Protein polymorphism in Atlantic salmon within a Scottish river: evidence for selection and estimates of gene flow between tributaries

.-li~liuc'rilltrrc'.

98 (

Elscv icr Scicncc

I991 I 2 I 7-230 Publishers

21:

I. .V., Amsterdam

Protein polymorphism in Atlantic salmon within a Scottish river: evidence for selection and estixates of gene flow between tributaries

\‘crspoor. E.. Fraser. N.H.C. and I’oungson. .A.F . IW i. Protein po )morphisrn #II I\.tlantic salmon withm a Scottish river: evidence for sclcctmn and csttmates ofgrm flow bci*rcen trtbutarics. :lyrrrl-

l~rrirrr,r. 98: 2 17-230. Significant hctcrogenci::. was found for alleltc variation at ctght protttn loci among .Atlanric salmon (.S~lr~ro.ru,‘~~~~from tr~bt ;,, irs it-. :hc ti>lcs of Sutherland r~vcr s!stcn in nortbmsi Scotland. Differentiation at tte ,.\fl:‘P.?* locus was grcatcst and correlated with summer water tcrilp:raturc. as found in other studies. Thissupports the conlcntion that thr polymorphism is affcctcd h! Acction. lndir:ct cstimatcsofgctrc flow among trtbutar) populations based on .v:,IN. the cffccttvc number of indiv itluals exchanged brtwcen tributap populations. and salculatcd from Wright’s F,l. were 6.1 for ,,, IlEt”-? and varied from 9.3 to 79.8 for the other loci. The overall mean csttmate r.as 15.1. -\n cstimatc of :Vettt based on the mean frcqurnc) of “prtvatc” alleles was 2.0. The pmportton ,f mtgram salmon among each trtbatary’s breeding population is likely to hc In the ord,:r of S’!o CT Irss. The gcncln suhstructuring of the .Atlantic salmon ohservcd within the rtvcr s)stcm pro\ I&S t lc scope for genctic Ltiptation of population, to local cnv tronmcntal condrtions.

The hypothesis that anadromous Atlantic salmon (SU/WO s&r) in different river systems belong to distinct pcpulations, between which gene flow is constrained, is supported by a wide body of circumstantial evidence (Saunders, 1981; Thorpe and M itchell. 1981; Stabell, 1984; Whl. 1987). Thz evidence has also been interpreted to suggest that, in many cases within rivers. gene flow is restricted between salmon in different tributaries. spatial heterogeneity of genetic variation at enzymatic protein loci is one type of evidence cited in support of multipto populations within river systeas (e.g. Mailer, 1970: Sttihl. 1987). Studies indicate that between-sample heterogeneity can provide evidence for the existence of multiptr ,senetic populations if certain assumptions hold true. First, samples must be taken at random from the population they repnO44-8486/91

ibO3.50

0 I99 I Elsevicr

Sctcnce Publishers 9.V.

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218

E. VERSf’OoR

ET Al..

resent; second, the effects of genetic drift. which promotes population differentiation, and gene flow, which counteracts it, must be more or less in balance; and third, allele frequencies must not be substantially affected by selection ( Allendorf and Phelps, 198 I; Chakraborty and Leimar, 1987 ). If these assumptions are met. an estimate of the mean historical level of gene flow between populations can be derived from the observed extent of differentiation (%’ tght, 1978; Slatkin, 1985; Chakraborty clr,d Lciniar, 1987). Alternatively. gene flow can be estimated indirectly from the frequency of”private” alleles i.e. those alleles which are found only in samples from one location ( Slatkin, 1985). Theoretically, the results obtained should be the same if the conditions pertaining to each of the two methods are satisfied (Barton and Slatkin. 1985 ). A study of genetic heterogeneity at enzymatic protein loci within the Kyles of Sutherland river system in northeast Scotland is reported here. The study set out to estimate gene flow among the tributaries indirectly from allele frequency variation. It also sought to test for an association of variation at MEP2* among juvenile Atlantic salmon from different tributaries within a river system with variation in tributary temperatures. An association has been found within and among other river systems (Verspoor and Jordan, 1989) in both North America and Europe, and strongly suggests the association results from selection acting directly, or indirectly, on the locus. That the locus is subject to the effects of selection, is further suggested by observed assuciations of ,,MEP-2* variation with timing of maturation (Jordan et al.. 1990) and juvenile growth (Jordan and Youngson, 199 I ). The estimates of gene flow obtained for MEP-2* have been compared with those from other polymorphic protein !oci examined and for which there is no evidence of their being affected by ssIection. M1;\TERI:\l-S

