Observations of migrant exchange and mixing in a coral reef fish metapopulation link scales of marine population connectivity

Journal of Heredity

Volumn 104, Issue 4, 2013, Pages 532-546

  Horne, John B ^a,d   Van Herwerden, Lynne ^a   Abellana, Sheena ^b   Mcilwain, Jennifer L ^b,c  

^a JAMES COOK UNIVERSITY   (Australia)

^b UNIVERSITY OF GUAM   (Guam)

^c CURTIN UNIVERSITY   (Australia)

^d UNIVERSITY OF ALGARVE   (Portugal)

Author keywords

Acanthuridae; kinship; Micronesia; population connectivity; recruitment

Indexed keywords

MICROSATELLITE DNA; MITOCHONDRIAL DNA;

ARTICLE; CONTROLLED STUDY; CORAL REEF; FISH; GENETIC VARIABILITY; MARINE SPECIES; METAPOPULATION; MIGRATION; NONHUMAN; PHYLOGEOGRAPHY; PRIORITY JOURNAL;

ACANTHURIDAE; KINSHIP; MICRONESIA; POPULATION CONNECTIVITY; RECRUITMENT;

ANIMAL MIGRATION; ANIMALS; COHORT STUDIES; CORAL REEFS; CROSSES, GENETIC; DEMOGRAPHY; ECOSYSTEM; FISHES; GUAM; HOMING BEHAVIOR; MICRONESIA; OBSERVATION; PHYLOGEOGRAPHY; POPULATION DYNAMICS; TIME FACTORS;

ACANTHURIDAE; ANTHOZOA; NASO UNICORNIS;

EID: 84879133456     PISSN: 00221503     EISSN: 14657333     Source Type: Journal    
DOI: 10.1093/jhered/est021     Document Type: Article

References (91)

