Genetic diversity, population structure, and demographic history of exploited sea urchin populations (Tripneustes gratilla) in the Philippines

Journal of Experimental Marine Biology and Ecology

Volumn 449, Issue , 2013, Pages 284-293

  Casilagan, Inggat Laya N ^a   Juinio Meñez, Marie Antonette ^a   Crandall, Eric D ^b,c  

^a University of the Philippines Diliman   (Philippines)

^b SOUTHWEST FISHERIES SCIENCE CENTER   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Demographic history; Genetic homogeneity; Microsatellite; MtDNA; Population genetics; Sea urchin

Indexed keywords

COMMERCIAL SPECIES; DEMOGRAPHIC HISTORY; ECHINODERM; EVOLUTIONARY BIOLOGY; GENETIC MARKER; GENETIC VARIATION; HOMOGENEITY; PLEISTOCENE; POPULATION DECLINE; POPULATION DISTRIBUTION; POPULATION GENETICS; POPULATION STRUCTURE; STOCK COLLAPSE;

PHILIPPINES;

EID: 84886862429     PISSN: 00220981     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jembe.2013.09.012     Document Type: Article

References (114)

1. Addison J.A., Hart M.W. Analysis of population genetic structure of the green sea urchin (Strongylocentrotus droebachiensis) using microsatellites. Mar. Biol. 2004, 144:243-251.
2. Addison J.A., Ort B.S., Mesa K.A., Pogson G.H. Range-wide genetic homogeneity in the California sea mussel (Mytilus californianus): a comparison of allozymes, nuclear DNA markers, and mitochondrial DNA sequences. Mol. Ecol. 2008, 17:4222-4232.
3. Alcoverro T., Mariani S. Effects of sea urchin grazing on seagrass (Thalassodendron ciliatum) beds of a Kenyan lagoon. Mar. Ecol. Prog. Ser. 2002, 226:255-263.
4. Andrew N., Agatsuma Y., Ballesteros E., Bazhin A., Creaser E., Barnes D., Botsford L.W., Bradbury A., Campbell A., Dixon J., Einarsson S., Gerring P., Hebert K., Hunter M., Hur S., Johnson C., Juinio-Meñez M.A., Kalvass P., Miller R., Moreno C., Palleiro J., Rivas D., Robinson S., Schroeter S.C., Steneck R.S., Vadas R., Woodby D., Xiaoqi Z. Status and management of world sea urchin fisheries. Oceanogr. Mar. Biol. Annu. 2002, 40:343-425.
5. Avise J.C., Arnold J., Ball R.M., Bermingham E., Lamb T., Neigel J.E., Reeb C.A., Saunders N.C. Intraspecific phylogeography: the population genetics and systematics. Annu. Rev. Ecol. Syst. 1987, 18:489-522.
6. Ballard J.W.O., Whitlock M.C. The incomplete natural history of mitochondria. Mol. Ecol. 2004, 13:729-744.
7. Bangi H.G.P. The Effect of Adult Nutrition on Somatic and Gonadal Growth, Egg Quality, and Larval Development of the Sea Urchin Tripneustes gratilla (Echinodermata: Echinoidea) 2001, (MS Thesis), University of the Philippines - Diliman, (106 pp.).
8. Barber P., Erdmann M., Palumbi S.R. Comparative phylogeography of three codistributed stomatopods: origins and timing of regional lineage diversification in the coral triangle. Evolution 2006, 60:1825-1839.
9. Beerli P., Palczewski M. Unified framework to evaluate panmixia and migration direction among multiple sampling locations. Genetics 2010, 185:313-326.
10. Benzie J.A.H. Genetic structure of coral reef organisms: ghosts of dispersal past. Coral Reefs 1999, 145:131-145.
11. Benzie J., Ballment E., Forbes A., Demetriades N., Sugama K., Moria S. Mitochondrial DNA variation in Indo-Pacific populations of the giant tiger prawn, Penaeus monodon. Mol. Ecol. 2002, 11:2553-2569.
12. Bernardo L.P. Development of a Particle Dispersal Model for Bohol Sea (Philippines) 2011, (MS Thesis), University of the Philippines - Diliman, (139 pp.).
