Skip to main content

Advertisement

SpringerLink
Log in

The application of genomics to inform conservation of a functionally important reef fish (Scarus niger) in the Philippines

  • Research Article
  • Published:
Conservation Genetics Aims and scope Submit manuscript

Abstract

Coral reefs within the Coral Triangle (CT) are home to the greatest marine diversity on the globe and are an important supplier of marine resources to densely populated coastal regions. Many coral reefs within the CT and around the world are under threat from over-exploitation. Marine protected areas (MPAs) have been proven to be effective tools in restoring fish stocks. However, the role that MPAs play in promoting connectivity at greater distances through larval dispersal is still unknown. RADseq was used to discover 4253 SNPs from 81 individuals of the dusky parrotfish (Scarus niger) collected from three sites within the Philippines. A lack of population structure suggested a high rate of gene flow (F ST = 0.007). Estimates of Ne from linkage disequilibrium are relatively large, ranging from 1200 to 2000. A sibling analysis revealed one pair of well-supported full siblings (r = 0.773) and one pair of putative half siblings (r = 0.191) between sites separated by more than 500 km. The low F ST values indicate a high degree of gene flow between the reefs within the sampling area while the sibling analysis suggests demographic connectivity between the Sibuyan Sea and the Sulu Sea. The Mindoro–Panay throughflow is a likely vector by which larvae are transported between these sites, suggesting that reefs in Romblon are sources for reefs near Basay, 400 km to the south. Given the reliance of a vast majority of coral reef fishes on larval dispersal, this study reveals that MPAs established within the central Philippines can supply varying levels of larvae to overfished reefs.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Ackiss AS, Pardede S, Crandall ED, Ablan-Lagman MCA, Ambariyanto Romena N, Barber PH, Carpenter KE (2013) Pronounced genetic structure in a highly mobile coral reef fish, Caesio cuning, in the Coral Triangle. Mar Ecol Prog Ser 480:185–197

    Article  Google Scholar 

  • Alcala AC (1988) Effects of marine reserves on coral fish abundances and yields of Philippine coral reefs. Ambio 17:194–199

    Google Scholar 

  • Allendorf FW, Hohenlohe PA, Luikart G (2010) Genomics and the future of conservation genetics. Nat Rev Genet 11(10):697–709

    Article  PubMed  CAS  Google Scholar 

  • Almany GR, Hamilton RJ, Bode M, Matawai M, Potuku T, Saez-Agudelo P, Planes S, Berumen ML, Rhodes KL, Thorrold SR, Russ GR, Jones GP (2013) Dispersal of grouper larvae drives local resource sharing in a coral reef fishery. Curr Biol 23(7):626–630

    Article  PubMed  CAS  Google Scholar 

  • Anderson EC, Dunham KK (2008) The influence of family groups on inferences made with the program Structure. Mol Ecol Resour 8(6):1219–1229

    Article  PubMed  CAS  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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bay LK, Choat JH, van Herwerden L, Robertson DR (2004) High genetic diversities and complex genetic structure in an Indo-Pacific tropical reef fish (Chlorurus sordidus): evidence of an unstable evolutionary past? Mar Biol 144(4):757–767

    Article  CAS  Google Scholar 

  • Bellwood DR, Choat JH (1990) A functional analysis of grazing in parrotfishes (family Scaridae): the ecological implications. Environ Biol Fishes 28:189–214

    Article  Google Scholar 

  • Bellwood DR, Hughes TP, Folke C, Nyström M (2004) Confronting the coral reef crisis. Nature 429:827–833

    Article  PubMed  CAS  Google Scholar 

  • Bierne N, Roze D, Welch JJ (2013) Pervasive selection or is it…? Why are FST outliers sometimes so frequent? Mol Ecol 22(8):2061–2064

    Article  PubMed  Google Scholar 

  • Burke L, Reytar K, Spalding M, Perry A (2012) Reefs at risk: revisted in the Coral Triangle. World Resources Institute, Washington, D.C.

