Riverscape genetics in brook lamprey: genetic diversity is less influenced by river fragmentation than by gene flow with the anadromous ecotype.


Journal

Heredity
ISSN: 1365-2540
Titre abrégé: Heredity (Edinb)
Pays: England
ID NLM: 0373007

Informations de publication

Date de publication:
02 2021
Historique:
received: 15 12 2019
accepted: 01 09 2020
revised: 28 08 2020
pubmed: 30 9 2020
medline: 26 10 2021
entrez: 29 9 2020
Statut: ppublish

Résumé

Understanding the effect of human-induced landscape fragmentation on gene flow and evolutionary potential of wild populations has become a major concern. Here, we investigated the effect of riverscape fragmentation on patterns of genetic diversity in the freshwater resident European brook lamprey (Lampetra planeri) that has a low ability to pass obstacles to migration. We tested the hypotheses of (i) asymmetric gene flow following water current and (ii) an effect of gene flow with the closely related anadromous river lamprey (L. fluviatilis) ecotype on L. planeri genetic diversity. We genotyped 2472 individuals, including 225 L. fluviatilis, sampled from 81 sites upstream and downstream barriers to migration, in 29 western European rivers. Linear modelling revealed a strong positive relationship between genetic diversity and the distance from the river source, consistent with expected patterns of decreased gene flow into upstream populations. However, the presence of anthropogenic barriers had a moderate effect on spatial genetic structure. Accordingly, we found evidence for downstream-directed gene flow, supporting the hypothesis that barriers do not limit dispersal mediated by water flow. Downstream L. planeri populations in sympatry with L. fluviatilis displayed consistently higher genetic diversity. We conclude that genetic drift and slight downstream gene flow drive the genetic make-up of upstream L. planeri populations whereas gene flow between ecotypes maintains higher levels of genetic diversity in L. planeri populations sympatric with L. fluviatilis. We discuss the implications of these results for the design of conservation strategies of lamprey, and other freshwater organisms with several ecotypes, in fragmented dendritic river networks.

Identifiants

pubmed: 32989279
doi: 10.1038/s41437-020-00367-9
pii: 10.1038/s41437-020-00367-9
pmc: PMC8027852
doi:

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

235-250

Références

Alonso H, Matias R, Granadeiro JP, Catry P (2009) Moult strategies of Cory’s Shearwaters Calonectris diomedea borealis the influence of colony location sex and individual breeding status. J Ornithol 150:329–337
Barson NJ, Cable J, Van Oosterhout C (2009) Population genetic analysis of microsatellite variation of guppies (Poecilia reticulata) in Trinidad and Tobago: evidence for a dynamic source-sink metapopulation structure, founder events and population bottlenecks. J Evol Biol 22:485–497
pubmed: 19210594
Bartoń K (2018) MuMIn: Multi-Model Inference. R package version 1.42.1. https://CRAN.R-project.org/package=MuMIn
Bates DM, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48
Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F (2004) GENETIX 4.05, logiciel sous Windows pour la génétique des populations. Laboratoire Génome, Populations, Interactions, CNRS UMR 5000 Université de Montpellier II, Montpellier, France
Bernard H (1909) Bulletin de la Société des Sciences Naturelle et d’Archeologie de l’Ain, vol 57 Imprimerie du Journal, Bourg-en-Bresse
Bernatchez L, Wilson CC (1998) Comparative phylogeography of Nearctic and Palearctic fishes. Mol Ecol 7:431–452
Blanchet S, Rey O, Etienne R, Lek S, Loot G (2010) Species-specific responses to landscape fragmentation: implications for management strategies. Evol Appl 3:291–304
pubmed: 25567925 pmcid: 3352461
Bracken FSA, Hoelzel AR, Hume JB, Lucas MC (2015) Contrasting population genetic structure among freshwater-resident and anadromous lampreys: the role of demographic history, differential dispersal, and anthropogenic barriers to movement. Mol Ecol 24:1188–1204
pubmed: 25689694 pmcid: 4413359
Brauer CJ, Hammer MP, Beheregaray LB (2016) Riverscape genomics of a threatened fish across a hydroclimatically heterogeneous river basin. Mol Ecol 25:5093–5113
pubmed: 27575282
Carlson SM, Cunningham CJ, Westley PAH (2014) Evolutionary rescue in a changing world. Trends Ecol Evol 29(9):521–530
pubmed: 25038023
Ceballos G, Ehrlich PR, Dirzo R (2017) Biological annihilation via the ongoing sixth mass extinction signaled by vertebrate population losses and declines. Proc Natl Acad Sci USA 30:6089–6096
Ceballos G, Ehrlich PR, Raven PH (2020) Vertebrates on the brink as indicators of biological annihilation and the sixth mass extinction Proc Natl Acad Sci USA 117:13596–13602
pubmed: 32482862
Coleman RA, Gauffre B, Pavlova A, Beheregaray LB, Kearns, Lyon J et al. (2018) Artificial barriers prevent genetic recovery of small isolated populations of a low-mobility freshwater fish. Heredity 120:515–532
pubmed: 29326479 pmcid: 5943333
Couvet D (2002) Deleterious effects of restricted gene flow in fragmented populations. Conserv Biol 16:369–376
Cyr F, Angers B (2011) Historical process lead to false genetic signal of current connectivity among populations. Genetica 139:1417–1428
pubmed: 22388987
Dawson HA, Quintella BR, Almeida PR, Treble AJ, Jolley JC (2015) The ecology of larval and metamorphosing lampreys. In: Docker MF (ed.), Lampreys: biology, conservation and control. Springer, Netherlands, pp. 75–137
Dehais C, Eudeline R, Berrebi P, Argillier C (2010) Microgeographic genetic isolation in chub (Cyprinidae: Squalius cephalus) population of the Durance River: estimating fragmentation by dams. Ecol Freshw Fish 19:267–278
DiBattista JD (2008) Patterns of genetic variation in anthropogenically impacted populations. Conserv Genet 9:141–156
Docker MF (2009) A review of the evolution of non-parasitism in lampreys and an update of the paired species concept. In: Brown LR, Chase SD, Mesa MG, Beamish RJ, Moyle PB (eds) Biology, management and conservation of lampreys in North America. Am Fish Soc Symp 72, Bethesda, MD, pp. 71–114
Dodson JJ, Aubin-Horth N, Thériault V, Páez DJ (2013) The evolutionary ecology of alternative migratory tactics in salmonid fishes. Biol Rev Camb Philos Soc 88:602–625
pubmed: 23347290
Dynesius M, Nilsson C (1994) Fragmentation and flow regulation of river systems in the northern third of the world. Science 266:753–762
pubmed: 17730396
Earl DA, vonHoldt BM (2011) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361
