Skip to main content

Advertisement

Log in

Outlier SNPs detect weak regional structure against a background of genetic homogeneity in the Eastern Rock Lobster, Sagmariasus verreauxi

  • Original paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Genetic differentiation is characteristically weak in marine species making assessments of population connectivity and structure difficult. However, the advent of genomic methods has increased genetic resolution, enabling studies to detect weak, but significant population differentiation within marine species. With an increasing number of studies employing high resolution genome-wide techniques, we are realising that the connectivity of marine populations is often complex and quantifying this complexity can provide an understanding of the processes shaping marine species genetic structure and to inform long-term, sustainable management strategies. This study aims to assess the genetic structure, connectivity, and local adaptation of the Eastern Rock Lobster (Sagmariasus verreauxi), which has a maximum pelagic larval duration of 12 months and inhabits both subtropical and temperate environments. We used 645 neutral and 15 outlier SNPs to genotype lobsters collected from the only two known breeding populations and a third episodic population—encompassing S. verreauxi’s known range. Through examination of the neutral SNP panel, we detected genetic homogeneity across the three regions, which extended across the Tasman Sea encompassing both Australian and New Zealand populations. We discuss differences in neutral genetic signature of S. verreauxi and a closely related, co-distributed rock lobster, Jasus edwardsii, determining a regional pattern of genetic disparity between the species, which have largely similar life histories. Examination of the outlier SNP panel detected weak genetic differentiation between the three regions. Outlier SNPs showed promise in assigning individuals to their sampling origin and may prove useful as a management tool for species exhibiting genetic homogeneity.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Data accessibility

Reference loci sequences are available through Dryad, https://doi.org/10.5061/dryad.d4q57s5.

References

  • Adrian AJ, Lack CE, Kamel SJ (2017) Kin aggregations occur in eastern oyster Crassostrea virginica reefs despite limited regional genetic differentiation. Mar Ecol Prog Ser 584:79–90

    Google Scholar 

  • Allendorf FW (2017) Genetics and the conservation of natural populations: allozymes to genomes. Mol Ecol 26:420–430

    CAS  PubMed  Google Scholar 

  • Allendorf FW, Hohenlohe PA, Luikart G (2010) Genomics and the future of conservation genetics. Nat Rev Genet 11:697–709

    CAS  PubMed  Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    CAS  PubMed  Google Scholar 

  • Amor MD, Norman MD, Cameron HE, Strugnell JM (2014) Allopatric speciation within a cryptic species complex of Australasian octopuses. PLoS One 9:e98982

    PubMed  PubMed Central  Google Scholar 

  • Antao T, Lopes A, Lopes RJ, Beja-Pereira A, Luikart G (2008) LOSITAN: a workbench to detect molecular adaptation based on a Fst-outlier method. BMC Bioinformatics 9:323

    PubMed  PubMed Central  Google Scholar 

  • Araneda C, Larrain MA, Hecht B, Narum S (2016) Adaptive genetic variation distinguishes Chilean blue mussels (Mytilus chilensis) from different marine environments. Ecol Evol 6:3632–3644

    PubMed  PubMed Central  Google Scholar 

  • Babraham Bioinformatics (2007) FastQC. Babraham Institute. http://www.bioinformatics.babraham.ac.uk/projects/fastqc/

  • Baird NA, Etter PD, Atwood TS, Currey MC, Shiver AL, Lewis ZA, Selker EU, Cresko WA, Johnson EA (2008) Rapid SNP discovery and genetic mapping using sequenced RAD markers. PLoS One 3:1–7

    Google Scholar 

  • Banks SC, Ling SD, Johnson CR, Piggott MP, Williamson JE, Beheregaray LB (2010) Genetic structure of a recent climate change-driven range extension. Mol Ecol 19:2011–2024

    PubMed  Google Scholar 

  • Beaumont MA, Nichols RA (1996) Evaluating loci for use in the genetic analysis of population structure. Proc R Soc Lond 263:1619–1626

    Google Scholar 

  • Beerli P (1998) Estimation of migration rates and population sizes in geographically structured populations. In: Carvalgo G (ed) Advances in molecular ecology. IOS Press, Amsterdam, pp 39–53

