Genetic Analyses and Simulations of Larval Dispersal Reveal Distinct Populations and Directional Connectivity across the Range of the Hawaiian Grouper (Epinephelus quernus)
Integration of ecological and genetic data to study patterns of biological connectivity can aid in ecosystem-based management. Here we investigated connectivity of the Hawaiian grouper Epinephelus quernus, a species of management concern within the Main Hawaiian Islands (MHI), by comparing genetic analyses with simulated larval dispersal patterns across the species range in the Hawaiian Archipelago and Johnston Atoll. Larval simulations revealed higher dispersal from the MHI to the Northwestern Hawaiian Islands (NWHI) than in the opposite direction and evidence for a dispersal corridor between Johnston and the middle of the Hawaiian Archipelago. Genetic analyses using mitochondrial DNA (mtDNA) control region sequences and microsatellites revealed relatively high connectivity across the Hawaiian Archipelago, with the exception of genetically distinct populations and higher mtDNA diversity in the mid-Archipelago. These analyses support the preservation of the mid-archipelago as a source of genetic diversity and a region of connectivity with locations outside the Hawaiian Archipelago. Additionally, our evidence for directional dispersal away from the MHI lends caution to any management decisions that would rely on the NWHI replenishing depleted MHI stocks. 1. Introduction Growing numbers of studies are integrating ecological and genetic data to investigate population connectivity [1–3]. These techniques have the potential to facilitate ecosystem-based management by increasing our understanding of the interactions between organisms and their environment. For marine species, these techniques may be particularly valuable because population genetic studies of these species are often thought to suffer from low power and therefore to be of limited value for management [4–6]. Studies of marine species commonly reveal weak population genetic structure that is described as “chaotic” due to its apparent unpredictability over space and time [7–10]. However, this weak structure may result from factors other than high genetic connectivity. For example, the presence of large population sizes in the marine environment may prevent genetic divergence due to the slow process by which large populations achieve migration-drift equilibrium [4, 11]. Additionally, violations of the assumptions of commonly used population genetic statistical models are thought to be particularly strong for marine populations; many of these populations have spatial and temporal heterogeneity in abundance and settlement rates which violate the assumptions of constant population sizes and migration
References
[1]
S. Manel, M. K. Schwartz, G. Luikart, and P. Taberlet, “Landscape genetics: combining landscape ecology and population genetics,” Trends in Ecology and Evolution, vol. 18, no. 4, pp. 189–197, 2003.
[2]
A. Storfer, M. A. Murphy, J. S. Evans et al., “Putting the ‘landscape’ in landscape genetics,” Heredity, vol. 98, no. 3, pp. 128–142, 2007.
[3]
G. Segelbacher, S. A. Cushman, B. K. Epperson et al., “Applications of landscape genetics in conservation biology: concepts and challenges,” Conservation Genetics, vol. 11, no. 2, pp. 375–385, 2010.
[4]
R. K. Grosberg and C. W. Cunningham, “Genetic structure in the sea: from populations to communities,” in Marine Community Ecology, M. D. Bertness, M. E. Hay, and S. D. Gaines, Eds., pp. 61–84, Sinauer, Sunderland, Mass, USA, 2001.
[5]
K. A. Selkoe, C. M. Henzler, and S. D. Gaines, “Seascape genetics and the spatial ecology of marine populations,” Fish and Fisheries, vol. 9, no. 4, pp. 363–377, 2008.
[6]
R. S. Waples, A. E. Punt, and J. M. Cope, “Integrating genetic data into management of marine resources: how can we do it better?” Fish and Fisheries, vol. 9, no. 4, pp. 423–449, 2008.
[7]
M. S. Johnson and R. Black, “Chaotic genetic patchiness in an intertidal limpet, Siphonaria sp,” Marine Biology, vol. 70, no. 2, pp. 157–164, 1982.
[8]
K. A. Selkoe, S. D. Gaines, J. E. Caselle, and R. R. Warner, “Current shifts and kin aggregation explain genetic patchiness in fish recruits,” Ecology, vol. 87, no. 12, pp. 3082–3094, 2006.
[9]
S. Arnaud-Haond, V. Vonau, C. Rouxel et al., “Genetic structure at different spatial scales in the pearl oyster (Pinctada margaritifera cumingii) in French Polynesian lagoons: beware of sampling strategy and genetic patchiness,” Marine Biology, vol. 155, no. 2, pp. 147–157, 2008.
[10]
R. J. Toonen and R. K. Grosberg, “Testing hypotheses for chaotic genetic structure: patterns of spatial and temporal genetic heterogeneity among recruits, subadults and adults of the intertidal anomuran Petrolisthes cinctipes,” in Phylogeography and Population Genetics in Crustacea, S. Koenemann, C. Held, and C. Schubart, Eds., 2010.
[11]
M. E. Hellberg, “Gene flow and isolation among populations of marine animals,” Annual Review of Ecology, Evolution, and Systematics, vol. 40, pp. 291–310, 2009.
[12]
M. E. Hellberg, R. S. Burton, J. E. Neigel, and S. R. Palumbi, “Genetic assessment of connectivity among marine populations,” Bulletin of Marine Science, vol. 70, no. 1, pp. 273–290, 2002.
