Skip to main content
SpringerLink
Log in

Dispersal in a stream dwelling salmonid: Inferences from tagging and microsatellite studies

  • Published:
Conservation Genetics Aims and scope Submit manuscript

Abstract

We used both direct (mark-recapture) andindirect (microsatellite analysis)methodologies to investigate dispersal betweentwo putative populations of brook charr (Salvelinus fontinalis) in Freshwater River,Cape Race, Newfoundland, Canada. Over a 5-yearstudy period, mark-recapture data revealed somemovement by fish, but the proportion ofrecaptured fish migrating from one populationarea to another was low (0–4.1%).Additionally, during sampling periods in thespawning seasons, no fish was found in thealternate population area to that of its firstcapture. Despite this pattern of limitedmovement, microsatellite analysis based onsixteen polymorphic loci provided no evidenceof genetic differentiation. Indirect estimatesof dispersal parameters varied greatly betweendifferent methods of analysis. While use of acoalescent-based model yielded estimatedmigration rates congruent with the results ofthe mark-recapture study, other methodsresulted in much higher estimates of migrationbetween the populations. In particular, thelack of genetic differentiation coupled withlikely violations of the assumed island modelprevented generation of meaningful estimates ofdispersal using Fst. The disparitiesbetween migration rates estimated from themark-recapture work and from the differentindirect methods highlight the difficulties ofusing indirect methods to estimate dispersal onan ecological timescale. However,mark-recapture methods can fail to detecthistorical or episodic movement that isimportant in an evolutionary context, and wetherefore argue that a combination of directand indirect methods can provide a morecomplete picture of dispersal than eitherapproach alone.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Adams BK, Hutchings JA (2003) Geographic population structure of brook char, Salvelinus fontinalisL., as revealed by microsatellite and tagging data. J. Fish Biol., in press.

  • Anderson EC, Williamson EG, Thompson EA (2000) Monte carlo evaluation of the likelihood for N e from temporally spaced samples. Genetics, 156, 2109–2118.

    Google Scholar 

  • Angers B, Bernatchez L, Angers A, Desgroseillers L (1995) Specific microsatellite loci for brook charr reveal strong population subdivision on a microgeographic scale. J. Fish Biol., 47(Suppl. A), 177–185.

    Google Scholar 

  • Ardren WR, Kapuskinski AR (2003) Demographic and genetic estimates of effective population size (Ne) reveals genetic compensation in steelhead trout. Mol. Ecol., 12, 35–49.

    Google Scholar 

  • Balloux F, Lugon-Moulin N (2002) The estimation of population differentiation with microsatellite markers. Mol. Ecol., 11, 155–165.

    Google Scholar 

  • Bardakci F, Skibinski DOF (1994) Applications of the RAPD technique in tilapia fish; species and subspecies identification. Heredity, 73, 117–123.

    Google Scholar 

  • Barton NH, Slatkin M (1986) A quasi-equilibrium theory of the distribution of rare alleles in a subdivided population. Heredity, 56, 409–415.

    Google Scholar 

  • Beerli P, Felsenstein J (1999) Maximum-likelihood estimation of migration rates and effective population numbers in two populations using a coalescent approach. Genetics, 152, 763–773.

    Google Scholar 

  • Beerli P, Felsenstein J (2001) Maximum likelihood estimation of a migration matrix and effective population sizes in n subpopulations by using a coalescent approach. P.N.A.S., 98, 4563–4568.

    Google Scholar 

  • Bernard DR, Hepler KR, Jones JD, Whalen ME, McBride DN (1995) Some tests of the “migration hypothesis” for anadromous Dolly Varden (southern form). Trans. Am. Fish. Soc., 124, 297–307.

    Google Scholar 

  • Berg LM, Lascoux M, Pamilo P (1998) The infinite island model with sex-differentiated gene flow. Heredity, 81, 63–68.

    Google Scholar 

  • Berthier P, Beaumont MA, Cornuet JM, Luikart G (2002) Likelihood-based estimation of the effective population size using temporal changes in allele frequencies: a genealogical approach. Genetics, 160, 741–751.

    Google Scholar 

  • Bohonak, AJ (1999) Dispersal, gene flow and population structure. Q. Rev. Biol., 74, 21–45.

    Google Scholar 

  • Bunn SE, Hughes JM (1997) Dispersal and recruitment in streams: Evidence from genetic studies. J. N. Am. Benthol. Soc., 16, 338–346.