    Google Scholar 

  • Beerli P, Felsenstein J (1999) Maximum-likelihood estimation of migration rates and effective population numbers in two populations using a coalescent approach. Genetics 152:763–773

    CAS  PubMed  PubMed Central  Google Scholar 

  • Beerli P, Felsenstein J (2001) Maximum-likelihood estimation of a migration matrix and effective population sizes in n subpopulations by using a coalescent approach. Proc Natl A Sci 98:4563–4568

    CAS  Google Scholar 

  • Benestan L, Gosselin T, Perrier C, Sainte-Marie B, Rochette R, Bernatchez L (2015) RAD genotyping reveals fine-scale genetic structuring and provides powerful population assignment in a widely distributed marine species, the American lobster (Homarus americanus). Mol Ecol 24:3299–3315

    PubMed  Google Scholar 

  • Bernatchez L, Wellenreuther M, Araneda C, Ashton DT, Barth JMI, Beacham TD, Maes GE, Martinsohn JT, Miller KM, Naish KA, Ovenden JR, Primmer GR, Suk HY, Therkildsen NO, Withler RE (2017) Harnessing the power of genomics to secure the future of seafood. Trends Ecol Evol 32:665–680

    PubMed  Google Scholar 

  • Bierne N, Welch J, Loire E, Bonhomme F, David P (2011) The coupling hypothesis: why genome scans may fail to map local adaptation genes. Mol Ecol 20:2044–2072

    PubMed  Google Scholar 

  • Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120

    CAS  PubMed  PubMed Central  Google Scholar 

  • Booth J (1979) North Cape—a ‘nursery area’ for the packhorse rock lobster, Jasus verreauxi (Decapoda: Palinuridae). New Zeal J Mar Fresh 13:521–528

    Google Scholar 

  • Booth J (1984) Size at onset of breeding in female Jasus verreauxi (Decapoda: Palinuridae) in New Zealand. New Zeal J Mar Fresh 18:159–169

    Google Scholar 

  • Booth J (1986) Recruitment of packhorse rock lobster Jasus verreauxi in New Zealand. Can J Fish Aquat Sci 43:2212–2220

    Google Scholar 

  • Booth J (2006) Jasus species. In: Phillips B (ed) Lobsters biology, management, aquaculture and fisheries. Blackwell Scientific Publications, Oxford, pp 340–358

    Google Scholar 

  • Booth J, Breen P (1994) The New Zealand fishery for Jasus edwardsii and J. verreauxi. In: Phillips B, Cobb J, Kittaka J (eds) Spiny Lobster Management. Blackwell Scientific Publications, Oxford, pp 64–75

    Google Scholar 

  • Booth J, Phillips B (1994) Early life history of spiny lobster. Crustaceana 66:271–294

    Google Scholar 

  • Booth JD, Stewart RA (1992) Distribution of phyllosoma larvae of the red rock lobster Jasus edwardsii off the east coast of New Zealand in relation to the oceanography. Larval Biol Proc 15:138–148

    Google Scholar 

  • Bowcock AM, Ruiz-Linares A, Tomfohrde J, Minch E, Kidd JR, Cavalli-Sforaz LL (1994) High resolution of human evolutionary trees with polymorphic microsatellites. Nature 368:455–457

    CAS  PubMed  Google Scholar 

  • Bradford R, Bruce B, Chiswell S, Booth J, Jeffs A, Wotherspoon S (2005) Vertical distribution and diurnal migration patterns of Jasus edwardsii phyllosomas off the east coast of the North Island, New Zealand. New Zeal J Mar Fresh 39:593–604

    Google Scholar 

  • Brasher DJ, Ovenden JR, Booth JD, White RWG (1992) Genetic subdivision of Australian and New Zealand populations of Jasus verreauxi (Decapoda: Palinuridae)—preliminary evidence from the mitochondrial genome. New Zeal J Mar Fresh 26:53–58

    Google Scholar 

  • Cai W, Shi G, Cowan T, Bi D, Ribbe J (2005) The response of the Southern Annular Mode, the East Australian Current, and the southern mid-latitude ocean circulation to global warming. Geophys Res Lett 32:L23706