13. Bowen B.W., Shanker K., Yasuda N., Malay M.C.D., von der Heyden S., Paulay G., Rocha L.A., Selkoe K.A., Barber P.H., Williams S.T., Lessios H.A., Crandall E.D., Bernardi G., Meyer C.P., Carpenter K.E., Toonen R.J. Phylogeography unplugged: comparative geographic surveys in the genomic era. Bull. Mar. Sci. 2013, 90.
14. Brookfield J.F.Y. A simple new method for estimating null allele frequency from heterozygote deficiency. Mol. Ecol. 1996, 5:453-455.
15. Calderón I., Giribet G., Turon X. Two markers and one history: phylogeography of the edible common sea urchin Paracentrotus lividus in the Lusitanian region. Mar. Biol. 2008, 154:137-151.
16. Carlon D.B., Lippé C. Eleven new microsatellite markers for the tropical sea urchin Tripneustes gratilla and cross-amplification in Tripneustes ventricosa. Mol. Ecol. Notes 2007, 7:1002-1004.
17. Casilagan I.L.N. Spatial and Temporal Aspects of Genetic Variation in Sea Urchin, Tripneustes gratilla Populations in Western Luzon, Philippines 2011, (MS Thesis), University of the Philippines - Diliman, (95 pp.).
18. Charlesworth B., Morgan M., Charlesworth D. The effect of deleterious mutations on neutral molecular variation. Genetics 1993, 134:1289-1303.
19. Chia F.S., Buckland-Nicks J., Young C.M. Locomotion of marine invertebrate larvae: a review. Can. J. Zool. 1984, 62(7):1205-1222.
20. Clement M., Posada D., Crandall K.A. TCS: a computer program to estimate gene genealogies. Mol. Ecol. 2000, 9:1657-1659.
21. Conklin E.J., Smith J.E. Abundance and spread of the invasive red algae, Kappaphycus spp. Biol. Invasions 2005, 7:1029-1039. K. ohe Bay (Ed.).
22. Corander J., Marttinen P., Sirén J., Tang J. Enhanced Bayesian modelling in BAPS software for learning genetic structures of populations. BMC Bioinforma. 2008, 9:539.
23. Cornuet J.M., Luikart G. Power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 1996, 144:2001-2014.
24. Cowen R.K., Sponaugle S. Larval dispersal and marine population connectivity. Annu. Rev. Mar. Sci. 2009, 1:443-466.
25. Crandall E.D., Frey M.A., Grosberg R.K., Barber P.H. Contrasting demographic history and phylogeographical patterns in two Indo-Pacific gastropods. Mol. Ecol. 2008, 17:611-626.
26. Crandall E.D., Jones M.E., Muñoz M., Akinronbi B., Erdmann M.V., Barber P.H. Comparative phylogeography of two seastars and their ectosymbionts within the Coral Triangle. Mol. Ecol. 2008, 17:5276-5290.
27. Crandall E.D., Sbrocco E.J., Deboer T.S., Barber P.H., Carpenter K.E. Expansion dating: calibrating molecular clocks in marine species from expansions onto the Sunda Shelf following the Last Glacial Maximum. Mol. Biol. Evol. 2012, 29:707-719.
28. Crandall E.D., Treml E.A., Barber P.H. Coalescent and biophysical models of stepping-stone gene flow in neritid snails. Mol. Ecol. 2012, 21:5579-5598.
29. Crawford N.G. SMOGD: software for the measurement of genetic diversity. Mol. Ecol. Resour. 2010, 10:556-557.
30. Crow J.F., Aoki K. Group selection for a polygenic behavioral trait: estimating the degree of population subdivision. Proc. Natl. Acad. Sci. U. S. A. 1984, 81:6073-6077.
31. Dibattista J.D., Rocha L.A., Craig M.T., Feldheim K.A., Bowen B.W. Phylogeography of two closely related Indo-Pacific butterflyfishes reveals divergent evolutionary histories and discordant results from mtDNA and microsatellites. J. Hered. 2012, 103:617-629.
