Abstract
Five polymorphic microsatellite loci were developed and then used to assess the population genetic structure of a commercially harvested merobenthic octopus species (Octopus maorum) in south-east Australian and New Zealand (NZ) waters. Beak and stylet morphometrics were also used to assess population differentiation in conjunction with the genetic data. Genetic variation across all loci and all sampled populations was very high (mean number alleles = 15, mean expected heterozygosity = 0.85). Microsatellites revealed significant genetic structuring (overall FST = 0.024, p < 0.001), which did not fit an isolation-by-distance model of population differentiation. Divergence was observed between Australian and NZ populations, between South Australia and north-east Tasmania, and between two relatively proximate Tasmanian sites. South Australian and southern Tasmanian populations were genetically homogeneous, indicating a level of connectivity on a scale of 1,500 km. Morphometric data also indicated significant differences between Australian and NZ populations. The patterns of population structuring identified can be explained largely in relation to regional oceanographic features.
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References
Avise JC (2004) Molecular markers, natural history and evolution. Sinauer Associates Publishers, Massachusetts
Banks SC, Piggott MP, Williamson JE, Bové U, Holbrook NJ, Beheregaray LB (2007) Oceanic variability and coastal topography shape genetic structure in a long-dispersing sea urchin. Ecology 88:3055–3064. doi:https://doi.org/10.1890/07-0091.1
Bradbury IR, Snelgrove PVR (2001) Contrasting larval transport in demersal fish and benthic invertebrates: the roles of behaviour and advective processes in determining spatial pattern. Can J Fish Aquat Sci 58:811–823. doi:https://doi.org/10.1139/cjfas-58-4-811
Brierley AS, Thorpe JP, Pierce GJ, Clarke MR, Boyle PR (1995) Genetic variation in the neritic squid Loligo forbesi (Myopsida: Loliginidae) in the northeast Atlantic Ocean. Mar Biol (Berl) 122:79–86. doi:https://doi.org/10.1007/BF00349280
Bruce B, Griffin D, Bradford R (2007) Larval transport and recruitment processes of southern rock lobster. CSIRO Marine and Atmospheric Research, Hobart
Buresch KM, Gerlach G, Hanlon RT (2006) Multiple genetic stocks of longfin squid Loligo pealeii in the NW Atlantic: stocks segregate inshore in summer, but aggregate offshore in winter. Mar Ecol Prog Ser 310:263–270. doi:https://doi.org/10.3354/meps310263
Cabranes C, Fernandez-Rueda P, Martínez JL (2008) Genetic structure of Octopus vulgaris around the Iberian Peninsula and Canary Islands as indicated by microsatellite DNA variation. ICES J Mar Sci 65:12–16. doi:https://doi.org/10.1093/icesjms/fsm178
Carvalho GR, Hauser L (1994) Molecular genetics and the stock concept in fisheries. Rev Fish Biol Fish 4:326–350. doi:https://doi.org/10.1007/BF00042908
Casu M, Maltagliati F, Meloni M, Casu D, Cossu P, Binelli G, Curini-Galletti M, Castelli A (2002) Genetic structure of Octopus vulgaris (Mollusca, Cephalopoda) from the Mediterranean Sea as revealed by a microsatellite locus. Ital J Zool (Modena) 69:295–300. doi:https://doi.org/10.1080/11250000209356472
Chapuis M, Estoup A (2007) Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol 24:621–631. doi:https://doi.org/10.1093/molbev/msl191
Crawford CM, Edgar GJ, Cresswell G (2000) The Tasmanian region. In: Shepard C, Zann LP (eds) Seas at the millennium. Elsevier, Netherlands, pp 647–660