    Google Scholar 

  • Catchen JM, Amores A, Hohenlohe P, Cresko W, Postlethwait JH (2011) Stacks: building and genotyping loci de novo from short-read sequences. G3 Genes Genomes Genet 1:171–182

    CAS  Google Scholar 

  • Caujapé-Castells J (2010) General GST and θ inflation due to biased intra-population sampling, and its consequences for the conservation of the Canarian Flora. Conserv Genet 11:709–720

    Google Scholar 

  • Chiswell S, Wilkin J, Booth JD, Stanton B (2003) Trans-Tasman Sea larval transport: is Australia a source for New Zealand rock lobsters? Mar Ecol Prog Ser 247:173–182

    Google Scholar 

  • Danecek P, Auton A, Abecasis G, Albers CA, Banks E, DePristo MA, Handsaker RE, Lunter G, Marth GT, Sherry ST, McVean G, Durbin R (2011) The variant call format and VCFtools. Bioinformatics 27:2156–2158

    CAS  PubMed  PubMed Central  Google Scholar 

  • Doyle SR, Griffith IS, Murphy NP, Strugnell JM (2015) Low-coverage MiSeq next generation sequencing reveals the mitochondrial genome of the eastern rock lobster, Sagmariasus verreauxi. Mitochondrial DNA 1736:1–2

    Google Scholar 

  • Earl DA, vonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361

    Google Scholar 

  • Estoup A, Garnery L, Solignac M, Cornuet JM (1995) Microsatellite variation in Honey Bee (Apis Mellifera L.) populations: hierarchical genetic structure and test of the infinite allele and stepwise mutation models. Genetics 140:679–695

    CAS  PubMed  PubMed Central  Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620

    CAS  PubMed  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

    CAS  Google Scholar 

  • Excoffier L, Hofer T, Foll M (2009) Detecting loci under selection in a hierarchically structured population. Heredity 103:285–298

    CAS  PubMed  Google Scholar 

  • Freamo H, O’Reilly P, Berg PR, Lien S, Boulding EG (2011) Outlier SNPs show more genetic structure between two Bay of Fundy metapopulations of Atlantic salmon than do neutral SNPs. Mol Ecol Resour 11:254–267

    PubMed  Google Scholar 

  • Gagnaire PA, Normandeau E, Côté C, Hansen MM, Bernatchez L (2012) The genetic consequences of spatially varying selection in the panmictic american eel (Anguilla rostrata). Genetics 190:725–736

    PubMed  PubMed Central  Google Scholar 

  • Gardener C, Bruce B, Montgomery S, Liggins G, Cawthorn A, Ibbott S (2000) Influx of Jasus verreauxi pueruli into Tasmania. Lobster Newsl 13:8–9

    Google Scholar 

  • George RW (1997) Tectonic plate movements and the evolution of Jasus and Panulirus spiny lobsters (Palinuridae). Mar Freshwater Res 48:1121–1130

    Google Scholar 

  • George RW (2005) Evolution of life cycles, including migration, in spiny lobsters (Palinuridae). New Zeal J Mar Fresh 39:503–514

    Google Scholar 

  • Gleason LU, Burton RS (2016) Genomic evidence for ecological divergence against a background of population homogeneity in the marine snail Chlorostoma funebralis. Mol Ecol 25:3557–3573

    PubMed  Google Scholar 

  • Goudet J (1995) FSTAT (Version 1.2): a computer program to calculate F-statistics. J Hered 86:485–486

    Google Scholar 

  • Green BS, Gardner C, Kennedy RB (2009) Generalised linear modelling of fecundity at length in southern rock lobsters, Jasus edwardsii. Mar Biol 156:1941–1947

    Google Scholar 

  • Hastings A (1993) Complex interactions between dispersal and dynamics: lessons from coupled logistic equations. Ecology 74:1362–1372

    Google Scholar 

  • Hauser L, Carvalho GR (2008) Paradigm shifts in marine fisheries genetics: ugly hypotheses slain by beautiful facts. Fish Fish 9:333–362

