Shared ancestral polymorphisms and chromosomal rearrangements as potential drivers of local adaptation in a marine fish.


Journal

Molecular ecology
ISSN: 1365-294X
Titre abrégé: Mol Ecol
Pays: England
ID NLM: 9214478

Informations de publication

Date de publication:
07 2020
Historique:
received: 25 09 2019
revised: 19 05 2020
accepted: 26 05 2020
pubmed: 5 6 2020
medline: 8 6 2021
entrez: 5 6 2020
Statut: ppublish

Résumé

Gene flow has tremendous importance for local adaptation, by influencing the fate of de novo mutations, maintaining standing genetic variation and driving adaptive introgression. Furthermore, structural variation as chromosomal rearrangements may facilitate adaptation despite high gene flow. However, our understanding of the evolutionary mechanisms impending or favouring local adaptation in the presence of gene flow is still limited to a restricted number of study systems. In this study, we examined how demographic history, shared ancestral polymorphism, and gene flow among glacial lineages contribute to local adaptation to sea conditions in a marine fish, the capelin (Mallotus villosus). We first assembled a 490-Mbp draft genome of M. villosus to map our RAD sequence reads. Then, we used a large data set of genome-wide single nucleotide polymorphisms (25,904 filtered SNPs) genotyped in 1,310 individuals collected from 31 spawning sites in the northwest Atlantic. We reconstructed the history of divergence among three glacial lineages and showed that they probably diverged from 3.8 to 1.8 million years ago and experienced secondary contacts. Within each lineage, our analyses provided evidence for large N

Identifiants

pubmed: 32497342
doi: 10.1111/mec.15499
doi:

Banques de données

Dryad
['10.5061/dryad.hx3ffbgbp']

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

2379-2398

Informations de copyright

© 2020 John Wiley & Sons Ltd.