.AND hlETHODS

Juvenile salmon were collected by electrofishing in rive tributaries of the Kyles of Sutherland system ( Fig. 1 ) between J sly and October 1989. One trih:rtan*. the Piver tiykel at Loch Ailsh (b) was sampicd both above and belov; the loch. Locations selected were sites of intensive natural spawning and had not been subject to supplemental stocking. They were chosen to rep resent the widest possible range of temperature conditions. The River Shin location bps lower spring and summer temperatures than found in other parts of the river system due to the upstream presence of a large hydroelectric reservoir which delivers subsurface water to the river (Fraser. 1989). Temperatures at the oth.:r locations vary in r.esponse to local climatic conditions, in part a reflection of differences in altitude, For each sample. juveniles were taken at approximately 5-m intervals in

PROTEIN

POLYMORPHISII.

EVIDENCE

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Fig. I. Map showing location of study area in notthcastcrn Potland and umpllng SW\ III Ihc Kytes of Sutherland river system. (a) River Oykrl al Ro$eball (5 I Rl\cr ( IykcI ;LI Ll~& 11lrh. (c) River Einig: (d) Riverr~rmn-and (c) Ribcr Shin.

the river. This increased the likelihood of obtaining a sample of fish that w*as representative of each tributary’s pcrpulation of salmon. The juveniles uzrc young of the year (0+ ), with the exception of the River Shir uhcrc I + j?lveniles were also included in the fish sampled. Electrophortvic

analyses

Samples were placed on solid CO2 in the field ;ind slor
En)) rnc IOU cumincd -tLnr)mc

(Et’.

in study showing new and old locus dcsrgrratmns --

Nurnbcr i

NW

198(i

(SW ~CXI for cnplanation - I987--

)

19KB LA!-3 ldh-4 LdhI-4 .lldh-3.4 .llc-2 Sdh-2 .Sdll - I St d -__----

Maximum and m inimum water temperatures were recorded at the locations on the Kyles of Sutherland rivers on a weekly basis during the period from 26 May to 28 July I989 using ther*rOmctc.-s and thermographs ! Fraser, 1989). A median temperature value for each location was calculated from the mean maximum and m inimum temperatures fo1 the period.

Samples were tested for departures from those expected under CastleHardy-Weinberg assumptions using the exact test in HIOSYS (Sil:ofTord slid Se!ander. 1989). The pl’esenczcf sigiiifi~a~t ~LILL.LL.X~;PETPE i.e. heterogcneity. among samples was tested using a log likelihood ratio (G) test or Fisher’,; exact test on genotype proportic; ns: probabilities were combined using Fisher’s method ( SaLI and Rohlf. 198 1a). Pooling of rare genotypes was carried out as requirea for both analyses. The correlation of allele frequencies with temperature was tested using Kendal’s r-coefficient (Sokal and Rohlf. I98 i a ). Nei’r; unbiased genetic distance (ID) was calculated usLlg BIGSYS. F,,, H mcasurc of allelic tixation in populations (Wright, 1978) was used to estimate NVrll, the effective number of individuals exchanged between populations. The formula of W right, based on the ‘island’ model of gene flow between pupulations. modified by Takahata ( 1983 j to take into account the number of samples. was used:

FST values were calculated using BIOSYS. Values for observed allele frequency differences among samples were compared v. ith “expected” values of FSTand N,m.