32. Doherty P., Planes S., Mather P. Gene flow and larval duration in seven species of fish from the Great Barrier Reef. Ecology 1995, 76:2373-2391.
33. Drummond A.J., Rambaut A., Shapiro B., Obexer-Ruff G. Bayesian coalescent inference of past population dynamics from molecular sequences. Mol. Biol. Evol. 2005, 22:1185-1192.
34. Edgar R.C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004, 32:1792-1797.
35. Eklöf J.S., De la Torre-Castro M., Gullström M., Uku J., Muthiga N., Lyimo T., Bandeira S.O. Sea urchin overgrazing of seagrasses: a review of current knowledge on causes, consequences, and management. Estuar. Coast. Shelf Sci. 2008, 79:569-580.
36. Emerson B.C., Paradis E., Thébaud C. Revealing the demographic histories of species using DNA sequences distributions. Trends Ecol. Evol. 2001, 16:707-716.
37. Emlet R.B., Young C.M., George S.B. Phylum Echinodermata: Echinoidea. Atlas of Marine Invertebrate Larvae 2006, 531-551. Elsevier, (Barcelona). C.M. Young, M.A. Sewell, M.E. Rice (Eds.).
38. Excoffier L., Lischer H.E.L. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol. Ecol. Resour. 2010, 10:564-567.
39. Excoffier L., Foll M., Petit R.J. Genetic consequences of range expansions. Annu. Rev. Ecol. Evol. Syst. 2009, 40:481-501.
40. Fu Y. Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 1997, 147:915-925.
41. Hare M.P., Nunney L., Schwartz M.K., Ruzzante D.E., Burford M., Waples R.S., Ruegg K., Palstra F. Understanding and estimating effective population size for practical application in marine species management. Conserv. Biol. 2011, 25:438-449.
42. Goudet J. FSTAT version 1.2: a computer program to calculate F statistics. J. Hered. 1995, 86:485-486.
43. Hedgecock D. Temporal and spatial genetic structure of marine animal populations in the California Current. California Cooperative Oceanic Fisheries Investigations Reports 1994, 35:73-81.
44. Hedgecock D., Pudovkin A.I. Sweepstakes reproductive success in highly fecund marine fish and shellfish: a review and commentary. Bull. Mar. Sci. 2011, 87(4):971-1002.
45. Hedgecock D., Barber P.H., Edmands S. Genetic approaches to measuring connectivity. Oceanography 2007, 20:70-79.
46. Hellberg M.E. Gene flow and isolation among populations of marine animals. Annu. Rev. Ecol. Syst. 2009, 40:291-310.
47. Jensen J.L., Bohonak A.J., Kelley S.T. Isolation by distance, web service. BMC Genet. 2005, 6:13.
48. Juinio-Meñez M.A., Villanoy C.L. Sea urchin recruitment studies for management considerations. Proceedings of the Joint Seminar on Marine Science at the 4th Meeting of the LIPI-JSPS 1994, 15-20. Indonesian Institute of Science (LIPI), (Jakarta, Indonesia). S. Soemodihardjo, K. Tsukamoto, K. Romimoharto (Eds.).
49. Juinio-Meñez M.A., Macawaris N., Bangi H.G.P. Community-based sea urchin (Tripneustes gratilla) grow-out culture as a resource management tool. Proceedings of the North Pacific Symposium on Invertebrate Stock Assessment and Management 1998, 393-399. Can. Spec. Publ. Fish. Aquat. Sci. G.S. Jamieson, A. Campbell (Eds.).
50. Juinio-Meñez M.A., Magsino R.M., Ravago-Gotanco R.G., Yu E.T. Genetic structure of Linckia laevigata and Tridacna crocea populations among Palawan shelf & shoal reefs. Mar. Biol. 2003, 142:717-726.
51. Juinio-Meñez M.A., Bangi H.G.P., Malay M.C.D., Pastor D. Enhancing the recovery of depleted Tripneustes gratilla stocks through grow-out culture and restocking. Rev. Fish. Sci. 2008, 16:35-43.