1. Almany GR, Berumen ML, Thorrold SR, Planes S, Jones GP. 2007. Local replenishment of coral reef fish populations in a marine reserve. Science. 316:742-744
2. Armsworth PR. 2002. Recruitment limitation, population regulation, and larval connectivity in reef fish metapopulations. Ecology. 83:1092-1104
3. Avise JC, Shapiro DY. 1986. Evaluating kinship of newly settled juveniles within social groups of the coral reef fish Anthias squamipinnis. Evolution. 40:1051-1059
4. Beldade R, Holbrook SJ, Schmitt RJ, Planes S, Malone D, Bernardi G. 2012 Larger female fish contribute disproportionately more to self-replenishment. Proc R Soc Lond Ser B Biol Sci. 279:2116-2121
5. Benjamini BY, Yekutieli D. 2001. The control of the false discovery rate in multiple testing under dependency. Ann Stat. 29:1165-1188
6. Bernardi G, Beldade R, Holbrook SJ, Schmitt RJ. 2012. Full-sibs in cohorts of newly settled coral reef fishes. PLoS ONE. 7:e44953
7. Betancur-R R, Hines A, Acero AP, Orti G, Wilbur AE, Freshwater DW. 2011. Reconstructing the lionfish invasion: Insights into greater Caribbean biogeography. J Biogeography. 38:1281-1293
8. Botsford LW, Hastings A, Gaines SD. 2001. Dependence of sustainability on the configuration of marine reserves and larval dispersal distance. Ecol Lett. 4:144-150
9. Buston PM, Fauvelot C, Wong MY, Planes S. 2009. Genetic relatedness in groups of the humbug damselfish Dascyllus aruanus: Small, similar-sized individuals may be close kin. Mol Ecol. 18:4707-4715
10. Buston PM, Jones GP, Planes S, Thorrold SR. 2012. Probability of successful larval dispersal declines fivefold over 1 km in a coral reef fish. Proc R Soc Lond Ser B Biol Sci. 279:1883-1888
11. Butler MJ, Paris CB, Goldstein JS, Matsuda H, Cowen RK. 2011. Behavior constrains the dispersal of long-lived spiny lobster dispersal. Mar Ecol Prog Ser. 422:223-237
12. Chapuis MP, Estoup A. 2007. Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol. 24:621-631
13. Christie MR, Johnson DW, Stallings CD, Hixon MA. 2010a. Self-recruitment and sweepstakes reproduction amid extensive gene flow in a coral-reef fish. Mol Ecol. 19:1042-1057
14. Christie MR, Tissot BN, Albins MA, Beets JP, Jia Y, Ortiz DM, Thompson SE, Hixon MA. 2010b. Larval connectivity in an effective network of marine protected areas. PLoS ONE. 5:e15715
15. Cowen RK, Sponaugle S. 2009. Larval dispersal and marine population connectivity. Ann Rev Mar Sci. 1:443-466
16. Doherty PJ. 1991. Spatial and temporal patterns in recruitment. In: Sale PF, editor. The ecology of fishes on coral reefs. San Diego (CA): Academic Press. p. 261-292
17. Doherty PJ, Dufour V, Galzin R, Hixon MA, Meekan MG, Planes S. 2004 High mortality during settlement is a population bottleneck for a tropical surgeonfish. Ecology. 85:2422-2428
18. Domeier ML, Colin PL. 1997. Tropical reef fish spawning aggregations: Defined and reviewed. Bull Mar Sci. 60:698-726
19. Eble JA, Toonen RJ, Sorenson L, Basch LV, Papastamatiou YP, Bowen BW. 2011. Escaping paradise: Larval export from Hawaii in an Indo-Pacific reef fish, the Yellow Tang Zebrasoma flavescens. Mar Ecol Prog Ser. 428:245-258
20. 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. 10:564-567
21. Fisher R, Hogan JD. 2007. Morphological predictors of swimming speed: A case study of pre-settlement juvenile coral reef fishes. J Exp Biol. 210(Pt 14):2436-2443
22. Fogarty MJ, Botsford LW. 2007. Population connectivity and spatial management of marine fisheries. Oceanography. 20:112-123
23. Gaither MR, Bowen BW, Toonen RJ, Planes S, Messmer V, Earle J, Ross Robertson D. 2010. Genetic consequences of introducing allopatric lineages of Bluestriped Snapper (Lutjanus kasmira) to Hawaii. Mol Ecol. 19:1107-1121
24. Gerlach G, Atema J, Kingsford MJ, Black KP, Miller-Sims V. 2007. Smelling home can prevent dispersal of reef fish larvae. Proc Natl Acad Sci U S A. 104:858-863
25. Gilbert-Horvath EA, Larson RJ, Garza JC. 2006. Temporal recruitment patterns and gene flow in kelp rockfish (Sebastes atrovirens). Mol Ecol. 15:3801-3815
26. Goudet J. 2001. FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3)[Internet]. Available from: Http://www2.unil. ch/popgen/softwares/fstat.htm
27. Guo SW, Thompson EA. 1992. Performing the exact test of Hardy-Weinberg proportion for multiple alleles. Biometrics. 48:361-372
28. Hall TA. 1999. BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acid Symp Ser. 41:95-98
29. Harrison HB, Williamson DH, Evans RD, Almany GR, Thorrold SR, Russ GR, Feldheim KA, van Herwerden L, Planes S, Srinivasan M, et al. 2012 Larval export from marine reserves and the recruitment benefit for fish and fisheries. Curr Biol. 22:1023-1028
