Populations and Pathways: Genomic Approaches to Understanding Population Structure and Environmental Adaptation

  • Melody S. Clark
  • Arnaud Tanguy
  • Didier Jollivet
  • François Bonhomme
  • Bruno Guinand
  • Frédérique Viard
Chapter
Part of the Advances in Marine Genomics book series (AMGE, volume 1)

Abstract

The field of Genomics has essentially been fuelled by medical research with developments in human gene therapy, such as the Human Genome Project. This major international undertaking resulted in a significantly increased sequencing capacity, a dramatic decrease in the time and cost of sequencing and also the computational effort required for the analysis. Marine biologists are taking advantage of this high throughput technology, hence, the tools are now available to answer questions that would have not been possible even five years ago. Genomics, in terms of studying DNA, can effectively define the genetic structure of populations and as a consequence the mapping of species boundaries, approximate drift in populations and accurately measure biodiversity. Studying transcribed sequences (RNA) enables the identification of changes at the cellular level associated with the adaptation of species to particular habitats and now, in our changing environment, predicts their ability to survive perturbation.

The aim of this chapter is to familiarize the reader with the most commonly used genomic techniques that are available for population and adaptation studies. These encompass both DNA based methodologies for population studies and RNA based techniques for expression studies. Which technique is used largely depends on the species under study and the resources available. In environmental research it is important to understand that “resources” does not just refer to money for sequencing and library production, but also access to starting material and the ability to store the material successfully, often under difficult conditions. For example, a cruise to investigate a particular hydrothermal vent may only happen once in a researcher’s lifetime and so material will be scarce, numbers will be limited and it may not be possible to store the material at a low enough temperature to prevent RNA degradation (thereby excluding expression studies). Also species availability tends to be on what is there at the time, rather than being able to perform a calculated choice for which species is the best to study. In other studies such as aquaculture or invasive species, a means has to be found to work on a particular species even if the material is intractable as there is a defined requirement for work in that area. So having outlined the techniques, the question is how to use them?

In this chapter specific examples will be used to demonstrate how such techniques are being used to address these important ecological issues in the marine environment, concentrating on lower vertebrates (fish) and invertebrates. These encompass both population analyses and gene expression (functional) studies to understand how populations have adapted to and interact with, their environment.

Ultimately, the challenge for the marine biologist is to utilize the tools produced for the study of model organisms, where significant amounts of sequence data exist (i.e. resource rich) and to develop these for non-model species, essentially from a zero base-line. It is not an easy task.

Keywords

Atlantic Salmon Hydrothermal Vent Gene Chip Genome Scan Massive Parallel Signature Sequencing 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Abbreviations