Références

Albers, P. K., & McVean, G. (2020). Dating genomic variants and shared ancestry in population-scale sequencing data. PLoS Biology, 18, e3000586. https://doi.org/10.1371/journal.pbio.3000586
Altschul, S. F., Gish, W., Miller, W., Myers, E. W., & Lipman, D. J. (1990). Basic local alignment search tool. Journal of Molecular Biology, 215, 403-410. https://doi.org/10.1016/S0022-2836(05)80360-2
Barrett, R. D., & Schluter, D. (2008). Adaptation from standing genetic variation. Trends in Ecology and Evolution, 23, 38-44. https://doi.org/10.1016/j.tree.2007.09.008
Barth, J. M., Berg, P. R., Jonsson, P. R., Bonanomi, S., Corell, H., Hemmer-Hansen, J., … André, C. (2017). Genome architecture enables local adaptation of Atlantic cod despite high connectivity. Molecular Ecology, 26, 4452-4466. https://doi.org/10.1111/mec.14207
Barton, N. H. (1998). The effect of hitch-hiking on neutral genealogies. Genetical Research, 72, 123-133. https://doi.org/10.1017/S0016672398003462
Barton, N., & Bengtsson, B. O. (1986). The barrier to genetic exchange between hybridising populations. Heredity, 57, 357. https://doi.org/10.1038/hdy.1986.135
Beaumont, M. A., & Nichols, R. A. (1996). Evaluating loci for use in the genetic analysis of population structure. Proceedings of the Royal Society of London. Series B: Biological Sciences, 263, 1619-1626.
Benestan, L., Quinn, B. K., Maaroufi, H., Laporte, M., Clark, F. K., Greenwood, S. J., … Bernatchez, L. (2016). Seascape genomics provides evidence for thermal adaptation and current-mediated population structure in American lobster (Homarus americanus). Molecular Ecology, 25, 5073-5092.
Berg, P. R., Star, B., Pampoulie, C., Bradbury, I. R., Bentzen, P., Hutchings, J. A., … Jakobsen, K. S. (2017). Trans-oceanic genomic divergence of Atlantic cod ecotypes is associated with large inversions. Heredity, 119, 418. https://doi.org/10.1038/hdy.2017.54
Bierne, N., Welch, J., Loire, E., Bonhomme, F., & David, P. (2011). The coupling hypothesis: Why genome scans may fail to map local adaptation genes. Molecular Ecology, 20, 2044-2072. https://doi.org/10.1111/j.1365-294X.2011.05080.x
Bitter, M. C., Kapsenberg, L., Gattuso, J. P., & Pfister, C. A. (2019). Standing genetic variation fuels rapid adaptation to ocean acidification. Nature Communications, 10, 1-10. https://doi.org/10.1038/s41467-019-13767-1
Blanquart, F., & Gandon, S. (2011). Evolution of migration in a periodically changing environment. The American Naturalist, 177(2), 188-201. https://doi.org/10.1086/657953
Blanquart, F., Kaltz, O., Nuismer, S. L., & Gandon, S. (2013). A practical guide to measuring local adaptation. Ecology Letters, 16(9), 1195-1205. https://doi.org/10.1111/ele.12150
Bosch, S., Tyberghein, L., & De Clerck, O. (2017). Sdmpredictors: Species distribution modeling predic-tor datasets. R package version 0.2. 6.
Bradbury, I. R., Hubert, S., Higgins, B., Borza, T., Bowman, S., Paterson, I. G., … Bentzen, P. (2010). Parallel adaptive evolution of Atlantic cod on both sides of the Atlantic Ocean in response to temperature. Proceedings of the Royal Society B: Biological Sciences, 277, 3725-3734. https://doi.org/10.1098/rspb.2010.0985
Bradbury, I. R., Laurel, B., Snelgrove, P. V., Bentzen, P., & Campana, S. E. (2008). Global patterns in marine dispersal estimates: The influence of geography, taxonomic category and life history. Proceedings of the Royal Society B: Biological Sciences, 275, 1803-1809.
Buren, A. D., Koen-Alonso, M., Pepin, P., Mowbray, F., Nakashima, B., Stenson, G., … Montevecchi, W. A. (2014). Bottom-up regulation of capelin, a keystone forage species. PLoS One, 9, e87589. https://doi.org/10.1371/journal.pone.0087589
Burri, R. (2017). Linked selection, demography and the evolution of correlated genomic landscapes in birds and beyond. Molecular Ecology, 26, 3853-3856. https://doi.org/10.1111/mec.14167
Burri, R., Nater, A., Kawakami, T., Mugal, C. F., Olason, P. I., Smeds, L., … Ellegren, H. (2015). Linked selection and recombination rate variation drive the evolution of the genomic landscape of differentiation across the speciation continuum of Ficedula flycatchers. Genome Research, 25, 1656-1665.
Camacho, C., & Hendry, A. P. (2020). Matching habitat choice: It's not for everyone. Oikos, 129(5), 689-699. https://doi.org/10.1111/oik.06932
Carscadden, J. E., Frank, K. T., & Leggett, W. C. (2001). Ecosystem changes and the effects on capelin (Mallotus villosus), a major forage species. Canadian Journal of Fisheries and Aquatic Sciences, 58, 73-85.