    Google Scholar 

  • Holland LP, Jenkins TL, Stevens JR (2017) Contrasting patterns of population structure and gene flow facilitate exploration of connectivity in two widely distributed temperate octocorals. Heredity 119:35–48

    CAS  PubMed  PubMed Central  Google Scholar 

  • Horne JB, Van Herwerden L (2013) Long-term panmixia in a cosmopolitan Indo-Pacific coral reef fish and a nebulous genetic boundary with its broadly sympatric sister species. J Evol Biol 26:783–799

    CAS  PubMed  Google Scholar 

  • Jasonowicz AJ, Goetz FW, Goetz GW, Nichols KM (2017) Love the one you’re with: genomic evidence of panmixia in the sablefish (Anoplopoma fimbria). Can J Fish Aquat Sci 74:377–387

    CAS  Google Scholar 

  • Johnson CR, Banks SC, Barrett NS, Cazassus F, Dunstan PK, Edgar GJ, Frusher SD, Gardner C, Haddon M, Helidoniotis F, Hill KL, Holbrook NJ, Hosie GW, Last PR, Ling SD, Melbourne-Thomas J, Miller K, Pecl GT, Richardson AJ, Ridgway KR, Rintoul SR, Ritz DA, Ross DJ, Sanderson JC, Shepard SA, Slotwinski A, Swadling KM, Taw N (2011) Climate change cascades: shifts in oceanography, species’ ranges and subtidal marine community dynamics in eastern Tasmania. J Exp Mar Bio Ecol 400:17–32

    Google Scholar 

  • Jombart T (2008) adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405

    CAS  PubMed  Google Scholar 

  • Jombart T, Devillard S, Balloux F (2010) Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genet 11:94

    PubMed  PubMed Central  Google Scholar 

  • Keenan K, McGinnity P, Cross TF, Crozier WW, Prodöhl PA (2013) diveRsity: an R package for the estimation and exploration of population genetics parameters and their associated errors. Methods Ecol Evol 4:782–788

    Google Scholar 

  • Kelly RP, Palumbi SR (2010) Genetic structure among 50 species of the northeastern pacific rocky intertidal community. PLoS One 5:e8594

    PubMed  PubMed Central  Google Scholar 

  • Kelly RP, Oliver TA, Sivasundar A, Palumbi SR (2010) A method for detecting population genetic structure in diverse, high gene-flow species. J Hered 101:423–436

    CAS  PubMed  Google Scholar 

  • Kensler CB (1967) Fecundity in the marine spiny lobster Jasus verreauxi (H. Milne Edwards) (Crustacea: Decapoda: Palinuridae). New Zeal J Mar Fresh 1:143–155

    Google Scholar 

  • Kensler C, Skrzynski W (1970) Commercial landings of the spiny lobster Jasus verreauxi in New Zealand (Crustacea: Decapoda: Palinuridae). New Zeal J Mar Fresh 4:46–54

    Google Scholar 

  • Kopelman NM, Mayzel J, Jakobsson M, Rosenberg NA, Mayrose I (2015) Clumpak: a program for identifying clustering modes and packaging population structure inferences across K. Mol Ecol Resour 15:1179–1191

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li H (2011) A statistical framework for SNP calling, mutation discovery, association mapping and population genetical parameter estimation from sequencing data. Bioinformatics 27:2987–2993

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25:2078–2079

    PubMed  PubMed Central  Google Scholar 

  • Ling SD, Johnson CR, Ridgway K, Hobday AJ, Haddon M (2009) Climate-driven range extension of a sea urchin: inferring future trends by analysis of recent population dynamics. Glob Chang Biol 15:719–731

    Google Scholar 

  • Linnane A, Dimmlich W, Ward T (2005) Movement patterns of the southern rock lobster, Jasus edwardsii, off South Australia. New Zeal J Mar Fresh 39:335–346

    Google Scholar 

  • Liu JX, Gao TX, Yokogawa K, Zhang YP (2006) Differential population structuring and demographic history of two closely related fish species, Japanese sea bass (Lateolabrax japonicus) and spotted sea bass (Lateolabrax maculatus) in Northwestern Pacific. Mol Phylogenet Evol 39:799–811

