Abstract
The diadematid sea urchin Centrostephanus rodgersii occurs in Australia and New Zealand and has undergone recent southward range extension in Australia as a result of regional warming. Clarifying the population genetic structure of this species across its New Zealand range would allow a better understanding of recent and future mechanisms driving range changes in the species. Here, we use microsatellite DNA data to assess connectivity and genetic structure in 385 individuals from 14 locations across the Australian and New Zealand ranges of the species. We detected substantial genetic differentiation among C. rodgersii populations from Australia and New Zealand. However, the population from Port Stephens (located north of Newcastle), Australia, strongly clustered with New Zealand samples. This suggests that the New Zealand populations recently originated from this area, likely via larval transport in the Tasman Front flow that arises in this region. The weak population genetic structure and relatively low genetic diversity detected in New Zealand (global Fst = 0.0021) relative to Australia (global Fst = 0.0339) is consistent with the former population’s inferred history of recent climate-driven expansion. Population-level inbreeding is low in most populations, but were higher in New Zealand (global Fis = 0.0833) than in Australia (global Fis = 0.0202), suggesting that self-recruitment is playing an increasingly important role in the New Zealand region. Our results suggest that C. rodgersii is likely to spread southwards as ocean temperatures increase; therefore, it is crucial that researchers develop a clearer understanding of how New Zealand ecosystems will be reshaped by this species (and others) under climate change.
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All voucher specimens are stored at the Department of Zoology, University of Otago and tissue collections held at Massey University are findable via the Genomics Observatories Metadatabase (GEOME). All genotype files and sample metadata are deposited in appropriate repositories (genotype files are available at https://doi.org/10.6084/m9.figshare.14450163.v1; sample metadata are available at GEOME [GUID https://n2t.net/ark:/21547/DpW2] as part of the Ira Moana Project, https://sites.massey.ac.nz/iramoana/). These samples and derived data have a Biocultural (BC) Notice attached. The BC Notice is a visible notification that there are accompanying cultural rights and responsibilities that need further attention for any future sharing and use of this material or data. The BC Notice recognises the rights of Indigenous peoples to permission the use of information, collections, data and digital sequence information generated from the biodiversity or genetic resources associated with traditional lands, waters, and territories. The BC Notice may indicate that BC (Biocultural) Labels are in development and their implementation is being negotiated. For more information about the BC Notices, visit https://localcontexts.org/notice/bc-notice/.
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References
Agassiz A (1863) Synopsis of the echinoids collected by Dr. W. Stimpson on the North Pacifis explering expedition, under the command of captains ringgold and rodgers. In: Proceedings of the academy of natural sciences of Philadelphia, pp 352–361
Banks SC, Piggott MP, Williamson JE, Beheregaray LB (2007a) Microsatellite DNA markers for analysis of population structure in the sea urchin Centrostephanus rodgersii. Mol Ecol Notes 7:321–323. https://doi.org/10.1111/j.1471-8286.2006.01594.x
Banks SC, Piggott MP, Williamson JE, Bové U, Holbrook NJ, Beheregaray LB (2007b) Oceanic variability and coastal topography shape genetic structure in a long-dispersing sea urchin. Ecology 88:3055–3064. https://doi.org/10.1890/07-0091.1
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. https://doi.org/10.1111/j.1365-294X.2010.04627.x
Bronstein O, Kroh A, Tautscher B, Liggins L, Haring E (2017) Cryptic speciation in pan-tropical sea urchins: a case study of an edge-of-range population of Tripneustes from the Kermadec Islands. Sci Rep 7:5948. https://doi.org/10.1038/s41598-017-06183-2
Bronstein O, Kroh A, Miskelly AD, Smith SDA, Dworjanyn SA, Mos B, Byrne M (2019) Implications of range overlap in the commercially important pan-tropical sea urchin genus Tripneustes (Echinoidea: Toxopneustidae). Mar Biol 166:34. https://doi.org/10.1007/s00227-019-3478-4