Catchen, J., Hohenlohe, P. A., Bassham, S., Amores, A., & Cresko, W. A. (2013). Stacks: An analysis tool set for population genomics. Molecular Ecology, 22, 3124-3140. https://doi.org/10.1111/mec.12354
Charlesworth, B., Morgan, M. T., & Charlesworth, D. (1993). The effect of deleterious mutations on neutral molecular variation. Genetics, 134, 1289-1303.
Clobert, J., Le Galliard, J. F., Cote, J., Meylan, S., & Massot, M. (2009). Informed dispersal, heterogeneity in animal dispersal syndromes and the dynamics of spatially structured populations. Ecology Letters, 12, 197-209. https://doi.org/10.1111/j.1461-0248.2008.01267.x
Colbeck, G. J., Turgeon, J., Sirois, P., & Dodson, J. J. (2011). Historical introgression and the role of selective vs. neutral processes in structuring nuclear genetic variation (AFLP) in a circumpolar marine fish, the capelin (Mallotus villosus). Molecular Ecology, 20, 1976-1987. https://doi.org/10.1111/j.1365-294X.2011.05069.x
Coyne, J. A., & Orr, H. A. (2004). Speciation. Sunderland, MA: Sinauer.
Cruickshank, T. E., & Hahn, M. W. (2014). Reanalysis suggests that genomic islands of speciation are due to reduced diversity, not reduced gene flow. Molecular Ecology, 23, 3133-3157. https://doi.org/10.1111/mec.12796
Csilléry, K., Rodríguez-Verdugo, A., Rellstab, C., & Guillaume, F. (2018). Detecting the genomic signal of polygenic adaptation and the role of epistasis in evolution. Molecular Ecology, 27, 606-612. https://doi.org/10.1111/mec.14499
DeWoody, J. A., & Avise, J. C. (2000). Microsatellite variation in marine, freshwater and anadromous fishes compared with other animals. Journal of Fish Biology, 56, 461-473. https://doi.org/10.1111/j.1095-8649.2000.tb00748.x
Dodson, J. J., Tremblay, S., Colombani, F., Carscadden, J. E., & Lecomte, F. (2007). Trans-Arctic dispersals and the evolution of a circumpolar marine fish species complex, the capelin (Mallotus villosus). Molecular Ecology, 16, 5030-5043. https://doi.org/10.1111/j.1365-294X.2007.03559.x
Dorant, Y., Benestan, L., Rougemont, Q., Normandeau, E., Boyle, B., Rochette, R., & Bernatchez, L. (2019). Comparing Pool-seq, Rapture, and GBS genotyping for inferring weak population structure: The American lobster (Homarus americanus) as a case study. Ecology and Evolution, 9, 6606-6623.
Dormann, C. F., Elith, J., Bacher, S., Buchmann, C., Carl, G., Carré, G., … Lautenbach, S. (2013). Collinearity: A review of methods to deal with it and a simulation study evaluating their performance. Ecography, 36, 27-46. https://doi.org/10.1111/j.1600-0587.2012.07348.x
Edelaar, P., Siepielski, A. M., & Clobert, J. (2008). Matching habitat choice causes directed gene flow: A neglected dimension in evolution and ecology. Evolution, 62, 2462-2472. https://doi.org/10.1111/j.1558-5646.2008.00459.x
Ewing, G. B., & Jensen, J. D. (2016). The consequences of not accounting for background selection in demographic inference. Molecular Ecology, 25, 135-141. https://doi.org/10.1111/mec.13390
Faria, R., Johannesson, K., Butlin, R. K., & Westram, A. M. (2019). Evolving inversions. Trends in Ecology & Evolution, 34, 239-248. https://doi.org/10.1016/j.tree.2018.12.005
Faria, R., & Navarro, A. (2010). Chromosomal speciation revisited: Rearranging theory with pieces of evidence. Trends in Ecology & Evolution, 25, 660-669. https://doi.org/10.1016/j.tree.2010.07.008
Forester, B. R., Lasky, J. R., Wagner, H. H., & Urban, D. L. (2018). Comparing methods for detecting multilocus adaptation with multivariate genotype-environment associations. Molecular Ecology, 27, 2215-2233. https://doi.org/10.1111/mec.14584
Frank, K. T., & Leggett, W. C. (1981a). Wind regulation of emergence times and early larval survival in capelin (Mallotus villosus). Canadian Journal of Fisheries and Aquatic Sciences, 38, 215-223.
Frank, K. T., & Leggett, W. C. (1981b). Prediction of egg development and mortality rates in capelin (Mallotus villosus) from meteorological, hydrographic, and biological factors. Canadian Journal of Fisheries and Aquatic Sciences, 38, 1327-1338.
Frank, K. T., & Leggett, W. C. (1982). Environmental regulation of growth rate, efficiency, and swimming performance in larval capelin (Mallotus villosus), and its application to the match/mismatch hypothesis. Canadian Journal of Fisheries and Aquatic Sciences, 39, 691-699.
François, O., Martins, H., Caye, S. D. (2015). Schoville. Controlling false discoveries in genome scans for selection. Molecular Ecology, 25(2), 454-469.
Frichot, E., & François, O. (2015). LEA: An R package for landscape and ecological association studies. Methods in Ecology and Evolution, 6, 925-929. https://doi.org/10.1111/2041-210X.12382