“Expected” valcles of FST were calculstr d by generating samples from a single statistical population whose allele frequencies were equal to the mean observed allele frequencies for the Kyles of Sutherland tributaries. Each generated value of Fsf was ba:=ld on the same number and size of samples 2s fur the observed values but fenresented the mean of five simulated sets of samples. Estimates of gene flow based on the average frequency of “private” alleles were calculated using the following formula put forward by Barton and Slatkin ( 1985):

hh b( 1) I = -0.612 log,(J[&n]

- 1.21

This was corrected for sample size as they suggest by multiplying by SO, the sample size which pertains to their equation. and dividing by the mean sample size for the Kyles tributaries. 103. RESULTS

Genotype proportions within samples were consistent with expectations under Castle-Hardy-Weinberg assumptions. Also, no heterogeneity was detected between the two saiiip:cs from the River Oyke! at LGcli Aiish. The ohserved genotype proportions at the loci examined for the two sites were not significantly differel.1 overall, based on the combined test ot’the significance of Frobabilities of tke significance fes?s of differences at the individual loci (G-test or Fisher’s exact test; combined probabilities, x2= 13.07, d.f. = 16. 3=0.07 j. Therefore, the Loch Ailsh samples wcrc cons&red to deri*:e from the same population and pooied. The pooled sample, when considered with the samples from the other si?es, did show significant heterogeneity in genotype proportions (Table 2) for five of the seven loci tested. Genotype proportions at LDH-4*, though they appeared to differ among the sites, could not be tested as the variant was found at only one location. thlz River Shin, at low frequencies. However, the variant was detected amongst both 0+ and I+ year classes in the sample suggesting that the L-OH-C*frequencies observed are characteristic of the local population and not just the chance sampling of a rare variant in a single family. Heterogeneity among samp!e r, st the ,MEP-2* locus (Table 2 ) was not randomly distributed. Aliele frequencies at the locus were significantly correlated with the median temperatures recorded for the late spring-early summer peri& (Fig. 2; Table 3); Kendal’s coefficient of association, T, was 0.8 (P
2

--

RiverOykcl Rosehall Loch .L\ilsh abet e below combined Rivrr Einig Riwr Carron River Shin Hcterogcncily I Ii-trst )

Tributar)/Sne

Frequencies 5) stem

TABLE

of variam

0.03P 0.140 0.094 0.042 0.050 0.018

40-50 49 90-99 48-50 7% 109 76-156 G

P

0.099

96- I34

0.04

0.125 0. I50 0. I67 0.1 I5 0.194 0.142 10.0

0. I20

alleles ohserved at protein

-

0.000 0.000 0.000 0.000 o.ooo 0.026 -

0.013 0.010 0.01 I 0.000 0.02 o.oco 2.6 0.26

0.000

0.015 0.010 0.000 0.005 O.GOO 0.020 0.034

0.010 0.000 0.005 0.000 0.004 0.007

I x IO-’

0.440 0.419 0.43 0.542 0.512 0.609 22.7

0.358

0.310 0.388 0.348 0.323 0.173 C’38 *

0.010 0.02 : 0.015 0.000 0.006 0.000 2.2 0.34

0.343

0.000

2x IO-5

0.070 0.09 1 0.08 I 0.021 0.065 0.037 31.4

0.066

river

0.02

0.000 0.000 0.000 o.oocl o.ooo 0.020 11.4

O.ti20

salmon taken from t~~~utarics ;If the Kylcs of Sutherland

0.@26

0.0 I

12.6

Atlantic

0.000

loci in samples of juvenile

r; IJ

PROlElh

R)LY!.‘lORt’tiISM~

14.0

14.5 Mediara

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16.0 Weekly

16.0

15.5 Temperature

(OC)

Fig. 2. Plot of ,.1IEP-2*( 100) frequency against median rhc K:,lcs of Sutherland rive; system. Letters corrrspo:ld TASLF

16.5

temperature for sampling lo those shown in Fig. 1.

locations

3

Kendal’s ‘I ccic!Ec~~~ of association belweer allele frequencies and median weekly tcmpcraturcs the period of 26 Mi,y to 28 July 1989 for locations in the Kyles of Sutherland river system

0.60

in

-0.20

0.74

-0.63

-0.31

0.10

o.!w

0.12

0.49

0.40

for

0.00

“P=O.O5.