    Google Scholar 

  • Candy JR, Campbell NR, Grinnell MH, Beacham, TD, Larson WA, Narum SR (2015) Population differentiation determined from putative neutral and divergent adaptive genetic markers in Eulachon (Thaleichthys pacificus, Osmeridae), an anadromous Pacific smelt. Mol Ecol Resour. doi:10.1111/1755-0998.12400

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

    Google Scholar 

  • Cowen RK, Paris CB, Srinivasan A (2006) Scaling of connectivity in marine populations. Science 311(5760):522–527

    Article  PubMed  CAS  Google Scholar 

  • Do C, Waples RS, Peel D, Macbeth GM, Tillett BJ, Ovenden JR (2014) NeEstimator v2: re-implementation of software for the estimation of contemporary effective population size (Ne) from genetic data. Mol Ecol Resour 14:209–214

    Article  PubMed  CAS  Google Scholar 

  • Dudgeon CL, Gust N, Blair D (2000) No apparent genetic basis to demographic differences in scarid fishes across continental shelf of the Great Barrier Reef. Mar Biol 137:1059–1066

    Article  Google Scholar 

  • Edwards CB, Friedlander AM, Green AG, Hardt MJ, Sala E, Sweatman HP, Williams ID, Zgliczynski B, Sandin SA, Smith JE (2014) Global assessment of the status of coral reef herbivorous fishes: evidence for fishing effects. Proc Biol Sci 281(1774):20131835

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Evans RD, Russ GR, Kritzer JP (2008) Batch fecudnity of Lutjanus carponotatus (Lutjanidae) and implications of no-take marine reserves on the Great Barrier Reef, Australia. Coral Reefs 27:179–189

    Article  Google Scholar 

  • Everett MV, Miller MR, Seeb JE (2012) Meiotic maps of sockeye salmon derived from massively parallel DNA sequencing. BMC Genom 13:521

    Article  CAS  Google Scholar 

  • Excoffier L, Lischer HE (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10(3):564–567

    Article  PubMed  Google Scholar 

  • Excoffier L, Hofer T, Foll M (2009) Detecting loci under selection in a hierarchically structured population. Heredity 103(4):285–298

    Article  PubMed  CAS  Google Scholar 

  • Fitzpatrick JM, Carlon DB, Lippe C, Robertson DR (2011) The West Pacific diversity hotspot as a source or sink for new species? Population genetic insights from the Indo-Pacific parrotfish Scarus rubroviolaceus. Mol Ecol 20(2):219–234

    Article  PubMed  CAS  Google Scholar 

  • Foll M, Gaggiotti O (2008) A genome-scan method to identify selected loci appropriate for both dominant and codominant markers: a Bayesian perspective. Genetics 180:977–993

    Article  PubMed  PubMed Central  Google Scholar 

  • Gell FR, Roberts CM (2003) Benefits beyond boundaries: the fishery effects of marine reserves. Trends Ecol Evol 18(9):448–455

    Article  Google Scholar 

  • Gordon AL, Sprintall J, Ffield A (2011) Regional oceanography of the Philippine Archipelago. Oceanography 24(1):14–27. doi:10.5670/oceanog.2011.01

    Article  Google Scholar 

  • Goudet J, Raymond M, deMeeus T, Rousset F (1996) Testing differentiation in diploid populations. Genetics 144:1933–1940

    PubMed  PubMed Central  CAS  Google Scholar 

  • Green AL, Fernandes L, Almany G, Abesamis R, McLeod Alino PM, White AT, Salm R, Tanzer J, Pressey RL (2014) Designing marine reserves for fisheries management, biodiversity conservation, and climate change adaptation. Coast Manag 42:143–159

    Article  Google Scholar 

  • Gruenthal KM, Witting DA, Ford T, Neuman MJ, Williams JP, Pondella DJ II, Bird A, Caruso N, Hyde JR, Seeb LW, Larson WA (2014) Development and application of genomic tools to the restoration of green abalone in southern California. Conserv Genet 15:109–121

    Article  Google Scholar 

  • Halpern BS, Lester SE, McLeod KL (2010) Placing marine protected areas onto the ecosystem-based management seascape. Proc Natl Acad Sci U S A 107(43):18312–18317

    Article  PubMed  PubMed Central  Google Scholar 

  • Han W, Moore AM, Levin J, Zhang B, Arango HG, Curchitser E, Lorenso ED, Gordon AL, Lin J (2009) Seasonal surface ocean circulation and dynamics in the Philippine Archipelago region during 2004-2008. Dyn Atmos Oceans 47:114–137

    Article  Google Scholar 

  • Hansen MM, Nielsen EE, Mensberg KL (1997) The problem of sampling families rather than populations: relatedness among individuals in samples of juvenile brown trout Salmo trutta L. Mol Ecol 6(5):469–474

