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Genetic admixture between captive-bred and wild individuals affects patterns of dispersal in a brown trout (Salmo trutta) population

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Abstract

Genetic admixture between captive-bred and wild individuals has been demonstrated to affect many individual traits, although little is known about its potential influence on dispersal, an important trait governing the eco-evolutionary dynamics of populations. Here, we quantified and described the spatial distribution of genetic admixture in a brown trout (Salmo trutta) population from a small watershed that was stocked until 1999, and then tested whether or not individual dispersal parameters were related to admixture between wild and captive-bred fish. We genotyped 715 fish at 17 microsatellite loci sampled from both the mainstream and all populated tributaries, as well as 48 fish from the hatchery used to stock the study area. First, we used Bayesian clustering to infer local genetic structure and to quantify genetic admixture. We inferred first generation migrants to identify dispersal events and test which features (genetic admixture, sex and body length) affected dispersal parameters (i.e. probability to disperse, distance of dispersal and direction of the dispersal event). We identified two genetic clusters in the river basin, corresponding to wild fish on the one hand and to fish derived from the captive strain on the other hand, allowing us to define an individual gradient of admixture. Individuals with a strong assignment to the captive strain occurred almost exclusively in some tributaries, and were more likely to disperse towards a tributary than towards a site of the mainstream. Furthermore, dispersal probability increased as the probability of assignment to the captive strain increased, and individuals with an intermediate level of admixture exhibited the lowest dispersal distances. These findings show that various dispersal parameters may be biased by admixture with captive-bred genotypes, and that management policies should take into account the differential spread of captive-bred individuals in wild populations.

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References

  • Aljanabi S (1997) Universal and rapid salt-extraction of high quality genomic DNA for PCR- based techniques. Nucleic Acids Res 25:4692–4693

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Amar A, Arroyo BE, Bretagnolle V (2008) Post-fledging dependence and dispersal in hacked and wild Montagu’s Harriers Circus pygargus. Ibis 142:21–28

    Article  Google Scholar 

  • Andreu J, Barba E (2006) Breeding dispersal of Great Tits Parus major in a homogeneous habitat: effects of sex, age, and mating status. Ardea-Wageningen 94:1–45

    Google Scholar 

  • Antao T, Lopes A, Lopes RJ et al (2008) LOSITAN: a workbench to detect molecular adaptation based on a Fst-outlier method. BMC Bioinform 9:323

    Article  CAS  Google Scholar 

  • Araki H, Schmid C (2010) Is hatchery stocking a help or harm? Aquaculture 308:S2–S11

    Article  Google Scholar 

  • Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F (2004) GENETIX 4.05, logiciel sous Windows TM pour la génétique des populations. Laboratoire Génome, Populations, Interactions, CNRS UMR 5000, Université de Montpellier II, Montpellier (France)

  • Bettinger JM, Bettoli PW (2002) Fate, dispersal, and persistence of recently stocked and resident rainbow trout in a Tennessee tailwater. North Am J Fish Manag 22:425–432

    Article  Google Scholar 

  • Blanchet S, Páez DJ, Bernatchez L, Dodson JJ (2008) An integrated comparison of captive-bred and wild Atlantic salmon (Salmo salar): implications for supportive breeding programs. Biol Conserv 141:1989–1999

    Article  Google Scholar 

  • Blanchet S, Bernatchez L, Dodson JJ (2009) Does interspecific competition influence relationships between heterozygosity and fitness-related behaviors in juvenile Atlantic salmon (Salmo salar)? Behav Ecol Sociobiol 63(4):605–615

    Google Scholar 

  • Bolnick DI, Nosil P (2007) Natural selection in populations subject to a migration load. Evolution 61:2229–2243

    Article  PubMed  Google Scholar 

  • Burnside RJ, Collar NJ, Scotland KM, Dolman PM (2016) Survival rates of captive-bred Asian Houbara Chlamydotis macqueenii in a hunted migratory population. Ibis 158:353–361

    Article  Google Scholar 

  • Cagigas ME, Vazquez E, Blanco G, Sanchez JA (1999) Genetic effects of introduced hatchery stocks on indigenous brown trout (Salmo trutta L.) populations in Spain. Ecol Freshw Fish 8:141–150

    Article  Google Scholar 

  • Campbell Grant EH, Nichols JD, Lowe WH, Fagan WF (2010) Use of multiple dispersal pathways facilitates amphibian persistence in stream networks. Proc Natl Acad Sci 107:6936–6940