Frichot, E., Schoville, S. D., Bouchard, G., & François, O. (2013). Testing for associations between loci and environmental gradients using latent factor mixed models. Molecular Biology and Evolution, 30, 1687-1699. https://doi.org/10.1093/molbev/mst063
Gagnaire, P.-A., Lamy, J.-B., Cornette, F., Heurtebise, S., Dégremont, L., Flahauw, E., … Lapègue, S. (2018). Analysis of genome-wide differentiation between native and introduced populations of the cupped oysters Crassostrea gigas and Crassostrea angulata. Genome Biology and Evolution, 10, 2518-2534. https://doi.org/10.1093/gbe/evy194
Graffelman, J. (2015). Exploring diallelic genetic markers: The hardy weinberg package. Journal of Statistical Software, 64, 1-23.
Gutenkunst, R. N., Hernandez, R. D., Williamson, S. H., & Bustamante, C. D. (2009). Inferring the joint demographic history of multiple populations from multidimensional SNP frequency data. PLOS Genetics, 5, e1000695. https://doi.org/10.1371/journal.pgen.1000695
Haenel, Q., Roesti, M., Moser, D., MacColl, A. D., & Berner, D. (2019). Predictable genome-wide sorting of standing genetic variation during parallel adaptation to basic versus acidic environments in stickleback fish. Evolution Letters, 3, 28-42. https://doi.org/10.1002/evl3.99
Hancock, A. M., Alkorta-Aranburu, G., Witonsky, D. B., & Di Rienzo, A. (2010). Adaptations to new environments in humans: The role of subtle allele frequency shifts. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 365(1552), 2459-2468. https://doi.org/10.1098/rstb.2010.0032
Hedges, S. B., Marin, J., Suleski, M., Paymer, M., & Kumar, S. (2015). Tree of life reveals clock-like speciation and diversification. Molecular Biology and Evolution, 32, 835-845. https://doi.org/10.1093/molbev/msv037
Hedrick, P. W. (2013). Adaptive introgression in animals: Examples and comparison to new mutation and standing variation as sources of adaptive variation. Molecular Ecology, 22, 4606-4618. https://doi.org/10.1111/mec.12415
Hudson, R. R. (2002). Generating samples under a Wright-Fisher neutral model of genetic variation. Bioinformatics, 18, 337-338. https://doi.org/10.1093/bioinformatics/18.2.337
Jacob, S., Legrand, D., Chaine, A. S., Bonte, D., Schtickzelle, N., Huet, M., & Clobert, J. (2017). Gene flow favours local adaptation under habitat choice in ciliate microcosms. Nature Ecology & Evolution, 1, 1407. https://doi.org/10.1038/s41559-017-0269-5
Jombart, T. (2008). adegenet: A R package for the multivariate analysis of genetic markers. Bioinformatics, 24, 1403-1405. https://doi.org/10.1093/bioinformatics/btn129
Jones, F. C., Chan, Y. F., Schmutz, J., Grimwood, J., Brady, S. D., Southwick, A. M., … Kingsley, D. M. (2012). A genome-wide SNP genotyping array reveals patterns of global and repeated species-pair divergence in sticklebacks. Current Biology, 22, 83-90. https://doi.org/10.1016/j.cub.2011.11.045
Kaplan, N. L., Hudson, R. R., & Langley, C. H. (1989). The “hitchhiking effect” revisited. Genetics, 123, 887-899.
Kawecki, T. J., & Ebert, D. (2004). Conceptual issues in local adaptation. Ecology Letters, 7, 1225-2124. https://doi.org/10.1111/j.1461-0248.2004.00684.x
Kelley, J. L., Brown, A. P., Therkildsen, N. O., & Foote, A. D. (2016). The life aquatic: Advances in marine vertebrate genomics. Nature Reviews Genetics, 17, 523. https://doi.org/10.1038/nrg.2016.66
Kern, D., & Schrider, D. R. (2018). diploS/HIC: An updated approach to classifying selective sweeps. G3: Genes, Genomes, Genetics, 8, 1959-1970.
Li, H., & Ralph, P. (2018). Local PCA Shows How the Effect of Population Structure Differs Along the Genome. Genetics, 211(1), 289-304. https://doi.org/10.1534/genetics.118.301747
Lai, Y. T., Yeung, C. K., Omland, K. E., Pang, E. L., Hao, Y., Liao, B. Y., … Hung, H. Y. (2019). Standing genetic variation as the predominant source for adaptation of a songbird. Proceedings of the National Academy of Sciences of the United Staes of America, 116, 2152-2157. https://doi.org/10.1073/pnas.1813597116
Lamichhaney, S., Barrio, A. M., Rafati, N., Sundström, G., Rubin, C. J., Gilbert, E. R., … Andersson, L. (2012). Population-scale sequencing reveals genetic differentiation due to local adaptation in Atlantic herring. Proceedings of the National Academy of Sciences of the United States of America, 109, 19345-19350. https://doi.org/10.1073/pnas.1216128109