    Google Scholar 

  • Chapman HF, Hughes JM, Jennings C, Kay BH, Ritchie SA (1999) Population structure and disperasl of the saltmarsh mosquito Aedes vigilaxin Queensland, Australia. Med. Vet. Entomol., 13, 423–430.

    Google Scholar 

  • Chenuil A, Crespin L, Pouyaud L, Patrick B (2000) Movements of adult fish in a hybrid zone revealed by microsatellite genetic analysis and capture-recapture data. Freshwater Biol., 43, 121–131.

    Google Scholar 

  • Cockerham C, Weir BS (1993) Estimation of gene flow from F-statistics. Evolution, 47, 855–863.

    Google Scholar 

  • Danzmann RG, Morgan RP, Jones MW, Bernatchez L and Ihssen PE (1998) A major sextet of mitochondrial DNA phylogenetics assemblages extant in eastern North American brook trout (Salvelinus fontinalis): distribution and postglacial dispersal patterns. Can. J. Zool., 76, 1300–1318.

    Google Scholar 

  • Diana JS, Lane ED (1978) The movement and distribution of Paiute cutthroat trout, Salmo clarki seleneris, in Cottonwood Creek, California. Trans. Am. Fish. Soc., 107, 444–448.

    Google Scholar 

  • DiCiccio TJ, Efron B (1986) Bootstrap confidence intervals. Stat. Sci., 11, 189–228.

    Google Scholar 

  • Ferguson MM, Danzmann RG, Hutchings JA (1991) Incongruent estimates of population differentiation among brook charr, Salvelinus fontinalis, from Cape Race, Newfoundland, Canada, based upon allozyme and mitochondrial DNA variation. J. Fish Biol., 39, 79–85.

    Google Scholar 

  • Forbes SH, Boyd DK (1997) Genetic structure and migration in native and reintroduced Rocky Mountain wolf populations. Conser. Biol., 11, 1226–1234.

    Google Scholar 

  • Frankham R (1995) Effective population size / adult population size ratios in wildlife: a review. Genet. Res. Camb., 66, 95–107.

    Google Scholar 

  • Geenen S, Jordaens K, De Block M, Stoks R, De Bruyn L (2000) Genetic differentiation and dispersal among populations of the damselfly Lestes viridis(Odonata). J. N. Am. Benthol. Soc, 19, 321–328.

    Google Scholar 

  • Gerking SD (1959) The restricted movement of fish populations. Biol. Rev., 34, 221–242.

    Google Scholar 

  • Goudet J (2000) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.1). Available from http://www.unil.ch/izea/softwares/fstat.html. Updated from Goudet (1995).

  • Goudet J, Raymond M, De Meeüs T, Rousset F (1996) Testing differentiation in diploid populations. Genetics, 144, 1933–1940.

    Google Scholar 

  • Gowan C, Fausch KD (1996) Mobile brook trout in two highelevation Colorado streams: Re-evaluating the concept of restricted movement. Can. J. Fish. Aquat. Sci., 53, 1370–1381.

    Google Scholar 

  • Gowan C, Young MK, Fausch KD, Riley SC (1994) Restricted movement in resident stream salmonids: A paradigm lost? Can. J. Fish. Aquat. Sci., 74, 2626–2637.

    Google Scholar 

  • Guo SW, Thompson EA (1992) Performing the exact test of Hardy-Weinberg proportions for multiple alleles. Biometrics, 48, 361–372.

    Google Scholar 

  • Hansen MM, Kenchington E, Nielsen EE (2001) Assigning individual fish to populations using microsatellite DNA markers. Fish Fish., 2, 93–112.

    Google Scholar 

  • Heath DD, Busch C, Kelly J, Atagi DY (2002) Temporal change in genetic structure and effective population size in steelhead trout (Oncorhynchus mykiss). Mol. Ecol., 11, 197–214.

    Google Scholar 

  • Heggenes J, Northcote TG, Peter A (1991) Spatial stability of cutthroat trout (Oncorhynchus clarki) in a small coastal stream. Can. J. Fish. Aquat. Sci., 48, 757–762.

    Google Scholar 

  • Hutchings JA (1990) The evolutionary significance of life history divergence among brook trout, Salvelinus fontinalis, populations. Ph.D. thesis, Memorial University of Newfoundland, St. John's, NF.

    Google Scholar 

  • Hutchings JA (1993) Adaptive life histories affected by age-specific survival and growth rate. Ecology, 74, 673–684.

    Google Scholar 

  • Hutchings JA (1996) Adaptive phenotypic plasticity in brook trout, Salvelinus fontinalis, life histories. Ecoscience, 3, 25–32.