    CAS  PubMed  Google Scholar 

  • Mastretta-Yanes A, Arrigo N, Alvarez N, Jorgensen TH, Piñero D, Emerson BC (2015) Restriction site-associated DNA sequencing, genotyping error estimation and de novo assembly optimization for population genetic inference. Mol Ecol Resour 15:28–41

    CAS  PubMed  Google Scholar 

  • McGrath LL, Vollmer SV, Kaluziak ST, Ayers J (2016) De novo transcriptome assembly for the lobster Homarus americanus and characterization of differential gene expression across nervous system tissues. BMC Genomics 17:1–16

    Google Scholar 

  • McKoy JL (1983) Movements of rock lobsters, Jasus edwardsii (Decapoda: Palinuridae), tagged near Stewart Island, New Zealand. New Zeal J Mar Fresh 17:357–366

    Google Scholar 

  • Meirmans PG, Van Tienderen PH (2004) GENOTYPE and GENODIVE: two programs for the analysis of genetic diversity of asexual organisms. Mol Ecol Notes 4:792–794

    Google Scholar 

  • Milano I, Babbucci M, Cariani A, Atanassova M, Bekkevold D, Carvalho GR, Espineira M, Fiorentino F, Garofalo G, Geffen AJ, Hansen JH, Helyar SJ, Nielsen EE, Ogden R, Patarnello T, Stagioni M, Fishpoptrace Consortium, Tinti F, Bargelloni L (2014) Outlier SNP markers reveal fine-scale genetic structuring across European hake populations (Merluccius merluccius). Mol Ecol 23:118–135

    PubMed  Google Scholar 

  • Minami H, Inoue N, Sekiguchi H (2001) Vertical distributions of phyllosoma larvae of palinurid and scyllarid lobsters in the Western North Pacific. J Oceanogr 57:743–748

    Google Scholar 

  • Momigliano P, Harcourt R, Robbins WD, Jaiteh V, Mahardika GN, Sembiring A, Stow A (2017) Genetic structure and signatures of selection in grey reef sharks (Carcharhinus amblyrhynchos). Heredity 119:142–153

    CAS  PubMed  PubMed Central  Google Scholar 

  • Montgomery S (1992) Sizes at first maturity and at onset of breeding in female Jasus verreauxi (Decapoda: Palinuridae) from New South Wales waters, Australia. Mar Freshw Res 43:1373

    Google Scholar 

  • Montgomery S, Craig J (2005) Distribution and abundance of recruits of the eastern rock lobster (Jasus verreauxi) along the coast of New South Wales, Australia. New Zeal J Mar Fresh 39:619–628

    Google Scholar 

  • Montgomery S, Kittaka J (1994) Occurrence of pueruli of Jasus verreauxi (H. Milne Edwards, 1851) (Decapoda, Palinuridae) in waters off Cronulla, New South Wales, Australia. Crustaceana 67:65–70

    Google Scholar 

  • Montgomery SS, Liggins GW, Craig JR, McLeod JR (2009) Growth of the spiny lobster Jasus verreauxi (Decapoda: Palinuridae) off the east coast of Australia. New Zeal J Mar Fresh 43:113–123

    Google Scholar 

  • Morgan EMJ, Green BS, Murphy NP, Strugnell JM (2013) Investigation of genetic structure between deep and shallow populations of the Southern rock lobster, Jasus edwardsii in Tasmania, Australia. PLoS One 8:e77978

    CAS  PubMed  PubMed Central  Google Scholar 

  • NSW Department of Primary Industries (2007) Fishery management strategy for the NSW lobster fishery. Cronulla

  • Ouborg NJ, Piquot Y, Van Groenendael JM (1999) Population genetics, molecular markers and the study of dispersal in plants. J Ecol 87:551–568

    Google Scholar 

  • Ovenden JR, Kashiwagi T, Broderick D, Giles J, Salini J (2009) The extent of population genetic subdivision differs among four co-distributed shark species in the Indo-Australian archipelago. BMC Evol Biol 9:1–15

