Skip to main content

Advertisement

Log in

Genetic structure of Pacific crown-of-thorns starfish (Acanthaster cf. solaris) in southern Japan based on genome-wide RADseq analysis

  • Note
  • Published:
Coral Reefs Aims and scope Submit manuscript

Abstract

Pacific crown-of-thorns starfish (Acanthaster cf. solaris) are known to be widely distributed, and previous studies (showing limited genetic structure) suggest that there are high levels of connectivity at regional scales. It is possible, however, that methods used in previous studies (e.g., microsatellites) did not effectively resolve genetic differentiation and structure for crown-of-thorns starfish. This study examined patterns of genetic structure for populations of the A. cf. solaris in the Ryukyu Archipelago and at Miyazaki, Japan, using restriction-site-associated DNA sequencing (RADseq) analysis, to identify genome-wide single nucleotide polymorphism (SNP) loci to examine genetic diversity and gene flow of CoTS populations. We obtained 186 biallelic SNPs completely shared among 33 individuals by utilizing the published genome sequence of CoTS. Population genomic analysis with biallelic SNPs confirmed that there is limited genetic differentiation and seemingly strong connectivity and gene flow among CoTS populations in the Ryukyu Archipelago and at Miyazaki, Japan. Our findings likely reflect the rapid range expansion of CoTS through southern Japan or panmixia facilitated by the northward flowing Kuroshio Current.

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

Similar content being viewed by others

References

  • Adjeroud M, Kayal M, Peignon C, Juncker M, Mills SC, Beldade R, Dumas P (2018) Ephemeral and localized outbreaks of the coral predator Acanthaster cf. solaris in the southwestern lagoon of New Caledonia. Zool Stud. 57:4

  • Babcock RC, Milton DA, Pratchett M (2016) Relationships between size and reproductive output in the crown-of-thorns starfish. Mar Biol 163:234

    Article  Google Scholar 

  • 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:e3376

  • Benzie JAH, Stoddart JA (1992) Genetic structure of crown-of-thorns starfish (Acanthaster planci) in Australia. Mar Biol 112:631–639

    Article  Google Scholar 

  • Birkeland C, Lucas JS (1990) Acanthaster planci: major management problem of coral reefs. CRC Press, Baton Rouge:272

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

    Article  CAS  Google Scholar 

  • Bruno JF, Selig ER (2007) Regional decline of coral cover in the Indo-Pacific: Timing, extent and subregional comparisons. PLoS ONE 2:e711

  • 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, Genetics 1:171–182

    CAS  Google Scholar 

  • Cowen RK, Lwiza KM, Sponaugle S, Paris CB, Olson DB (2000) Connectivity of marine populations: open or closed? Sci 287:857–859

    Article  CAS  Google Scholar 

  • Cowen RK, Sponaugle S (2009) Larval dispersal and marine population connectivity. Ann Rev Mar Sci 1:443–466

    Article  Google Scholar 

  • D’Aloia CC, Andrés JA, Bogdanowicz SM, McCune AR, Harrison RG, Buston PM (2020) Unraveling hierarchical genetic structure in a marine metapopulation: A comparison of three high-throughput genotyping approaches. Mol Ecol 29:2189–2203

    Article  Google Scholar 

  • Goudet J (2013) Hierfstat, a package for R to compute and test hierarchical F-statistics. Mol Ecol Notes 5:184–186

    Article  Google Scholar 

  • Hall MR, Kocot KM, Baughman KW, Fernandez-Valverde SL, Gauthier MEA, Hatleberg WL, Krishnan A, McDougall C, Motti CA, Shoguchi E, Wang T, Xiang X, Zhao M, Bose U, Shinzato C, Hisata K, Fujie M, Kanda M, Cummins SF, Satoh N, Degnan SM, Degnan BM (2017) The crown-of-thorns starfish genome as a guide for biocontrol of this coral reef pest. Nature 544:231

    Article  CAS  Google Scholar 

  • Harrison H, Pratchett M, Messmer V, Saenz-Agudelo P, Berumen M (2017) Microsatellites reveal genetic homogeneity among outbreak populations of crown-of-thorns starfish (Acanthaster cf. solaris) on Australia’s Great Barrier Reef. Divers 9:16

  • Haszprunar G, Vogler C, Wörheide G (2017) Persistent gaps of knowledge for naming and distinguishing multiple species of crown-of-thorns-seastar in the Acanthaster planci species complex. Divers 9:22

    Article  Google Scholar 

  • Henderson JA, Lucas JS (1971) Larval development and metamorphosis of Acanthaster planci (Asteroidea). Nature 232:655–657

    Article  CAS  Google Scholar 

  • Hock K, Wolff NH, Condie SA, Anthony KR, Mumby PJ. Connectivity networks reveal the risks of crown‐of‐thorns starfish outbreaks on the Great Barrier Reef. J Appl Ecol 51:1188–1196

