Do North Atlantic eels show parallel patterns of spatially varying selection?

BMC Evolutionary Biology

Michael M Hansen³  Louis Bernatchez⁵  Bjarni Jónsson²  Peder K Bøcher³  Jane Frydenberg³  Pierre Alexandre Gagnaire¹  Thomas D Als⁴  Magnus W Jacobsen³  Anne-Laure Ferchaud³  José Martín Pujolar³  Malene G Ulrik³ 

[1] ISEM (Institut des Sciences de l’Evolution Montpellier), Université Montpellier II, 34095 Montpellier, France;Biopol, Marine Biology and Biotechnology Center, Einbúastígur 2, IS545 Skagastrond, Iceland;Department of Bioscience, Aarhus University, Ny Munkegade 114, Bldg. 1540, DK-8000 Aarhus C, Denmark;Department of Biomedicine-Human Genetics, Aarhus University, DK-8000 Aarhus C, Denmark;IBIS (Institut de Biologie Intégrative et des Systèmes), Université Laval, G1V 0A6 Québec, Canada

关键词: Single nucleotide polymorphisms;    Parallel selection;    Genetic-by-environment associations;    European eel;    Adaptation;   

Others  :  855195
DOI  :  10.1186/1471-2148-14-138

 received in 2014-03-27, accepted in 2014-06-16,  发布年份 2014

【 摘 要 】

Background

The two North Atlantic eel species, the European and the American eel, represent an ideal system in which to study parallel selection patterns due to their sister species status and the presence of ongoing gene flow. A panel of 80 coding-gene SNPs previously analyzed in American eel was used to genotype European eel individuals (glass eels) from 8 sampling locations across the species distribution. We tested for single-generation signatures of spatially varying selection in European eel by searching for elevated genetic differentiation using F_ST-based outlier tests and by testing for significant associations between allele frequencies and environmental variables.

Results

We found signatures of possible selection at a total of 11 coding-gene SNPs. Candidate genes for local selection constituted mainly genes with a major role in metabolism as well as defense genes. Contrary to what has been found for American eel, only 2 SNPs in our study correlated with differences in temperature, which suggests that other explanatory variables may play a role. None of the genes found to be associated with explanatory variables in European eel showed any correlations with environmental factors in the previous study in American eel.

Conclusions

The different signatures of selection between species could be due to distinct selective pressures associated with the much longer larval migration for European eel relative to American eel. The lack of parallel selection in North Atlantic eels could also be due to most phenotypic traits being polygenic, thus reducing the likelihood of selection acting on the same genes in both species.