AFLP

Amplified fragment length polymorphism

BAC

Bacterial artificial chromosome

cDNA

copy/complementary DNA

COI

Cytochrome C oxidase

dbEST

database for ESTs: http://www.ncbi.nlm.nih.gov/dbEST/

DNA

Deoxyribonucleic acid

ER

Endoplasmic reticulum

EST

Expressed sequence tag

GH

Growth hormone

GHRH

Growth hormone releasing hormone

GMPD

Glycosylase mediated polymorphism detection

HSP

Heat shock protein

IPCC

Intergovernmental panel on climate change

MPA

Marine protected area

MPSS

Massively parallel sequencing signature

PR

Prolactin

Q-PCR

Quantitative or Real Time PCR

QTL

Quantitative trait locus/loci

RNA

Ribonucleic acid

SNP

Single nucleotide polymorphism

SSR

Simple sequence repeat

SYBR Green

Fluorescent green dye

UTR

Untranslated region

References

  1. Akey JM, Zhang G, Zhang K, Jin L, Shriver MD (2002) Interrogating a high-density SNP map for signatures of natural selection. Genome Res 12:1805–1814PubMedGoogle Scholar
  2. Albert V, Jonsson B, Bernatchez L (2006) Natural hybrids in Atlantic eels (Anguilla anguilla, A. rostrata): evidence for successful reproduction and fluctuating abundance in space and time. Mol Ecol 15:1903–1916PubMedGoogle Scholar
  3. Almuly R, Skopal T, Funkenstein B (2008) Regulatory regions in the promoter and first intron of Sparus aurata growth hormone gene: Repression of gene activity by a polymorphic minisatellite. Comp Biochem Physiol D 3:43–50Google Scholar
  4. Ashrafi K, Chang FY, Watts JL, Fraser AG, Kamath RS, Ahringer, Ruvkun G (2003) Genome-wide RNAi analysis of Caenorhabditis elegans fat regulatory genes. Nature 421:268–272PubMedGoogle Scholar
  5. Backström N, Ovarström A, Gustafsson L, Hellegren H (2006) Levels of linkage disequilibrium in a wild bird population. Biol Lett 2:435–438PubMedGoogle Scholar
  6. Bailly X, Jollivet D, Vanin S, Deutsch J, Zal Z, Lallier FH, Toulmond A (2002) Evolution of the sulfide-binding function within the globin multigenic family of the deep-sea hydrothermal vent tubeworm Riftia pachyptila. Mol Biol Evol 19:1421–1433PubMedGoogle Scholar
  7. Bailly X, Leroy R, Carney S, Collin O, Zal F, Toulmond A, Jollivet D (2003) The loss of the hemoglobin H2S-binding function reveals molecular adaptation driven by Darwinian positive selection in annelids from sulfide-free habitats. Proc Natl Acad Sci USA 100:5885–5890PubMedGoogle Scholar
  8. Balloux F, Amos W, Coulson T (2004) Does heterozygosity estimate inbreeding in real populations?. Mol Ecol 13:3021–3031PubMedGoogle Scholar
  9. Baranski M, Loughnan S, Austin CM et al. (2006) A microsatellite linkage map of the blacklip abalone, Haliotis rubra. Anim Genet 37:563–570PubMedGoogle Scholar
  10. Barrett RD, Schluter D (2008) Adaptation from standing genetic variation. Trends Ecol Evol 23:38–44PubMedGoogle Scholar
  11. Barretto FS, McCartney MA (2008) Extraordinary AFLP fingerprint similarity despite strong assortative mating between reef fish color morphospecies. Evolution 62:226–233PubMedGoogle Scholar
  12. Baus E, Darrock DJ, Bruford MW (2005) Gene-flow patterns in Atlantic and Mediterranean populations of the Lusitanian sea star Asterina gibbosa. Mol Ecol 14:3373–3382PubMedGoogle Scholar
  13. Bayne BL, Hedgecock D, McGoldrick D, Rees R (1999) Feeding behaviour and metabolic efficiency contribute to may growth heterosis in Pacific oysters [Crassostrea gigas (Thunberg)]. J Exp Mar Biol Ecol 233:115–130Google Scholar
  14. Beaumont MA, Nichols RA (1996) Evaluating loci for use in the genetic analysis of population structure. Proc R Soc Lond B 263:1619–1626Google Scholar
  15. Bensch S, Helbig AJ, Salomon M, Seibold I (2002) Amplified fragment length polymorphism analysis identifies hybrids between two subspecies of warblers. Mol Ecol 11:473– 481PubMedGoogle Scholar
  16. Beraldi D, McRae AF, Gratten J et al (2006) Development of a linkage map and mapping of phenotypic polymorphisms in a free-living population of Soay sheep (Ovis aries). Genetics 173:1521–1537PubMedGoogle Scholar
  17. Bierne N, Borsa P, Daguin C, Jollivet D, Viard F, Bonhomme F, David P (2003) Introgression patterns in the mosaic hybrid zone between Mytilus edulis and M. galloprovincialis. Mol Ecol 12:447–462PubMedGoogle Scholar
  18. Bierne N, David P, Langlade A, Bonhomme F (2002) Can habitat specialisation maintain a mosaic hybrid zone in marine bivalves?. Mar Ecol Progr Ser 245:157–170Google Scholar
  19. Black WC, Baer CF, Antolin MF, DuTeau NM (2001) Population genomics: genome-wide sampling of insect populations. Annu Rev Entomol 46:441–469PubMedGoogle Scholar
  20. Boguski MS, Lowe TMJ, Tolstoshev CM (1993) dbEST – database for ‘expressed sequence tags’. Nat Genet 4:332–333PubMedGoogle Scholar
  21. Bonin A, Taberlet P, Miaud C, Pompanon F (2006) Explorative genome scan to detect candidate loci for adaptation along a gradient of altitude in the common frog (Rana temporaria). Mol Biol Evol 23:773–783PubMedGoogle Scholar
  22. Boutet I, Ky CL, Bonhomme F (2006) A transcriptomic approach of salinity response in the euryhaline teleost, Dicentrarchus labrax. Gene 379:40–50PubMedGoogle Scholar
  23. Boutet I, Nebel C, De Lorgeril J, Guinand B (2007) Molecular characterisation and extrapituitary prolactin expression in the European sea bass Dicentrarchus labrax under salinity stress. Comp Biochem Physiol D 2:74–83Google Scholar
  24. Boutet I, Tanguy A, Le Guen D, Piccino P, Hourdez S, Ravaux J, Shillito B, Legendre P, Jollivet D (2008) Global depression in gene expression as a response to rapid changes of temperature in the hydrothermal vent mussel Bathymodiolus azoricus. PLOS Biol 276:3071–3079Google Scholar
  25. Bradley B, Theodorakis C (2002) The post-genomic era and ecotoxicology. Ecotoxicology 11:7–9PubMedGoogle Scholar
  26. Brenner S, Johnson M, Bridgham J, Golda G, Lloyd DH, Johnson D, Luo S, McCurdy S, Foy M, Ewan M et al. (2000a) Gene expression analysis by massively parallel signature sequencing (MPSS) on microbead arrays. Nat Biotech 18:630–634Google Scholar
  27. Britten RJ, Rowen L, Williams J, Cameron RA (2003) Majority of divergence between closely related DNA samples is due to indels. Proc Natl Acad Sci USA 100:4661–4665PubMedGoogle Scholar
  28. Buckley BA (2007) Comparative environmental genomics in non-model species: using heterologous hybridisation to DNA-based arrays. J Exp Biol 210:1602–1606PubMedGoogle Scholar
  29. Buckley BA, Owen M-E, Hofmann GE (2001) Adjusting the thermostat: the threshold induction temperature for the heat-shock response in intertidal mussels (genus Mytilus) changes as a function of thermal history. J Exp Biol 204:3571–3579PubMedGoogle Scholar
  30. Buckley BA, Somero GN (2009) cDNA analysis reveals the capacity of the cold adapted Antarctic fish Trematomus bernacchii to alter gene expression in response to heat stress. Polar Biol 32:403–415Google Scholar
  31. Caldeira K, Wicket ME (2003) Oceanography: anthropogenic carbon and ocean pH. Nature 425:365PubMedGoogle Scholar
  32. Caldeira K, Wicket ME (2005) Ocean model prediction of chemistry changes from carbon dioxide emission to the atmosphere and ocean. Geophy Res Lett 110:C09S04. doi:10.1029/2004JC002671Google Scholar
  33. Company R, Serafim A, Cosson RP, Fiala-Medioni A, Camus L, Colaco A, Serrao-Santos R, Bebianno MJ (2008) Antioxidant biochemical responses to long-term copper exposure in Bathymodiolus azoricus from Menez-Gwen hydrothermal vent. Sci Total Environ 389:407–417PubMedGoogle Scholar
  34. Campbell D, Bernatchez L (2004) Generic scan using AFLP markers genes as a means to assess the role of directional selection in the divergence of sympatric whitefish ecotypes. Mol Biol Evol 21:945–956PubMedGoogle Scholar
  35. Campbell D, Duchesne P, Bernatchez L (2003) AFLP utility for population assignment studies: analytical investigation and empirical comparison with microsatellites. Mol Ecol 12:1979–1991PubMedGoogle Scholar
  36. Campbell NR, Narum SR (2008) Identification of novel SNPs in Chinook salmon and variation among life history types. Trans Am Fish Soc 137:96–106Google Scholar