[13]
S. R. Palumbi, “Marine reserves and ocean neighborhoods: the spatial scale of marine populations and their management,” Annual Review of Environment and Resources, vol. 29, pp. 31–68, 2004.
[14]
K. A. Selkoe, J. R. Watson, C. White et al., “Taking the chaos out of genetic patchiness: seascape genetics reveals ecological and oceanographic drivers of genetic patterns in three temperate reef species,” Molecular Ecology, vol. 19, no. 17, pp. 3708–3726, 2010.
[15]
C. White, K. A. Selkoe, J. Watson, D. A. Siegel, D. C. Zacherl, and R. J. Toonen, “Ocean currents help explain population genetic structure,” Proceedings of the Royal Society B, vol. 277, no. 1688, pp. 1685–1694, 2010.
[16]
M. T. Craig and P. A. Hastings, “A molecular phylogeny of the groupers of the subfamily Epinephelinae (Serranidae) with a revised classification of the Epinephelini,” Ichthyological Research, vol. 54, no. 1, pp. 1–17, 2007.
[17]
W. L. Smith and M. T. Craig, “Casting the percomorph net widely: the importance of broad taxonomic sampling in the search for the placement of serranid and percid fishes,” Copeia, no. 1, pp. 35–55, 2007.
[18]
J. E. Randall, Reef and Shore Fishes of the Hawaiian Islands, Sea Grant College Program, University of Hawaii, Honolulu, Hawaii, USA, 2007.
[19]
J. Brodziak, R. Moffitt, and G. DiNardo, “Hawaiian bottomfish assessment update for 2008,” Administrative Report H-09-02, PIFSC, 2009.
[20]
A. R. Everson, “Sexual maturity and seasonal spawning of Hapuupuu, Epinephelus quernus, in Hawaii,” Administrative Report H-92-13, Southwest Fisheries Science Center, 1992.
[21]
R. S. Nichols and E. E. DeMartini, “Preliminary estimates of age and growth for the endemic Hawai‘ian grouper (Hapu‘upu‘u, Epinephelus quernus, F. Serranidae),” Administrative Report H-08-06, Pacific Islands Fisheries Science Center, 2008.
[22]
S. E. Lester, B. I. Ruttenberg, S. D. Gaines, and B. P. Kinlan, “The relationship between dispersal ability and geographic range size,” Ecology Letters, vol. 10, no. 8, pp. 745–758, 2007.
[23]
P. L. Colin, W. A. Laroche, and E. B. Brothers, “Ingress and settlement in the Nassau grouper, Epinephelus striatus (Pisces: Serranidae), with relationship to spawning occurrence,” Bulletin of Marine Science, vol. 60, no. 3, pp. 656–667, 1997.
[24]
M. R. Lara, J. Schull, D. L. Jones, and R. Allman, “Early life history stages of goliath grouper Epinephelus itajara (Pisces: Epinephelidae) from Ten Thousand Islands, Florida,” Endangered Species Research, vol. 7, no. 3, pp. 221–228, 2009.
[25]
M. A. J. Rivera, C. D. Kelley, and G. K. Roderick, “Subtle population genetic structure in the Hawaiian grouper, Epinephelus quernus (Serranidae) as revealed by mitochondrial DNA analyses,” Biological Journal of the Linnean Society, vol. 81, no. 3, pp. 449–468, 2004.
[26]
J. M. Pringle, F. Lutscher, and E. Glick, “Going against the flow: effects of non-Gaussian dispersal kernels and reproduction over multiple generations,” Marine Ecology Progress Series, vol. 377, pp. 13–17, 2009.
[27]
J. J. Polovina, P. Kleiber, and D. R. Kobayashi, “Application of TOPEX-POSEIDON satellite altimetry to simulate transport dynamics of larvae of spiny lobster, Panulirus marginatus, in the Northwestern Hawaiian Islands, 1993–1996,” Fishery Bulletin, vol. 97, no. 1, pp. 132–143, 1999.
[28]
G. S. E. Lagerloef, G. T. Mitchum, R. B. Lukas, and P. P. Niiler, “Tropical Pacific near-surface currents estimated from altimeter, wind, and drifter data,” Journal of Geophysical Research C, vol. 104, no. 10, pp. 23313–23326, 1999.
[29]
K. Weersing and R. J. Toonen, “Population genetics, larval dispersal, and connectivity in marine systems,” Marine Ecology Progress Series, vol. 393, pp. 1–12, 2009.
[30]
W. H. F. Smith and D. T. Sandwell, “Global sea floor topography from satellite altimetry and ship depth soundings,” Science, vol. 277, no. 5334, pp. 1956–1962, 1997.
[31]
R. Lumpkin and M. Pazos, “Measuring surface currents with Surface Velocity Program drifters: the instrument, its data, and some recent results,” in Lagrangian Analysis and Prediction of Coastal and Ocean Dynamics (LAPCOD), A. Griffa, A. D. Kirwan, A. J. Mariano, T. Ozgokmen, and T. Rossby, Eds., 2006.