Edmands S (2007) Between a rock and a hard place: evaluating the relative risks of inbreeding and outbreeding for conservation and management. Mol Ecol 16:463–475
pubmed: 17257106
Eneqvist P (1937) The brook lamprey as an ecological modification of the river lamprey. On the river and brook lampreys of Sweden. Ark Zool 29:1–22
Espanhol R, Almeida PR, Alves MJ (2007) Evolutionary history of lamprey paired species Lampetra fluviatilis (L.) and Lampetra planeri (Bloch) as inferred from mitochondrial DNA variation. Mol Ecol 16:1909–1924
pubmed: 17444901
Estoup A (1996) Rapid one-tube DNA extraction for reliable PCR detection of fish polymorphic markers and transgenes. Mol Mar Biol Biotechnol 5:295–298
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620
pubmed: 15969739 pmcid: 15969739
Fahrig L (2003) Effects of habitat fragmentation on biodiversity. Annu Rev Ecol, Evolution, Syst 34:487–515
Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587
pubmed: 1462648 pmcid: 1462648
Faubet P, Waples RS, Gaggiotti OE (2007) Evaluating the performance of a multilocus Bayesian method for the estimation of migration rates. Mol Ecol 16:1149–1166
pubmed: 17391403
Faulks LK, Gilligan DM, Beheregaray LB (2010) Islands of water in a sea of dry land: hydrological regime predicts genetic diversity and dispersal in a widespread fish from Australia’s arid zone, the golden perch (Macquaria ambigua). Mol Ecol 19:4723–4737
pubmed: 20887362
Fox J, Weisberg S (2011) An {R} companion to applied regression, 2nd edn. Sage, Thousand Oaks, CA
Foulds WL, Lucas MC (2013) Extreme inefficiency of two conventional, technical fishways used by European river lamprey (Lampetra fluviatilis). Ecol Eng 58:423–433
Frankham R (1998) Inbreeding and extinction: island populations. Conserv Biol 12:665–675
Frankham R (2005) Genetics and extinction. Biol Conserv 126:131–140
Frankham R (2015) Genetic rescue of small inbred populations: meta-analysis reveals large and consistent benefits of gene flow. Mol Ecol 24:2610–2618
pubmed: 25740414
Frankham R (2016) Genetic rescue benefits persist to at least the F3 generation, based on a meta-analysis. Biol Conserv 195:33–36
Frankham R, Bradshaw CJA, Brook BW (2014) Genetics in conservation management: revised recommendations for the 50/500 rules, Red List criteria and population viability analyses. Biol Conserv 170:56–63
Gaigher A, Launey S, Lasne E, Besnard AL, Evanno G (2013) Characterization of thirteen microsatellite markers in river and brook lampreys (Lampetra fluviatilis and L. planeri). Conserv Genet Resour 5:141–143
Gensoul J (1907) Monographie des poisons d’eau douce de Saone et Loire. Extrait du Bulletin de la société d’histoire naturelle d’Autun. 20è Bulletin
Germis G, Arago MA, Ampen N, Moulin C, Deleys, N (2018) Plan de Gestion des poissons migrateurs 2018–2023. available at http://www.bretagne.developpement-durable.gouv.fr/IMG/pdf/plagepomi_2018.pdf
Glémin S (2003) How are deleterious mutations purged? Drift versus nonrandom mating. Evolution 57:2678–2687
pubmed: 14761049
Goudet J (1995) FSTAT (version 1.2): a computer program to calculate F-statistics. J Hered 86:485–486
Gouskov A, Reyes M, Wirthner‐Bitterlin L, Vorburger C (2015) Fish population genetic structure shaped by hydroelectric power plants in the upper Rhine catchment. Evol Appl 9:394–408
Guirec A Guillerme N, Sauvader C, Diouach O, Chapon PM, Beaulaton L (2018) Synthèse sur la répartition des lamproies et des aloses amphihalines enFrance. Rapport final. 2018.032 available at https://www.documentation.eauetbiodiversite.fr/notice/000000000168991aeaf427a64ba5487a
Hänfling B, Weetman D (2006) Concordant genetic estimators of migration reveal anthropogenically enhanced source–sink population structure in the River Sculpin, Cottus gobio. Genetics 173:1487–1501
pubmed: 16624916 pmcid: 1526653
Hardisty MW, Potter IC (1971) The biology of lampreys. Academic Press, London‐New York
Hedrick PW (2005) A standardized genetic differentiation measure. Evolution 59:1633–1638
pubmed: 16329237
Hess JE, Campbell NR, Close DA, Docker MF, Narum SR (2013) Population genomics of Pacific lamprey: adaptive variation in a highly dispersive species. Mol Ecol 22:2898–2916
pubmed: 23205767