18.9. The observed mean value of FSTdiffered from that generated for the hypothetical single statistical population with allele frequencies equal to the means of the five Kyles of Sutherland locations (Table 4). The distribution of “expected” values :br the loci differtd significantly from these observed (Wilcoxon Matched Pairs test: T= 4, .V= 8, P=O.O25;Siegel,1956). The mean “expected” Npm was 63.8 compared with the observed mean I5 I. Differences in observed and “expected” values of FSTwere greatest for IDDH-2*, LDH-4* and ,ME.D-2* (Table 4). Only a single “private” allele, LDH-4*( 68), was detected. Basedon its frequency, the formula of Barton and Slatkin ( 1985) gave an estimate of 2.0 for NCm. Approximate 95%-confidence limits were 0.5 and 16 0 based on the confidence limits for the LDH-4* (68) frequency. This was interpolated from Sokal and Rohlf ( I98 I b. table 23 ). Genetic distances between samples taken from the different tributaries of the Kyles of Sutherland (Table 5 ) showed only a weak cqrrtspsndence with geographic distance (Fig. I ). For example, while the two sites on the main

23 TABLE

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ET AL.

4

Comparison of values of .Yrv~ and FST for samples from locations sampled in the Kylcs of Sutherland ri\rr s!.slem !Wtserve!i ! with \,aluec trh*ainrd fv the samt number nf samples of the same size gcncrated at random from a single statistical population with allele frequencies eql al to the mean for all the Kylcsof Sutherland w!nples (Expected) Locus

Expected”

Observed F bT

.V,lll

F ST

h;,rn

;I.4 7--j* in/l P-3+ i.Dll-4’ ,slDIi-J,J* m.\itL.I’- 2* IDDli- I’ fDDlt-.?+ .son*

0.004 0.00’ 0.0 I9 0.007 0.025 0.003 0.016 0.008

39.8 79.8 8.3 "-a. 7 6.2 53.2 9.8 19.8

0.005 o.oll4 0.003 0.004 0.0004 0.002 o.m4 0.002

31.8 39.8 52 39.8 399.8 79.8 399.8 79.8

h&n

0.0105

15.1

0.0025

63.8

‘Mean of values for five SCISof gcncrated

T-\BLE

5

Xei’s unbiased genetic distances (D) the li! Ies of Sutherland river s>stcm Location ; : c -____.--

samules.

between samples of .Aflantic salmon taken from tributaries

of

3

h

C

d

e

0.000 9.005 0.008 0.012

0.002 0.005 0.008

0.002 0.001

0.002

-

Q.QO!i

Genetic

1 0

D ,tance

(Nei’s S) Fig. 3. ! lPCiM,A Cluster Dendrogram of Nei’s Unbiased CJcnetic Distance ‘?v sampling locations in the K! les of Sutherland river sysrem. Letters correspond to those shown in Fig. I.

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stem o.‘the River Oykel, Loch Ailsh and Rosehall. are geographically thz closest and cluster separately from the remaining sites (Fig. 3), the next grouping based on genetic distance is of the River Einig site with the River Shin. Based on geographical proximity, this site would group with the two River Oykel sites. DISCUSSION

‘The positive association of MEP-2* ( 100) frequencies with summer water temperatures in the Kyles of Sutherland river system is consistent with prcvious observatiuns. The associatiotl has been found to occur within other rivers as well as among salmon ppy)l!lations from different rive; systems in both Europe and North America (Verspoor and Jordan. I989 ). Thf ahi!& IO detect the association ir, a river system as small as thp! sf ihe Kyles of Sutherland is the result of the unuslrally wide IX+ of temperature habitat types (Fraser. 1983) found there. In particular. colder spring and summer water conditions than occur naturally. are found in the River Shin as a rcsu:t of the discharge of subsurface water from the ~~~dlcrelectricreservoir. At the same time, this is complimented by temperatur: variation resulting from considerable variation in altitude among different parts of the system. The lower half of the River Oykel and the lower Shin are 100 m or les: above sea level while the Carron and parts of the upper C!j%c! ratchments are between 200 and 900 m . The consistent detection of the same gene-environment association pr+ vides compelling evidence that allele frequencies at the locus are influenced by selection. Whether this acts through differential mortality among juvenile or through subsequent differer,ces in reproductive performance is not clear. The latter is conceivable as genotypic variation a; the locus is associated with differences in growth rates and maturation phenotypes (Jordan et al.. 1990: W .C. Jordan. unpubl.). The association with temperature may arise from direct selection on variation in the kinetic properties of the different allozymes with regard to cellular metabolism; it would c;j:a!!;f 2r+‘ z-. .‘;?selection acting ~11:he locus through another variable related to temijtrerure or, indirectly, through selection on a structurally linked locus or set lr‘loci. Evidence for selection acting on protein polymorphism in the Atlantic salmon is confined !argely to M IZP-?*. Some evidence llas been fvund to suggest selecilon may be acting on the locus coding for the blood protein, transferrin. in the Atlantic salmon (Verspoor, 1986). There is no evidence to suggrbt that selection is operating on the other enzyme loci examined in the present study. Genetic heterogeneity among samples of iuvenile anadromous Atlantic salmon frcv different tributaries within the same river ;jrstem could potentially arise even if they represent a single breeding population. The chance