    Article  PubMed  PubMed Central  Google Scholar 

  • Christie MR, Marine ML, Fox SE et al (2016) A single generation of domestication heritably alters the expression of hundreds of genes. Nat Commun 7:10676

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clobert J (ed) (2012) Dispersal ecology and evolution, 1st edn. Oxford University Press, Oxford

    Google Scholar 

  • Conti L, Comte L, Hugueny B, Grenouillet G (2015) Drivers of freshwater fish colonisations and extirpations under climate change. Ecography 38:510–519

    Article  Google Scholar 

  • Cornuet JM, Piry S, Luikart G et al (1999) New methods employing multilocus genotypes to select or exclude populations as origins of individuals. Genetics 153:1989–2000

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cote J, Clobert J, Brodin T et al (2010) Personality-dependent dispersal: characterization, ontogeny and consequences for spatially structured populations. Philos Trans R Soc B 365:4065–4076

    Article  CAS  Google Scholar 

  • Cressman R, Křivan V (2006) Migration dynamics for the ideal free distribution. Am Nat 168:384–397

    Article  PubMed  Google Scholar 

  • Cucherousset J, Ombredane D, Charles K et al (2005) A continuum of life history tactics in a brown trout (Salmo trutta) population. Can J Fish Aquat Sci 62:1600–1610

    Article  Google Scholar 

  • Cyr F, Angers B (2011) Historical process lead to false genetic signal of current connectivity among populations. Genetica 139:1417–1428

    Article  PubMed  Google Scholar 

  • Dahirel M, Olivier E, Guiller A et al (2015) Movement propensity and ability correlate with ecological specialization in European land snails: comparative analysis of a dispersal syndrome. J Anim Ecol 84:228–238

    Article  PubMed  Google Scholar 

  • Debeffe L, Morellet N, Bonnot N et al (2014) The link between behavioural type and natal dispersal propensity reveals a dispersal syndrome in a large herbivore. Proc R Soc B 281:20140873

    Article  PubMed  PubMed Central  Google Scholar 

  • Dingemanse NJ, Both C, van Noordwijk AJ et al (2003) Natal dispersal and personalities in great tits (Parus major). Proc R Soc B 270:741–747

    Article  PubMed  PubMed Central  Google Scholar 

  • Drake JM (2006) Heterosis, the catapult effect and establishment success of a colonizing bird. Biol Lett 2:304–307

    Article  PubMed  PubMed Central  Google Scholar 

  • Earl DA, vonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361

    Article  Google Scholar 

  • Ebner BC, Thiem JD (2009) Monitoring by telemetry reveals differences in movement and survival following hatchery or wild rearing of an endangered fish. Mar Freshw Res 60:45

    Article  Google Scholar 

  • Edelaar P, Bolnick DI (2012) Non-random gene flow: an underappreciated force in evolution and ecology. Trends Ecol Evol 27:659–665

    Article  PubMed  Google Scholar 

  • Edelaar P, Siepielski AM, Clobert J (2008) Matching habitat choice causes directed gene flow: a neglected dimension in evolution and ecology. Evolution 62:2462–2472

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Facon B, Jarne P, Pointier JP, David P (2005) Hybridization and invasiveness in the freshwater snail Melanoides tuberculata: hybrid vigour is more important than increase in genetic variance: hybrid vigour in an invasive snail. J Evol Biol 18:524–535

    Article  CAS  PubMed  Google Scholar 

  • Frankham R (2008) Genetic adaptation to captivity in species conservation programs. Mol Ecol 17:325–333

    Article  PubMed  Google Scholar 

  • Frankham R, Hemmer H, Ryder OA et al (1986) Selection in captive populations. Zoo Biol 5:127–138

    Article  Google Scholar 

  • Frumkin NB, Wey TW, Exnicios M et al (2016) Inter-annual patterns of aggression and pair bonding in captive American flamingos (Phoenicopterus ruber): flamingo behavior. Zoo Biol 35:111–119

    Article  PubMed  Google Scholar 

  • Gachot-Neveu H, Lefevre P, Roeder J-J et al (2009) Genetic detection of sex-biased and age-biased dispersal in a population of wild carnivore, the red fox, Vulpes vulpes. Zoolog Sci 26:145–152