  37. Canadell JG, Le Quere C, Raupach MR, Field CB, Buitenhuis ET, Ciais P, Conway TJ, Gillett NP, Houghton RA, Marland G (2007) Contributions to accelerating atmospheric CO2 growth from economic activity, carbon intensity, and efficiency of natural sinks. Proc Natl Acad Sci USA doi:10.1073/pnas.0702737104Google Scholar
  38. Cao L, Caldeira K, Jain AK (2007) Effects of carbon dioxide and climate change on ocean acidification and carbonate mineral saturation. Geophys Res Lett 34:L05607. doi:10.1029/2006GL028605Google Scholar
  39. Carninci P, Shibata Y, Hayatsu N, Sugahara Y, Shibata K, Itoh M, Konno H, Okazaki Y, Muramatsu M (2002) Normalization and subtraction of cap-trapper-selected cDNAs to prepare full-length cDNA libraries for rapid discovery of new genes. Genome Res 10:1617–1630Google Scholar
  40. Caroll SP (2008) Facing change: forms and foundations of contemporary adaptation to biotic invasions. Mol Ecol 17:361–372Google Scholar
  41. Chatziplis D, Batargias C, Tsigenopoulos CS, Magoulas A, Kollias S, Kotoulas G, Volckaert FAM, Haley CS (2007) Mapping quantitative trait loci in European sea bass (Dicentrarchus labrax): The BASSMAP pilot study. Aquaculture 272:S172–S182Google Scholar
  42. Cherry R, Desbruyeres D, Heyraud M, Nolan C (1992) High levels of natural radioactivity in hydrothermal vent polychaetes. C R Acad Sci Paris ser III 315:21–26Google Scholar
  43. Childress JJ, Fisher CR (1992) The biology of hydrothermal vent animals: physiology, biochemistry, and autotrophic symbioses. Oceanogr Mar Biol 30:337–441Google Scholar
  44. Chini V, Rimoldi S, Terova G, Saroglia M, Rossi F, Bernardini G, Gornati R (2006) EST-based identification of genes expressed in the liver of adult seabass (Dicentrarchus labrax, L.). Gene 376:102–106PubMedGoogle Scholar
  45. Chistiakhov DA, Hellemans B, Haley CS, Law AS, Tsigenopoulos CS, Kotoulas G, Bertotto D, Libertini A, Volckaert FAM (2005) A microsatellite linkage map of the European sea bass Dicentrarchus labrax L. Genetics 170:1821–1826Google Scholar
  46. Clark MS, Clarke A, Cockell CS, Convey P, Detrich IIIHW, Fraser KPP, Johnston I, Methe B, Murray AE, Peck LS, Romisch K, Rogers A (2004) Antarctic genomics. Comp Func Genom 5:230–238Google Scholar
  47. Clark MS, Fraser KPP, Burns G, Peck LS (2008a) The HSP70 heat shock response in the Antarctic fish Harpagifer antarcticus. Polar Biol 31:171–180Google Scholar
  48. Clark MS, Fraser KPP, Peck LS (2008b) Antarctic marine molluscs do have an HSP70 heat shock response. Cell Stress Chaperones 13:39–49PubMedGoogle Scholar
  49. Clark MS, Fraser KPP, Peck LS (2008c) Lack of an HSP70 heat shock response in two Antarctic marine invertebrates. Polar Biol 31:1059–1065Google Scholar
  50. Clark MS, Geissler P, Waller C, Fraser KPP, Barnes DKA, Peck LS (2008d) Low heat shock thresholds inwild Antarctic inter-tidal limpets (Nacella concinna). Cell Stress Chaperones 13:51–58PubMedGoogle Scholar
  51. Clark MS, Peck LS (2009) Triggers of the HSP70 stress response: environmental responses and laboratory manipulation in an Antarctic marine invertebrate (Nacella concinna). Cell Stress Chaperones (in press)Google Scholar
  52. Clarke A, Johnston IA (1996) Evolution and adaptive radiation of Antarctic fishes. Trends Ecol Evol 11:212–218PubMedGoogle Scholar
  53. Cohen S (2002) Strong positive selection and habitat-specific amino acid substitution patterns in Mhc from an estuarine fish under intense pollution stress. Mol Biol Evol 19:1870–1880PubMedGoogle Scholar
  54. Colosimo PF, Hosemann KE, Balabhadra S, Villarreal G Jr, Dickson M, Grimwood J et al (2005) Widespread parallel evolution in sticklebacks by repeated fixation of ectodysplasin alleles. Science 307:1928–1933PubMedGoogle Scholar
  55. Comai L, Young K, Till BJ et al. (2004) Efficient discovery of DNA polymorphisms in natural populations by ecotilling. Plant J 37:778–786PubMedGoogle Scholar
  56. Company R, Serafim A, Bebianno MJ, Cosson R, Shillito B, Fiala-Médioni A (2004) Effect of cadmium, copper and mercury on antioxidant enzyme activities and lipid peroxidation in the gills of the hydrothermal vent mussel Bathymodiolus azoricus. Mar Environ Res 58:377–381PubMedGoogle Scholar
  57. Crawford DL, Oleksiak MJ (2007) The biological importance of measuring individual variation. J Exp Biol 210:1613–1621PubMedGoogle Scholar
  58. Cresko WA, Amores A, Wilson C, Murphy J, Currey M, Philips P, Bell MA, Kimmel CB, Postlewaith JH (2004) Parallel genetic basis for repeated evolution of armorloss in Alaskan threespine stickleback populations. Proc Natl Acad Sci USA 101:6050–6055PubMedGoogle Scholar
  59. Crow JF (1998) 90 years: the beginning of hybrid maize. Genetics 148:923–928PubMedGoogle Scholar
  60. Dahlhoff E, O’Brien J, Somero GN, Vetter RD (1991) Temperature effects on mitochondria from hydrothermal vent invertebrates: evidence for adaptation to elevated and variable habitat temperatures. Physiol Zool 64:1490–1508Google Scholar
  61. Daib AM, Williams TD, Sabine VS, Chipman JK, George SG (2008) The GENIPOL European flounder Platichthys flesus L. toxicogenomics microarray: application for investigation of the response to furunculosis vaccination. Fish Biol 72:2154–2169Google Scholar
  62. Darling JA, Blum MJ (2008) DNA-based methods for monitoring invasive species: a review and prospectus. Biol Invasions 9:751–765Google Scholar
  63. Dasmahapatra KK, Lacy RC, Amos W (2008) Estimating levels of inbreeding using AFLP markers. Heredity 100:286–295PubMedGoogle Scholar
  64. DeVries AL (1970) Freezing resistance in Antarctic fishes. In: Holdgate MW (ed) Antarctic biology. Academic Press, New YorkGoogle Scholar
  65. DeVries AL (1982) Biological antifreeze agents in coldwater fishes. Comp Biochem Physiol 73A:627–640Google Scholar
  66. DeWoody JA, Avise JC (2000) Microsatellite variation in marine, freshwater and anadromous fishes compared with other animals. J Fish Biol 56:461–473Google Scholar
  67. DeWoody YD, DeWoody JA (2005) On the estimation of genome-wide heterozygosity using molecular markers. J Hered 96:85–88PubMedGoogle Scholar
  68. DeWoody JA, Nason JD, Hipkins VD (2006) Mitigating scoring errors in microsatellite data from wild populations. Mol Ecol Notes 6:951–957Google Scholar
  69. Deere JA, Chown SL (2006) Testing the beneficial acclimation hypothesis and its alternatives for locomotor performance. Am Nat 5:630–644Google Scholar
  70. Degnan BM, Degnan SM, Fentenany G, Morse DE (1997) A Mox homeobox gene in the gastropod mollusc Haliotis rufescens is differentially expressed during larval morphogenesis and metamorphosis. FEBS Lett 411:119–122PubMedGoogle Scholar
  71. Detrich HWIII, Fitzgerald TJ, Dinsmore JH, Marchese-Ragona SP (1992) Brain and egg tubulins from Antarctic fishes are functionally and structurally distinct. J Biol Chem 267:18766–18775PubMedGoogle Scholar
  72. Detrich HWIII, Johnson KA, Marchese-Ragona SP (1989) Polymerization of Antarctic fish tubulins at low temperatures: energetic aspects. Biochem 28:10085–10093Google Scholar
  73. di Prisco G, Cocca E, Parker S, Detrich HW III (2002) Tracking the evolutionary loss of hemoglobin expression by the white blooded Antarctic icefishes. Gene 295:185–191PubMedGoogle Scholar
  74. Douglas SE, Knickle LC, Kimball J, Reith ME (2007) Comprehensive EST analysis of Atlantic halibut (Hippoglossus hippoglossus), a commercially relevant aquaculture species. BMC Genom doi:10.1186/1471-2164-8-144Google Scholar
  75. Dunton K (1992) Arctic biogeography: the paradox of the marine benthic fauna and flora. Trends Ecol Evol 7:183–189PubMedGoogle Scholar
  76. Duperron S, Sibuet M, MacGregor BJ, Kuypers MMM, Fisher CR, Dubilier N (2007) Diversity, relative abundance and metabolic potential of bacterial endosymbionts in three Bathymodiolus mussel species from cold seeps in the Gulf of Mexico. Environ Microbiol 9:1423–1438PubMedGoogle Scholar