,

216

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distribution of ‘Jreed;n& adults, or even locally varying sciective pressures, could generate signrficant. but unstable, differences between :oca!ions, where dispersal and m ixing of juveniles after hatching and prior to sampling, is restricted (e.g. AYendorf and Phelps, I98 I ). This will be a particular problem where spawning artas are dispersed and each is used by only a small numb?:. of breeders. The genetic heterogeneity detected between tributaries in the Kyles of Sutherland system cannot be attributed to the analysis of samples of juveniles which are unrepresentative of the populations from which they were derived. Each sample was collected over a distance of several hundred meters in areas where large numbers of adults are known to spawn. Consistent with this, no departures were detected of genotype proportions from Castle-Harcly-Wcinberg expectations. The representativeness of the samples is further supported by evidence for spatial and temporal stability of genotype proportions. The River Oykel samples from Loch Ailsh showed no heterogeneity even though they were separated by over 2 km of lacustrine habitat over which dispersal of 0+ juveniies would be significantly constrained. At the same time, the River Shin 0+ fish sample, sampled for the present study, did not differ from a sample of Oi- juveniles taken from the Shin the previous year (W.C. Jordan, unpubl.. 1988). This is further supported by studies which demonstrate general temporal stability of allele frequencies for salmon populations in other Scottish rivers (W.C. Jordan, unpublished). It seems reasonable to conclude, therefore. that the genetic differentiation detected represents more or less fixed differences among the populations of Atl;lntic salmon breeding in the different tributaries sampled. ‘The genetic differentiation among the samples indicates that the Kyles of Sutherland river system contains more than one genetic stock of Atlantic saimon. 4t the loci not subject to selection, the differentiation is only possible tnrov.igti ;he process of genetic drift which requires the subdivision of the sslmun in the river system into a number of more or less reproductively separate ropu!ations. Differentiation at the ,MEP-P locus is likely to result from differential selection for the genotypes at the locus in the various tributaries and wiil be maintained by the restricted gene flow among the sampling sites In the absence of restricted gene flow, the selection differentials between genotypes required to achieve the observed differentiation would need to be extremely large. ‘The success of one homozygote compared with the other would have to be about twice as great in some tributaries and half as great in others. This seems unlikely. The !;ighest genetic divergence among samples and the lowest estimates of gene flow are obtainid for MEP-2. This would appear to be associated with the action of locally varying selecti-/e pressures acting on the locus. Hcwever, the effect of including the value of Nem derived from ,MEP-T* on the overall estimate of gene flow between tribularies was small, This is because the vari-