Laporte, M., Pavey, S. A., Rougeux, C., Pierron, F., Lauzent, M., Budzinski, H., … Bernatchez, L. (2016). RAD sequencing reveals within-generation polygenic selection in response to anthropogenic organic and metal contamination in North Atlantic Eels. Molecular Ecology, 25, 219-237. https://doi.org/10.1111/mec.13466
Lasky, J. R., Des Marais, D. L., McKay, J. K., Richards, J. H., Juenger, T. E., & Keitt, T. H. (2012). Characterizing genomic variation of Arabidopsis thaliana: The roles of geography and climate. Molecular Ecology, 21, 5512-5529.
Le Moan, A., Bekkevold, D., & Hemmer-Hansen, J. (2019). Evolution at two-time frames shape structural variants and population structure of European plaice (Pleuronectes platessa). BioRxiv, 662577.
Le Moan, A. L., Gagnaire, P.-A., & Bonhomme, F. (2016). Parallel genetic divergence among coastal-marine ecotype pairs of European anchovy explained by differential introgression after secondary contact. Molecular Ecology, 25, 3187-3202. https://doi.org/10.1111/mec.13627
Legendre, P., & Legendre, L. F. (2012). Numerical ecology. Amsterdam, the Netherland: Elsevier.
Leggett, W. C., Frank, K. T., & Carscadden, J. E. (1984). Meteorological and hydrographic regulation of year-class strength in capelin (Mallotus villosus). Canadian Journal of Fisheries and Aquatic Sciences, 41, 1193-1201.
Lenormand, T. (2002). Gene flow and the limits to natural selection. Trends in Ecology & Evolution, 17, 183-189. https://doi.org/10.1016/S0169-5347(02)02497-7
Leroy, T., Rougemont, Q., Dupouey, J.-L., Bodénès, C., Lalanne, C., Belser, C., … Plomion, C. (2019). Massive postglacial gene flow between European white oaks uncovered genes underlying species barriers. New Phytologist, 214, 865-878.
Li, H. (2013). Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. arXiv preprint arXiv:1303.3997.
Linnen, C. R., Kingsley, E. P., Jensen, J. D., & Hoekstra, H. E. (2009). On the origin and spread of an adaptive allele in deer mice. Science, 325, 1095-1109. https://doi.org/10.1126/science.1175826
Lotterhos, K. E. (2019). The effect of neutral recombination variation on genome scans for selection. G3: Genes, Genomes, Genetics, 9, 1851-1867. https://doi.org/10.1534/g3.119.400088
Lowe, W. H., & Addis, B. R. (2019). Matching habitat choice and plasticity contribute to phenotype-environment covariation in a stream salamander. Ecology, 100, e02661. https://doi.org/10.1002/ecy.2661
Lowry, D. B., Hoban, S., Kelley, J. L., Lotterhos, K. E., Reed, L. K., Antolin, M. F., & Storfer, A. (2017). Breaking RAD: an evaluation of the utility of restriction site-associated DNA sequencing for genome scans of adaptation. Mol Ecol Resour, 17, 142-152. https://doi.org/10.1111/1755-0998.12635
Ma, J., & Amos, C. I. (2012). Investigation of inversion polymorphisms in the human genome using principal components analysis. PLoS One, 7, e40224. https://doi.org/10.1371/journal.pone.0040224
Martin, M. (2011). Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet.journal, 17, 10-12. https://doi.org/10.14806/ej.17.1.200
Mérot, C., Berdan, E. L., Babin, C., Normandeau, E., Wellenreuther, M., & Bernatchez, L. (2018). Intercontinental karyotype-environment parallelism supports a role for a chromosomal inversion in local adaptation in a seaweed fly. Proceedings of the Royal Society B: Biological Sciences, 285, 20180519. https://doi.org/10.1098/rspb.2018.0519
Monnahan, P. J., Colicchio, J., & Kelly, J. K. (2015). A genomic selection component analysis characterizes migration-selection balance. Evolution, 69, 1713-1727. https://doi.org/10.1111/evo.12698
Moore, J. S., Harris, L. N., Le Luyer, J., Sutherland, B. J. G., Rougemont, Q., Tallman, R. F., & Bernatchez, L. (2017). Genomics and telemetry suggest a role for migration harshness in determining overwintering habitat choice, but not gene flow, in anadromous Arctic Char. Molecular Ecology, 26(24), 1713-6800. https://doi.org/10.1111/mec.14393
Nakashima, B. S., & Wheeler, J. P. (2002). Capelin (Mallotus villosus) spawning behaviour in Newfoundland waters-The interaction between beach and demersal spawning. ICES Journal of Marine Science, 59, 909-916. https://doi.org/10.1006/jmsc.2002.1261
Oziolor, E. M., Reid, N. M., Yair, S., Lee, K. M., Guberman VerPloeg, S., Bruns, P. C., … Matson, C. W. (2019). Adaptive introgression enables evolutionary rescue from extreme environmental pollution. Science, 364, 455-457. https://doi.org/10.1126/science.aav4155
Palumbi, S. R. (1992). Marine speciation on a small planet. Trends in Ecology & Evolution, 7, 114-118. https://doi.org/10.1016/0169-5347(92)90144-Z
