191

    Google Scholar 

  • Slatkin M (1985) Gene flow in natural populations. Ann Rev Ecol Syst 16:393–430

    Article  Google Scholar 

  • Sotka EE, Wares JP, Barth JA, Grosberg RK, Palumbi SR (2004) Strong genetic clines and geographical variation in gene flow in the rocky intertidal barnacle Balanus glandula. Mol Ecol 13:2143–2156

    Article  CAS  PubMed  Google Scholar 

  • Sponer R, Roy MS (2002) Phylogeographic analysis of the brooding brittle star Amphipholis squamata (Echinodermata) along the coast of New Zealand reveals high cryptic genetic variation and cryptic dispersal potential. Evolution 56:1954–1967

    Article  PubMed  Google Scholar 

  • Steele CA, Storfer A (2006) Coalescent-based hypothesis testing supports multiple Pleistocene refugia in the Pacific Northwest for the Pacific giant salamander (Dicamptodon tenebrosus). Mol Ecol 15:2477–2487

    Article  CAS  PubMed  Google Scholar 

  • Swearer SE, Caselle JE, Lea DW, Warner RR (1999) Larval retention and recruitment in an island population of a coral-reef fish. Nature 402:799

    Article  CAS  Google Scholar 

  • Swofford DL (2002) Paup*—phylogenetic analysis using parsimony (*and other methods), version 4.0b10. Sinauer Associates, Sunderland

    Google Scholar 

  • Taylor MS, Hellberg ME (2003) Genetic evidence for local retention of pelagic larvae in a Caribbean reef fish. Science 299:107

    Article  CAS  PubMed  Google Scholar 

  • Templeton AR (2004) Statistical phylogeography: methods of evaluating and minimizing inference errors. Mol Ecol 13:789–809

    Article  PubMed  Google Scholar 

  • Templeton AR, Boerwinkle C, Sing CF (1987) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping. I. Basic theory and analysis of Alcohol Dehydrogenase activity in Drosophila. Genetics 117:343–351

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 132:619–633

    CAS  PubMed  PubMed Central  Google Scholar 

  • Teske PR, Wooldridge T (2001) A comparison of the macrobenthic faunas of permanently open and temporarily open/closed South African estuaries. Hydrobiologia 464:227–243

    Article  Google Scholar 

  • Teske PR, Hamilton H, Palsboll PJ, Choo CK, Gabr H, Lourie SA, Santos M, Sreepada A, Cherry MI, Matthee CA (2005) Molecular evidence for long-distance colonization in an Indo-Pacific seahorse lineage. Mar Ecol Prog Ser 286:249–260

    Article  CAS  Google Scholar 

  • Teske PR, McQuaid CD, Froneman CD, Barker NP (2006) Impacts of marine biogeographic boundaries on phylogeographic patterns of three South African estuarine crustaceans. Mar Ecol Prog Ser 314:283–293

    Article  Google Scholar 

  • Valentine JW, Jablonski D (1986) Mass extinctions: sensitivity of marine larval types. Proc Nat Acad Sci USA 83:6912–6914

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 10:506–513

    CAS  PubMed  Google Scholar 

  • Wares JP, Cunningham CW (2001) Phylogeography and historical ecology of the North Atlantic Intertidal. Evolution 55:2455–2469

    Article  CAS  PubMed  Google Scholar 

  • Waters JM, Roy MS (2004) Out of Africa: the slow train to Australasia. Syst Biol 53:18–24

    Article  PubMed  Google Scholar 

  • Whitfield AK (2004) Estuarine databases in South Africa: available scientific information on individual South African estuarine systems. Available online at http://www.ru.ac.za/cerm/datab.html

  • Wooldridge TH (1991) Exchange of two species of decapod larvae across an estuarine mouth inlet and implications of anthropogenic changes in the frequency and duration of mouth closure. S Afr J Zool 87:519–525

    Google Scholar 

  • Wooldridge TH (1994) The effect of periodic inlet closure on recruitment in the estuarine mudprawn, Upogebia africana. In: Dyer KR, Orth RJ (eds) Changes in fluxes in estuaries: implications from science to management. Olsen & Olsen, Fredensborg, pp 329–333

    Google Scholar 

  • Wooldridge TH (1999) Estuarine zooplankton community structure and dynamics. In: Allanson BK, Baird D (eds) Estuaries of South Africa. Cambridge University Press, Cambridge, pp 141–166

    Chapter  Google Scholar 

  • Wooldridge TH, Callahan R (2000) The effects of a single freshwater release into the Kromme Estuary, 3: estuarine zooplankton response. Water SA, 26, 311–318

    CAS  Google Scholar 

  • Zardi GI, McQuaid CD, Teske PR, Barker NP (2007) Unexpected genetic structure of indigenous (Perna perna) and invasive (Mytilus galloprovincialis) mussel populations in South Africa. Mar Ecol Prog Ser 337:135–144

    Article  CAS  Google Scholar 

  • Zouros E, Ball AO, Saavedra C, Freeman KR (1994) Mitochondrial DNA inheritance. Nature 368:817–818

    Article  Google Scholar 

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Acknowledgements

This is a contribution from the African Coelacanth Ecosystem Programme/Agulhas & Somali Current Large Marine Ecosystems Project. We thank our field assistants Ingo Jastram, Georgia Schäfer and Zeen Weight. Three anonymous reviewers are gratefully acknowledged for useful comments on an earlier version of this manuscript. This study was supported by a postdoctoral research fellowship from the Claude Harris Leon Foundation awarded to PRT, the National Research Foundation (GUN 2069119), and Rhodes University.

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Teske, P.R., Papadopoulos, I., Zardi, G.I. et al. Implications of life history for genetic structure and migration rates of southern African coastal invertebrates: planktonic, abbreviated and direct development. Mar Biol 152, 697–711 (2007). https://doi.org/10.1007/s00227-007-0724-y

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