    Article  CAS  Google Scholar 

  • Harrison HB, Williamson DH, Evans RD, Almany GR, Thorrold SR, Russ GR, Feldheim KA, van Herwerden L, Planes S, Srinivasan M, Berumen ML, Jones GP (2012) Larval export from marine reserves and the recruitment benefit for fish and fisheries. Curr Biol 22:1023–1028

    Article  PubMed  CAS  Google Scholar 

  • Hill WG (1981) Estimation of effective population-size from data on linkage disequilibrium. Genet Res 38:209–216

    Article  Google Scholar 

  • Hoegh-Guldberg GH, Veron JEN, Green A, Gomez ED, Lough J, King M, Ambariyanto, Hansen L, Cinner J, Dews G, Russ G, Schuttenberg HZ, Peñaflor EL, Eakin CM, Christensen TRL, Abbey M, Areki F, Kosaka RA, Tewfik A, Oliver J (2009) The Coral Triangle and climate change: ecosystems, people and societies at risk. WWF Australia, Bribane. http://www.panda.org/coraltriangle)

  • Hogan JD, Thiessen RJ, Sale PF, Heath DD (2012) Local retention, dispersal and fluctuating connectivity among populations of a coral reef fish. Oecologia 168:61–71

    Article  PubMed  Google Scholar 

  • Horigue V, Alino PM, Pressey RL (2014) Evaluating management performance of marine protected area networks in the Philippines. Ocean Coast Manag 95:11–25

    Article  Google Scholar 

  • Houk P, Rhodes K, Cuetos-Bueno J, Lindfield S, Fread V, McIlwain JL (2011) Commercial coral-reef fisheries across Micronesia: a need for improving management. Coral Reefs 31(1):13–26

    Article  Google Scholar 

  • Ishihara T, Tachihara K (2011) Pelagic larval duration and settlment size of Apogonidae, Labridae, Scaridae, and Tripterygiidae species in a coral lagoon of Okinawa Island, southern Japan. Pac Sci 65:87–93

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Jones GP, Almany GR, Russ GR, Sale PF, Steneck RS, Oppen MJH, Willis BL (2009) Larval retention and connectivity among populations of corals and reef fishes: history, advances and challenges. Coral Reefs 28(2):307–325

    Article  Google Scholar 

  • Kalinowski ST, Wagner AP, Taper ML (2006) ML-RELATE: a computer program for maximum likelihood estimation of relatedness and relationship. Mol Ecol Notes 6:576–579

    Article  CAS  Google Scholar 

  • Kritzer JP, Sale PF (2004) Metapopulation ecology in the sea: from Levins’ model to marine ecology and fisheries science. Fish Fish 5:131–140

    Article  Google Scholar 

  • Larson WA, Seeb LW, Everett MV, Waples RK, Templin WD, Seeb JE (2014) Genotyping by sequencing resolves shallow population structure to inform conservation of Chinook salmon (Oncorhynchus tshawytscha). Evol Appl 7(3):355–369

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Li CC, Weeks DE, Chakravarti A (1993) Similarity of DNA fingerprints due to chance and relatedness. Hum Hered 43:45–52

    Article  PubMed  CAS  Google Scholar 

  • Lotterhos KE, Whitlock MC (2014) Evaluation of demographic history and neutral parameterization on the performance of FST outlier tests. Mol Ecol 23(9):2178–2192

    Article  PubMed  PubMed Central  Google Scholar 

  • Lynch M, Ritland K (1999) Estimation of pairwise relatedness with molecular markers. Genetics 152(4):1753–1766

    PubMed  PubMed Central  CAS  Google Scholar 

  • Magsino RM, Juinio-Meñez MA (2008) The influence of contrasting life history traits and oceanic processes on genetic structuring of rabbitfish populations Siganus argenteus and Siganus fuscescens along the eastern Philippine coasts. Mar Biol 154(3):519–532

    Article  Google Scholar 

  • McLeod E, Salm R, Green A, Almany J (2009) Designing marine protected area networks to address the impacts of climate change. Front Ecol Environ 7:362–370

    Article  Google Scholar 

  • Milligan BG (2003) Maximum-likelihood estimation of relatedness. Genetics 163(3):1153–1167

    PubMed  PubMed Central  Google Scholar 

  • Minoche AE, Dohm JC, Himmelbauer H (2011) Evaluation of genomic high-throughput sequencing data generated on Illumina HiSeq and genome analyzer systems. Genome Biol 12(11):R112