【 授权许可】

   
2014 Ulrik et al.; licensee BioMed Central Ltd.

【 图 表 】

【 参考文献 】

• [1]Kawecki TJ, Ebert D: Conceptual issues in local adaptation. Ecol Lett 2004, 7:1225-1241.
• [2]Stapley J, Reger J, Feulner PGD, Smadja C, Galindo J, Ekblom R, Bennison C, Ball AD, Beckerman AP, Slate J: Adaptation genomics: the next generation. Trends Ecol Evol 2010, 12:705-712.
• [3]Wood TE, Burke JM, Reiseberg LH: Parallel genotypic adaptation: when evolution repeats itself. Genetica 2005, 123:157-170.
• [4]Elmer KR, Meyer A: Adaptation in the age of ecological genomics: insights from parallelism and convergence. Trends Ecol Evol 2011, 26:298-306.
• [5]Conte GL, Arnegard ME, Peichel CL, Schluter D: The probability of genetic parallelism and convergence in natural populations. Proc R Soc Lond B 2012, 279:5039-5047.
• [6]Colosimo PF, Hosemann KE, Balabhadra W, Villarreal G, Dickson M, Grimwood J, Schmutz J, Myers RM, Schluter D, Kingsley DM: Widespread parallel evolution in sticklebacks by repeated fixation of Ectodysplasin alleles. Science 2005, 307:1928-1933.
• [7]Hohenlohe PA, Bassham S, Etter PD, Stiffler N, Johnson EA, Cresko WA: Population genomics of parallel adaptation in threespine stickleback using sequenced RAD tags. PLoS Genet 2010, 6:e1000862.
• [8]DeFaveri J, Shikano T, Shimada Y, Goto A, Merilä J: Global analysis of genes involved in freshwater adaptation in threespine sticklebacks (Gasterosteus aculeatus). Evolution 2011, 65:1800-1807.
• [9]Jones FC, Chan YF, Schmutz J, Grimwood J, Brady SD, Southwick AM, Absher DM, Myers RM, Reimchen T, Deagle BE, Schluter D, Kingslet DM: A genome-wide SNP genotyping array reveals patterns of global and repeated species-pair divergence in sticklebacks. Curr Biol 2012, 22:83-90.
• [10]Jones FC, Grabherr MG, Chan YF, Russell P, Mauceli E, Johnson J, Swofford R, Pirun M, Zody MC, White S, Birney E, Searle S, Schmutz J, Grimwood J, Dickson MC, Myers RM, Miller CT, Summers BR, Knecht AK, Brady SD, Zhang H, Pollen AA, Howes T, Amemiya C: The genomic basis of adaptive evolution in threespine sticklebacks. Nature 2012, 484:55-61.
• [11]Renault S, Owens GL, Rieseberg LH: Shared selective pressure and local genomic landscape lead to repeatable patterns of genomic divergence in sunflowers. Mol Ecol 2014, 23:311-324.
• [12]Boëtius J: Atlantic Anguilla: a presentation of old and new data of total number of vertebrae with special reference to the occurrence of Anguilla rostrata in Europe. Dana 1980, 1:93-112.
• [13]Avise JC, Helfman GS, Saunders NC, Hales LS: Mitochondrial DNA differentiation in North Atlantic eels: population genetic consequences of an unusual life history pattern. Proc Natl Acad Sci U S A 1986, 83:4350-4354.
• [14]Mineguishi Y, Aoyama J, Inoue JG, Miya M, Nishida M, Tsukamoto K: Molecular phylogeny and evolution of the freshwater eels genus Anguilla based on the whole mitochondrial genome sequences. Mol Phylogenet Evol 2005, 34:134-146.
• [15]Jacobsen MW, Pujolar JM, Gilbert TP, Mayar JVM, Bernatchez L, Als TD, Hansen MM: Speciation and demographic history of Atlantic eels (Anguilla anguilla and A. rostrata) revealed by mitogenome sequencing. Heredity 2014. in press
• [16]Mank JE, Avise JC: Microsatellite variation and differentiation in North Atlantic eels. J Hered 2003, 94:30-34.
• [17]Wirth T, Bernatchez L: Decline of Atlantic eels: a fatal synergy? Proc R Soc Lond B 2003, 270:681-688.
• [18]Gagnaire PA, Albert V, Jónsson B, Bernatchez L: Natural selection influences AFLP intraspecific variability and introgression patterns in Atlantic eels. Mol Ecol 2009, 18:1678-1691.
• [19]Als TD, Hansen MM, Maes GE, Castonguay M, Riemann L, Aerestrup K, Munk P, Sparholt T, Hanel R, Bernatchez L: All roads lead to home: panmixia of European eel in the Sargasso Sea. Mol Ecol 2011, 20:1333-1346.
• [20]McCleave JD, Kleckner RC, Castonguay M: Reproductive sympatry of American and European eels and implications for migration and taxonomy. Am Fish Soc Symp 1987, 1:286-297.