Hewitt GM (1996) Some genetic consequences of ice ages, and their role in divergence and speciation. Biol J Linn Soc 58:247–276
Higgins K, Lynch M (2001) Metapopulation extinction caused by mutation accumulation. Proc Natl Acad Sci USA 98:2928–2933
pubmed: 11226343
Hohenlohe PA, Bassham S, Etter PD, Stiffler N, Johnson EA, Cresko WA (2010) Population genomics of parallel adaptation in threespine stickleback using sequenced RAD Tags. PLoS Genet 6:e1000862
pubmed: 20195501 pmcid: 2829049
Hohenlohe PA, Catchen J, Cresko WA (2012) Population genomic analysis of model and nonmodel organisms using sequenced RAD tags. Methods Mol Biol 888:235–260
pubmed: 22665285
Jonsson B, Jonsson N (1993) Partial migration: niche shift versus sexual maturation in fishes. Rev Fish Biol Fish 3:348–365
Jost L (2008) GST and its relatives do not measure differentiation. Mol Ecol 17:4015–4026
pubmed: 19238703
Kawecki TJ, Holt RD (2002) Evolutionary consequences of asymmetric dispersal rates. Am Nat 160:333–347
pubmed: 18707443
Keith P, Persat H, Feuteun É. AllardiI J (2011) Les Poissons d’eau douce de France. Muséum national d’Histoire naturelle, Paris; Biotope, Mèze, 552 p. (Inventaires & biodiversité)
Kelly K, Lai K (2012) Package ‘MBESS.’ R Package version 3.3.3. http://www3.nd.edu/~kkelley/site/MBESS.html
Kemp PS, Russon IJ, Vowles AS, Lucas MC (2011) The influence of discharge and temperature on the ability of upstream migrant adult river lamprey (Lampetra fluviatilis) to pass experimental overshot and undershot weirs. River Res Appl 27:488–498
Landguth EL, Cushman SA, Schwarte MK, McKelvey KS, Murphy M, Luikart G (2010) Quantifying the lag time to detect barriers in landscape genetics. Mol Ecol 19:4179–4191
pubmed: 20819159
Leclerc E, Mailhot Y, Mingelbier M, Bernatchez L (2008) The landscape genetics of yellow perch (Perca flavescens) in a large fluvial ecosystem. Mol Ecol 17:1702–1717
pubmed: 18331242
Lenormand T (2002) Gene flow and the limits to natural selection. Trends Ecol Evol 17:183–189
Loiselle BA, Sork VL, Nason J, Graham C (1995) Spatial genetic structure of a tropical understory shrub, Psychotria officinalis (Rubiaceae). Am J Bot 82:1420–1425
Lucas MC, Bubb DH, Jang MH, Ha K, Masters JEG (2009) Availability of and access to critical habitats in regulated rivers: effects of low-head barriers on threatened lampreys. Freshw Biol 54:621–634
Lynch M (1991) The genetic interpretation of inbreeding depression and outbreeding depression. Evolution 45:622–629
pubmed: 28568822
Lynch M, Conery J, Burger R (1995) Mutation accumulation and the extinction of small populations. Am Nat 146:489–518
Maitland P, Renaud C, Quintella BA, Close D, Docker M (2015) Conservation of native lampreys. In: Docker M (ed.) Lampreys: Biology, Conservation and Control. Fish & Fisheries Series, vol 37. Springer, Dordrecht. https://doi.org/10.1007/978-94-017-9306-3_8
Malmqvist B (1980) The spawning migration of the brook lamprey, Lampetra planeri Bloch, in a South Swedish stream. J Fish Biol 16:105–114
Mateus CS, Almeida PR, Quintella BR, Alves MJ (2011) MtDNA markers reveal the existence of allopatric evolutionary lineages in the threatened lampreys Lampetra fluviatilis (L.) and Lampetra planeri (Bloch) in the Iberian glacial refugium. Conserv Genet 12:1061–1074
Mateus CS, Almeida PR, Mesquita N, Quintella BR, Alves MJ (2016) European Lampreys: New Insights on Postglacial Colonization, Gene Flow and Speciation. PLoS ONE 11:e0148107
pubmed: 26871930 pmcid: 4752455
McPhee MV, Whited DC, Kuzishchin KV, Stanford JA (2014) The effects of riverine physical complexity on anadromy and genetic diversity in steelheador rainbow trout Oncorhynchus mykiss around the Pacific Rim. J Fish Biol 85:132–150
pubmed: 24766581
Meirmans PG (2012) The trouble with isolation by distance. Mol Ecol 21:2839–2846
pubmed: 22574758
Morita K, Yamamoto S (2002) Effects of habitat fragmentation by damming on the persistence of stream‐dwelling charr populations. Conserv Biol 16:1318–1323
Morrissey MB, de Kerckhove DT (2009) The maintenance of genetic variation due to asymmetric gene flow in dendritic metapopulations. Am Nat. 174:875–889
pubmed: 19860541