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mora C, Andréfouët S, Costello MJ, Kranenburg C, Rollo A, Veron J (2006) Coral reefs and the global network of marine protected areas. Science 312:1750–1751

    Article  PubMed  CAS  Google Scholar 

  • Narum SR, Hess JE (2011) Comparison of FST outlier tests for SNP loci under selection. Mol Ecol Resour 11(s1):184–194

    Article  PubMed  Google Scholar 

  • Patterson HM, Swearer SE (2007) Long-distance dispersal and local retention of larvae as mechanisms of recruitment in an island population of a coral reef fish. Austral Ecol 32:122–130

    Article  Google Scholar 

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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Peel D, Waples RS, Macbeth GM, Do C, Ovenden JR (2013) Accounting for missing data in the estimation of contemporary genetic effective population size (Ne). Mol Ecol Resour 13:243–253

    Article  PubMed  CAS  Google Scholar 

  • Pelc RA, Warner RR, Gaines SD, Paris CB (2010) Detecting larval export from marine reserves. Proc Natl Acad Sci U S A 107(43):18266–18271

    Article  PubMed  PubMed Central  Google Scholar 

  • Pew J, Muir PH, Wang J, Frasier TR (2015) related: an R package for analysing pairwise relatedness from codominat molecular markers. Mol Ecol Resour 15:557–561

    Article  PubMed  Google Scholar 

  • Puebla O, Bermingham E, McMillan WO (2012) On the spatial scale of dispersal in coral reef fishes. Mol Ecol 21(23):5675–5688

    Article  PubMed  CAS  Google Scholar 

  • Queller DC, Goodnight KF (1989) Estimating relatedness using molecular markers. Evolution 43:258–275

    Article  Google Scholar 

  • Raymond M, Rousset F (1995) An exact test for population differentiation. Evolution 49:1280–1283

    Article  Google Scholar 

  • Raynal JM, Crandall ED, Barber PH, Mahardika GN, Lagman MC, Carpenter KE (2014) Basin isolation and oceanographic features influencing lineage diversification in the humbug damselfish (Dascyllus aruanus) in the Coral Triangle. Bull Mar Sci 90(1):513–532

    Article  Google Scholar 

  • Rhodes KL, Tupper MH, Wichilmel CB (2007) Characterization and management of the commercial sector of the Pohnpei coral reef fishery, Micronesia. Coral Reefs 27(2):443–454

    Article  Google Scholar 

  • Ritland K (1996) Estimators for pairwise relatedness and individual inbreeding coefficients. Genet Res 67(02):175–185

    Article  Google Scholar 

  • Roesti M, Salzburger W, Berner D (2012) Uninformative polymorphisms bias genome scans for signatures of selection. BMC Evol Biol 12(1):94

    Article  PubMed  PubMed Central  Google Scholar 

  • Rousset F (2008) GENEPOP ‘ 007: a complete re-implementation of the GENEPOP software for Windows and Linux. Mol Ecol Resour 8:103–106

    Article  PubMed  Google Scholar 

  • Russ GR (2002) Yet another review of marine reserves as reef fisheries management tools. In: Sale PF (ed) Coral reef fishes: dynamics and diversity in a complex ecosystem. Academic Press, San Diego, pp 421–443

    Chapter  Google Scholar 

  • Sale PF, Cowen RK, Danilowicz BS, Jones GP, Kritzer JP, Lindeman KC, Planes S, Polunin NV, Russ GR, Sadovy YJ, Steneck RS (2005) Critical science gaps impede use of no-take fishery reserves. Trends Ecol Evol 20(2):74–80

    Article  PubMed  Google Scholar 

  • Slatkin M (1987) Gene flow and the geographic structure of natural populations. Science 236(4803):787–792

    Article  PubMed  CAS  Google Scholar 

  • Steneck RS, Paris CB, Arnold MC, Ablan-Lagman MC, Alcala AC, Butler MJ, McCook LJ, Russ GR, Sale PF (2009) Thinking and managing outside the box: coalescing connectivity networks to build region-wide resilience in coral reef ecosystems. Coral Reefs 28:367–378

    Article  Google Scholar 

  • Stockwell B, Jadloc CRL, Abesamis RA, Alcala AC, Russ GR (2009) Trophic and benthic responses to no-take marine reserve protection in the Philippines. Mar Ecol Prog Ser 389:1–15