    Google Scholar 

  • Ovenden JR, Berry O, Welch DJ, Buckworth RC, Dichmont CM (2013) Ocean’s eleven: a critical evaluation of the role of population, evolutionary and molecular genetics in the management of wild fisheries. Fish Fish 16:125–159

    Google Scholar 

  • Paetkau D, Slade R, Burden M, Estoup A (2004) Genetic assignment methods for the direct, real-time estimation of migration rate: a simulation-based exploration of accuracy and power. Mol Ecol 13:55–65

    CAS  PubMed  Google Scholar 

  • Paradis E, Claude J, Strimmer K (2004) APE: Analyses of phylogenetics and evolution in R language. Bioinformatics 20:289–290

    CAS  PubMed  Google Scholar 

  • Pecl G, Frusher S, Gardner C, Haward M, Hobday A, Jennings S, Nursey-Bray M, Punt A, Revill H, van Putten I (2009). The east coast Tasmanian rock lobster fishery: vulnerability to climate change impacts and adaptation response options. Report to the Department of Climate Change, Australia

  • Perez-Figueroa A, Garcai-Pereira MJ, Saura M, Rolan-Alvarez E, Caballero A (2010) Comparing three different methods to detect selective loci using dominant markers. J Evol Biol 23:2267–2276

    CAS  PubMed  Google Scholar 

  • Peterson BK, Weber JN, Kay EH, Fisher HS, Hoekstra HE (2012) Double digest RADseq: an inexpensive method for de novo SNP discovery and genotyping in model and non-model species. PLoS One 7:e37135

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pierce AA, Zalucki MP, Bangura M, Udawatta M, Kronforst MR, Altizer S, Haeger JF, de Roode JC (2014) Serial founder effects and genetic differentiation during worldwide range expansion of monarch butterflies. Proc R Soc B 281:1–9

    Google Scholar 

  • Piry S, Alapetite A, Cornuet JM, Paetkau D, Baudouin L, Estoup A (2004) GENECLASS2: a software for genetic assignment and first-generation migrant detection. J Hered 95:536–539

    CAS  PubMed  Google Scholar 

  • Pringle JM, Wares JP (2007) Going against the flow: maintainance of alongshore variation in allele frequency in a coastal ocean. Mar Ecol Prog Ser 335:69–84

    CAS  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pujolar JM, Jacobsen MW, Als TD, Frydenberg J, Munch K, Jonsson B, Jian JB, Cheng L, Maes GE, Bernatchez L, Hansen MM (2014) Genome-wide single-generation signatures of local selection in the panmictic European eel. Mol Ecol 23:2514–2528

    CAS  PubMed  Google Scholar 

  • Rannala B, Mountain JL (1997) Detecting immigration by using multilocus genotypes. Proc Natl Acad Sci 94:9197–9201

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ridgway K, Hill K (2012) East Australian Current. In: Poloczanska ES, Hobday AJ, Richardson AJ (eds) A marine climate change impacts and adaption support report card for Australia 2012. CSIRO Publishing, Clayton, pp 47–60

    Google Scholar 

  • Rimmer D, Phillips B (1979) Diurnal migration and vertical distribution of phyllosoma larvae of the western rock lobster Panulirus cygnus. Mar Biol 54:109–124

    Google Scholar 

  • Robinson LM, Gledhill DC, Moltschaniwskyj NA, Hobday AJ, Frusher S, Barrett N, Stuart-Smith J, Pecl GT (2015) Rapid assessment of an ocean warming hotspot reveals ‘high’ confidence in potential species’ range extensions. Glob Environ Chang 31:28–37

    Google Scholar 

  • Sansaloni C, Petroli C, Jaccoud D, Carling J, Detering F, Grattapaglia D, Kilian A (2011) Diversity Arrays Technology (DArT) and next-generation sequencing combined: genome-wide, high throughput, highly informative genotyping for molecular breeding of Eucalyptus. BMC Proc 5:P54

    PubMed Central  Google Scholar 

  • Saville-Kent W (1886) Note upon the occurence of the Sydney crawfish, Palinurus huegelli, on the coast of Tasmania. Papers Proc Roy Soc Tasmania 116–117