PROTEIN POL’~‘MORPIflSM

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I’r

ante among values derived for the other, apparently unselected loci. was large, with the highest values of N,m over 10 times that of the lowest. The relative insensitivity of the estimate to the effects of selection is consistent with the results of simulation studies referred to by Slatkin ( 1987). His results also suggest that, except in unusual and extreme cases, the effects of selection on gene flow estimates made from spatial variation in allele frequencies will be small. The accuracy with which Il;m estimates derived from FS., reflect the average historical levels of genetic exchange among popuiations may be questionable if the genetic differentiation between tributaries at the loci examined has not reached a more or less stable equilibrium with regard to the opposing effects of genetic drift and gene flow. However, it has been suggested that within river systems, this equilibrium should be reached within a few huncred geirerations ( Allendorf and Phelps, 198 1; Chakraborty and Leimar. 1987 ). This is much less than the number of generations likely to have transprred since the colonization of most northern European salmon rivers after the last glaciation c. 10 000- 13 000 years ago. The estimates of N,m derived from FSr for the Kyles of Sutherland river system are in line with values of N,m calculated from genetic differsntiation between river systems in other studies. Stahl ( 198 1 ) estimated Npr between Baltic rivers to be 2.5, while Verspoor (unpublished ) estimated values of h;,.m between populations of anadromous salmon !n Newfoundland to be 5.4. Similarly derived estimates of N,m for geographically isolated populations of nonanadromous populations in Newfoundland are 0.5, consistent with thf: expected absence of gene flow for a large part of the time since they were er;tablished. The somewhat greater gene flow estimated to occur between tribdtaries compared with among rivers is consistent with the smaller geographical separation involved and with straying rates being a positive function of distance. In theory, the estimates of Ncm derived from values of FST and from the frequency of “private” alleles as proposed by Slatkin ( 1985 ) should concur (Barton and Slatkin, I985 ). However, where smell numbers of private alleles are used to derive an estimate, as in the present case. differences miQtt be expected due to vartation in estimates between loci. This may explain why the estimate based on private alleles is an order of magnitude lower than that found using F,,. The difference does not appear to restlt from an error in estimating the frequency of the LDH-4* (68) allele. The value of ,Ycrn derived from the mean FST is outside the 95?&confidence limits for the estimate of Ncm based on the LDH-4*( 68) frequency. Additionally, the estimate for LDH4*( 68) frequency was not heterogeneous between the 0+ and I+ juveniles samp!ed, suggesting that the estimate based on LDH-4* was not substantially influenced by sampling error. While the cause of the discrepancy must remain specula!ive, a low estimate would be realized if spatial differentiation at the

2x3

E ~ERSPOOR ET AL.

LDH-4’. locus has been increased by selection, as appears to be the case for MLP-2*. However, while the estimates differ they both suggest that the effective number of individuals exchanged between tributary populations is small. Interpretation of estimates of Y,m with regard to the substructuring c?fthe salmon population within Lire Kyies oCSuriler1and river system is dependent on the relative values of Iv,, the effective numbers of salmon in breeding populations irk cacil t! ibutary and IPI,the proportion of each which are migrants. For example. with an Ncrn of i5 as found in the present study, if Y, were small. say 15, then m would be 100% i.e. the whole of the breeding population would be migrants: if Iv, was 1500. then the i;roporGon of migrants would only be I TO. Thus what is required to interpret the implications of Nem values obtained is some sort of quantification of N,. Unfortunately, the sizes of the breeding populations of salmon in the tributaries of !bc Kyles of SlItherland river system are not known. Based on numbers of salmon angled in the rivers and average exploitation rates (Department of Agriculture and Fisheries for Scotland, unpubl. ), the number of spawners in each tributary is likely to be in the order of 1300~.Ic) 000. Conservatively, assuming a minimum effective number of breeders in each tributary of just 300, the average historical proportion of migrants among the breeders of each tributary should be less than 5%. Effective rates of migration between tributaries of 59’0or less are small and indicaye that samples taken in the Kyles of Sutherlarid river system derive from a number of more or less reproductively separa:c breeding populations. This supports the wider body of circumstantial evidence that many river systems contain multiple, distinct salmon populations (Saunders, I98 I ; Thorpe and Mitchell. 198 1: St&hi, 1987 ). in some cases these may represent different populations of anadromous and non-anadromous glmon (Verspocr and Cole, 1989: Vuorinen and Berg, 1989). Division of salmon in river systems into spatially distinct populations provides the necessary basis for natural selection to evolve local populations adapted to local conditions. That locally varying szlective pressures can affect the genetic composition of the populatior?s is indicated by the association of ,MEP--F allele frequencies with temperature. To the: extent that local adaptation has evolved, it will contribute positively to the productivity of each population. Factors which d;;turb the adaptive components of population differentiation by Lhe introduction of less well adapted gene combinations should be viewed with concern. In this regard. large or persistent influxes of genetically different sslmon, sucfi as farm escapees, may pose a problem where they interbreed. The extent of the problem will depend on both the numbers of non-lo4 fish involved and the extent and nature of p,enetic ditfferences belween native and non-native salmon.