    Google Scholar 

  • Hutchings JA, Gerber L (2002) Sex-biased dispersal in a salmonid fish. Proc. R. Soc. Lond. B, 269, 2487–2493.

    Google Scholar 

  • Jehle R, Arntzen JW, Burke T, Krupa AP, Hödl W (2001) The annual number of breeding adults and the effective population size of syntopic newts (Trturus cristatus, T. marmoratus). Mol. Ecol., 10, 839–850.

    Google Scholar 

  • Koenig WD, Van Huren D, Hooge PN (1996) Detectability, philopatry, and the distribution of dispersal distances in vertebrates. Trends Ecol. Evol., 11, 514–517.

    Google Scholar 

  • Krebs CJ (1998) Ecological Methodology. Addison-Wesley, Boston.

    Google Scholar 

  • Leclerc J (1979) Ecologie des populations d'ombles de fontaine (Salvelinus fontinalis) et d'ouananiches (Salmo salar) de la riviere Meo, Nouveau Quebec.M.Sc. thesis, Université Laval, Québec.

    Google Scholar 

  • McDonald G (2001) Relatedness determination and detection of spawning time QTL in rainbow trout (Oncorhynchus mykiss).M.Sc. thesis, University of Guelph, Ontario.

    Google Scholar 

  • McElhany P, Ruckelshaus MH, Ford MJ, Wainwright TC, Bjorkstedt EP (2000) Viable salmonid populations and the recovery of evolutionarily significant units. U.S. Dept. Commerce, NOAA Tech. Memo. NMFS-NWFSC-42, 156 pp.

  • Morris DB, Richard KR, Wright JM (1996) Microsatellites from rainbow trout (Oncorhynchus mykiss) and their use for genetic study of salmonids. Can. J. Fish. Aquat. Sci., 53, 120–121.

    Google Scholar 

  • Nei M, Chakravarti A (1977) Drift variances of FST and GST statistics obtained from a finite number of isolated populations. Theor. Popul. Biol., 11, 307–325.

    Google Scholar 

  • Neraas LP, Spruell P (2001) Fragmentation of riverine systems: the genetic effects of dams on bull trout (Salvelinus confluentus) in the Clark Fork River system. Mol. Ecol., 10, 1153–1164.

    Google Scholar 

  • Newman RA, Squire T (2001) microsatellite variation and fine-scale population structure in the wood frog (Rana sylvatica). Mol. Ecol., 10, 1087–1100.

    Google Scholar 

  • Nichols RA, Bruford MW, Groombridge JJ (2001) Sustaining genetic variation in a small population: Evidence from the Mauritius kestrel. Mol. Ecol., 10, 593–602.

    Google Scholar 

  • O'Reilly PT, Hamilton LC, McConnell SK, Wright JM (1996) Rapid detection of genetic variation in Atlantic salmon (Salmo salar) by PCR multiplexing of dinucleotide and tetranucleotide microsatellites. Can. J. Fish. Aquat. Sci., 53, 2292–2298.

    Google Scholar 

  • Presa P, Guyomard R (1996) Conservation of microsatellites in three species of salmonids. J. Fish Biol., 49, 1326–1329.

    Google Scholar 

  • Prosser MR, Gibbs HL, Weatherhead PJ (1999) Microgeographic population genetic structure in the northern water snake, Nerodia sipedon sipedondetected using microsatellite DNA loci. Mol. Ecol., 8, 329–333.

    Google Scholar 

  • Quinn TP (1993) A review of homing and straying of wild and hatchery-produced salmon. Fish. Res., 18, 29–44.

    Google Scholar 

  • Rannala B, Hartigan JA (1996) Estimating gene flow in island populations. Genet. Res., 67, 147–158.

    Google Scholar 

  • Raymond M, Rousset F (2001) Genepop (version 3.3): population genetics software for exact tests and ecumenicism. Available from http://www.cefe.cnrs-mop.fr/ Updated from Raymond, M. and Rousset, F. 1995.

  • Rice WR (1989) Analysing tables of statistical tests. Evolution, 43, 223–225.

    Google Scholar 

  • Rodríguez MA (2002) Restricted movement in stream fish: the paradigm is incomplete, not lost. Ecology, 83, 1–13.

    Google Scholar 

  • Roslin T (2001) Spatial population structure in a patchily distributed beetle. Mol. Ecol., 10, 823–837.