  77. Dupont S, Havenhand J, Thorndyke W, Peck LS, Thorndyke M (2008) CO2-driven ocean acidification radically affects larval survival and development in the brittlestar Ophiothrix fragilis. Mar Ecol Prog Ser 373:285–294Google Scholar
  78. Ellegren H (2004) Microsatellites: simple sequences with complex evolution. Nat Rev Genet 5:435–445PubMedGoogle Scholar
  79. Ellegren H (2008) Sequencing goes 454 and takes large-scale genomics into the wild. Mol Ecol 17:1629–1631PubMedGoogle Scholar
  80. Ellegren H, Sheldon BC (2008) Genetic basis of fitness differences in natural populations. Nature 452:169–175PubMedGoogle Scholar
  81. Ellis JR, Burke JM (2007) EST-SSRs as a resource for population genetic analyses. Heredity 99:125–132PubMedGoogle Scholar
  82. Enevoldsen LT, Heiner I, DeVries AL, Steffensen JF (2003) Does fish from the Disko Bay area of Greenland possess antifreeze proteins during the summer?. Polar Biol 26:365–370Google Scholar
  83. Engel C, Billard E, Voisin M, Viard F (2008) Conservation and polymorphism of mitochondrial intergenic sequences in brown algae. Eur J Phycol 43:195–205Google Scholar
  84. Erickson DL, Fenster CB, Stenoien HK, Price D (2004) Quantitative trait locus analyses and the study of evolutionary process. Mol Ecol 13:2505–2522PubMedGoogle Scholar
  85. Faure B, Bierne N, Tanguy A, Bonhomme F, Jollivet D (2007) Evidence for a slightly deleterious effect of intron polymorphisms at the EF1a gene in the deep-sea hydrothermal vent bivalve Bathymodiolus. Gene 406:99–107PubMedGoogle Scholar
  86. Faure M, David P, Bonhomme F, Bierne N (2008) Genetic hitchhiking in a subdivided population of Mytilus edulis. BMC Evol Biol 8:164. doi:10.1186/1471-2148-8-164PubMedGoogle Scholar
  87. Faure B, Jollivet D, Tanguy A, Bonhomme F, Bierne N (2009) Secondary contact zone in the deep sea: a multi-locus analysis of divergence and gene flow between two closely-related species of Bathymodiolus. Genetics 4:e6485Google Scholar
  88. Feder ME (2007) Evolvability of physiological and biochemical traits: evolutionary mechanisms including and beyond single-nucleotide mutation. J Exp Biol 310:1653–1660Google Scholar
  89. Feder ME, Mitchell-Olds T (2003) Evolutionary and ecological functional genomics. Nat Rev Genet 4:649–655Google Scholar
  90. Fernandes JMO, MacKenzie MG, Kinghorn JR, Johnston IA (2007) FoxK1 splice variants show developmental stage-specific plasticity of expression with temperature in the tiger pufferfish. J Exp Biol 210:3461–3472PubMedGoogle Scholar
  91. Fernandes JMO, MacKenzie MG, Wright PA, Steele SL, Suzuki Y, Kinghorn JR, Johnston IA (2006) Myogenin in model pufferfish species: comparative genomic analysis and thermal plasticity of expression during early development. Comp Biochem Physiol D 1:35–45Google Scholar
  92. Fields PA, Kim Y-S, Carpenter JF, Somero GN (2002) Temperature adaptation in Gillichthys (Teleost: Gobiidae) A4-lactate dehydrogenases: identical primary structures produce subtly different conformations. J Exp Biol 205:1293–1303PubMedGoogle Scholar
  93. Fields PA, Somero GN (1998) Hot spots in cold adaptation: localised increases in conformational flexibility in lactate dehydrogenase A4 orthologs of Antarctic Notothenioid fishes. Proc Natl Acad Sci USA 95:11476–11481PubMedGoogle Scholar
  94. Flannery BG, Wenburg JK, Gharrett AJ (2007) Variation of amplified fragment length polymorphisms in yukon river chum salmon: population structure and application to mixed-stock analysis. Trans Am Fish Soc 136:911–925Google Scholar
  95. Ford MJ (2002) Applications of selective neutrality tests to molecular ecology. Mol Ecol 11:1245–1262PubMedGoogle Scholar
  96. Franch R, Louro B, Tsalavouta M, Chatziplis D, Tsigenopoulos CS, Sarropoulou E, Antonello J, Magoulas A, Mylonas CC, Babbucci M, Patarnello T, Power DM, Kotoulas G, Bargelloni L (2006) A genetic linkage map of the hermaphrodite teleost fish Sparus aurata L.. Genetics 174:851–861PubMedGoogle Scholar
  97. Fuchs Y, Douek J, Rinkevich B, Ben-Shlomo R (2006) Gene diversity and mode of reproduction in the brooded larvae of the coral Heteroxenia fuscescens. J Hered 97:493–498PubMedGoogle Scholar
  98. Gaill F, Mann K, Wiedemann H, Engel J, Timpl R (1995) Structural comparison of cuticle and interstitial collagens from annelids living in shallow sea-water and at deep-sea hydrothermal vents. J Mol Biol 246:284–294PubMedGoogle Scholar
  99. Garoia F, Guarniero I, Grifoni D, Marzola S, Tinti F (2007) Comparative analysis of AFLPs and SSRs efficiency population genetic structure of Mediterranean Solea vulgaris. Mol Ecol 16:1377–1387PubMedGoogle Scholar
  100. Gibson G (2002) Microarrays in ecology and evolution: a preview. Mol Ecol 11:17–24Google Scholar
  101. Gibson G, Riley-Berger R, Harshman L, Kopp A, Vacha S, Nuzhdin S, Wayne M (2004) Extensive sex-specific nonadditivity of gene expression in Drosophila melanogaster. Genetics 167:1791–1799PubMedGoogle Scholar
  102. Gort G, Koopman WJM, Stein A (2006) Fragment length distributions and collision probabilities for AFLP markers. Biometrics 62:1107–1115PubMedGoogle Scholar
  103. Govoroun M, Le Gac F, Guiguen Y (2006) Generation of a large-scale repertoire of Expressed Sequence Tags (ESTs) from normalised rainbow trout cDNA libraries. BMC Genom doi:10.1186/1471-2164-7-196Google Scholar
  104. Gracey AY, Fraser EJ, Li W, Fang Y, Taylor RR, Rogers J, Brass A, Cossins AR (2004) Coping with cold: An integrative, multitissue analysis of the transcriptome of a poikilothermic vertebrate. Proc Natl Acad Sci USA 101:16970–16975PubMedGoogle Scholar
  105. Gruenthal KM, Acheson LK, Burton RS (2007) Genetic structure of natural populations of California red abalone (Haliotis rufescens) using multiple genetic markers. Mar Biol 152:1237–1248Google Scholar
  106. Gruenthal KM, Burton RS (2008) Genetic structure of natural populations of the California black abalone (Haliotis cracherodii Leach, 1814), a candidate for endangered species status. J Exp Mar Biol Ecol 355:47–58Google Scholar
  107. Guinand B, Lemaire C, Bonhomme F (2004) How to detect polymorphisms undergoing selection in marine fishes? A review of methods and case studies, including flatfishes. J Sea Res 51:167–182Google Scholar
  108. Hadfield MG (1998) Research on settlement and metamorphosis of marine invertebrate larvae: past, present and future. Biofouling 12:9–29Google Scholar
  109. Hadfield MG, Carpizo-Ituarte EJ, del Carmen K, Nedved BT (2001) Metamorphic competence, a major adaptive convergence in marine invertebrate larvae. Am Zool 41:1123–1131Google Scholar
  110. Halpin PM, Sorte CJ, Hofmann GE, Menge BA (2002) Patterns of variation in levels of Hsp70 in natural rocky shore populations from microscales to mesoscales. Am J Physiol Integ Comp Biol 42:815–824Google Scholar
  111. Hamady M, Walker JJ, Harris JK, Gold NJ, Knight R (2008) Error-correcting barcoded primers for pyrosequencing hundreds of samples in multiplex. Nat Meth 5:235–237Google Scholar
  112. Hardivillier Y, Denis F, Demattei MV, Bustamante P, Laulier M, Cosson R (2006) Metal influence on metallothionein synthesis in the hydrothermal vent mussel Bathymodiolus thermophilus. Comp Biochem Physiol C Toxicol Pharmacol 143:321–332PubMedGoogle Scholar
  113. Hayes BJ, Gjuvsland A, Omholt S (2006) Power of QTL mapping experiments in commercial Atlantic salmon populations, exploiting linkage and linkage disequilibrium and effect of limited recombination in males. Heredity 97:19–26PubMedGoogle Scholar
  114. Hayes B, Laerdahl JK, Lien S, Moen T, Berg P, Hindar K, Davidson WS, Koop BF, Adzhubei A, Høyheim B (2007) An extensive resource of single nucleotide polymorphism markers associated with Atlantic salmon (Salmo salar) expressed sequences. Aquaculture 265:82–90Google Scholar
  115. Hedgecock D, Lin JZ, DeCola S, Haudenschild CD, Meyer E, Manahan DT, Bowen B (2007) Transcriptomic analysis of growth heterosis in larval Pacific oysters (Crassostrea gigas). Proc Natl Acad Sci USA 104:2313–2318PubMedGoogle Scholar
  116. Hedgecock D, McGoldrick DJ, Bayne BL (1995) Hybrid vigor in Pacific oysters: an experimental approach using crosses among inbred lines. Aquaculture 137:285–298Google Scholar