52. Juinio-Meñez M., Pastor D., Bangi H.G.P. Indications of recruitment enhancement in the sea urchin Tripneustes gratilla due to stock restoration efforts. Proceedings of the 11th International Coral Reef Symposium 2009, 1017-1021. Nova Southeastern University - National Coral Reef Institute, (Ft. Lauderdale, Florida).
53. Klumpp D.W., Salita-Espinosa J.T., Fortes M.D. Feeding ecology and trophic role of sea urchins in a tropical seagrass community. Aquat. Bot. 1993, 45:205-229.
54. Kochzius M., Seidel C., Hauschild J., Kirchhoff S., Mester P., Meyer-Wachsmuth I., Nuryanto A., Timm J. Genetic population structures of the blue starfish Linckia laevigata and its gastropod ectoparasite Thyca crystallina. Mar. Ecol. Prog. Ser. 2009, 396:211-219.
55. Koike I., Mukai H., Nojima S. The role of the sea urchin, Tripneustes gratilla (Linnaeus), in decomposition and nutrient cycling in a tropical seagrass bed. Ecol. Res. 1987, 2:19-29.
56. Larson R.J., Julian R. Spatial and temporal genetic patchiness in marine populations and their implications for fisheries management. California Cooperative Oceanic Fisheries Investigations Report 1999, 40:94-99.
57. Lawrence J., Agatsuma Y. The ecology of Tripneustes. Edible Sea Urchins: Biology and Ecology 2 2001, 395-413. Elsevier Science, Amsterdam. J. Lawrence (Ed.).
58. Lessios H.A., Kane J., Robertson D.R. Phylogeography of the pantropical sea urchin Tripneustes: contrasting patterns of population structure between oceans. Evolution 2003, 57:2026-2036.
59. Liu Z.J., Cordes J.F. DNA marker technologies and their applications in aquaculture genetics. Aquaculture 2004, 238:1-37.
60. Liu J.-X., Gao T.-X., Wu S.-F., Zhang Y.-P. Pleistocene isolation in the Northwestern Pacific marginal seas and limited dispersal in a marine fish, Chelon haematocheilus (Temminck & Schlegel, 1845). Mol. Ecol. 2007, 16:275-288.
61. Lowe W.H., Allendorf F.W. What can genetics tell us about population connectivity?. Mol. Ecol. 2010, 19:3038-3051.
62. Magsino R.M., Juinio-Meñez M.A. 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. 2008, 154:519-532.
63. Malay M., Juinio-Meñez M., Villanoy C. Population genetic structure of the sea urchin Tripneustes gratilla from selected sites in western Luzon and eastern Philippines. Proceedings 9th International Coral Reef Symposium 2002, 1-5. Ministry of Environment, Indonesian Institute of Sciences, and International Society for Reef Studies, (Bali, Indonesia).
64. Manel S., Gaggiotti O.E., Waples R.S. Assignment methods: matching biological questions with appropriate techniques. Trends Ecol. Evol. 2005, 20:136-142.
65. Marko P.B., Hart M.W. The complex analytical landscape of gene flow inference. Trends Ecol. Evol. 2011, 26:448-456.
66. McCartney M., Keller G., Lessios H.A. Dispersal barriers in tropical oceans and speciation in Atlantic and eastern Pacific sea urchins of the genus Echinometra. Mol. Ecol. 2000, 9:1391-1400.
67. McCook L.J., Almany G.R., Berumen M.L., Day J.C., Green A.L., Jones G.P., Leis J.M., Planes S., Russ G.R., Sale P.F., Thorrold S.R. Management under uncertainty: guide-lines for incorporating connectivity into the protection of coral reefs. Coral Reefs 2009, 28:353-366.
68. Miller M.P. Tools for Population Genetic Analyses (TFPGA). A Windows program for the analysis of allozyme and molecular population genetic data. Ver. 1.3 Available via. http://bioweb.usu.edu/mpmbio.
69. Moritz C. Defining 'evolutionarily significant units' for conservation. Trends Ecol. Evol. 1994, 9:373-374.