Pauly, D. (1980). On the interrelationships between natural mortality, growth parameters, and mean environmental temperature in 175 fish stocks. ICES Journal of Marine Science, 39, 175-192. https://doi.org/10.1093/icesjms/39.2.175
Pavlidis, P., Jensen, J. D., Stephan, W., Stamatakis, A. (2012). A critical assessment of storytelling: gene ontology categories and the importance of validating genomic scans. Molecular Biology and Evolution, 29(10), 3237-3248. https://doi.org/10.1093/molbev/mss136
Pembleton, L. W., Cogan, N. O., & Forster, J. W. (2013). stampp: An R package for calculation of genetic differentiation and structure of mixed-ploidy level populations. Molecular Ecology Resources, 13, 946-952. https://doi.org/10.1111/1755-0998.12129
Pettersson, M. E., Rochus, C. M., Han, F., Chen, J., Hill, J., Hill, J., … Andersso, L. (2019). A chromosome-level assembly of the Atlantic herring genome-detection of a supergene and other signals of selection. Genome Research, 29, 1919-1928.
Praebel, K., Christiansen, J. S., Kettunen-Praebel, A., & Fevolden, S. E. (2013). Thermohaline tolerance and embryonic development in capelin eggs (Mallotus villosus) from the Northeast Atlantic Ocean. Environmental Biology of Fishes, 96, 753-761. https://doi.org/10.1007/s10641-012-0069-3
Praebel, K., Westgaard, J. I., Fevolden, S. E., & Christiansen, J. S. (2008). Circumpolar genetic population structure of capelin Mallotus villosus. Marine Ecology Progress Series, 360, 189-199. https://doi.org/10.3354/meps07363
Prezeworski, M., Coop, G., & Wall, J. D. (2005). The signature of positive selection on standing genetic variation. Evolution, 59, 2312-2323. https://doi.org/10.1111/j.0014-3820.2005.tb00941.x
Pritchard, J. K., & Di Rienzo, A. (2010). Adaptation-not by sweeps alone. Nature Reviews Genetics, 11, 665-667. https://doi.org/10.1038/nrg2880
Purchase, C. F. (2018). Low tolerance of salt water in a marine fish: New and historical evidence for surprising local adaption in the well-studied commercially exploited capelin. Canadian Journal of Fisheries and Aquatic Sciences, 75, 673-681. https://doi.org/10.1139/cjfas-2017-0058
Racimo, F., Sankararaman, S., Nielsen, R., & Huerta-Sánchez, E. (2015). Evidence for archaic adaptive introgression in humans. Nature Reviews Genetics, 16, 359-371. https://doi.org/10.1038/nrg3936
Riquet, F., Liautard-Haag, C., Woodall, L., Bouza, C., Louisy, P., Hamer, B., … Bierne, N. (2019). Parallel pattern of differentiation at a genomic island shared between clinal and mosaic hybrid zones in a complex of cryptic seahorse lineages. Evolution, 73, 817-835. https://doi-org.acces.bibl.ulaval.ca/10.1111/evo.13696
Rose, G. A. (2005). Capelin (Mallotus villosus) distribution and climate: A sea “canary” for marine ecosystem change. ICES Journal of Marine Science, 62, 1524-1530. https://doi.org/10.1016/j.icesjms.2005.05.008
Rougemont, Q., & Bernatchez, L. (2018). The demographic history of Atlantic salmon (Salmo salar) across its distribution range reconstructed from approximate Bayesian computations. Evolution, 72, 1261-1277.
Rougemont, Q., Carrier, A., Le Luyer, J., Ferchaud, A. L., Farrell, J. M., Hatin, D., … Bernatchez, L. (2019). Combining population genomics and forward simulations to investigate stocking impacts: A case study of Muskellunge (Esox masquinongy) from the St. Lawrence River Basin. Evolutionary Applications, 12, 902-922.
Rougemont, Q., Gagnaire, P.-A., Perrier, C., Genthon, C., Besnard, A.-L., Launey, S., & Evanno, G. (2017). Inferring the demographic history underlying parallel genomic divergence among pairs of parasitic and nonparasitic lamprey ecotypes. Molecular Ecology, 20, 142-162.
Roux, C., Castric, V., Pauwels, M., Wright, S. I., Saumitou-Laprade, P., & Vekemans, X. (2011). Does speciation between Arabidopsis halleri and Arabidopsis lyrata coincide with major changes in a molecular target of adaptation? PLoS One, 6, e26872. https://doi.org/10.1371/journal.pone.0026872
Roux, C., Fraïsse, C., Castric, V., Vekemans, X., Pogson, G. H., & Bierne, N. (2014). Can we continue to neglect genomic variation in introgression rates when inferring the history of speciation? A case study in a Mytilus hybrid zone. Journal of Evolutionary Biology, 27, 1662-1675. https://doi.org/10.1111/jeb.12425
Roux, C., Fraïsse, C., Romiguier, J., Anciaux, Y., Galtier, N., & Bierne, N. (2016). Shedding light on the grey zone of speciation along a continuum of genomic divergence. PLoS Biology, 14, e2000234. https://doi.org/10.1371/journal.pbio.2000234
Roux, C., Tsagkogeorga, G., Bierne, N., & Galtier, N. (2013). Crossing the species barrier: Genomic hotspots of introgression between two highly divergent Ciona intestinalis species. Molecular Biology and Evolution, 30, 1574-1587. https://doi.org/10.1093/molbev/mst066