    Article  CAS  PubMed  Google Scholar 

  • Geiser F, Ferguson C (2001) Intraspecific differences in behaviour and physiology: effects of captive breeding on patterns of torpor in feathertail gliders. J Comp Physiol B 171:569–576

    Article  CAS  PubMed  Google Scholar 

  • Goudet J (1995) FSTAT (Version 1.2): a computer program to calculate F-statistics. J Hered 86:485–486

    Article  Google Scholar 

  • Gutiérrez D, Menéndez R (2003) Patterns in the distribution, abundance and body size of carabid beetles (Coleoptera: Caraboidea) in relation to dispersal ability. J Biogeogr 24:903–914

    Article  Google Scholar 

  • Hansen MM, Nielsen EE, Bekkevold D, Mensberg K-LD (2001) Admixture analysis and stocking impact assessment in brown trout (Salmo trutta), estimated with incomplete baseline data. Can J Fish Aquat Sci 58:1853–1860

    Article  Google Scholar 

  • Hansen MM, Fraser DJ, Meier K, Mensberg K-LD (2009) Sixty years of anthropogenic pressure: a spatio-temporal genetic analysis of brown trout populations subject to stocking and population declines. Mol Ecol 18:2549–2562

    Article  CAS  PubMed  Google Scholar 

  • Hanski I (1998) Metapopulation dynamics. Nature 396:41–49

    Article  CAS  Google Scholar 

  • Harrison JF, Taylor OR Jr, Hall HG (2005) The flight physiology of reproductives of Africanized, European, and hybrid Honeybees (Apis mellifera). Physiol Biochem Zool 78:153–162

    Article  PubMed  Google Scholar 

  • Hudina S, Žganec K, Hock K (2015) Differences in aggressive behaviour along the expanding range of an invasive crayfish: an important component of invasion dynamics. Biol Invasions 17:3101–3112

    Article  Google Scholar 

  • Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801–1806

    Article  CAS  PubMed  Google Scholar 

  • Johnson JR, Fitzpatrick BM, Shaffer HB (2010) Retention of low-fitness genotypes over six decades of admixture between native and introduced tiger salamanders. BMC Evol Biol 10:147

    Article  PubMed  PubMed Central  Google Scholar 

  • Johnsson JI, Abrahams MV (1991) Interbreeding with domestic strain increases foraging under threat of predation in juvenile steelhead trout (Oncorhynchus mykiss): an experimental study. Can J Fish Aquat Sci 48:243–247

    Article  Google Scholar 

  • Johnsson JI, Nobbelin F, Bohlin T (1999) Territorial competition among wild brown trout fry: effects of ownership and body size. J Fish Biol 54:469–472

    Article  Google Scholar 

  • Jombart T (2008) adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405

    Article  CAS  PubMed  Google Scholar 

  • Jorgensen J, Berg S (1991) Stocking experiments with 0 + and 1 + trout parr, Salmo trutta L., of wild and hatchery origin: 2. Post-stocking movements. J Fish Biol 39:171–180

    Article  Google Scholar 

  • Keller SR, Taylor DR (2010) Genomic admixture increases fitness during a biological invasion: admixture increases fitness during invasion. J Evol Biol 23:1720–1731

    Article  CAS  PubMed  Google Scholar 

  • Keller I, Taverna A, Seehausen O (2011) Evidence of neutral and adaptive genetic divergence between European trout populations sampled along altitudinal gradients. Mol Ecol 20(9):1888–1904

    Article  CAS  PubMed  Google Scholar 

  • Kelley JL, Magurran AE, Macías García C (2006) Captive breeding promotes aggression in an endangered Mexican fish. Biol Conserv 133:169–177

    Article  Google Scholar 

  • Lowe WH, McPeek MA (2014) Is dispersal neutral? Trends Ecol Evol 29:444–450

    Article  PubMed  Google Scholar 

  • Marie AD, Bernatchez L, Garant D (2010) Loss of genetic integrity correlates with stocking intensity in brook charr (Salvelinus fontinalis): Impacts of stocking on Salvelinus fontinalis. Mol Ecol 19:2025–2037

    Article  CAS  PubMed  Google Scholar 

  • McClelland EK, Naish KA (2007) What is the fitness outcome of crossing unrelated fish populations? A meta-analysis and an evaluation of future research directions. Conserv Genet 8:397–416