  • Horoiwa M, Nakamura T, Yuasa H, Kajitani R, Ameda Y, Sasaki T, Taninaka H, Kikuchi T, Yamakita T, Toyoda A, Itoh T, Yasuda N (2021) Integrated population genomic analysis and numerical simulation to estimate larval dispersal of Acanthaster cf. solaris between Ogasawara and other Japanese regions. bioRxiv preprint 2021.03.25.436911

  • Iguchi A, Yoshioka Y, Forsman ZH, Knapp IS, Toonen RJ, Hongo Y, Nagai S, Yasuda N (2019) RADseq population genomics confirms divergence across closely related species in blue coral (Heliopora coerulea). BMC Evol Biol 19:187

    Article  Google Scholar 

  • Inoue N, Sekiguchi H (2005) Distribution of scyllarid phyllosoma larvae (Crustacea: Decapoda: Scyllaridae) in the Kuroshio Subgyre. J Oceanogr 61:389–398

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Keenan K, McGinnity P, Cross T, 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

    Article  Google Scholar 

  • Keesing JK, Thomson DP, Haywood MD, Babcock RC (2019) Two time losers: selective feeding by crown-of-thorns starfish on corals most affected by successive coral-bleaching episodes on western Australian coral reefs. Mar Biol 166:72

    Article  Google Scholar 

  • Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9:357–359

    Article  CAS  Google Scholar 

  • Ling SD, Johnson CR, Frusher S, King CK (2008) Reproductive potential of a marine ecosystem engineer at the edge of a newly expanded range. Glob Change Biol 14:907–915

    Article  Google Scholar 

  • Ling SD, Cowan ZL, Boada J, Flukes EB, Pratchett MS (2020) Homing behaviour by destructive crown-of-thorns starfish is triggered by local availability of coral prey. Proc R Soc B 287:20201341

    Article  CAS  Google Scholar 

  • Makino A, Yamano H, Beger M, Klein CJ, Yara Y, Possingham HP (2014) Spatio-temporal marine conservation planning to support high-latitude coral range expansion under climate change. Divers Distrib 20:859–871

    Article  Google Scholar 

  • Munday PL, Leis JM, Lough JM, Paris CB, Kingsford MJ, Berumen ML, Lambrechts J (2009) Climate change and coral reef connectivity. Coral Reefs 28:379–395

    Article  Google Scholar 

  • Nakabayashi A, Yamakita T, Nakamura T, Aizawa H, Kitano YF, Iguchi A, Yamano H, Nagai S, Agostini S, Teshima KM, Yasuda N (2019) The potential role of temperate Japanese regions as refugia for the coral Acropora hyacinthus in the face of climate change. Sci Rep 9:1892

    Article  Google Scholar 

  • Nakajima Y, Nishikawa A, Iguchi A, Sakai K (2010) Gene flow and genetic diversity of a broadcast-spawning coral in northern peripheral populations. PLoS ONE 5:e11149

  • Nishihira M, Veron J (1995) Hermatypic corals of Japan. Kaiyusha, Tokyo

  • Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O'Hara RB, Simpson GL, Solymos PM, Stevens HH, Szoecs E, Wagner H (2019) vegan: Community Ecology Package. R package version 2.5–6. https://CRAN.R-project.org/package=vegan

  • Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research – an update. Bioinform 28:2537–2539

    Article  CAS  Google Scholar 

  • Pratchett MS, Caballes CF, Rivera-Posada JA, Sweatman HPA (2014) Limits to understanding and managing outbreaks of crown-of-thorns starfish (Acanthaster spp). Oceanogr Mar Biol Annu Rev 52:133–200

    Google Scholar 

  • Pratchett MS, Dworjanyn S, Mos B, Caballes CF, Thompson CA, Blowes S (2017) Larval survivorship and settlement of crown-of-thorns starfish (Acanthaster cf. solaris) at varying algal cell densities. Diversity 9:9010002

  • Pratchett MS, Nadler LE, Burn D, Lang BJ, Messmer V, Caballes CF (2021) Reproductive investment and fecundity of Pacific crown-of-thorns starfish (Acanthaster cf. solaris) on the Great Barrier Reef. Marine Biology 168:87

  • Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MA, Bender D, Maller J, Sklar P, de Bakker PI, Daly MJ, Sham PC (2007) PLINK: a tool set for whole-genome association and population-based linkage analyses. American J Hum Genet 81:559–575

    Article  CAS  Google Scholar 

  • R Core Team (2015) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/

  • Rosser NL, Edyvane K, Malina AC, Underwood JN, Johnson MS (2020) Geography and spawning season drive genetic divergence among populations of the hard coral Acropora tenuis from Indonesia and Western Australia. Coral Reefs 39:989–999

    Article  Google Scholar 

  • Sakaguchi S, Sugino T, Tsumura Y, Ito M, Crisp MD, Bowman DMJS, Nagano AJ, Honjo MN, Yasugi M, Kudoh H, Matsuki Y, Suyama Y, Isagi Y (2015) High-throughput linkage mapping of Australian white cypress pine (Callitris glaucophylla) and map transferability to related species. Tree Genet Genomes 11:121