Brooks A (2020) Using ecological niche modelling to predict climate change responses of ten key fishery species in Aotearoa New Zealand. Dissertation, Victoria University of Wellington, Wellington
Burgess SC, Nickols KJ, Griesemer CD, Barnett LA, Dedrick AG, Satterthwaite EV, Yamane L, Morgan SG, White JW, Botsford LW (2014) Beyond connectivity: how empirical methods can quantify population persistence to improve marine protected-area design. Ecol App 24:257–270
Byrne M, Andrew N (2020) Centrostephanus rodgersii and Centrostephanus tenuispinus. Dev Aquacult Fish Sci 43:379–396. https://doi.org/10.1016/B978-0-12-819570-3.00022-6
Byrne M, Gall M (2017) A tale of two urchins Heliocidaris erythrogramma and H. tuberculata. Australian Echinoderms: Biology Ecology and Evolution, CSIRO Publishing Melbourne and ABRS, Canberra
Casquet J, Thebaud C, Gillespie RG (2012) Chelex without boiling, a rapid and easy technique to obtain stable amplifiable DNA from small amounts of ethanol-stored spiders. Mol Ecol Resour 12:136–141. https://doi.org/10.1111/j.1755-0998.2011.03073.x
Chiswell SM, Roemmich D (1998) The East Cape Current and two eddies: a mechanism for larval retention? N Z J Mar Freshw Res 32:385–397. https://doi.org/10.1080/00288330.1998.9516833
Edgar GJ, Stuart-Smith RD, Thomson RJ, Freeman DJ (2017) Consistent multi-level trophic effects of marine reserve protection across northern New Zealand. PLoS ONE 12:e0177216. https://doi.org/10.1371/journal.pone.0177216
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. https://doi.org/10.1111/j.1365-294X.2005.02553.x
Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567. https://doi.org/10.1111/j.1755-0998.2010.02847.x
Faubet P, Waples RS, Gaggiotti OE (2007) Evaluating the performance of a multilocus Bayesian method for the estimation of migration rates. Mol Ecol 16:1149–1166. https://doi.org/10.1111/j.1365-294X.2007.03218.x
Gardner JPA, Bell JJ, Constable HB, Hannan D, Ritchie PA, Zuccarello GC (2010) Multi-species coastal marine connectivity: a literature review with recommendations for further research. New Zealand Aquatic Environment and Biodiversity Report No. 58. Victoria University, Wellington, New Zealand
Gaylord B, Gaines SD (2000) Temperature or transport? Range limits of marine species mediated solely by flow. Am Nat 155:769–789
Goudet J (2005) hierfstat, a package for r to compute and test hierarchical F-statistics. Mol Ecol Notes 5:184–186. https://doi.org/10.1111/j.1471-8286.2004.00828.x
Hardy NA, Lamare M, Uthicke S, Wolfe K, Doo S, Dworjanyn S, Byrne M (2014) Thermal tolerance of early development in tropical and temperate sea urchins: inferences for the tropicalization of eastern Australia. Mar Biol 161:395–409. https://doi.org/10.1007/s00227-013-2344-z
Hill KL, Rintoul SR, Ridgway KR, Oke PR (2011) Decadal changes in the South Pacific western boundary current system revealed in observations and ocean state estimates. J Geophys Res 116:C01009. https://doi.org/10.1029/2009JC005926
Huggett MJ, King CK, Williamson JE, Steinberg PD (2005) Larval development and metamorphosis of the Australian diadematid sea urchin Centrostephanus rodgersii. Invertebr Reprod Dev 47:197–204. https://doi.org/10.1080/07924259.2005.9652160
IPCC (2019) IPCC Special Report on the Ocean and Cryosphere in a Changing Climate. In: Pörtner H-O, Roberts DC, Masson-Delmotte V, Zhai P, Tignor M, Poloczanska E, Mintenbeck K, Alegría A, Nicolai M, Okem A, Petzold J, Rama B, Weyer NM (eds) In press
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, Shepherd 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 Biol Ecol 400:17–32. https://doi.org/10.1016/j.jembe.2011.02.032
Jombart T (2008) Adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405. https://doi.org/10.1093/bioinformatics/btn129
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. https://doi.org/10.1186/1471-2156-11-94
Jost L (2008) GST and its relatives do not measure differentiation. Mol Ecol 17:4015–4026. https://doi.org/10.1111/j.1365-294X.2008.03887.x
Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649. https://doi.org/10.1093/bioinformatics/bts199
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. https://doi.org/10.1111/2041-210X.12067
Kimura M, Crow JF (1964) The number of alleles that can be maintained in a finite population. Genetics 49:725–738
Kimura M, Ohta T (1978) Stepwise mutation model and distribution of allelic frequencies in a finite population. Proc Natl Acad Sci 75:2868–2872. https://doi.org/10.1073/pnas.75.6.2868