  • Shanks AL, Grantham BA, Carr MH (2003) Propagule dispersal distance and the size and spacing of marine reserves. Ecol Appl 13:S159–S169

    Google Scholar 

  • Siegel DA, Kinlan BP, Gaylord B, Gaines SD (2003) Lagrangian descriptions of marine larval dispersion. Mar Ecol Prog Ser 260:83–96

    Google Scholar 

  • Slatkin M (1993) Isolation by distance in equilibrium and non-equilibrium populations. Evolution 47:264–279

    PubMed  Google Scholar 

  • Sundqvist L, Keenan K, Zackrisson M, Prodöhl P, Kleinhans D (2016) Directional genetic differentiation and relative migration. Ecol Evol 6:3461–3475

    PubMed  PubMed Central  Google Scholar 

  • Sutton PJH, Bowen M (2014) Flows in the Tasman Front south of Norfolk Island. J Geophys Res Ocean 119:3041–3053

    Google Scholar 

  • Thomas L, Bell JJ (2013) Testing the consistency of connectivity patterns for a widely dispersing marine species. Heredity 111:1–10

    Google Scholar 

  • Villacorta-Rath C, Ilyushkina I, Strugnell JM, Green BS, Murphy NP, Doyle SR, Doyle SR, Hall NE, Robinson AJ, Bell JJ (2016) Outlier SNPs enable food traceability of the southern rock lobster, Jasus edwardsii. Mar Biol 163:223

    Google Scholar 

  • Villacorta-Rath C, Souza CA, Murphy NP, Green BS, Gardner C, Strugnell JM (2018) Temporal genetic patterns of diversity and structure evidence chaotic genetic patchiness in a spiny lobster. Mol Ecol 27:54–65

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Wares JP, Pringle JM (2008) Drift by drift: effective population size is limited by advection. BMC Evol Biol 8:235

    PubMed  PubMed Central  Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370

    CAS  PubMed  Google Scholar 

  • Wood DE, Salzberg SL (2014) Kraken: ultrafast metagenomic sequence classification using exact alignments. Genome Biol 15:R46

    PubMed  PubMed Central  Google Scholar 

  • Zardoya R, Castilho R, Grande C, Favre-Krey L, Caetano S, Marcato S, Krey G, Patarnello T (2004) Differential population structuring of two closely related fish species, the mackerel (Scomber scombrus) and the chub mackerel (Scomber japonicus), in the Mediterranean Sea. Mol Ecol 13:1785–1798

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We would like to thank Marcus Miller and Giles Ballinger for collecting and organising the New South Wales S. verreauxi samples, which were obtained during fishery independent spawning stock survey and commercial catch observer survey routinely undertaken by the New South Wales Department of Primary Industries. We thank Irina Ilyushkina and Darrel Sykes for collection and organisation of New Zealand S. verreauxi samples. Thanks to the Tasmanian Rock Lobster Fishing Industry, University of Tasmania students, dive team and recreational divers that collected specimens in Tasmania. We are grateful to Michael Amor for laboratory assistance and Cecilia Villacorta-Rath for assistance in RAD-LOCI pipeline development. We thank the editor and two reviewers for their time and their constructive feedback.

Funding

This research was funded by ARC DP 150101491, a La Trobe University Securing Food, Water and Environment Grant, the Holsworth Wildlife Research Endowment, the Institute for Marine and Antarctic Studies, the NSW Department of Primary Industries and shareholders in the NSW Rock Lobster Fishery.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Laura N. Woodings.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed and all necessary approvals were obtained.

Additional information

Responsible Editor: O. Puebla.

Reviewed by N. Jeffery and an undisclosed expert.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 15 kb)

Supplementary material 2 (PDF 1812 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Woodings, L.N., Murphy, N.P., Doyle, S.R. et al. Outlier SNPs detect weak regional structure against a background of genetic homogeneity in the Eastern Rock Lobster, Sagmariasus verreauxi. Mar Biol 165, 185 (2018). https://doi.org/10.1007/s00227-018-3443-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00227-018-3443-7

Navigation