    Article  Google Scholar 

  • Salas EM, Bernardi G, Berumen ML, Gaither MR, Rocha LA (2019) RADseq analyses reveal concordant Indian Ocean biogeographic and phylogeographic boundaries in the reef fish Dascyllus trimaculatus. Royal Soc Open Sci 6:172413

  • Sherman KD, Paris JR, King RA, Moore KA, Dahlgren CP, Knowles LC, Stump K, Tyler CR, Stevens JR (2020) RAD-Seq analysis and in situ monitoring of Nassau Grouper reveal fine-scale population structure and origins of aggregating fish. Front Mar Sci 7:157

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Thomas L, Underwood JN, Adam AA, Richards ZT, Dugal L, Miller KJ, Gilmour JP (2020) Contrasting patterns of genetic connectivity in brooding and spawning corals across a remote atoll system in northwest Australia. Coral Reefs 39:55–60

    Article  Google Scholar 

  • Timmers MA andrews KR, Bird CE, deMaintenton MJ, Brainard RE, Toonen RJ (2011) Widespread dispersal of the crown-of-thorns sea star, Acanthaster planci, across the Hawaiian Archipelago and Johnston Atoll. J Mar Bio 2011:934269

  • Timmers MA, Bird CE, Skillings DJ, Smouse PE, Toonen RJ (2012) There's no place like home: crown-of-thorns outbreaks in the Central Pacific are regionally derived and independent events. PLoS ONE 7:e31159

  • Truelove NK, Kough AS, Behringer DC, Paris CB, Box SJ, Preziosi RF, Butler MJ (2017) Biophysical connectivity explains population genetic structure in a highly dispersive marine species. Coral Reefs 36:233–244

    Article  Google Scholar 

  • Uthicke S, Logan M, Liddy M, Francis D, Hardy N, Lamare M (2015) Climate change as an unexpected co-factor promoting coral eating seastar (Acanthaster planci) outbreaks. Sci Rep 5:8402

    Article  CAS  Google Scholar 

  • Vanhatalo J, Hosack GR, Sweatman H (2017) Spatiotemporal modelling of crown-of-thorns starfish outbreaks on the Great Barrier Reef to inform control strategies. J Appl Ecol 54:188–197

    Article  Google Scholar 

  • Xuereb A, Benestan L, Normandeau É, Daigle RM, Curtis JM, Bernatchez L, Fortin MJ (2018) Asymmetric oceanographic processes mediate connectivity and population genetic structure, as revealed by RADseq, in a highly dispersive marine invertebrate (Parastichopus californicus). Mol Ecol 27:2347–2364

    Article  Google Scholar 

  • Yamaguchi M (1986) Acanthaster planci infestations of reefs and coral assemblages in Japan: a retrospective analysis of control efforts. Coral Reefs 5:23–30

    Article  Google Scholar 

  • Yamano H, Sugihara K, Nomura K (2011) Rapid poleward range expansion of tropical reef corals in response to rising sea surface temperatures. Geophys Res Lett 38:L04601

    Article  Google Scholar 

  • Yasuda N (2018) Distribution Expansion and Historical Population Outbreak Patterns of Crown-of-Thorns Starfish, Acanthaster planci sensu lato, in Japan from 1912 to 2015. In: Coral Reef Studies of Japan. Springer, Singapore, pp 125–148

  • Yasuda N, Nagai S, Hamaguchi M, Okaji K, Gérard K, Nadaoka K (2009) Gene flow of Acanthaster planci (L.) in relation to ocean currents revealed by microsatellite analysis. Mol Ecol 18:1574–1590

    Article  Google Scholar 

  • Yasuda N, Taquet C, Nagai S, Yoshida T, Adjeroud M (2015) Genetic connectivity of the coral-eating sea star Acanthaster planci during the severe outbreak of 2006–2009 in the Society Islands, French Polynesia. Mar Ecol 36:668–678

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This study was supported by the Global Environment Research Fund 4RF-1501 of the Ministry of the Environment of Japan, KAKENHI Grants-in-Aid (grant no. 17H04996) from the Japan Society for the Promotion of Science, and the Research Laboratory on Environmentally-conscious Developments and Technologies (E-code) at the National Institute of Advanced Industrial Science and Technology (AIST). The authors are grateful to M. Pratchett who helped edit the paper ahead of publication.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Akira Iguchi.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Additional information

Topic Editor Carly Kenkel

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 36 kb)

Supplementary file2 (DOCX 14 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Iguchi, A., Tada, I., Nagano, A.J. et al. Genetic structure of Pacific crown-of-thorns starfish (Acanthaster cf. solaris) in southern Japan based on genome-wide RADseq analysis. Coral Reefs 40, 1379–1385 (2021). https://doi.org/10.1007/s00338-021-02145-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00338-021-02145-3

Keywords

Navigation