Cresswell G (2000) Currents of the continental shelf and upper slope of Tasmania. Papers and Proceedings of the Royal Society of Tasmania 133: 21-30
Dillane E, Galvin P, Coughlan J, Lipinski MR, Cross TF (2005) Genetic variation in the lesser flying squid Todaropsis eblanae (Cephalopoda, Ommastrephidae) in east Atlantic and Mediterranean waters. Mar Ecol Prog Ser 292:225–232. doi:https://doi.org/10.3354/meps292225
Doubleday ZA, Pecl GT, Semmens JM, Danyushevsky L (2008) Using stylet elemental signatures to determine the population structure of Octopus maorum. Mar Ecol Prog Ser 360:125–133. doi:https://doi.org/10.3354/meps07389
Goudet J (1995) Fstat (version 1.2): a computer program to calculate F-statistics. J Hered 86:485–486
Greatorex EC, Jones CS, Murphy J, Key LN, Emery AM, Boyle PR (2000) Microsatellite markers for investigating population structure in Octopus vulgaris (Mollusca: cephalopoda). Mol Ecol 9:641–642. doi:https://doi.org/10.1046/j.1365-294x.2000.00882-7.x
Grewe PM, Smolenski AJ, Ward RD (1994) Mitochondrial DNA diversity in Jackass Morwong (Nemadactylus macropterus: Teleostei) from Australian and New Zealand waters. Can J Fish Aquat Sci 51:1101–1109. doi:https://doi.org/10.1139/f94-109
Hauser L, Adcock GJ, Smith PJ, Bernal Ramirez JH, Carvalho GR (2002) Loss of microsatellite diversity and low effective population size in an overexploited population of New Zealand snapper (Pagrus auratus). Proc Natl Acad Sci USA 99:11742–11747. doi:https://doi.org/10.1073/pnas.172242899
Hermosilla C (2004) Morphological and genetic variation between populations of red octopus Enteroctopus megalocyathus (cephalopoda, octopoda) in southern Chile and Argentina Degree. School of Marine Biology, Santiago
Kassahn KS, Donnellan S, Fowler SW, Hall KC, Adams M, Shaw PW (2003) Molecular and morphological analyses of the cuttlefish Sepia apama indicate a complex population structure. Mar Biol (Berl) 143:947–962. doi:https://doi.org/10.1007/s00227-003-1141-5
Katsanevakis S, Verriopoulos G (2006) Modelling the effect of temperature on hatching and settlement patterns of meroplanktonic organisms: the case of the octopus. Sci Mar 70:699–708. doi:https://doi.org/10.3989/scimar.2006.70n4699
Kritzer JP, Sale PF (2004) Metapopulation ecology in the sea: from Levin’s model to marine ecology and fisheries science. Fish Fish 5:131–140. doi:https://doi.org/10.1111/j.1467-2979.2004.00131.x
Maltagliati F, Belcari P, Casu D, Casu M, Sator P, Vargiu G, Castelli A (2002) Allozyme genetic variability and gene flow in Octopus vulgaris (Cephalopoda, Octopodidae) from the Mediterranean Sea. Bull Mar Sci 71:437–486
Milton DA, Chenery SR (2001) Can otolith chemistry detect the population structure of the shad hilsa Tenualosa ilisha? Comparison with the results of genetic and morphological studies. Mar Ecol Prog Ser 222:239–251. doi:https://doi.org/10.3354/meps222239
Murphy JM, Baguerias E, Key LN, Boyle PR (2002) Microsatellite DNA markers discriminate between two Octopus vulgaris (Cephalopoda: Octopoda) fisheries along the northwest African coast. Bull Mar Sci 71:545–553
Oosthuizen A, Jiwaji M, Shaw P (2004) Genetic analysis of the Octopus vulgaris population on the coast of South Africa. S Afr J Sci 100:603–607
Palumbi SR (1995) Using genetics as an indirect estimator of larval dispersal. In: McEdward L (ed) Ecology of marine invertebrate larvae. CRC Press, Boca Raton, pp 369–387