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. https://doi.org/10.1111/1755-0998.12387
Last PR, White WT, Gledhill DC, Hobday AJ, Brown R, Edgar GJ, Pecl G (2011) Long-term shifts in abundance and distribution of a temperate fish fauna: a response to climate change and fishing practices. Glob Ecol Biogeogr 20:58–72
Law CS, Rickard GJ, Mikaloff-Fletcher SE, Pinkerton MH, Behrens E, Chiswell SM, Currie K (2018) Climate change projections for the surface ocean around New Zealand. N Z J Mar Freshw Res 52:309–335. https://doi.org/10.1080/00288330.2017.1390772
Liggins L, Gleeson L, Ciginos C (2014) Evaluating edge-of-range genetic patterns for tropical echinoderms, Acanthaster planci and Tripneustes gratilla, of the Kermadec Islands, southwest Pacific. Bull Mar Sci 90(1):379–397. https://doi.org/10.5343/bms.2013.1015
Ling SD, Johnson CR (2009) Population dynamics of an ecologically important range-extender: kelp beds versus sea urchin barrens. Mar Ecol Prog Ser 374:113–125. https://doi.org/10.3354/meps07729
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 Change Biol 15:719–731. https://doi.org/10.1111/j.1365-2486.2008.01734.x
Luikart G, Cornuet J-M (1998) Empirical evaluation of a test for identifying recently bottlenecked populations from allele frequency data. Conserv Biol 12:228–237
Meirmans PG (2014) Nonconvergence in Bayesian estimation of migration rates. Mol Ecol Resour 14:726–733. https://doi.org/10.1111/1755-0998.12216
Middleton I, Aguirre JD, Trnski T, Francis M, Duffy C, Liggins L (2021) Introduced alien, range extension or just visiting? Combining citizen science observations and expert knowledge to classify range dynamics of marine fishes. Divers Distrib. https://doi.org/10.1111/ddi.13273
Misra R, Sérazin G, Meissner K, Gupta AS (2021) Projected changes to Australian marine heatwaves. Geophys Res Lett 48:e2020GL091323. https://doi.org/10.1029/2020GL091323
Monaco CJ, Booth DJ, Figueira WF, Gillanders BM, Schoeman DS, Bradshaw CJA, Nagelkerken I (2021) Natural and anthropogenic climate variability shape assemblages of range-extending coral-reef fishes. J Biogeogr 2021(00):1–13. https://doi.org/10.1111/jbi.14058
Mos B, Byrne M, Dworjanyn SA (2020) Effects of low and high pH on sea urchin settlement, implications for the use of alkali to counter the impacts of acidification. Aquaculture 528:735618. https://doi.org/10.1016/j.aquaculture.2020.735618
Oosterhout CV, 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. https://doi.org/10.1111/j.1471-8286.2004.00684.x
Paradis E (2010) pegas: an R package for population genetics with an integrated–modular approach. Bioinformatics 26:419–420. https://doi.org/10.1093/bioinformatics/btp696
Pecl GT, Araújo MB, Bell JD, Blanchard J, Bonebrake TC, Chen I-C, Clark TD, Colwell RK, Danielsen F, Evengård B, Falconi L, Ferrier S, Frusher S, Garcia RA, Griffis RB, Hobday AJ, Janion-Scheepers C, Jarzyna MA, Jennings S, Lenoir J, Linnetved HI, Martin VY, McCormack PC, McDonald J, Mitchell NJ, Mustonen T, Pandolfi JM, Pettorelli N, Popova E, Robinson SA, Scheffers BR, Shaw JD, Sorte CJB, Strugnell JM, Sunday JM, Tuanmu M-N, Vergés A, Villanueva C, Wernberg T, Wapstra E, Williams SE (2017) Biodiversity redistribution under climate change: impacts on ecosystems and human well-being. Science 355:eeai9214. https://doi.org/10.1126/science.aai9214
Pecorino D, Lamare MD, Barker MF, Byrne M (2013) How does embryonic and larval thermal tolerance contribute to the distribution of the sea urchin Centrostephanus rodgersii (Diadematidae) in New Zealand? J Exp Mar Biol Ecol 445:120–128. https://doi.org/10.1016/j.jembe.2013.04.013
Perry AL, Low PJ, Ellis JR, Reynolds JD (2005) Climate change and distribution shifts in marine fishes. Science 308:1912–1915
Pinsky ML, Selden RL, Kitchel ZJ (2020) Climate-driven shifts in marine species ranges: scaling from organisms to communities. Annu Rev Mar Sci 12:153–179
Piry S, Luikart G, Cornuet J-M (1999) BOTTLENECK: a computer program for detecting recent reductions in the effective size using allele frequency data. J Heredity 90:502–503. https://doi.org/10.1093/jhered/90.4.502
Pitt NR, Poloczanska ES, Hobday AJ (2010) Climate-driven range changes in Tasmanian intertidal fauna. Mar Freshw Res 61:963–970
Poloczanska ES, Brown CJ, Sydeman WJ, Kiessling W, Schoeman DS, Moore PJ, Brander K, Bruno JF, Buckley LB, Burrows MT, Duarte CM (2013) Global imprint of climate change on marine life. Nat Clim Chang 3:919–925