70. Nei M. Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 1978, 89:583-590.
71. Ovenden J.R., Peel D., Street R., Courtney A.J., Hoyle S.D., Peel S.L., Podlich H. The genetic effective and adult census size of an Australian population of tiger prawns (Penaeus esculentus). Mol. Ecol. 2007, 16:127-138.
72. Palumbi S.R. Population genetics, demographic connectivity, and the design of marine reserves. Ecol. Appl. 2003, 13:146-158.
73. Palumbi S.R. Marine reserves and ocean neighborhoods: the spatial scale of marine populations and their management. Annu. Rev. 2004, 29:31-68.
74. Palumbi S.R., Lessios H.A. Evolutionary animation: how do molecular phylogenies compare to Mayr's reconstruction of speciation patterns in the sea?. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:6566-6572.
75. Pearse D.E., Crandall K.A. Beyond FST: analysis of population genetic data for conservation. Fish. Sci. 2004, 5:585-602.
76. Pike N. Using false discovery rates for multiple comparisons in ecology and evolution. Methods Ecol. Evol. 2011, 2:278-282.
77. Piry S., Luikart G., Cornuet J.M. BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data. J. Hered. 1999, 502-503.
78. Posada D. jModelTest: phylogenetic model averaging. Mol. Biol. Evol. 2008, 25:1253-1256.
79. Rambaut A. FigTree v1.3.1 http://tree.bio.ed.ac.uk/software/figtree.
80. Rambaut A., Drummond A.J. Tracer v1.5 Available via. http://tree.bio.ed.ac.uk/software/tracer.
81. Ravago-Gotanco R.G., Juinio-Meñez M.A. Phylogeography of the mottled spinefoot Siganus fuscescens: Pleistocene divergence and limited genetic connectivity across the Philippine archipelago. Mol. Ecol. 2010, 1-15.
82. Rohfritsch A., Borsa P. Genetic structure of Indian scad mackerel Decapterus russelli: Pleistocene vicariance and secondary contact in the Central Indo-West Pacific Seas. Heredity 2005, 95:315-326.
83. Rohling E.J., Fenton M., Jorissen F.J., Bertrand P., Ganssen G., Caulet J.P. Magnitudes of sea-level lowstands of the past 500,000years. Nature 1998, 394:162-165.
84. Rousset F. GENEPOP'007: a complete re-implementation of the GENEPOP software for Windows and Linux. Mol. Ecol. Resour. 2008, 8:103-106.
85. Roy K., Valentine J.W., Jablonski D., Kidwell S.M. Scales of climatic variability and time averaging in Pleistocene biotas: implications for ecology and evolution. Trends Ecol. Evol. 1996, 11:458-463.
86. Ryman N., Laikre L. Effects of supportive breeding on the genetically effective population size. Conserv. Biol. 1991, 5:325-329.
87. Saenz-Agudelo P., Jones G.P., Thorrold S.R., Planes S. Connectivity dominates larval replenishment in a coastal reef fish metapopulation. Proc. R. Soc. B Biol. 2011, 278:2954-2961.
88. Selkoe K.A., Toonen R.J. Microsatellites for ecologists: a practical guide to using and evaluating microsatellite markers. Ecol. Lett. 2006, 9:615-629.
89. Shimabukuro S. Tripneustes gratilla (sea urchin). Aquaculture in Tropical Areas 1991, 313-318. Midori Shobo Co. Ltd., Japan. S.K. Shokita, K. Kakasu, A. Tomori, T. Toma (Eds.).
90. Siddall M., Rohling E., Almogi-Labin A., Hemleben C., Meischner D., Schmelzer I., Smeed D.A. Sea-level fluctuations during the last glacial cycle. Nature 2003, 423:853-858.
91. Slatkin M. Isolation by distance in equilibrium and non-equilibrium populations. Evolution 1993, 47:264-279.