Palumbi SR (2004) Marine reserves and ocean neighbourhoods: the spatial scale of marine populations and their management. Annu Rev Environ Resour 29:31–68. doi:https://doi.org/10.1146/annurev.energy.29.062403.102254
Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel, population genetic software for teaching and research. Mol Ecol Notes 6:288–295. doi:https://doi.org/10.1111/j.1471-8286.2005.01155.x
Perez-Losada M, Guerra A, Carvalho GR, Sanjuan A, Shaw PW (2002) Extensive population subdivision of the cuttlefish Sepia officinalis (Mollusca: Cephalopoda) around the Iberian Peninsula indicated by microsatellite DNA variation. Heredity 89:417–424. doi:https://doi.org/10.1038/sj.hdy.6800160
Pierce GJ, Thorpe JP, Hastie LC, Brierley AS, Guerra A, Boyle PR, Jamieson R, Avila P (1994) Geographic variation in Loligo forbesi in northeast Atlantic Ocean: analysis of morphometric data and tests of causal hypotheses. Mar Biol (Berl) 119:541–547. doi:https://doi.org/10.1007/BF00354316
Purcell JF, Cowen RK, Hughes CR, Williams DA (2006) Weak genetic structure indicates strong dispersal limits: a tale of two coral reef fish. Proc R Soc B Biol Sci 273:1483–1490
Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249
Reichow D, Smith MJ (2001) Microsatellites reveal high levels of gene flow among populations of the California squid Loligo opalescens. Mar Ecol (Berl) 10:1101–1109
Rice WR (1989) Analyzing tables of statistical significance. Evolution 43:223–225. doi:https://doi.org/10.2307/2409177
Ridgway KR (2004) The 5500-km-long boundary flow off western and southern Australia. J Geophys Res 109:C10016. doi:https://doi.org/10.1029/2003JC001921
Ridgway KR (2007) Seasonal circulation around Tasmania: an interface between eastern and western boundary dynamics. J Geophys Res 112:C04017. doi:https://doi.org/10.1029/2006JC003898
Rigby PR, Sakurai Y (2005) Multidimensional tracking of giant Pacific octopuses in northern Japan reveals unexpected foraging behaviour. Mar Technol Soc J 39:64–67
Rocha FJ, Vega MA (2003) Overview of cephalopod fisheries in Chilean waters. Fish Res 60:151–159. doi:https://doi.org/10.1016/S0165-7836(02)00080-2
Rozen S, Skaletsky HJ (2000) Primer3 on the WWW for general users and for biologist programmers. Humana Press, Totowa
Semmens JM, Pecl GT, Gillanders BM, Waluda CM, Shea EK, Jouffre D, Ichii T, Zumholz K, Katugin OL, Leporati SC, Shaw PW (2007) Approaches to resolving cephalopod movement and migration patterns. Rev Fish Biol Fish 17:401–423. doi:https://doi.org/10.1007/s11160-007-9048-8
Shaw PW, Pierce GJ, Boyle PR (1999) Subtle population structuring within a highly vagile marine invertebrate, the veined squid Loligo forbesi, demonstrated with microsatellite DNA markers. Mol Ecol 8:407–417. doi:https://doi.org/10.1046/j.1365-294X.1999.00588.x
Shaw PW, Arkhipkin AI, Adcock GJ, Burnett WJ, Carvalho GR, Scherbich JN, Villegas PA (2004) DNA markers indicate that distinct spawning cohorts and aggregations of Patagonian squid, Loligo gahi, do not represent genetically discrete subpopulations. Mar Biol (Berl) 144:961–970. doi:https://doi.org/10.1007/s00227-003-1260-z
Stranks TN (1996) Biogeography of Octopus species (Cephalopoda: Octopodidae) from southeastern Australia. Am Malacol Bull 12:145–151
Swain D, Foote C (1999) Stocks and chameleons: the use of phenotypic variation in stock identification. Fish Res 43:113–128. doi:https://doi.org/10.1016/S0165-7836(99)00069-7
Thorpe JP, Sole-Cava AM, Watts PC (2000) Exploited marine invertebrates: genetics and fisheries. Hydrobiologia 420:165–184. doi:https://doi.org/10.1023/A:1003987117508