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Reisser CM, Bell JJ, Gardner JP (2014) Correlation between pelagic larval duration and realised dispersal: long-distance genetic connectivity between northern New Zealand and the Kermadec Islands archipelago. Mar Biol 161:297–312
Ridgway KR, Dunn JR (2003) Mesoscale structure of the mean East Australian Current System and its relationship with topography. Prog Oceanogr 56:189–222. https://doi.org/10.1016/S0079-6611(03)00004-1
Ross PM, Hogg ID, Pilditch C, Lundquist CJ (2009) Phylogeography of New Zealand’s coastal benthos. N Z J Mar Freshwater Res 43:1009–1027
Sloyan BM, O’Kane TJ (2015) Drivers of decadal variability in the Tasman Sea. J Geophys Res 120:3193–3210. https://doi.org/10.1002/2014JC010550
Soars NA, Prowse TAA, Byrne M (2009) Overview of phenotypic plasticity in echinoid larvae, “Echinopluteus transversus” type vs. typical echinoplutei. Mar Ecol Prog Ser 383:113–125. https://doi.org/10.3354/meps07848
Spencer HG, Waters JM, Eichhorst TE (2007) Taxonomy and nomenclature of black nerites (Gastropoda: Neritimorpha: Nerita) from the South Pacific. Invertebr Syst 21:229–237. https://doi.org/10.1071/IS06038
Stanton BR (1979) The Tasman front. N Z J Mar Freshw Res 13:201–214. https://doi.org/10.1080/00288330.1979.9515795
Sutton P, Chiswell S, Gorman R, Kennan S, Rickard G (2012) Physical marine environment of the Kermadec Islands region. New Zealand Department of Conservation
Waters JM, King TM, O’loughlin PM, Spencer HG (2005) Phylogeographical disjunction in abundant high-dispersal littoral gastropods. Mol Ecol 14:2789–2802. https://doi.org/10.1111/j.1365-294X.2005.02635.x
Wernberg T, Russell BD, Thomsen MS, Gurgel CFD, Bradshaw CJA, Poloczanska ES, Connell SD (2011) Seaweed communities in retreat from ocean warming. Curr Biol 21:1828–1832
Wolanski E, Hamner W (1988) Topographically controlled fronts in the ocean and their biological influence. Science 241:177–181
Acknowledgements
We thank Tania King for lab assistance, Felix Vaux for assisting with figure production and Robert Smith for discussions on physical oceanography and various members of MEGMAR (Molecular Ecology Group for Marine Research at Flinders University) for assistance with the sampling in Australia. Expeditions to the Kermadec Islands were made possible by the Sir Peter Blake Trust, the Commanding Officer and ship’s company of HMNZS Canterbury, the RV Braveheart crew (Stoney Creek Shipping Company), and the RV Tangaroa with the support of the Auckland Museum Institute, Auckland Museum, the Pew Charitable Trusts, and the School of Natural and Computational Sciences (SNCS) Massey University, the Marine Funding Advisory Research Group, NIWA (Project COBR1705), Te Papa Tongarewa, and Ministry for the Environment. We thank J. David Aguirre, Tom Trnski, Adam N. H. Smith, David Acuña-Marrero, Emma Betty, Mat Betty, Crispin Middleton, Phil Ross, Sam McCormack, and Severine Hannam for collecting help. We wish to thank and acknowledge mana whenua (the traditional owners), the Māori iwi of Ngāti Kuri and Ngātiwai, for their support. We thank Te Komite Rakahau ki Kāi Tahu (the Ngāi Tahu Research Consultation Committee) for reviewing our proposed research and providing advice on establishing partnerships with iwi and exchanging new knowledge generated by the research. We thank the two anonymous reviewers for their careful and detailed suggestions on earlier drafts which have greatly improved this manuscript.
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Research was supported by a University of Otago Research Grant to M. Lamare. L. Liggins was supported by a Rutherford Foundation New Zealand Postdoctoral Fellowship.
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Conceptualisation: MDL, LL, SCB, LBB, JMW, MB, and LC. Methodology: MDL, JMW, LL, SCB, LBB, GAMcC, and LJT. Field sampling: MDL, LL, and ML. Formal analysis and investigation: all the authors. Writing—original draft preparation: MDL, LL, SCB, LBB, JMW, MB, LC, GAMcC, and LJT. Writing—review and editing: MDL, LL, SCB, LBB, JMW, MB, GAMcC, and LJT. Funding acquisition: MDL, LL, SCB, LBB, JMW, MB, and LC. Resources: MDL, LL, and JMW.
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Thomas, L.J., Liggins, L., Banks, S.C. et al. The population genetic structure of the urchin Centrostephanus rodgersii in New Zealand with links to Australia. Mar Biol 168, 138 (2021). https://doi.org/10.1007/s00227-021-03946-4
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DOI: https://doi.org/10.1007/s00227-021-03946-4