[32]
M. A. J. Rivera, G. C. Graham, and G. K. Roderick, “Isolation and characterization of nine microsatellite loci from the Hawaiian grouper Epinephelus quernus (Serranidae) for population genetic analyses,” Marine Biotechnology, vol. 5, no. 2, pp. 126–129, 2003.
[33]
R. W. Chapman, G. R. Sedberry, C. C. Koenig, and B. M. Eleby, “Stock identification of Gag, Mycteroperca microlepis, along the Southeast Coast of the United States,” Marine Biotechnology, vol. 1, no. 2, pp. 137–146, 1999.
[34]
L. Excoffier, L. G. Laval, and S. Schneider, “Arlequin ver. 3.0: an integrated software package for population genetics data analysis,” Evolutionary Bioinformatics Online, vol. 1, pp. 47–50, 2005.
[35]
C. Van Oosterhout, W. F. Hutchinson, D. P. M. Wills, and P. Shipley, “MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data,” Molecular Ecology Notes, vol. 4, no. 3, pp. 535–538, 2004.
[36]
T. Antao, A. Lopes, R. J. Lopes, A. Beja-Pereira, and G. Luikart, “LOSITAN: a workbench to detect molecular adaptation based on a -outlier method,” BMC Bioinformatics, vol. 9, article 323, 2008.
[37]
J. Goudet, “FSTAT, a program to estimate and test gene diversities and fixation indices,” 2001, http://www2.unil.ch/popgen/softwares/fstat.htm.
[38]
H.-J. Bandelt, P. Forster, and A. R？hl, “Median-joining networks for inferring intraspecific phylogenies,” Molecular Biology and Evolution, vol. 16, no. 1, pp. 37–48, 1999.
[39]
M. T. Craig, J. A. Eble, B. W. Bowen, and D. R. Robertson, “High genetic connectivity across the Indian and Pacific Oceans in the reef fish Myripristis berndti (Holocentridae),” Marine Ecology Progress Series, vol. 334, pp. 245–254, 2007.
[40]
J. A. Eble, R. J. Toonen, and B. W. Bowen, “Endemism and dispersal: comparative phylogeography of three surgeonfishes across the Hawaiian Archipelago,” Marine Biology, vol. 156, no. 4, pp. 689–698, 2009.
[41]
M. L. Ramon, P. A. Nelson, E. De Martini, W. J. Walsh, and G. Bernardi, “Phylogeography, historical demography, and the role of post-settlement ecology in two Hawaiian damselfish species,” Marine Biology, vol. 153, no. 6, pp. 1207–1217, 2008.
[42]
E. A. Treml, P. N. Halpin, D. L. Urban, and L. F. Pratson, “Modeling population connectivity by ocean currents, a graph-theoretic approach for marine conservation,” Landscape Ecology, vol. 23, no. 1, pp. 19–36, 2008.
[43]
A. Friedlander, D. Kobayashi, B. Bowen, et al., “Connectivity and integrated ecosystem studies,” in A Marine Biogeographic Assessment of the Northwestern Hawaiian Islands, A. Friedlander, K. Keller, L. Wedding, A. Clarke, and M. Monaco, Eds., pp. 291–330, NCCOS’s Biogeography Branch in Cooperation with the Office of National Marine Sanctuaries Papahanaumokuakea Marine National Monument, Silver Spring, Md, USA, 2009.
[44]
C. E. Bird, B. S. Holland, B. W. Bowen, and R. J. Toonen, “Contrasting phylogeography in three endemic Hawaiian limpets (Cellana spp.) with similar life histories,” Molecular Ecology, vol. 16, no. 15, pp. 3173–3186, 2007.
[45]
D. Skillings, C. E. Bird, and R. J. Toonen, “Gateways to Hawai‘i—genetic population structure of the tropical sea cucumber Holothuria atra,” Journal of Marine Biology (in review).
[46]
B. Qiu, D. A. Koh, C. Lumpkin, and P. Flament, “Existence and formation mechanism of the North Hawaiian Ridge Current,” Journal of Physical Oceanography, vol. 27, no. 3, pp. 431–444, 1997.
[47]
R. W. Grigg, “Acropora in Hawaii USA 2. Zoogeography,” Pacific Science, vol. 35, pp. 15–24, 1981.
[48]
M. A. Timmers, R. J. Toonen, K. Andrews, M. J. deMaintenton, and R. Brainard, “Widespread dispersal of the crown-of-thorns sea star, Acanthaster planci, across the Hawaiian Archipelago and Johnston Atoll,” Journal of Marine Biology (in review).
[49]
A. Faucci, The influence of larval dispersal potential on speciation, phylogeography, and genetic population structure in two pacific marine snail groups, Ph.D. thesis, University of Hawai'i at Manoa, Honolulu, Hawaii, USA, 2007.
[50]
D. R. Kobayashi, “Colonization of the Hawaiian Archipelago via Johnston Atoll: a characterization of oceanographic transport corridors for pelagic larvae using computer simulation,” Coral Reefs, vol. 25, no. 3, pp. 407–417, 2006.