Moser ML, Almeida PR, Kemp PS, Sorensen PW (2015) Lamprey spawning migration. In: Docker MF (ed) Lampreys: biology, conservation and control. Springer, Netherlands, pp. 215–252
Mulligan M, van Soesbergen A, Sáenz L (2020) GOODD, a global dataset of more than 38,000 georeferenced dams. Sci Data 7:31
pubmed: 31964896 pmcid: 6972789
Nilsson C, Reidy CA, Dynesius M, Revenga C (2005) Fragmentation and flow regulation of the world’s large river systems. Science (New York, NY) 308:405–408
Nimon K, Lewis M, Kane R, Haynes RM (2008) An R package to compute commonality coefficients in the multiple regression case: an introduction to the package and a practical example. Behav Res Methods 40:457–466
pubmed: 18522056
Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D et al. (2019) vegan: community ecology package. R package version 2.5-6
Palumbi SR (2001) Humans as the world’s greatest evolutionary force. Science 293:1786–1790
pubmed: 11546863
Pavlova A, Beheregaray LB, Coleman R, Gilligan D, Harrisson KA, Ingram BA et al. (2017) Severe consequences of habitat fragmentation on genetic diversity of an endangered Australian freshwater fish: a call for assisted gene flow. Evol Appl 10:531–550
pubmed: 5469170 pmcid: 5469170
Paz-Vinas I, Loot G, Stevens VM, Blanchet S (2015) Evolutionary processes driving spatial patterns of intraspecific genetic diversity in river ecosystems. Mol Ecol 24:4586–4604
pubmed: 26284462
Paz-Vinas I, Quéméré E, Chikhi L, Loot G, Blanchet S (2013) The demographic history of populations experiencing asymmetric gene flow: combining simulated and empirical data. Mol Ecol 22:3279–3291
pubmed: 23718226
Pereira AM, Robalo JI, Freyhof J, Maia C, Fonseca JP, Valente A et al. (2010) Phylogeographical analysis reveals multiple conservation units in brook lampreys Lampetra planeri of Portuguese streams. J Fish Biol 77:361–371
pubmed: 20646161
Perrier C, Bourret V, Kent MP, Bernatchez L (2013) Parallel and nonparallel genome-wide divergence among replicate population pairs of freshwater and anadromous Atlantic salmon. Mol Ecol 22:5577–5593
pubmed: 24730037
Pollux BJA, Luteijn A, Van Groenendael JM, Ouborg NJ (2008) Gene flow and genetic structure of the aquatic macrophyte Sparganium emersum in a linear unidirectional river. Freshw Biol 54:64–76
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
pubmed: 10835412 pmcid: 10835412
Prunier JG, Colyn M, Legendre X, Nimon KF, Flamand MC (2015) Multicollinearity in spatial genetics: separating the wheat from the chaff using commonality analyses. Mol Ecol 24:263–283
pubmed: 25495950
Quéméré E, Baglinière JL, Roussel JM, Evanno G, McGinnity P, Launey S (2016) Seascape and its effect on migratory life‐history strategy influences gene flow among coastal brown trout (Salmo trutta) populations in the English Channel. J Biogeogr 43:498–509
R Development Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria
Raeymaekers JAM, Maes GE, Geldof S, Hontis I, Nackaerts K, Volckaert FAM (2008) Modeling genetic connectivity in sticklebacks as a guideline for river restoration. Evol Appl 1:475–488
pubmed: 25567729 pmcid: 3352376
Ralls K, Ballou JD, Dudash MR, Eldridge MDB, Fenster CB, Lacy RC et al. (2018) Call for a paradigm shift in the genetic management of fragmented populations. Conserv Lett 11:e12412
Renaud CB (1997) Conservation status of Northern Hemisphere lampreys (Petromyzontidae). J Appl Ichthyol 13:143–148
Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223
pubmed: 28568501 pmcid: 28568501
Rosenberg NA (2003) DISTRUCT: a program for the graphical display of population structure. Molecular Ecology Notes
Rougemont Q, Gagnaire PA, Perrier C, Genthon C, Besnard AL, Launey S, Evanno G (2017) Inferring the demographic history underlying parallel genomic divergence among pairs of parasitic and nonparasitic lamprey ecotypes. Mol Ecol 26:142–162
pubmed: 27105132
Rougemont Q, Gaigher A, Lasne E, Côte J, Coke M, Besnard AL et al. (2015) Low reproductive isolation and highly variable levels of gene flow reveal limited progress towards speciation between European river and brook lampreys. J Evol Biol 28:2248–2263
pubmed: 26348652
Rougemont Q, Roux C, Neuenschwander S, Goudet J, Launey S, Evanno G (2016) Reconstructing the demographic history of divergence between European river and brook lampreys using approximate Bayesian computations. PeerJ 4e1910
Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145:1219–1228
pubmed: 9093870 pmcid: 1207888
Rousset F (2008) genepop’007: a complete re-implementation of the genepop software for Windows and Linux. Mol Ecol Resour 8:103–106
pubmed: 21585727 pmcid: 21585727
Russon IJ, Kemp PS, Lucas MC (2011) Gauging weirs impede the upstream migration of adult river lamprey Lampetra fluviatilis: lamprey ability to pass gauging weirs. Fish Manag Ecol 18:201–210
Saccheri I, Kuussaari M, Kankare M, Vikman P, Fortelius W, Hanski I (1998) Inbreeding and extinction in a butterfly metapopulation. Nature 392:491–494
Smith TB, Kinnison MT, Strauss SY, Fuller TL, Carroll SP (2014) Prescriptive evolution to conserve and manage biodiversity. Ann Rev Ecol Evol Syst 45:1–22
Spice EK, Goodman DH, Reid SB, Docker MF (2012) Neither philopatric nor panmictic: microsatellite and mtDNA evidence suggests lack of natal homing but limits to dispersal in Pacific lamprey. Mol Ecol 21:2916–2930
pubmed: 22564149
Spice EK, Whitesel TA, Silver GS, Docker MF (2019) Contemporary and historical river connectivity influence population structure in western brooklamprey in the Columbia River Basin. Conserv Genet
Spielman D, Brook BW, Frankham R (2004) Most species are not driven to extinction before genetic factors impact them. Proc Natl Acad Sci USA 101:15261–15264
pubmed: 15477597
Taberlet P, Fumagalli L, Wust-Saucy AG, Cosson JF (1998) Comparative phylogeography and postglacial colonization routes in Europe. Mol Ecol 7:453–464
Taverny C, Elie P (2010) Les lamproies en Europe de l‟Ouest – Ecophases, espèces et habitats. Quae, Versailles, France
Tonteri A, Veselov AJ, Titov S, Lumme J, Primmer CR (2007) The effect of migratory behaviour on genetic diversity and population divergence: a comparison of anadromous and freshwater Atlantic salmon Salmo salar. J Fish Biol 70:381–398
Torterotot JB, Perrier C, Bergeron NE, Bernatchez L (2014) Influence of forest road culverts and waterfalls on the fine‐scale distribution of brook trout genetic diversity in a boreal watershed. Trans Am Fish Soc 143:1577–1591
Tummers JS, Kerr JR, O’Brien P, Kemp P, Lucas MC (2018) Enhancing the upstream passage of river lamprey at a microhydropower installation using horizontally-mounted studded tiles. Ecol Eng 125:87–97
UICN Comité français MNHN SFI & AFB (2019) La Liste rouge des espèces menacées en France—Chapitre Poissons d’eau douce de France métropolitaine. Paris, France
Vitousek PM, Mooney HA, Lubchenco J, Melillo JM (1997) Human domination of earth’s ecosystems. Science 277:494–499
Wang J, Hill WG, Charlesworth D, Charlesworth B (1999) Dynamics of inbreeding depression due to deleterious mutations in small populations: Mutation parameters and inbreeding rate. Genet Res 74(2):165–178. https://doi.org/10.1017/S0016672399003900
doi: 10.1017/S0016672399003900 pubmed: 10584559
Warnes GR, Bolker B, Bonebakker L, Gentleman R, Huber W, Liaw A, Lumley T, Maechler M, Magnusson A, Moeller S, Schwartz M, Venables B (2015) gplots: Various R Programming Tools for Plotting Data. R package version 3.0.4. https://CRAN.R-project.org/package=gplots
Weir B, Cockerham C (1984) Estimating F-statistics for the analysis of population-structure. Evolution 38:1358–1370
Whiteley AR, Coombs JA, Hudy M, Robinson Z, Colton AR, Nislow KH, Letcher BH (2013) Fragmentation and patch size shape genetic structure of brook trout populations. Can J Fish Aquat Sci 70:678–688
Wilson GA, Rannala B (2003) Bayesian inference of recent migration rates using multilocus genotypes. Genetics 163:1177–1191
pubmed: 12663554 pmcid: 1462502
Yamamoto S, Morita K, Koizumi I, Maekawa K (2004) Genetic differentiation of white-spotted charr (Salvelinus leucomaenis) populations after habitat fragmentation: spatial–temporal changes in gene frequencies. Conserv Genet 5:529–538
Yamazaki Y, Yamano A, Oura K (2011) Recent microscale disturbance of gene flow in threatened fluvial lamprey, Lethenteron sp. N, living in a paddywater system. Conserv Genet 12:1373
Young A, Boyle T, Brown T (1996) The population genetic consequences of habitat fragmentation for plants. Trends Ecol Evol 11:413–418
pubmed: 21237900