• [21]Avise JC, Nelson WS, Arnold J, Koehn RK, Williams GC, Thorsteinsson V: The evolutionary genetic status of Icelandic eels. Evolution 1990, 44:1254-1262.
• [22]Albert V, Jónsson B, Bernatchez L: Natural hybrids in Atlantic eels (Anguilla anguilla, A. rostrata): evidence for successful reproduction and fluctuating abundance in space and time. Mol Ecol 2006, 15:1903-1916.
• [23]Pujolar JM, Jacobsen MW, Als TD, Frydenberg J, Magnussen E, Jónsson B, Jiang X, Cheng L, Bekkevold D, Maes GE, Bernatchez L, Hansen MM: Assessing patterns of hybridization between North Atlantic eels using diagnostic single-nucleotide polymorphisms. Heredity 2014. in press
• [24]Van den Thillart G, Rankin JC, Dufour S: Spawning migration of the European eel: reproduction index, a useful tool for conservation management. Dordecht, The Netherlands: Springer; 2009.
• [25]Fraser DJ, Weir LK, Bernatchez L, Hansen MM, Taylor EB: Extend and scale of local adaptation in salmonid fishes: review and meta-analysis. Heredity 2011, 106:404-420.
• [26]Gagnaire PA, Normandeau E, Côté C, Hansen MM, Bernatchez L: The genetic consequences of spatially varying selection in the panmictic American eel (Anguilla rostrata). Genetics 2012, 190:725-736.
• [27]Levene H: Genetic equilibrium when more than one ecological niche is available. Am Nat 1953, 87:331-333.
• [28]Hedrick PW: Genetic polymorphism in heterogeneous environments: the age of genomics. Annu Rev Ecol Evol Syst 2006, 37:67-93.
• [29]Yeaman S, Otto SP: Establishment and maintenance of adaptive genetic divergence under migration, selection and drift. Evolution 2011, 65:2123-2129.
• [30]Dannewitz J, Maes GE, Johansson L, Wickström H, Volckaert FAM, Jarvi T: Panmixia in the European eel: a matter of time. Proc R Soc Lond B 2005, 272:1129-1137.
• [31]Côté C, Gagnaire PA, Bourret V, Verrault G, Castonguay M, Bernatchez L: Population genetics of the American eel (Anguilla rostrata): FST = 0 and North Atlantic Oscillation effects on demographic fluctuations of a panmictic species. Mol Ecol 2013, 22:1763-1776.
• [32]Maes GE, Volckaert FAM: Clinal genetic variation and isolation by distance in the European eel Anguilla anguilla. Biol J Linn Soc 2002, 77:509-522.
• [33]Williams GC, Koehn RK, Mitton JB: Genetic differentiation without isolation in the American eel, Anguilla rostrata. Evolution 1973, 27:192-204.
• [34]Schmidt PS, Serrao EA, Pearson GA, Riginos C, Rawson PD, Hilbish TJ, Brawley SH, Trussell GC, Carrington E, Wethey DS, Grahame JW, Bonhomme F, Rand DM: Ecological genetics in the North Atlantic: environmental gradients and adaptation at specific loci. Ecology 2008, 89:S91-S107.
• [35]Hancock AM, Witonsky DB, Ehler E, Alkorta-Aranburu G, Beall C, Gebremedhin A, Sukernik R, Utermann G, Pritchard J, Coop G, Di Rienzo A: Colloquium paper: human adaptations to diet, subsistence, and ecoregion are due to subtle shifts in allele frequency. Proc Natl Acad Sci U S A 2010, 107:8924-8930.
• [36]Ma XF, Hall D, Onge KR, Jansson S, Ingvarsson PK: Genetic differentiation, clinal variation and phenotypic associations with growth cessation across the Populus tremula photoperiodic pathway. Genetics 2010, 186:1033-1044.
• [37]Keller SR, Levsen N, Olson MS, Tiffin P: Local adaptation in the flowering-time gene network of balsam poplar, Populus balsamifera. Mol Biol Evol 2012, 29:3143-3152.
• [38]Coop G, Witonsky D, Di Rienzo A, Pritchard JK: Using environmental correlations to identify loci underlying local adaptation. Genetics 2010, 185:411-1423.
• [39]Somero GN: Adaptation of enzymes to temperature: searching for basic “strategies”. Comp Biochem Physiol B Biochem Mol Biol 2004, 139:321-333.
• [40]Lim ST, Kay RM, Bailey GS: Lactate dehydrogenase isozymes in salmonid fish: evidence for unique and rapid functional divergence of duplicated H-4 lactate dehydrogenases. J Biol Chem 1975, 10:1790-1800.
• [41]Nyman L: Some effects of temperature on eel (Anguilla) behaviour. Rep Inst Freshw Res Drottingholm 1972, 52:90-102.
• [42]Walsh PJ, Foster GD, Moon TW: The effects of temperature and metabolism of the American eel Anguilla rostrata: compensation in the summer and torpor in the winter. Physiol Zool 1983, 56:532-540.