    Article  Google Scholar 

  • McGinnity P, Prodohl P, Ferguson A et al (2003) Fitness reduction and potential extinction of wild populations of Atlantic salmon, Salmo salar, as a result of interactions with escaped farm salmon. Proc R Soc B 270:2443–2450

    Article  PubMed  PubMed Central  Google Scholar 

  • Miller RJ, Frey DF (1972) The establishment of dominance relationships in the blue gourami, Trichogaster trichopterus (Pallas). Behaviour 42:8–60

    Article  Google Scholar 

  • Morrissey MB, de Kerckhove DT (2009) The maintenance of genetic variation due to asymmetric gene flow in dendritic metapopulations. Am Nat 174:875–889

    Article  PubMed  Google Scholar 

  • Olsson IC, Greenberg LA, Bergman E, Wysujack K (2006) Environmentally induced migration: the importance of food. Ecol Lett 9:645–651

    Article  PubMed  Google Scholar 

  • Ovidio M, Larinier M, Burgun V, Chanseau M, Sremski W, Steinbach P, Voegtle B, Baudoin P (2015) The ICE protocol for ecological continuity: a new tool to evaluate the upstream fish passage success at physical barriers. Fish Passage 2015. International conference on river connectivity best practices and innovations. http://hdl.handle.net/2268/183243

  • Paetkau D, Calvert W, Stirling I, Strobeck C (1995) Microsatellite analysis of population structure in Canadian polar bears. Mol Ecol 4:347–354

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Perrier C, Guyomard R, Bagliniere J-L et al (2013) Changes in the genetic structure of Atlantic salmon populations over four decades reveal substantial impacts of stocking and potential resiliency. Ecol Evol 3:2334–2349

    Article  PubMed  PubMed Central  Google Scholar 

  • Piry S, Alapetite A, Cornuet J-M et al (2004) GENECLASS2: a software for genetic assignment and first-generation migrant detection. J Heredity 95:536–539

    Article  CAS  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    CAS  PubMed  PubMed Central  Google Scholar 

  • Prunier JG, Colyn M, Legendre X et al (2015) Multicollinearity in spatial genetics: separating the wheat from the chaff using commonality analyses. Mol Ecol 24:263–283

    Article  CAS  PubMed  Google Scholar 

  • Prunier JG, Dubut V, Loot G et al (2018) The relative contribution of river network structure and anthropogenic stressors to spatial patterns of genetic diversity in two freshwater fishes: a multiple-stressors approach. Freshw Biol 63:6–21

    Article  Google Scholar 

  • Pusey AE (1987) Sex-biased dispersal and inbreeding avoidance in birds and mammals. Trends Ecol Evol 2:295–299

    Article  CAS  PubMed  Google Scholar 

  • Quéméré E, Perrier C, Besnard A-L et al (2014) An improved PCR-based method for faster sex determination in brown trout (Salmo trutta) and Atlantic salmon (Salmo salar). Conserv Genet Resour 6:825–827

    Article  Google Scholar 

  • Radinger J, Wolter C (2014) Patterns and predictors of fish dispersal in rivers. Fish Fish 15:456–473

    Article  Google Scholar 

  • Randi E (2008) Detecting hybridization between wild species and their domesticated relatives. Mol Ecol 17:285–293

    Article  PubMed  Google Scholar 

  • Rannala B, Mountain JL (1997) Detecting immigration by using multilocus genotypes. Proc Natl Acad Sci 94:9197–9201

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rasmussen JB, Robinson MD, Hontela A, Heath DD (2012) Metabolic traits of westslope cutthroat trout, introduced rainbow trout and their hybrids in an ecotonal hybrid zone along an elevation gradient: metabolic traits of trout hybrids. Biol J Linn Soc 105:56–72

    Article  Google Scholar 

  • Robert S, Dancosse J, Dallaire A (1987) Some observations on the role of environment and genetics in behaviour of wild and domestic forms of Sus scrofa (European wild boars and domestic pigs). Appl Anim Behav Sci 17:253–262

    Article  Google Scholar 

  • Ronce O (2007) How does it feel to be like a rolling stone? Ten questions about dispersal evolution. Annu Rev Ecol Evol Syst 38:231–253

    Article  Google Scholar 

  • Rosenberg NA (2003) DISTRUCT: a program for the graphical display of population structure: program note. Mol Ecol Notes 4:137–138

    Article  Google Scholar 

  • Rousset F (2008) genepop’007: a complete re-implementation of the genepop software for Windows and Linux. Mol Ecol Resour 8:103–106