Tracey SR, Smolenski A, Lyle JM (2007) Genetic structuring of Latris lineata at localized and transoceanic scales. Mar Biol (Berl) 152:119–128. doi:https://doi.org/10.1007/s00227-007-0666-4
Triantafillos L, Jackson GD, Adams M, McGrath Steer BL (2004) An allozyme investigation of the stock structure of arrow squid Nototodarus gouldi (Cephalopoda: Ommastrephidae) from Australia. ICES J Mar Sci 61:829–835. doi:https://doi.org/10.1016/j.icesjms.2003.12.010
Truett GE, Heeger P, Mynatt RL, Truett AA, Walker JA, Warman ML (2000) Preparation of PCR-quality mouse genomic DNA with hot sodium and Tris (HotSHOT). Biotechniques 29:52–54
Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538. doi:https://doi.org/10.1111/j.1471-8286.2004.00684.x
Vega MA, Rocha FJ, Guerra A, Osorio C (2002) Morphological differences between the Patagonian squid Loligo gahi populations from the Pacific and Atlantic oceans. Bull Mar Sci 71:903–913
Villanueva R (1995) Experimental rearing and growth of planktonic Octopus vulgaris from hatching to settlement. Can J Fish Aquat Sci 52:2639–2650. doi:https://doi.org/10.1139/f95-853
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 15:1419–1439. doi:https://doi.org/10.1111/j.1365-294X.2006.02890.x
Waters JM (2008) Marine biogeographical disjunction in temperate Australia: historical landbridge, contemporary currents, or both? Divers Distrib 14:692–700. doi:https://doi.org/10.1111/j.1472-4642.2008.00481.x
Weetman D, Hauser L, Bayes MK, Ellis JR, Shaw PW (2006) Genetic population structure across a range of geographic scales in the commercially exploited marine gastropod Buccinum undatum. Mar Ecol Prog Ser 317:157–169. doi:https://doi.org/10.3354/meps317157
Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370. doi:https://doi.org/10.2307/2408641
Wolfram K, Mark FC, Uwe J, Lucassen M, Pörtner HO (2006) Microsatellite DNA variation indicates low levels of genetic differentiation among cuttlefish (Sepia officinalis L.) populations in the English Channel and the Bay of Biscay. Comp Biochem Physiol D 1:375–383
Zane L, Bargelloni L, Patarnello T (2002) Strategies for microsatellite isolation: a review. Mol Ecol 11:1–16. doi:https://doi.org/10.1046/j.0962-1083.2001.01418.x
Acknowledgments
We thank J. Ricketts, N. Perryman, W. Beven, W. Combe, D. Palmer, Moana Pacific Fisheries, South Pacific Fisheries, Burkhart Fisheries, and Austar Fisheries for the collection of octopuses in Tasmania, NZ and SA, and M. Oliver (National Institute of Water and Atmospheric Research, NIWA) and D. Sykes (NZ Rock Lobster Industry Council) for overseeing the collection and storage of octopuses in NZ. We also thank Ben Smethurst for all his assistance with the DNA extractions. This study was supported by Holsworth Wildlife Research Endowment, Department of Primary Industries and Water (Tasmania), Winifred Violet Scott Estate grant, and Unitas Malacologica.
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Communicated by S. Uthicke.
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Doubleday, Z.A., Semmens, J.M., Smolenski, A.J. et al. Microsatellite DNA markers and morphometrics reveal a complex population structure in a merobenthic octopus species (Octopus maorum) in south-east Australia and New Zealand. Mar Biol 156, 1183–1192 (2009). https://doi.org/10.1007/s00227-009-1160-y
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DOI: https://doi.org/10.1007/s00227-009-1160-y