• [43]Linton ED, Jónsson B, Noakes DLG: Effects of water temperature on the swimming and climbing behavior of glass eels Anguilla spp. Environ Biol Fishes 2007, 78:189-192.
• [44]Henry DN, Delmonte M, Greene DA, Killen PD: Altered aldose reductase regulation in human retinal-pigment epithelial-cells. J Clin Invest 1993, 92:617-623.
• [45]Daverat F, Limburg K, Thibaut I, Shiao JC, Dodson JJ, Caron F, Tzeng WN, Iizuka Y, Wickström H: Phenotypic plasticity of habitat use by three temperate eel species Anguilla anguilla, A. japonica and A. rostrata. Mar Ecol Prog Ser 2006, 308:231-241.
• [46]Carthagena L, Bergamaschi A, Luna JM, David A, Uchil PD, Margottin-Goguet F, Mothes W, Hazan U, Transy C, Pancino G, Nisole S: Human TRIM gene expression in response to interferons. PLoS One 2009, 4:e4894.
• [47]Bonhommeau S, Blanke B, Tréguier AM, Grima N, Rivot E, Vermard Y, Greiner E, Le Pape O: How fast can the European eel (Anguilla anguilla) larvae cross the Atlantic Ocean? Fish Oceanogr 2009, 18:371-385.
• [48]Orr HA: The genetic theory of adaptation: a brief history. Nature Rev Genet 2005, 6:119-127.
• [49]Wainwright PC, Alfaro ME, Bolnick DI, Hulsey CD: Many-to-one mapping of form to function: a general principle in organismal design? Integr Comp Biol 2005, 45:256-262.
• [50]Raeymaekers JAM, Konijnendijk N, Larmuseau MHD, Hellemans B, De Meester L, Volckaert FAM: A gene with major phenotypic effects as a target for selection versus homogenizing gene flow. Mol Ecol 2014, 23:162-181.
• [51]Miller CT, Beleza S, Pollen AA, Schluter D, Kittles RA, Shriver MD, Kingsley DM: Cis-regulatory changes in Kit ligand expression and parallel evolution of pigmentation in sticklebacks and humans. Cell 2007, 131:1179-1189.
• [52]Hoekstra HE, Hirschmann RJ, Bundey RA, Insel PA, Crossland JP: A single amino acid mutation contributes to adaptive beach mouse color pattern. Science 2006, 313:101-104.
• [53]Roger SM, Bernatchez L: The genetic architecture of ecological speciation and the association with signatures of selection in natural lake whitefish (Coregonus sp.) species pairs. Mol Biol Evol 2007, 24:1423-1438.
• [54]Bernatchez L, Renault S, Whiteley AR, Derome N, Jeukens J, Landry L, Lu G, Nolte AW, Østbye K, Rogers SM, St-Cyr J: On the origin of species: insights from the ecological genomics of whitefish. Phil Trans R Soc B 2010, 367:354-363.
• [55]Gagnaire PA, Pavey SA, Normandeau E, Bernatchez L: The genetic architecture of reproductive isolation during speciation-with-gene-flow in lake whitefish species pairs assesed by RAD sequencing. Evolution 2013, 67:2483-2497.
• [56]Davey JW, Hohenlohe PA, Etter PD, Boone JQ, Catchen JM, Blaxter ML: Genome-wide genetic marker discovery and genotyping using next-generation sequencing. Nature Rev Genet 2011, 12:499-510.
• [57]Pujolar JM, Jacobsen MW, Frydenberg J, Als TD, Larsen PF, Maes GE, Zane L, Jian JB, Cheng L, Hansen MM: A resource of genome-wide single-nucleotide polymorphisms generated by RAD tag sequencing in the critically endangered European eel. Mol Ecol Resour 2013, 13:706-714.
• [58]Raymond M, Rousset F: GENEPOP (version 1.2): a population genetics software for exact tests and ecumenicism. J Hered 1995, 86:248-249.
• [59]Rice WR: Analyzing tables and statistical tests. Evolution 1989, 43:223-225.
• [60]Pritchard JK, Stephens M, Donnelly P: Inference of population structure using multilocus genotype data. Genetics 2000, 155:945-959.
• [61]Antao T, Lopes A, Lopes RJ, Beja-Pereira A, Luikart G: LOSITAN- a workbench to detect molecular adaptation based on a FST-outlier method. BMC Bioinformatics 2008, 9:323. BioMed Central Full Text
• [62]Beaumont MA, Nichols RA: Evaluating loci for use in the genetic analysis of population structure. Proc R Soc Lond B 1996, 263:1619-1626.
• [63]Foll M, Gaggiotti O: A genome-scan method to identify selected loci appropriate for both dominant and codominant markers: a Bayesian perspective. Genetics 2008, 180:977-993.