    Google Scholar 

  • Rousset F (2001) Genetic approaches to the estimation of dispersal rates. In: Dispersal (eds. Clobert J, Danchin E, Dhondt AA, Nichols JD), pp. 18–28. Oxford University Press, Oxford.

    Google Scholar 

  • Sanchez JA, Clabby C, Ramos D, Blanco G, Flavin F, Vasquez E, Powell R (1996) Protein and microsatellite single-locus variability in Salmo salarL. (Atlantic salmon). Heredity, 77, 423–432.

    Google Scholar 

  • Schilthuizen M, Lombaerts M (1994) Population structure and levels of gene flow in the Mediterranean land snail Albinaria corrugata(Pulmonata: Clausiliidae). Evolution, 48, 577–586.

    Google Scholar 

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

    Google Scholar 

  • Slatkin M (1985) Rare alleles as indicators of gene flow. Evolution, 39, 53–65.

    Google Scholar 

  • Slatkin M, Barton NH (1989) A comparison of three indirect methods for estimating average levels of gene flow. Evolution, 43, 1349–1368.

    Google Scholar 

  • Spruell P, Rieman BE, Knudsen KL, Utter FM, Allendorf FW (1999) Genetic population structure within streams: Microsatellite analysis of bull trout populations. Ecol. Freshw. Fish, 8, 114–121.

    Google Scholar 

  • Sumner J, Rousset F, Estoup A, Moritz C (2001) 'Neighbourhood' size, dispersal and density estimates in the prickly forest skink (Gnypetoscincus queenslandiae) using individual genetic and demographic methods. Mol. Ecol., 10, 1917–1927.

    Google Scholar 

  • Tallman RF, Healey MC (1994) Homing, straying, and gene flow among seasonally separated populations of chum salmon (Oncorhynchus keta). Can. J. Fish. Aquat. Sci., 51, 577–588.

    Google Scholar 

  • Taylor EB, Redenbach Z, Costello AB, Pollard SM, Pacas CJ (2001) Nested analysis of genetic diversity in northwestern North American char, Dolly Varden (Salvelinus malma) and bull trout (Salvelinus confluentus). Can. J. Fish. Aquat. Sci., 58, 406–420.

    Google Scholar 

  • Van Oppen MJH, Turner GF, Rico C et al. (1997) Unusually finescale genetic structuring found in rapidly speciating Malawi cichlid fishes. P. Roy. Soc. Lon. B Bio., 264, 1803–1812.

    Google Scholar 

  • Vitalis R, Couvet D (2001a) Estimation of effective population size and migration rate from one-and two-locus identity measures. Genetics, 157, 911–925.

    Google Scholar 

  • Vitalis R, Couvet D (2001b) ESTIM 1.0: A computer program to infer population parameters from one-and two-locus gene identity probabilities. Mol. Ecol. Notes, 1, 354–356.

    Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution, 38, 1358–1370.

    Google Scholar 

  • Waples RS (1991) Genetic methods for estimating the effective size of cetacean populations. In: Genetic Ecology of Whales and Dolphins (ed. Hoezel AR), pp. 279–300. International Whaling Commission (Special Issue No. 13).

  • Waples RS (1998) Separating the wheat from the chaff: patterns of genetic differentiation in high gene flow species. J. Hered., 89, 438–450.

    Google Scholar 

  • Waples RS (2002) Definition and estimation of effective population size in the conservation of endangered species. In: Population Viability Analysis (eds. Beissinger SR, McCullough DR), pp. 147–168. The University of Chicago Press, Chicago.

    Google Scholar 

  • Whitlock MC, McCauley DE (1999) Indirect measures of gene flow and migration: FST not equal to 1/(4Nm + 1). Heredity, 82, 117–125.

    Google Scholar 

  • Wright S (1931) Evolution in Mendelian populations. Genetics, 28, 114–138.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Zoology, University of Guelph, Guelph, ON, N1G 2W1, Canada

    A.J. Wilson & M.M. Ferguson

  2. Department of Biology, Dalhousie, University, Halifax, NS, B3H 4J1, Canada

    J.A. Hutchings

Authors
  1. A.J. Wilson
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. J.A. Hutchings
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. M.M. Ferguson
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to A.J. Wilson.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wilson, A., Hutchings, J. & Ferguson, M. Dispersal in a stream dwelling salmonid: Inferences from tagging and microsatellite studies. Conservation Genetics 5, 25–37 (2004). https://doi.org/10.1023/B:COGE.0000014053.97782.79

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/B:COGE.0000014053.97782.79

Search

Navigation