    Article  PubMed  Google Scholar 

  • Rustadbakken A, L’Abee-Lund JH, Arnekleiv JV, Kraabol M (2004) Reproductive migration of brown trout in a small Norwegian river studied by telemetry. J Fish Biol 64:2–15

    Article  Google Scholar 

  • Seddon PJ, Armstrong DP, Maloney RF (2007) Developing the science of reintroduction biology. Conserv Biol 21:303–312

    Article  PubMed  Google Scholar 

  • Skalski GT, Gilliam JF (2000) Modeling diffusive spread in a heterogeneous population: a movement study with stream fish. Ecology 81:1685–1700

    Article  Google Scholar 

  • Smouse PE, Long JC, Sokal RR (1986) Multiple regression and correlation extensions of the mantel test of matrix correspondence. Syst Zool 35:627

    Article  Google Scholar 

  • Söderquist P, Gunnarsson G, Elmberg J (2013) Longevity and migration distance differ between wild and hand-reared mallards Anas platyrhynchos in Northern Europe. Eur J Wildl Res 59:159–166

    Article  Google Scholar 

  • Stoinski TS, Maple TL, Beck BB, Bloomsmith MA (2003) A behavioral comparison of captive-born, reintroduced golden lion tamarins and their wild-born offspring. Behaviour 140:137–160

    Article  Google Scholar 

  • Symons PEK (1969) Greater dispersal of wild compared with hatchery-reared juvenile atlantic salmon released in streams. J Fish Res Board Can 26:1867–1876

    Article  Google Scholar 

  • Tymchuk WE, Devlin RH (2005) Growth differences among first and second generation hybrids of domesticated and wild rainbow trout (I). Aquaculture 245:295–300

    Article  Google Scholar 

  • Vähä J-P, Primmer CR (2005) Efficiency of model-based Bayesian methods for detecting hybrid individuals under different hybridization scenarios and with different numbers of loci: genetic detection of hybrids. Mol Ecol 15:63–72

    Article  CAS  Google Scholar 

  • Valiquette E, Perrier C, Thibault I, Bernatchez L (2014) Loss of genetic integrity in wild lake trout populations following stocking: insights from an exhaustive study of 72 lakes from Québec, Canada. Evol Appl 7:625–644

    Article  PubMed  PubMed Central  Google Scholar 

  • Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538

    Article  CAS  Google Scholar 

  • Vøllestad LA, Serbezov D, Bass A et al (2012) Small-scale dispersal and population structure in stream-living brown trout (Salmo trutta) inferred by mark–recapture, pedigree reconstruction, and population genetics. Can J Fish Aquat Sci 69:1513–1524

    Article  Google Scholar 

  • Wollebæk J, Røed KH, Brabrand Å, Heggenes J (2012) Interbreeding of genetically distinct native brown trout (Salmo trutta) populations designates offspring fitness. Aquaculture 356–357:158–168

    Article  Google Scholar 

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Acknowledgements

We warmly thank the AAPPMA of Luchon (Jean Lérimé, Daniel Estrade and colleagues) and ECOGEA (Jean-Marc Lascaux, Philippe Baran and colleagues) for field sampling support. The genetic data were generated at the molecular genetics technical facilities of the Genopole Midi-Pyrénées (Toulouse, France). This work was undertaken at SETE, which forms part of the “Laboratoire d’Excellence” (LABEX) entitled TULIP (ANR-10-LABX-41).

Funding

This work was funded by the French Agency for Biodiversity (No. 136406) and Electricité De France (No. 8619-5920011137).

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SB, NP and LT designed the experiment and coordinated the study; KSP, SB, NP, LT, OP, GL and CV conducted sampling; KSP, GL and CV carried out the experimental lab work; KSP and JGP ran the statistical analyses; KSP, JGP, SB, NP, LT, OP, GL and CV interpreted the data. KSP, SB, and JGP wrote the first draft of the manuscript. NP, LT, OP, GL and CV read, commented and corrected the initial draft, and all authors gave final approval for publication.

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Correspondence to Keoni Saint-Pé or Simon Blanchet.

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Saint-Pé, K., Blanchet, S., Tissot, L. et al. Genetic admixture between captive-bred and wild individuals affects patterns of dispersal in a brown trout (Salmo trutta) population. Conserv Genet 19, 1269–1279 (2018). https://doi.org/10.1007/s10592-018-1095-2

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