  117. Hoekstra HE, Coyne JA (2007) The locus of evolution: evo-devo and the genetics of adaptation. Evolution 61:995–1016PubMedGoogle Scholar
  118. Hoekstra HE, Nachman MW (2003) Different genes underlie adaptive melanism in different populations of rock pocket mice. Mol Ecol 12:1185–1194PubMedGoogle Scholar
  119. Hofmann GE (2005) Patterns of gene expression in ectothermic marine organisms on small to large-scale biogeographical patterns. Intergr Comp Biol 45:247–255Google Scholar
  120. Hofmann GE, Buckley BA, Airaksinen S, Keen JE, Somero GN (2000) Heat-shock protein expression is absent in the Antarctic fish Trematomus bernacchii family Nototheniidae. J Exp Biol 203:2331–2339PubMedGoogle Scholar
  121. Hogstrand C, Balesaria S, Glover CN (2002) Application of genomics and proteomics for study of the integrated response to zinc exposure in a non-model fish species, the rainbow trout. Comp Biochem Physiol Mol Biol 133:523–535Google Scholar
  122. Holland BS (2000) Genetics of marine bioinvasions. Hydrobiologia 420:63–71Google Scholar
  123. Hourdez S, Weber RE (2005) Molecular and functional adaptations in deep-sea hemoglobins. J Inorg Biochem 99:130–131PubMedGoogle Scholar
  124. Hubert S, Hedgecock D (2004) Linkage maps of microsatellite DNA markers for the pacific oyster Crassostrea gigas. Genetics 168:351–362PubMedGoogle Scholar
  125. Hudson ME (2008) Sequencing breakthrough for genomic ecology and and evolutionary biology. Mol Ecol Res 8:3–17Google Scholar
  126. IPCC (2007) Climate change 2007: synthesis report. Contribution of work groups I, II and III to the 4th Assessment Report of the Intergovernmental Panel on Climate Change. Core writing team: Pachauri RK and Reisinger A (eds). IPCC, Geneva, Switzerland.Google Scholar
  127. Irwin RD, Boorman GA, Cunningham ML, Heinloth AN, Malarkey DE, Paules RS (2004) Application of toxicogenomics to toxicology: basic concepts in the analysis of microarray data. Toxicol Pathol 32:72–83PubMedGoogle Scholar
  128. Jackson DJ, Ellemor N, Degnan BM (2005) Correlating gene expression with larval competence, and the effect of age and parentage on metamorphosis in the tropical abalone Haliotis asinina. Mar Biol 147:681–697Google Scholar
  129. Jin Y, deVries AL (2006) Antifreeze glycoprotein levels in Antarctic notthenioid fishes inhabiting different thermal environments and the effect of warm acclimation. Comp Biochem Physiol B 144:290–300PubMedGoogle Scholar
  130. Johannesson K, Andre C (2006) Life on the margin: genetic isolation and diversity loss in a peripheral marine ecosystem, the Baltic Sea. Mol Ecol 15:2013–2029PubMedGoogle Scholar
  131. Jollivet D, Desbruyeres D, Ladrat C, Laubier L (1995) Evidence for differences in the allozyme thermostability of deep-sea hydrothermal vent polychaetes (Alvinellidae):a possible selection by habitat. Mar Ecol Prog Ser 123:125–136Google Scholar
  132. Jorde LB (2000) Linkage disequilibrium and the search for complex disease genes. Gen Res 10:1435–1444Google Scholar
  133. Kashi Y, King D, Soller M (1997) Simple sequence repeats as a source of quantitative genetic variation. Trends Genet 13:74–78PubMedGoogle Scholar
  134. Kassahn KS (2008) Microarrays for comparative and ecological genomics: beyond single-species applications for array technologies. J Fish Biol 72:2407–2434Google Scholar
  135. Kim A, Misra A (2007) SNP genotyping: technologies and biomedical applications. Ann Rev Biomed Eng 9:289–320Google Scholar
  136. Kim KS, Ratcliffe ST, French BW, Liu L, Sappington TW (2008) Utility of EST-Derived SSRs as population genetics markers in a beetle. J Hered 99:112–124PubMedGoogle Scholar
  137. Klinbunga S, Khetpu K, Khamnamtong B, Menasveta P (2007) Genetic heterogeneity of the blue swimming crab (Portunus pelagicus) in Thailand determined by AFLP analysis. Biochem Genet 45:725–736PubMedGoogle Scholar
  138. Kumar S, Tsai CJ, Nussinov R (2000) Factors enhancing protein thermostability. Protein Eng 13:179–191PubMedGoogle Scholar
  139. Lallias D, Beaumont AR, Haley CS, Boudry P, Heurtebise S, Lapègue S (2007a) A first-generation genetic linkage map of the European flat oyster Ostrea edulis (L.) based on AFLP and microsatellite markers. Anim Genet 38:560–568PubMedGoogle Scholar
  140. Lallias D, Lapegue S, Hecquet C, Boudry P, Beaumont AR (2007b) AFLP-based genetic linkage maps of the blue mussel (Mytilus edulis). Anim Genet 38:340–349PubMedGoogle Scholar
  141. Langaee T, Ronaghi M (2005) Genetic variation analyses by Pyrosequencing. Mut Res 573:96–102Google Scholar
  142. Launey S, Hedgecock D (2001) High Genetic Load in the Pacific Oyster Crassostrea gigas. Genetics 159:255–265PubMedGoogle Scholar
  143. Le Bris N, Zbinden M, Gaill F (2005) Processes controlling the physico-chemical micro-environments associated with Pompeii worms. Deep-Sea Res 52:1071–1083Google Scholar
  144. Lee M, Kwon J, Kim SN, Kim JE, Koh WS, Kim EJ, Chung MK, Han SS, Song CW (2003) cDNA microarray gene expression profiling of hydroxyurea, paclitaxel, and p-anisidine, genotoxic compounds with differing tumorigenicity results. Environ Mol Mutagen 42:91–97PubMedGoogle Scholar
  145. Lennard Richard ML, Bengten E, Wilson MR, Miller NW, Warr GW, Hikima J (2007) Comparative genomics of transcription factors driving expression of the immunoglobulin heavy chain locus in teleost fish. J Fish Biol 71(Suppl. B):153–173Google Scholar
  146. Li L, Guo X (2004) AFLP-based genetic linkage maps of the Pacific oyster Crassostrea gigas Thunberg. Mar Biotech 6:26–36Google Scholar
  147. Luikart G, Allendorf FW, Cornuet JM, Sherwin WB (1998) Distortion of allele frequency distributions provides a test for recent population bottlenecks. J Hered 89:238–247PubMedGoogle Scholar
  148. Luikart G, England PR, Tallmon D, Jordan S, Taberlet P (2003) The power and promise of population genomics: from genotyping to genome typing. Nat Rev Genet 4:981–994PubMedGoogle Scholar
  149. Luther GW, Rozan TF, Taillefert M, Nuzzio DB, Meo CD, Shank TM, Lutz RA, Cary SC (2001) Chemical speciation drives hydrothermal vent ecology. Nature 410:813–816PubMedGoogle Scholar
  150. Lynch M, Walsh B (1998) Genetics and analysis of quantitative traits. Sinauer Associates, Sunderland, MAGoogle Scholar
  151. Mackay TFC (2001) Quantitative trait loci in Drosophila. Nat Rev Genet 2:11–20PubMedGoogle Scholar
  152. Mackenzie MG (2006) Characterisation of genes regulating muscle development and growth in two model pufferfish species (Takifugu rubripes and Tetraodon nigroviridis). Thesis St Andrews University, Scotland, UKGoogle Scholar
  153. Maldini M, Marzano FN, Fortes GG, Papa R, Gandolfi G (2006) Fish and seafood traceability based on AFLP markers: Elaboration of a species database. Aquaculture 261:487–494Google Scholar
  154. Marcil A, Dumontier E, Chamberland M, Camper SA, Drouin J (2003) Pitx1 and Pitx2 are required for development of hindlimb buds. Development 130:45–55PubMedGoogle Scholar
  155. Marden JH (2008) Quantitative and evolutionary biology of alternative splicing: how changing the mix of alternative transcripts affects phenotypic plasticity and reaction norms. Heredity 100:111–120PubMedGoogle Scholar
  156. Margulies M et al. (2005) Genome sequencing in microfabricated high-density picolitre reactors. Nature 437:376–380PubMedGoogle Scholar
  157. Maynard Smith J, Haigh J (1974) The hitchhiking effect of a favorable gene. Genet Res 23:23–35Google Scholar
  158. Medina M (2009) Functional genomics opens doors to understanding metamorphosis in nonmodel invertebrate organisms. Mol Ecol 18(5):763–764Google Scholar
  159. Meredith MP, King JC (2005) Rapid climate change in the ocean west of the Antarctic Peninsula during the second half of the 20th century. Geophys Lett 32:L19604–L19609Google Scholar
  160. Meudt HM, Clarke AC (2007) Almost forgotten or latest practice? AFLP applications, analyses and advances. Trends Plant Sci 12:106–117PubMedGoogle Scholar