92. Stimson J., Cunha T., Philippoff J. Food preferences and related behavior of the browsing sea urchin Tripneustes gratilla (Linnaeus) and its potential for use as a biological control agent. Mar. Biol. 2007, 151:1761-1772.
93. Talaue-McManus L., Kesner K. Valuation of a Philippine municipal sea urchin fishery and implications of its collapse. Philippine Coastal Resources Under Stress 1995, 229-239.
94. Tamura K., Dudley J., Nei M., Kumar S. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 2007, 24:1596-1599.
95. Thorpe J.P., Sole-Cava A.M., Watts P.C. Exploited marine invertebrates: genetics and fisheries. Hydrobiologia 2000, 420:165-184.
96. Toonen R.J., Hughes S. Increased throughput for fragment analysis on ABI Prism 377 automated sequencer using a membrane comb and STRand software. Biotechniques 2001, 31:1320-1324.
97. Tuason A.Y. The Reproductive Biology of Tripneustes gratilla (Linnaeus) (Echinodermata: Echinoidea) with Some Notes on Diadema setosum (Leske) 1980, (MS Thesis), University of the Philippines - Diliman, (77 pp.).
98. Valentine J., Edgar G. Impacts of a population outbreak of the urchin Tripneustes gratilla amongst Lord Howe Island coral communities. Coral Reefs 2010, 29:399-410.
99. Van Oosterhout C., Hutchinson W. MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol. Ecol. 2004, 4:535-538.
100. Van Oppen M.J.H., Lutz A., De'ath G., Peplow L., Kininmonth S. Genetic traces of recent long-distance dispersal in a predominantly self-recruiting coral. PLoS One 2008, 3:e3401.
101. Verhoeven K.J., Simonsen K.L., McIntyre L.M. Implementing false discovery rate control: increasing your power. Oikos 2005, 108:643-647.
102. Villesen P. FaBox: an online toolbox for fasta sequences. Mol. Ecol. Notes 2007, 7:965-968.
103. Voris H.K. Maps of Pleistocene sea levels in Southeast Asia: shorelines, river systems and time durations. J. Biogeogr. 2000, 27:1153-1167.
104. Walsh P.S., Metzger D.A., Higuchi R. Chelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Biotechniques 1991, 10:506.
105. Waples R.S. A multispecies approach to the analysis of gene flow in marine shore fishes. Evolution 1987, 41:385-400.
106. Waples R.S. A bias correction for estimates of effective population size based on linkage disequilibrium at unlinked gene loci*. Conserv. Genet. 2006, 7:167-184.
107. Waples R.S., Do C. LDNe: a program for estimating effective population size from data on linkage disequilibrium. Mol. Ecol. Resour. 2008, 8:753-756.
108. Waples R.S., Do C. Linkage disequilibrium estimates of contemporary Ne using highly variable genetic markers: a largely untapped resource for applied conservation and evolution. Evol. Appl. 2010, 3(3):244-262.
109. Waples R.S., England P.R. Estimating contemporary effective population size on the basis of linkage disequilibrium in the face of migration. Genetics 2011, 189:633-644.
110. Ward R.D. The importance of identifying spatial population structure in restocking and stock enhancement programmes. Fish. Res. 2006, 80:9-18.
111. Watts R.J., Johnson M.S., Black R. Effects of recruitment on genetic patchiness in the urchin Echinometra mathaei in Western Australia. Mar. Biol. 1990, 105:145-151.
112. Weersing K., Toonen R.J. Population genetics, larval dispersal, and connectivity in marine systems. Mar. Ecol. Prog. Ser. 2009, 393:1-12.
113. Zhang Z., Schwartz S., Wagner L., Miller W. A greedy algorithm for aligning DNA sequences. J. Comput. Biol. 2000, 7:203-214.
114. Zigler K.S., Lessios H. 250 million years of bindin evolution. Biol. Bull. 2003, 205:8-15.