Auteurs

Quentin Rougemont (Q)

ESE, Ecology and Ecosystem Health, INRAE, Agrocampus Ouest, 35042, Rennes, France. quentinrougemont@orange.fr.
Département de biologie, Institut de Biologie Intégrative etsu des Systèmes (IBIS), Université Laval, Québec, G1V 0A6, Canada. quentinrougemont@orange.fr.

Victoria Dolo (V)

ESE, Ecology and Ecosystem Health, INRAE, Agrocampus Ouest, 35042, Rennes, France.

Adrien Oger (A)

ESE, Ecology and Ecosystem Health, INRAE, Agrocampus Ouest, 35042, Rennes, France.

Anne-Laure Besnard (AL)

ESE, Ecology and Ecosystem Health, INRAE, Agrocampus Ouest, 35042, Rennes, France.

Dominique Huteau (D)

ESE, Ecology and Ecosystem Health, INRAE, Agrocampus Ouest, 35042, Rennes, France.

Marie-Agnès Coutellec (MA)

ESE, Ecology and Ecosystem Health, INRAE, Agrocampus Ouest, 35042, Rennes, France.

Charles Perrier (C)

Centre de Biologie pour la Gestion des Populations UMR CBGP, INRA, CIRAD, IRD, Montpellier SupAgro, Univ Montpellier, Montpellier, France.

Sophie Launey (S)

ESE, Ecology and Ecosystem Health, INRAE, Agrocampus Ouest, 35042, Rennes, France.

Guillaume Evanno (G)

ESE, Ecology and Ecosystem Health, INRAE, Agrocampus Ouest, 35042, Rennes, France.
OFB, INRAE, Agrocampus Ouest, University Pau Pays Adour, Management of Diadromous Fish in their Environment, Rennes, France.

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