  161. Minic Z, Herve G (2004) Biochemical and enzymological aspects of the symbiosis between the deep-sea tubeworm Riftia pachyptila and its bacterial endosymbiont. Eur J Biochem 271:3093–3102PubMedGoogle Scholar
  162. Mitchell-Olds T, Willis JH, Goldstein DB (2007) Which evolutionary processes influence natural genetic variation for phenotypic traits?. Nat Rev Genet 8:845–856PubMedGoogle Scholar
  163. Moen T, Hayes B, Nilsen F, Delghandi M, Fjalestad K, Fevolden S-E, Berg PR, Lien S (2008) Identification and characterization of novel SNP markers in Atlantic cod: evidence for directional selection. BMC Genet 9:18PubMedGoogle Scholar
  164. Moore MN (2001) Biocomplexity: the post-genome challenge in ecotoxicology. Aquat Toxicol 59:1–15Google Scholar
  165. Morand P, Briand X (1996) Excessive growth of macroalgae: a symptom of environmental disturbance. Botanica Marina 39:491–516Google Scholar
  166. Morin PA, Luikart G, Wayne RK SNP Workshop Group (2004) SNPs in ecology, evolution and conservation. Trends Ecol Evol 19:208–216Google Scholar
  167. Moy GW, Springer SA, Adams SL, Swanson WJ, Vacquier VD (2008) Extraordinary intraspecific diversity in oyster sperm bindin. Proc Natl Acad Sci USA 105:1993–1998PubMedGoogle Scholar
  168. Moylan TJ, Sidell BD (2000) Concentrations of myoglobin and myoglobin mRNA in heart ventricles from Antarctic fishes. J Exp Biol 203:1277–1286PubMedGoogle Scholar
  169. Murphy JM, Mitchell JFB (1995) Transient-response of the Hadley-Center coupled ocean-atmosphere model to increasing carbon-dioxide. 2. Spatial and temporal structure of response. J Climate 1:57–80Google Scholar
  170. Murray MC, Hare MP (2006) A genomic scan for divergent selection in a secondary contact zone between Atlantic and Gulf of Mexico oysters, Crassostrea virginica. Mol Ecol 15:4229–4242PubMedGoogle Scholar
  171. Nielsen R (2005) Molecular signatures of natural selection. Ann Rev Genet 39:197–218PubMedGoogle Scholar
  172. Nishio Y, Nakamura Y, Kawarabayasi Y, Usuda Y, Kimura E, Sugimoto S, Matsui K, Yamagishi A, Kikuchi H, Ikeo K, Gojobori T (2003) Comparative complete genome sequence analysis of the amino acid replacements responsible for the thermostability of Corynebacterium efficiens. Genome Res 13:1572–1579PubMedGoogle Scholar
  173. Nordborg M, Tavare S (2002) Linkage disequilibrium: what history has to tell us. Trends Genet 18:83–90PubMedGoogle Scholar
  174. Oetjen K, Reusch TBH (2007a) Genome scans detect consistent divergent selection among subtidal vs. intertidal populations of the marine angiosperm Zostera marina. Mol Ecol 16:5156–5157PubMedGoogle Scholar
  175. Oetjen K, Reusch TBH (2007b) Identification and characterization of 14 polymorphic EST-derived microsatellites in eelgrass (Zostera marina). Mol Ecol Notes 7:777–780Google Scholar
  176. O’Leary DB, Couglan J, McCarthy TV, Cross TF (2006) Application of a rapid method of SNP analysis (glycosylase mediated polymorphism detection) to mtDNA and nuclear DNA of cod Gadus morhua. J Fish Biol 69(Suppl. A):145–153Google Scholar
  177. Orr JC, Fabry VJ, Aumont O, Bopp L, Doney SC, Feely RA, Gnandesikan A, Gruber N, Ishida A, Joos F, Key RM, Lindsay K, Plattner GK, Rodgers KB, Sabine CL, Sarmiento JL, Schlitzer R, Slater RD, Totterdell IJ, Weirig MF, Yamanaka Y, Yool A (2005) Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437:681–686PubMedGoogle Scholar
  178. Osovitz CJ, Hofmann GE (2005) Thermal history-dependant expression of the hsp70 gene in purple sea urchins: biogeographic patterns and the effect of temperature acclimation. J Exp Mar Biol Ecol 327:134–143Google Scholar
  179. Otsuka M, Arai M, Mori M, Kato M, Kato N, Yokosuka O, Ochiai T, Takiguchi M, Omata M, Seki N (2003) Comparing gene expression profiles in human liver, gastric, and pancreatic tissues using full-length-enriched cDNA libraries. Hepato Res 1:76–82Google Scholar
  180. Oudot M-P, Kloareg B, de Goër S (2002) The complete sequence of the mitochondrial genome of Laminaria digitata (Laminariales). Eur J Phycol 37:163–172Google Scholar
  181. Oudot-Le Secq M-P, Fontaine J-M, Rousvoal S, Kloareg B, Loiseaux-de Goër S (2001) The complete sequence of a brown algal mitochondrial genome, the ectocarpale Pylaiella littoralis (L.) Kjellm. J Mol Evol 53:80–88PubMedGoogle Scholar
  182. Pace DA, Marsh AG, Leong P, Green A, Hedgecock D, Manahan DT (2006) Physiological bases of genetically determined variation in growth of marine invertebrate larvae: a study of growth heterosis in the bivalve Crassostrea gigas. J Exp Mar Biol Ecol 353:188–209Google Scholar
  183. Palumbi SR (1999) All males are not created equal: fertility differences depend on gamete recognition polymorphisms in sea urchins. Proc Natl Acad Sci 96:12632–12637PubMedGoogle Scholar
  184. Pechenik JA (1999) On the advantages and disadvantages of larval stages in benthic marine invertebrate life cycles. Mar Ecol Prog Ser 177:269–297Google Scholar
  185. Peck LS, Clark MS, Clarke A, Cockell CS, Convey P, Detrich IIIHW, Fraser KPP, Johnston I, Methe B, Murray AE, Romisch K, Rogers A (2005) Genomics: Applications to Antarctic Ecosystems. Polar Biol 28:351–365Google Scholar
  186. Peck LS, Clark MS, Morley SA, Massey A, Rosetti H (2009) Animal temperature limits: effects of size, activity and rates of change. Func Ecol 23:248–256Google Scholar
  187. Peck LS, Webb KE, Bailey DM (2004) Extreme sensitivity of biological function to temperature in Antarctic marine species. Func Ecol 18:625–630Google Scholar
  188. Pemberton JM (2004) Measuring inbreeding depression in the wild: the old ways are the best. Trends Ecol Evol 19:613–615PubMedGoogle Scholar
  189. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucl Acids Res 29:2002–2007Google Scholar
  190. Pfaffl MW, Horgan GW, Dempfle L (2002) Relative expression software tool (REST©) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucl Acids Res 30:1–10Google Scholar
  191. Phillips C (2007) Online resources for SNP analysis – a review and route map. Mol Biotechnol 35:65–97PubMedGoogle Scholar
  192. Piccino P, Viard F, Sarradin PM, Le Bris N, Le Guen D, Jollivet D (2004) Thermal selection of PGM allozymes in newly founded populations of the thermotolerant vent polychaete Alvinella pompejana. Proc Roy Soc Lond B 271:2351–2359Google Scholar
  193. Place SP, O’Donnell MJ, Hofmann GE (2008) Gene expression in the intertidal mussel Mytilus californianus: physiological response to environmental factors on a biogeographic scale. Mar Ecol Prog Ser 356:1–14Google Scholar
  194. Podrabsky JE, Somero GN (2004) Changes in gene expression associated with acclimation to constant temperatures and fluctuating daily temperatures in an annual killifish Austrofundulus limnaeus. J Exp Biol 207:2237–2254PubMedGoogle Scholar
  195. Pompanon F, Bonin A, Bellemain E, Taberlet P (2005) Genotyping errors: causes, consequences and solutions. Nat Rev Genet 6:847–859PubMedGoogle Scholar
  196. Price AH (2006) Believe it or not, QTLs are accurate!. Trends Plant Sci 11:213–216PubMedGoogle Scholar
  197. Pruski AM, Dixon DR (2003) Toxic vents and DNA damage: first evidence from a naturally contaminated deep-sea environment. Aquat Toxicol 64:1–13PubMedGoogle Scholar
  198. Purać J, Burns B, Thorne MAS, Grubor-Lajšić G, Worland MR, Clark MS (2008) Cold hardening processes in the Antarctic springtail, Cryptopygus antarcticus: clues from a microarray. J Insect Physiol 54:1356–1362PubMedGoogle Scholar
  199. Qin Y, Liu X, Zhang H, Zhang G, Guo X (2007) Genetic mapping of size-related quantitative trait loci (QTL) in the bay scallop (Argopecten irradians) using AFLP and microsatellite markers. Aquaculture 272:281–290Google Scholar
  200. Radonic A, Thulke S, Mackay IM, Landt O, Siegert W, Nitsche A (2004) Guideline to reference gene selection for quantitative real-time PCR. Biochem Biophys Res Comm 313:856–862PubMedGoogle Scholar
  201. Renn SCP, Aubin-Horth N, Hofmann HA (2004) Biologically meaningful expression profiling across species using hetrerologous hybridisation to a cDNA microarray. BMC Genom doi: 10.1186/1471-2164-5-42Google Scholar