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ACKNOWLEDGEMENTS

The support of the River Shin Board and c r”t$e proprietors of the Estates who granted pcrmisslon to conduct the study is gratefully ackrro4edged. In particular, the help provided by Henry Morrice. Superintendent of the Board was invaluable. David Hay assistedwith the col’ection the samplesofjuveniie salmon. Discussions with Bill Jordan provided valuable insight into many aspectsof the study. REFERErZCES Allendorf, F.W. and Phelps, S.R.. 198 I. Use of allelic I-cquencies IO describe population structure. Can. J. Fish. Aquat. Sci.. 38: 1507-l 514. 3arton. N. and sratkin. M.. 1985. A quasisquilibriun: theon rrf the distribution of rare alleles in a subdivided population. Heredity, 56: 409-415. Chakrabony. R. and Leimx. 0.. 1987. Genetic variation within a subdivided population. In: N. Ryman and F. Utter (Editors), Population Genetlcs and Fisheries Management. Univcrsity of Washington Press, Seattle. WA, pp.89-120. Cross, T.F. and Ward. R.D.. 1980. Protein variation, and duplicarc loci in the 4ilantic salmon, S&no s&r 1. Genet. Res.. Camb., 36: I47- I65 Fraser, N.H.C.. 1984. The association of allele frequency variation at the ;\I,?,7 locus in rhe Atlantic salmon (Su/r,~o s&r and water temperature in the four main rivers of the Kyles of Sutherland catchment area. M.Sc. thesis, Unrvcnity of Aberdeen. UK. 75 pp. Jordan, W-C. and Youngmn. A-F.. 1991. Genetic protein variation and natural selection in Atlantic salmon (S&n; salclr 1. ) Parr. J. Fish Blol., in press. Jordan, W.C.. Youngson. A.F. and Webb, J.H., ISQO. Genetic variation at the malic enzyme-2 locusand age at maturity in sea-run Atlantic sdll,lon (Sulrna s&r). Can 1. Fish. Aquat. Sci.. 47: 1672-1677. Meller. D.. 1970. Transferrin polymorphism ic Atlantic salmon (Sdlr?ro ~alur!. J. Fish. Res. Board Can., 27: I61 7-l 625. Saunders. R.L.. I98 I. Atlantic salmon ( SU/!,IO s&r) s!ocks and management i.r.plications in the Canadian Atlantic Provinces and New Endand. USA. Carl. J. Fish. .4quai. Sci.. 38: I6 I21625. Shaklee, J.B.. .Qllendorf. F.W., Morizot, D.C. and Whitt. G.S.. 1989. Genetic nomenclature for proteincc%linp loci in fish: proposed guidelines. Trans. Am. Fish. !Soc.. I 18: 2 18-227. Siegel, S.. 19156. Nonparametric Statistics for the Behavioral Scichces. McGraw-Hill KogaEusha. Tokyc. 3 I2 pp. Slatkin. M.. 1985. Rare alleles as indicators of gene tlow. Evolution. 39: 53-65. Slatkin. M.. 1987. Gene flow and the geogl’aphic structure ;f natbial populations. Nature. 236: X7-792. Sokal. R.R. and Rohlf. F.J.. I98 I a. Biometry. W.H. Freeman. San Fraucisco. CA. 859 pp. Sokal. R.R. and Rohlf. F.J.. 1981b. Statistical Tables. W.H. Freeman, San Francisco. CA. 219 PP. Stabell, O.B.. 1934. Homing and olfaction in salmonids: a critical review with special reference to the Atranfic salmon. Biol. Rev., 59: 333-338. Stbhl. ci.. 198 I. Genetic differentiation am’.. ~gnatal ,+I populations of Atlantic salmop (Sal0r0 rulur) in northern Sweden. Ecol. Bull.. 34: 95- 105. Stbhl. G.. 1987. Genetic population structure of Atlantic salmon. In: N. Ryman and F. Utter (Editors). Populations Genetics and Fisheries Management. University of Washington Press, Seattle, WA, pp. I2 I - 140. Swofford. D.L. and Selander, R.B., 1989. Biosys-I: a Comput,r Program for the Analysis of

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iI. \‘ERSPOOR

FT AL.

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