    Article  Google Scholar 

  • Veron JEN (2000) Corals of the world. Australian Institute of Marine Science, Townsville

    Google Scholar 

  • Visram S, Yang MC, Pillay RM, Said S, Henriksson O, Grahn M, Chen CA (2010) Genetic connectivity and historical demography of the blue barred parrotfish (Scarus ghobban) in the western Indian Ocean. Mar Biol 157(7):1475–1487

    Article  Google Scholar 

  • Wang J (2002) An estimator for pairwise relatedness using molecular markers. Genetics 160(3):1203–1215

    PubMed  PubMed Central  CAS  Google Scholar 

  • Wang J (2007) Triadic IBD coefficients and applications to estimating pairwise relatedness. Genet Res 89(03):135–153

    Article  PubMed  CAS  Google Scholar 

  • Wang J (2009) A new method for estimating effective population sizes from a single sample of multilocus genotypes. Mol Ecol 18:2148–2164

    Article  PubMed  Google Scholar 

  • Waples RS (2006) A bias correction for estimates of effective population size based on linkage disequilibrium at unlinked gene loci. Conserv Genet 7:167–184

    Article  Google Scholar 

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

    Article  Google Scholar 

  • White AT, Alino PM, Cros A, Fatan NA, Green AL, Teoh SJ, Laroya L, Peterson N, Tan S, Tighe S, Vengas-Li R, Walton A, Wen W (2014) MArine protected areas in the Coral Triangle: progress, Issues, and Options. Coast Manag 42:87–106

    Article  Google Scholar 

  • Willette DA, Allendorf FW, Barber PH, Barshis DJ, Carpenter KE, Crandall ED, Cresko WA, Fernandez-Silva I, Matz MV, Meyer E, Santos MD, Seeb LW, Seeb JE (2014) So, you want to use next-generation sequencing in marine systems? Insight from the Pan-Pacific Advanced Studies Institute. Bull Mar Sci 90(1):1–43

    Article  Google Scholar 

  • Williams I, Polunin N (2014) Large-scale associations between macroalgal cover and grazer biomass on mid-depth reefs in the Caribbean. Coral Reefs 19(4):358–366

    Article  Google Scholar 

Download references

Acknowledgments

We are thankful for the Philippine National Fisheries Research and Development Institute (NFRDI) and Bureau of Fisheries and Aquatic Research (BFAR) assistance in granting collection permits (0208/FRP/SM/IX/2009). We thank Silliman University and particularly Hilconida Calumpong for providing laboratory space. This work was supported by NSF-PIRE (OISE-0,730,256) grant to KE Carpenter and PH Barber and by GIZ ACCCoast (No. 83099096). Additional funding was provided by a grant from the Gordon and Betty Moore Foundation to LWS. WAL was supported by an NSF Graduate Research Fellowship (Grant # DGE-0718124). The views expressed herein do not necessarily reflect the views of those organizations. We would like to thank individuals that aided in fieldwork and collection of samples, including K Hachenberg, CR Jadloc, O Paderanga and A Scalabrin. We would like to thank Seeb Lab members Carita Pascal and Marissa Jones for lab instruction and Jim Seeb for comments on the manuscript.

Author information

Authors and Affiliations

  1. Department of Biological Sciences, Old Dominion University, Norfolk, VA, 23529, USA

    Brian L. Stockwell & Kent E. Carpenter

  2. School of Aquatic and Fisheries Sciences, University of Washington, 1122 NE Boat St., Seattle, WA, 98105, USA

    Wesley A. Larson, Ryan K. Waples & Lisa W. Seeb

  3. Silliman University Angelo King Center for Research and Environmental Management, Dumaguete, 6200, Negros Oriental, Philippines

    Rene A. Abesamis

Authors
  1. Brian L. Stockwell
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Wesley A. Larson
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ryan K. Waples
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Rene A. Abesamis
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Lisa W. Seeb
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Kent E. Carpenter
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Brian L. Stockwell.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (XLSX 432 kb)

Supplementary material 2 (XLSX 801 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Stockwell, B.L., Larson, W.A., Waples, R.K. et al. The application of genomics to inform conservation of a functionally important reef fish (Scarus niger) in the Philippines. Conserv Genet 17, 239–249 (2016). https://doi.org/10.1007/s10592-015-0776-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-015-0776-3

Keywords

Search

Navigation