  202. Ricciardi A, MacIsaac HJ (2000) Recent mass invasion of the north american great lakes by ponto-caspian species. Trends Ecol Evol 15:62–65PubMedGoogle Scholar
  203. Roberts DA, Hofmann GE, Somero GN (1997) Heat shock protein expression in Mytilus californianus: Acclimatization (seasonal and tidal height comparisons) and acclimation effects. Biol Bull 192:309–320Google Scholar
  204. Roberts S, Romano C, Gerlach G (2005) Characterization of EST derived SSRs from the bay scallop, Argopecten irradians. Mol Ecol Notes 5:567–568Google Scholar
  205. Robinson-Rechavi M, Alibes A, Godzik A (2006) Contribution of electrostatic interactions, compactness and quaternary structure to protein thermostability: Lessons from structural genomics of Thermotoga maritime. J Mol Biol 356:547–557PubMedGoogle Scholar
  206. Roff DA (2007) Contributions of genomics to life-history theory. Nat Rev Genet 8:116–125PubMedGoogle Scholar
  207. Rogers SM, Bernatchez L (2005) Integrating QTL mapping and genome scans towards the characterization of candidate loci under parallel selection in the lake whitefish (Coregonus clupeaformis). Mol Ecol 14:351–361PubMedGoogle Scholar
  208. Rogers SM, Campbell D, Baird SJE, Danzmann RG, Bernatchez L (2001) Combining the analyses of introgressive hybridisation and linkage mapping to investigate the genetic architecture of population divergence in the lake whitefish (Coregonus clupeaformis, Mitchill). Genetica 111:25–41PubMedGoogle Scholar
  209. Roman J, Darling JA (2007) Paradox lost: genetic diversity and the success of aquatic invasions. Trends Ecol Evol 22:454–464PubMedGoogle Scholar
  210. Römisch K, Collie N, Soto N, Logue J, Lindsay M, Scheper W, Cheng C-H C (2003) Protein translocation across the endoplasmic reticulum membrane in cold adapted organisms. J Cell Sci 116:2875–2883PubMedGoogle Scholar
  211. Royal Society (2005) Ocean acidification due to increasing atmospheric carbon dioxide. Policy Document 12/05, The Royal SocietyGoogle Scholar
  212. Rungis D, Berube Y, Zhang J, Ralph S, Ritland CE, Ellis BE et al. (2004) Robust simple sequence repeat markers for spruce (Picea spp.) from expressed sequence tags. Theor Appl Genet 109:1283–1294PubMedGoogle Scholar
  213. Ryynänen HJ, Primmer C (2006) Single nucleotide polymorphism (SNP) discovery in duplicated genomes: intron-primed exon-crossing (IPEC) as a strategy for avoiding amplification of duplicated loci in Atlantic salmon (Salmo salar) and other salmonid fishes. BMC Genom 7:192Google Scholar
  214. Ryynänen HJ, Tonteri A, Vasemägi A, Primmer CR (2007) A comparison of the efficiency of single nucleotide polymorphisms (SNPs) and microsatellites for the estimates of population and conservation genetic parameters in Atlantic salmon (Salmo salar). J Hered 98:692–704PubMedGoogle Scholar
  215. Saastamoinen M, Hanski I (2008) Genotypic and environmental effects on flight activity and oviposition in the Glanville fritillary butterfly. Am Nat 171:701–712PubMedGoogle Scholar
  216. Saavedra C, Bachere E (2006) Bivalve genomics. Aquaculture 256:1–14Google Scholar
  217. Sanchez S, Hourdez S, Lallier F (2007) Identification of proteins involved in the functioning of Riftia pachyptila symbiosis by Subtractive Suppression Hybridization. BMC Genomics 8:337PubMedGoogle Scholar
  218. Sax DF, Stachowicz JJ, Brown JH, Bruno JF, Dawson MN, Gaines SD, Grosberg RK, Hastings A, Holt RD, Mayfield MM, O’Connor MI, Rice WR (2007) Ecological and evolutionary insights from species invasions. Trends Ecol Evol 22:465–471PubMedGoogle Scholar
  219. Schlotterer C (2003) Hitchhiking mapping – functional genomics from the population genetics perspective. Trends Genet 19:32–38PubMedGoogle Scholar
  220. Shank TM, Halanych KM (2007) Toward a mechanistic understanding of larval dispersal: insights from genomic fingerprinting of the deep-sea hydrothermal vent tubeworm Riftia pachyptila. Mar Ecol 28:25–35Google Scholar
  221. Shapiro MD, Marks ME, Peichel CL, Blackman BK, Nereng BJ, Schluter D et al. (2004) Genetic and developmental basis of evolutionary pelvic reduction in threespine sticklebacks. Nature 428:717–723PubMedGoogle Scholar
  222. Sheader DL, Williams TD, Lyons BP, Chipman JK (2006) Oxidative stress response of European flounder (Platichthys flesus) to cadmium determined by a custom cDNA microarray. Mar Environ Res 62:33–44PubMedGoogle Scholar
  223. Sicot FX, Mesnage M, Masselot M, Exposito JY, Garrone R, Deutsch J, Gaill F (2000) Molecular adaptation to an extreme environment: origin of the thermal stability of the Pompeii worm collagen. J Mol Biol 302:811–820PubMedGoogle Scholar
  224. Slate J, David P, Dodds KG, Veenvliet BA, Glass BC, Broad TE et al. (2004) Understanding the relationship between the inbreeding coefficient and multilocus heterozygosity: theoretical expectations and empirical data. Heredity 93:255–265PubMedGoogle Scholar
  225. Smith CT, Antonovich A, Templin WD, Elfstrom CM, Narum SR, Seeb LW (2007) Impacts of marker class bias relative to locus-specific variability on population inferences in chinook salmon: A comparison of single-nucleotide polymorphisms with short tandem repeats and allozymes. Trans Am Fish Soc 136:1674–1687Google Scholar
  226. Smith CT, Elfstrom CM, Seeb LW, Seeb JE (2005) Use of sequence data from rainbow trout and Atlantic salmon for SNP detection in Pacific salmon. Mol Ecol 14:4193–4203PubMedGoogle Scholar
  227. Somero GN (2002) Thermal physiology and vertical zonation of intertidal animals: optima, limits and costs of living. Am J Physiol Integ Comp Biol 42:780–789Google Scholar
  228. Stachowicz JJ, Terwin JR, Whitlatch RB, Osman RW (2002) Linking climate change and biological invasions: Ocean warming facilitates nonindigenous species invasions. Proc Natl Acad Sci USA 99:15497–15500PubMedGoogle Scholar
  229. Stern S, Dror T, Stolovicki E, Brenner N, Braun E (2007) Genome-wide transcriptional plasticity underlies cellular adaptation to novel challenge. Mol Sys Biol Doi:10.1038/msb4100147Google Scholar
  230. Stewart FJ, Cavanaugh CM (2006) Bacterial endosymbioses in Solemya (Mollusca: Bivalvia)—model systems for studies of symbiont–host adaptation. Antonie Leeuwenhoek 90:343–360PubMedGoogle Scholar
  231. Stinchcombe JR, Hoekstra HE (2008) Combining population genomics and quantitative genetics: finding the genes underlying ecologically important traits. Heredity 100:158–170PubMedGoogle Scholar
  232. Stolovitzky GA, Kundaje A, Held GA, Duggar KH, Haudenschild CD, Zhou D, Vasicek TJ, Smith KD, Aderem A, Roach JC (2005) Proc Natl Acad Sci USA 102:1402–1407PubMedGoogle Scholar
  233. Storz JF (2005) Using genome scans of DNA polymorphism to infer adaptive population divergence. Mol Ecol 14:671–688PubMedGoogle Scholar
  234. Streelman JT, Kocher TD (2002) Microsatellite variation associated with prolactin expression and growth of salt-challenged tilapia. Physiol Genom 9:1–4Google Scholar
  235. Suzuki Y, Yoshitomo-Nakagawa K, Maruyama K, Suyama A, Sugano S (1997) Construction and characterization of a full length-enriched and a 5ʹ-end-enriched cDNA library. Gene 1–2:149–156Google Scholar
  236. Swanson-Wagner RA, Jia Y, De Cook R, Borsuk LA, Nettleton D, Schnable PS (2006) All possible modes of gene action are observed in a global comparison of gene expression in a maize F-1 hybrid and its inbred parents. Proc Natl Acad Sci USA 103:6805–6810PubMedGoogle Scholar
  237. Tabor HK, Risch NJ, Myers RM (2002) Candidate gene approaches for studying complex genetic traits: practical considerations. Nat Rev Genet 3:391–397PubMedGoogle Scholar
  238. Tanguy A, Bierne N, Saavedra C, Pina B, Bachère E, Kube M, Bazin E, Bonhomme F, Boudry P, Boulo V, Boutet I, Cancela L, Dossat C, Favrel P, Huvet A, Jarque S, Jollivet D, Klages S, Lapegue S, Leite R, Moal J, Moraga D, Reinhardt R, Samain J-F, Zouros E, Canario A (2008) Increasing genomic information in bivalves through new EST collections in four species: Development of new genetic markers for environmental studies and genome evolution. Gene 408:27–36PubMedGoogle Scholar