Savolainen, O., Lascoux, M., & Merilä, J. (2013). Ecological genomics of local adaptation. Nature Reviews Genetics, 14, 807-820. https://doi.org/10.1038/nrg3522
Selkoe, K. A., Aloia, C. C., Crandall, E. D., Iacchei, M., Liggins, L., Puritz, J. B., … Toonen, R. J. (2016). A decade of seascape genetics: Contributions to basic and applied marine connectivity. Marine Ecology Progress Series, 554, 1-19. https://doi.org/10.3354/meps11792
Skatkin, M. (2005). "Seeing ghosts: the effect of unsampled populations on migration rates estimated for sampled populations". Molecular Ecology, 14, 67-73. https://doi.org/10.1111/j.1365-294X.2004.02393.x
Smith, J. M., & Haigh, J. (1974). The hitch-hiking effect of a favourable gene. Genetical Research, 23, 23-35. https://doi.org/10.1017/S0016672300014634
Sousa, V., Hey, J. (2013). Understanding the origin of species with genome-scale data: modelling gene flow. Nat Rev Genet, 14, 404-414.
Stankowski, S., Chase, M. A., Fuiten, A. M., Rodrigues, M. F., Ralph, P. L., & Streisfeld, M. A. (2019). Widespread selection and gene flow shape the genomic landscape during a radiation of monkeyflowers. BioRxiv, 342352.
Stanley, R. R. E., DiBacco, C., Lowen, B., Beiko, R. G., Jeffery, N. W., Van Wyngaarden, M., … Bradbury, I. R. (2018). A climate-associated multi-species cryptic genetic cline in the northwest Atlantic. Science Advances, 4, eaaq0929.
Tigano, A., & Friesen, V. L. (2016). Genomics of local adaptation with gene flow. Molecular Ecology, 25, 2144-2164. https://doi.org/10.1111/mec.13606
Tine, M., Kuhl, H., Gagnaire, P. A., Louro, B., Desmarais, E., Martins, R. S., … Reinhardt, R. (2014). European sea bass genome and its variation provide insights into adaptation to euryhalinity and speciation. Nature Communications, 5, 5770. https://doi.org/10.1038/ncomms6770
Van Wyngaarden, M., Snelgrove, P. V., DiBacco, C., Hamilton, L. C., Rodríguez-Ezpeleta, N., Jeffery, N. W., … Bradbury, I. R. (2017). Identifying patterns of dispersal, connectivity and selection in the sea scallop, Placopecten magellanicus, using RAD seq-derived SNPs. Evolutionary Applications, 10, 102-117.
Wang, J., Street, N. R., Scofield, D. G., & Ingvarsson, P. K. (2016). Variation in linked selection and recombination drive genomic divergence during allopatric speciation of European and American aspens. Molecular Biology and Evolution, 33, 1754-1767. https://doi.org/10.1093/molbev/msw051
Weir, B. S., & Cockerham, C. C. (1984). Estimating F-statistics for the analysis of population structure. Evolution, 38, 1358-1370.
Welch, J. J., & Jiggins, C. D. (2014). Standing and flowing: The complex origins of adaptive variation. Molecular Ecology, 23, 3935-3937. https://doi.org/10.1111/mec.12859
Wellband, K., Mérot, C., Linnansaari, T., Elliott, J. A. K., Curry, R. A., & Bernatchez, L. (2019). Chromosomal fusion and life history-associated genomic variation contribute to within-river local adaptation of Atlantic salmon. Molecular Ecology, 28, 1439-1459. https://doi.org/10.1111/mec.14965
Wellenreuther, M., & Bernatchez, L. (2018). Eco-evolutionary genomics of chromosomal inversions. Trends in Ecology & Evolution, 33, 427-440. https://doi.org/10.1016/j.tree.2018.04.002
Wellenreuther, M., Mérot, C., Berdan, E., & Bernatchez, L. (2019). Going beyond SNP s: The role of structural genomic variants in adaptive evolution and species diversification. Molecular Ecology, 28, 1203-1209. https://doi.org/10.1111/mec.15066
Westram, A. M., Rafajlovic, M., Chaube, P., Faria, R., Larsson, T., Panova, M., … Butlin, R. (2018). Clines on the seashore: The genomic architecture underlying rapid divergence in the face of gene flow. Evolution Letters, 2, 297-309. https://doi.org/10.1002/evl3.74
Wright, S. (1931). Evolution in Mendelian populations. Genetics, 16, 97-159.
Wu, C.-I. (2001). The genic view of the process of speciation. Journal of Evolutionary Biology, 14, 851-865. https://doi.org/10.1046/j.1420-9101.2001.00335.x
Xuereb, A., Kimber, C., Curtis, J., Bernatchez, L., & Fortin, M. J. (2018). Putatively adaptive genetic variation in the Giant California sea cucumber (Parastichopus californicus) as revealed by environmental association analysis of RADseq data. Molecular Ecology, 27, 5035-5048.
Yeaman, S., & Otto, S. P. (2011). Establishment and maintenance of adaptive genetic divergence under migration, selection, and drift. Evolution, 65, 2123-2129. https://doi.org/10.1111/j.1558-5646.2011.01277.x