30. Hastings A, Botsford LW. 2006. Persistence of spatial populations depends on returning home. Proc Natl Acad Sci U S A. 103:6067-6072
31. Hedgecock D, Barber PH, Edmands S. 2007. Genetic approaches to measuring marine connectivity. Oceanography. 20:70-79
32. Hellberg ME. 2007. Footprints on water: The genetic wake of dispersal among reefs. Coral Reefs. 26:463-473
33. Hellberg ME, Burton RS, Neigel JE, Palumbi SR. 2002. Genetic assessment of connectivity among marine populations. Bull Mar Sci. 70:S273-S290
34. Hepburn RI, Sale PF, Dixon B, Heath DD. 2009. Genetic structure of juvenile cohorts of bicolor damselfish (Stegastes partitus) along the Meso-American barrier reef: Chaos through time. Coral Reefs. 28:277-288
35. Higgins D, Thompson J, Gibson T, Thompson JD, Higgins DG, Gibson TJ. 1994. CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucl Acid Res. 22:4673-4680
36. Hixon MA. 2011. 60 years of coral reef fish ecology: Past, present and future. Bull Mar Sci. 87:727-765
37. Hixon MA, Webster MS. 2002. Density dependence in reef fish populations. In: Sale PF, editor. Coral reef fishes: Dynamics and diversity in a complex ecosystem. San Diego (CA): Academic Press. p. 303-325
38. Hoey AS, Bellwood DR. 2009. Limited functional redundancy in a high diversity ecosystem: Single species dominates key ecological process on coral reefs. Ecosystems. 12:1316-1328
39. Horne JB, McIlwain JL, van Herwerden L. 2010. Isolation of 15 new polymorphic microsatellite markers from the bluespine unicornfish Naso unicornis. Conserv Genet Resour. 2:191-194
40. Horne JB, Momigliano P, Welch DJ, Newman SJ, Van Herwerden L. 2011 Limited ecological population connectivity suggests low demands on selfrecruitment in a tropical inshore marine fish (Eleutheronema tetradactylum: Polynemidae). Mol Ecol. 20:2291-2306
41. Horne JB, van Herwerden L. Forthcoming. 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. doi:10.1111/jeb.12092
42. Horne JB, van Herwerden L, Choat JH, Robertson DR. 2008. High population connectivity across the Indo-Pacific: Congruent lack of phylogeographic structure in three reef fish congeners. Mol Phylogenet Evol. 49:629-638
43. Houk P, Rhodes K, Cuetos-Bueno J, Lindfield S, Fread V, McIlwain JL. 2012. Commercial coral reef-fisheries across Micronesia: A need for improving management. Coral Reefs. 31:13-26
44. Jombart T. 2008. adegenet: A R package for the multivariate analysis of genetic markers. Bioinformatics. 24:1403-1405
45. 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
46. Jones GP, Almany GR, Russ GR, Sale PF, Steneck RS, van Oppen MJH, Willis BL. 2009. Larval retention and connectivity among populations of corals and reef fishes: History, advances and challenges. Coral Reefs. 28:307-325
47. Jones DB, Jerry DR, McCormick MI, Bay LK. 2010. The population genetic structure of a common tropical damselfish on the Great Barrier Reef and eastern Papua New Guinea. Coral Reefs. 29:455-467
48. Jones GP, Milicich MJ, Emslie MJ, Lunow C. 1999. Self-recruitment in a coral reef fish population. Nature. 402:802-804
49. Jones GP, Planes S, Thorrold SR. 2005. Coral reef fish larvae settle close to home. Curr Biol. 15:1314-1318
50. Jost L. 2008. G(ST) and its relatives do not measure differentiation. Mol Ecol. 17:4015-4026
51. Klanten SO, Choat JH, van Herwerden L. 2007. Extreme genetic diversity and temporal rather than spatial partitioning in a widely distributed coral reef fish. Mar Biol. 150:659-670
52. Konovalov DA, Heg D. 2008. A maximum-likelihood relatedness estimator allowing for negative relatedness values. Mol Ecol Resour. 8:256-263
53. Konovalov DA, Manning C, Henshaw MT. 2004. Kingroup: A program for pedigree relationship reconstruction and kin group assignments using genetic markers. Mol Ecol Notes. 4:779-782
54. Kritzer JP, Sale PF. 2006. Marine metapopulations. London: Academic Press
55. Lee HJE. 2009. Spatial and temporal population genetic structure of four northeastern Pacific littorinid gastropods: The effect of mode of larval development on variation at one mitochondrial and two nuclear DNA markers. Mol Ecol. 18:2165-2184
56. Librado P, Rozas J. 2009. DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics. 25:1451-1452
57. Lieske E, Myers R. 1994. Collins pocket guide. Coral reef fishes. Indo-Pacific and Caribbean including the Red Sea. New York: Harper Collins
58. Lynch M, Ritland K. 1999. Estimation of pairwise relatedness with molecular markers. Genetics. 152:1753-1766
59. Manel S, Gaggiotti OE, Waples RS. 2005. Assignment methods: Matching biological questions with appropriate techniques. Trends Ecol Evol. 20:136-142