  239. Tao WJ, Boulding EG (2003) Associations between single nucleotide polymorphisms in candidate genes and growth rate in Arctic charr (Salvelinus alpinus L. Heredity 91:60–69PubMedGoogle Scholar
  240. Taris N, Comtet T, Viard F (2009) Inhibitory function of nitric oxide on the onset of metamorphosis in competent larvae of Crepidula fornicata: a transcriptional perspective. Mar Genomics 2:161–167Google Scholar
  241. Teranishi KS, Stillman JH (2007) A cDNA microarray analysis of the response to heat stress in hepatopancreas tissue of the porcelain crab Petrolisthes cinctipes. Comp Biochem Physiol D 2:53–62Google Scholar
  242. Teshima KM, Coop G, Preworski M (2006) How reliable are empirical genomic scans for selective sweeps?. Genome Res 16:702–712PubMedGoogle Scholar
  243. Tomanek L (2002) The heat shock response: its variation, regulation and ecological importance in intertidal gastropods (genus Tegula). Am J Physiol Integ Comp Biol 42:797–807Google Scholar
  244. Tomanek L (2005) Two-dimensional gel analysis of the heat shock response in marine snails (genus Tegula): interspecific variation in protein expression and acclimation ability. J Exp Biol 208:3133–3143PubMedGoogle Scholar
  245. Tomanek L, Somero GN (2000) Time course and magnitude of synthesis of heat shock proteins in congeneric marine snails (Genus Tegula) from differentb tidal heights. Physiol Biochem Zool 73:249–256PubMedGoogle Scholar
  246. Toth AL, Varala K, Newman TC, Miguez FE, Hutchison SK, Willoughby DA et al. (2007) Wasp brain gene expression supports an evolutionary link between maternal behavior and eusociality. Science 318:441–444PubMedGoogle Scholar
  247. Troester MA, Hoadley KA, Parker JS, Perou CM (2004) Prediction of toxicant-specific gene expression signatures after chemotherapeutic treatment of breast cell lines. Environ Health Perspect 112:1607–1613PubMedGoogle Scholar
  248. Ungerer MC, Johnson LC, Herman MA (2008) Ecological genomics: understanding gene and genome function in the natural environment. Heredity 100:178–183PubMedGoogle Scholar
  249. Uthicke S, Conand C (2005) Amplified fragment length polymorphism (AFLP) analysis indicates the importance of both asexual and sexual reproduction in the fissiparous holothurian Stichopus chloronotus (Aspidochirotida) in the Indian and Pacific Ocean. Coral Reefs 24:103–111Google Scholar
  250. Vasemägi A, Nilsson J, Primmer CR (2005) Expressed Sequence Tag-Linked Microsatellites as a Source of Gene-Associated Polymorphisms for Detecting Signatures of Divergent Selection in Atlantic Salmon (Salmo salar L). Mol Biol Evol 22:1067–1076PubMedGoogle Scholar
  251. Vasemägi A, Primmer CR (2005) Challenges for identifying functionally important genetic variation: the promise of combining complementary research strategies. Mol Ecol 14:3623–3642PubMedGoogle Scholar
  252. Vaughan P (2000) Use of uracil DNA glycosylase in the detection of known DNA mutations and polymorphisms. Glycosylase-mediated polymorphism detection (GMPD-check). Methods Mol Biol (Clifton, NJ) 152:169–177Google Scholar
  253. Venter JC, Remington K, Heidelberg JF, Halpern AL, Rusch D, Eisen JA et al. (2004) Environmental genome shotgun sequencing of the Sargasso Sea. Science 304:66–74PubMedGoogle Scholar
  254. Vera JC, Wheat CW, Fescemyer HW, Frilander MJ, Crawford DL, Hanski I, Marden JH (2008) Rapid transcriptome characterization for a nonmodel organism using 454 pyrosequencing. Mol Ecol 17:1636–1647PubMedGoogle Scholar
  255. Verde C, Lecointre G, di Prisco G (2007) The phylogeny of polar fishes and the structure and molecular evolution of hemoglobin. Polar Biol 30:523–539Google Scholar
  256. Voisin M, Engel C, Viard F (2005) Differential shuffling of native genetic diversity across introduced region in a brown alga: aquaculture vs. maritime traffic effects. Proc Natl Acad Sci USA 102:5432–5437PubMedGoogle Scholar
  257. Vos P, Hogers R, Bleeker M, Reijans M, van de Lee T, Hornes M, Frijters A, Pot J, Peleman J, Kuiper M, Zabeau M (1995) AFLP: a new technique for DNA fingerprinting. Nucl Acids Res 23:4407–4414PubMedGoogle Scholar
  258. Ward RD, Woodwark M, Skibinski DOF (1994) A comparison of genetic diversity levels in marine, freshwater, and anadromous fishes. J Fish Biol 44:213–232Google Scholar
  259. Wares JP, Blakeslee AMH (2007) Amplified fragment length polymorphism data provide a poor solution to the Littorina littorea puzzle. Mar Biol Res 3:168–174Google Scholar
  260. Weetman D, Ruggierro E, Mariani S, Shaw PW, Lawler AR, Hauser L (2007) Hierarchical population genetic structure in the commercially exploited shrimp Crangon crangon identified by AFLP analysis. Mar Biol 151:565–575Google Scholar
  261. Weiss E, Bennie M, Hodgins-Davis A, Roberts S, Gerlach G (2007) Characterization of new SSR-EST markers in cod, Gadus morhua. Mol Ecol Notes 7:866–867Google Scholar
  262. Wenne R, Boudry P, Hemmer-Hansen J, Lubieniecki KP, Was A, Kause A (2007) What role for genomics in fisheries management and aquaculture?. Aquatic Living Res 3:241–255Google Scholar
  263. Wilding CS, Butlin RK, Grahame J (2001) Differential gene exchange between parapatric morphs of Littorina saxatilis detected using AFLP markers. J Evol Biol 14:611–619Google Scholar
  264. Williams EA, Degnan BM, Gunter H, Jackson DJ, Woodcroft BJ, Degnan SM (2009) Widespread transcriptional changes pre-empt the critical pelagic–benthic transition in the vetigastropod Haliotis asinina. Mol Ecol 18:1006–1025PubMedGoogle Scholar
  265. Wilson K, Thorndyke M, Nilsen F, Rogers A, Martinez P (2005) Marine systems: moving into the genomics area. Mar Ecol 26:3–16Google Scholar
  266. Wolff WJ, Reise K (2002) Oyster imports as a vector for the introduction of alien species into northern and western European coastal waters. In: Leppäkoski E, Gollasch S, Olenin S (eds) Invasive aquatic species of Europe. Distribution, impacts and management. Kluwer Academic Publishers, Dordrecht/Boston/London, pp 193–205Google Scholar
  267. Woodhead M, Russell J, Squirrell J, Hollingsworth PM, Mackenzie K, Gibby M et al. (2005) Comparative analysis of population genetic structure in Athyrium distentifolium (Pteridophyta) using AFLPs and SSRs from anonymous and transcribed gene regions. Mol Ecol 14:1681–1695PubMedGoogle Scholar
  268. Wray GA (2007) The evolutionary significance of cis-regulatory mutation. Nat Rev Genet 8:206–216PubMedGoogle Scholar
  269. Yang Z, Bielawski J (2000) Statistical methods for detecting molecular adaptation. Trends Ecol Evol 15:496–503PubMedGoogle Scholar
  270. Yu J et al. (2006) A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nat Genet 38:203–208PubMedGoogle Scholar
  271. Yu Z, Guo X (2003) Genetic linkage map of the Eastern oyster Crassostrea virginica Gmelin. Biol Bull 204:327–338PubMedGoogle Scholar
  272. Zachos J, Pagani M, Sloan L, Thomas E, Billups K (2001) Trends, rhythms and aberrations in global climate 65 Ma to present. Science 292:686–693PubMedGoogle Scholar
  273. Zane L, Bargelloni L, Patarnello T (2002) Strategies for microsatellite isolation: a review. Mol Ecol 11:1–16PubMedGoogle Scholar
  274. Zhao YM, Li Q, Kong LF, Bao ZM, Zhang RC (2007) Genetic diversity and divergence among clam Cyclina sinensis populations assessed using amplified fragment length polymorphism. Fish Sci 73:1338–1343Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Melody S. Clark
    • 1
  • Arnaud Tanguy
    • 2
  • Didier Jollivet
    • 2
  • François Bonhomme
    • 3
  • Bruno Guinand
    • 3
  • Frédérique Viard
    • 2
  1. 1.Ecosystems, British Antarctic SurveyNatural Environment Research CouncilCambridgeUK
  2. 2.Equipe Evolution et Génétique des populations Marines (EGPM)UMR 7144, CNRS-UPMC Station Biologique de RoscoffRoscoff CedexFrance
  3. 3.Université Montpellier II, Institut des Sciences de l’Evolution de Montpellier (ISEM)Montpellier CedexFrance

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