Auteurs

Hugo Cayuela (H)

Institut de Biologie Intégrative et des Systèmes (IBIS), Université Laval, Quebec City, QC, Canada.

Quentin Rougemont (Q)

Institut de Biologie Intégrative et des Systèmes (IBIS), Université Laval, Quebec City, QC, Canada.

Martin Laporte (M)

Institut de Biologie Intégrative et des Systèmes (IBIS), Université Laval, Quebec City, QC, Canada.

Claire Mérot (C)

Institut de Biologie Intégrative et des Systèmes (IBIS), Université Laval, Quebec City, QC, Canada.

Eric Normandeau (E)

Institut de Biologie Intégrative et des Systèmes (IBIS), Université Laval, Quebec City, QC, Canada.

Yann Dorant (Y)

Institut de Biologie Intégrative et des Systèmes (IBIS), Université Laval, Quebec City, QC, Canada.

Ole K Tørresen (OK)

Centre for Ecological and Evolutionary Synthesis (CEES), Department of Biosciences, University of Oslo, Oslo, Norway.

Siv Nam Khang Hoff (SNK)

Centre for Ecological and Evolutionary Synthesis (CEES), Department of Biosciences, University of Oslo, Oslo, Norway.

Sissel Jentoft (S)

Centre for Ecological and Evolutionary Synthesis (CEES), Department of Biosciences, University of Oslo, Oslo, Norway.

Pascal Sirois (P)

Département des sciences fondamentales, Université du Québec à Chicoutimi, Chicoutimi, QC, Canada.

Martin Castonguay (M)

Fisheries and Oceans Canada, Institut Maurice-Lamontagne, Mont-Joli, QC, Canada.

Teunis Jansen (T)

GINR-Greenland Institute of Natural Resources, Nuuk, Greenland.
DTU Aqua-National Institute of Aquatic Resources, Technical University of Denmark, Charlottenlund Castle, Charlottenlund, Denmark.

Kim Praebel (K)

Norwegian College of Fishery Science, Faculty of Biosciences, Fisheries and Economics, UiT The Arctic University of Norway, Tromsø, Norway.

Marie Clément (M)

Center for Fisheries Ecosystems Research, Fisheries and Marine Institute of Memorial, University of Newfoundland, St. John's, NL, Canada.
Labrador Institute of Memorial University of Newfoundland, Happy Valley-Goose Bay, NL, Canada.

Louis Bernatchez (L)

Institut de Biologie Intégrative et des Systèmes (IBIS), Université Laval, Quebec City, QC, Canada.

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