60. Moberg PE, Burton RS. 2000. Genetic heterogeneity among adult and recruit red sea urchins, Strongylocentrotus franciscanus. Mar Biol. 136:773-784
61. Mora C, Treml EA, Roberts J, Crosby K, Roy D, Tittensor DP. 2012. High connectivity among habitats precludes the relationship between dispersal and range size in tropical reef fishes. Ecography. 35:89-96
62. Narum SR. 2006. Beyond Bonferroni: Less conservative analyses for conservation genetics. Conserv Genet. 7:783-787
63. Oliehoek PA, Windig JJ, van Arendonk JA, Bijma P. 2006. Estimating relatedness between individuals in general populations with a focus on their use in conservation programs. Genetics. 173:483-496
64. Palumbi SR. 2003. Population genetics, demographic connectivity and the design of marine reserves. Ecol Appl. 13:S146-S158
65. Patterson HM, Swearer SE. 2007. Long-distance dispersal and local retention of larvae as mechanisms of recruitment in an island population of coral reef fish. Austral Ecol. 32:122-130
66. 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
67. Planes S, Jones GP, Thorrold SR. 2009. Larval dispersal connects fish populations in a network of marine protected areas. Proc Natl Acad Sci U S A. 106:5693-5697
68. Planes S, Lecaillon G, Lenfant P, Meekan M. 2002. Genetic and demographic variation in new recruits of Naso unicornis. J Fish Biol. 61:1033-1049
69. Planes S, Lenfant P. 2002. Temporal change in the genetic structure between and within cohorts of a marine fish, Diplodus sargus, induced by a large variance in individual reproductive success. Mol Ecol. 11:1515-1524
70. Priest MA, Halford AR, McIlwain JL. 2012. Evidence of stable genetic structure across a remote island archipelago through self-recruitment in a widely dispersed coral reef fish. Ecol Evol. 2:3195-3213
71. Pringle JM, Wares JP. 2007. Going against the flow: Maintenance of alongshore variation in allele frequency in a coastal ocean. Mar Ecol Prog Ser. 335:69-84
72. Pritchard JK, Stephens M, Donnelly P. 2000. Inference of population structure using multilocus genotype data. Genetics. 155:945-959
73. Queller DC, Goodnight KF. 1989. Estimating relatedness using genetic markers. Evolution. 43:258-275
74. R Development Core Team. 2009. R: A language and environment for statistical computing [Internet]. Vienna (Austria): R Foundation for Statistical Computing. Available from: Http://www.r-project.org
75. Rhodes KL, Tupper MH, Wichilmel CB. 2008. Characterization and management of the commercial sector of the Pohnpei coral reef fish fishery, Micronesia. Coral Reefs. 27:443-454
76. Rousset F. 2008. genepop'007: A complete re-implementation of the genepop software for Windows and Linux. Mol Ecol Resour. 8:103-106
77. Saenz-Agudelo P, Jones GP, Thorrold SR, Planes S. 2011. Connectivity dominates larval replenishment in a coastal reef fish metapopulation. Proc R Soc Lond Ser B Biol Sci. 278:2954-2961
78. Sale PF. 1991. Reef fish communities: Open nonequilibrial systems. In: Sale PF, editor. The ecology of fishes on coral reefs. San Diego (CA): Academic Press. p. 564-598
79. Selkoe KA, Gaines SD, Caselle JE, Warner RR. 2006. Current shifts and kin aggregation explain genetic patchiness in fish recruits. Ecology. 87:3082-3094
80. Siegel DA, Mitarai S, Costello CJ, Gaines SD, Kendall BE, Warner RR, Winters KB. 2008. The stochastic nature of larval connectivity among nearshore marine populations. Proc Natl Acad Sci U S A. 105:8974-8979
81. Slatkin M. 1977. Gene flow and genetic drift in a species subject to frequent local extinctions. Theor Popul Biol. 12:253-262
82. Slatkin M. 1985. Rare alleles as indicators of gene flow. Evolution. 39:53-65
83. Small ST, Wares JP. 2010. Phylogeography and marine retention. J Biogeogr. 37:781-784
84. Swearer SE, Caselle JE, Lea DW, Warner RR. 1999. Larval retention and recruitment in an island population of a coral-reef fish. Nature. 402: 799-802
85. van Oosterhout C, 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
86. Vigliola L, Doherty PJ, Meekan MG, Drown DM, Jones ME, Barber PH. 2007. Genetic identity determines risk of post-settlement mortality of a marine fish. Ecology. 88:1263-1277
87. Walsh PS, Metzger DA, Higuchi R. 1991. Chelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. BioTechniques. 10:506-513
88. Wang J. 2002. An estimator for pairwise relatedness using molecular markers. Genetics. 160:1203-1215
89. 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
90. Weir BS, Anderson AD, Helper AB. 2006. Genetic relatedness analysis: Modern data and new challenges. Nat Rev Genet. 7:771-780
91. Wilson DT, McCormick MI. 1999. Microstructure of settlement marks in the otoliths of tropical reef fishes. Mar Biol. 134:29-41 Program