Electrophoretic study on Atlantic Salmon Populations. from the Miramichi River (New Brunswick) System, Canada
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1 paper not to be cited without pr.ior reference to the author International Council for the C.M. 1983/M:20 Exploration of the Sea Anadromous and Catadromous Fish Conunittee Electrophoretic study on Atlantic Salmon Populations from the Miramichi River (New Brunswick) System, Canada by Gunnar Stäh1 1, Eric J. Loudenslager 2 Richard L. Saunders 3 and Emerson J. Schofield 4 1Department of Genetics. University of Stockholm S Stockholm Sweden 2Huntsman Marine Laboratory, St. Andrews, N.B. EOG 2XO, Canada 3Biological Station, Department of Fisheries and Oceans, St. Andrews, N.B. EOG 2XO, Canada 4Department of Fisheries and Oceans Box 217, Chatham, N.B. E1N 3A6, Canada
2 2. Abstract A total of 311 individuals of Atlantic salmon (Salmo salar) were collected from five locations of the Miramichi River system in New Brunswick, Canada, and subjected to an electrophoretic analysis for genetically determined protein polymorphisms using 26 enzymes encoded by 42 genetic loci. Variation was observed at six loci and statistically significant allele frequency heterogeneities were obtained between populations. The absolute magnitudes of genetic differences observed are small (average genetic distance Ö = ), but nevertheless associated with considerable morphological divergence. On a procede a l'analyse electrophoretique de trois cent onze saumons de l'atlantique collectionnes a cinq endroits dans le systeme de la riviere Miramichi au Nouveau-Brunswick, pour etudier les polymorphismes proteiques hereditaires a l'aide de 26 systemes enzymatiques codes par 42 points genetiques. On a observe! des variations en six points et des heterogeneites de frequence allele statistiquement significative entre les populations. sont minimes Les grandeurs absolues des differences genetiques observees (distance genetique moyenne D = ), mais neanmoins associees avec une divergence morphologique considerable.
3 ..' 3 Introduction Riddell et al. (1981) used discriminant function analysis of morphological parameters together with breeding experiments under controlled eonditions to g~ve evidence of genetically distinct stocks of Atlantie salmon (Salmo salar) in separate tributaries of the Miramiehi River. New Brunswiek. Canada. Differences in body form and size observed in naturally produced fish from two S.W. Miramichi tributaries were found to be heritab1e (Riddell et a ). Stähl (1981) conducted electrophoretic examinations on Atlantic salmon from from six rivers in northern 4It Sweden and presented evidence that the species is naturally subdivided into genetieally distinct subpopulations between as weil as within river systems. The aim of the work presented here is to shed further light on the stock status of the Atlantic salmon in two S.W. Miramichi tributaries. Juvenile Atiantic salmon from these two and two additional Miramichi tributaries were subjected to eleetrophoretie analysis. Materials and Methods A total of 311 Atlantic salmon parr were sampled "during August 1982 from five locations, representing four tributaries in the Miramichi River drainage. New Brunswiek. Canada (Fig. 1). Specimens from eaeh location were collected along 200 m sections of each stream through eleetrofishing. The size range of fish was from 5.1 to 23 cm, with individuals representing underyearling fry, 1+ parr, and 2+ parr (Riedeil and Leggett 1981). Specimens were placed on wet iee in the field and frozen at -20 o C prior to shipment to Sweden for electrophoretic analysis. Methods of tissue preparation, eleetrophoresis, and staining procedures have been described previously (Utter et al. 1974; Allendorf et a ; Cross and Ward 1980; Grant 1981; Stählt 1981). Three different buffer systems wereused:
4 . 4. I. Described by Ridgway et al. (1970). Gel" buffer: 0.03 M Tris M citric acid. ph 8.5. Electrode buffer: 0.06 M lithium hydroxide t1 borie acid, ph 8.1. Gels were made using 99% gel buffer and 1% electrode buffer. 11. Described by Clayton and Tretiak (1972). Gel buffer: M citric acid ph 6.0. Electrode buffer: 0.04 M citric acid, ph 6.1. The ph of each buffer was adjusted with N-(3-k~inopropyl)-morpholine Described by Markert and Faulhaber (1965). Gel buffer: 1:4 dilution of electrode buffer, ph 8.7. Electrode buffer: 0.18 M Tris M boric acid M EDTA. ph 8.7. Loci are designated using the nomenclature suggested by Allendorf and Utter (1979); when in italics an abbreviation which corresponds to the name of a protein designates each locus. When there are multiple forms of a protein a numeral is included and the locus coding for the least anodally migrating form is designated =1, the next -2, and so on. Allelic variants are designated according to the relative mobility of their products, with one allele (usually the most Common one) designated 100. Allelic products rnigrating cathodally are prefixed with a minus 4It sign. Combinations of tissue, buffer system. and enzyme stained for are given in Table 1. The following 26 enz~nes were examined (abbreviations in parenthesis): aspartate aminotransferase (AAT), aconitase (ACON), adenosine deaminase (ADA), alcohol dehydrogenase (ADH), a-glycerophosphate dehydrogenase (AGP), adenylate kinase (AK), creatine phosphokinas(~ (CPK). diaphorase (DIA). fumarase (FUM), glyceraldehyde-3-phosphatedehydrogenase (GAPDH), glutamate dehydrogenase (GOH),
5 5. glueose-6-phosphate dehydrogenase (G-6-PDH), glutamate pyruvate transaminase (GPT), ß-glueoronidase (GUS), hexokinase (HK), isocitrate dehydroge~ase (loh),. lactate dehydrogenase (LDH), malate dehydrogenase (~roh). ~aiie enzyme (ME), 6-phosphoglueonate dehydrogenase (6-PGDH), phosphoglueose isomerase (PGI), phosphoglueomutase (PGM), phosphomannose isomerase (PMI), sorbitol dehydrogenase (SDH), superoxide dismutase (SOD), xanthine dehydrogenase (XDH). Results and Diseussion All specimens were suecessfully analyzed for 26 enzymes eneoded by at least 42 loci (Table 1). One enzyme, aspartate aminotransferase (AAT), which has been observed polymorphie in Irish and Swedish populations of Atlantie samon (Cross and Ward 1980; StAhl 1981) showed no or too weak activity in the present samples to permitreliable phenotypie elassifieation. This enzyme is stained for in liver tissue and might loose aetivity due to longterm storage. Genetie variation was observed at six loei; LDH-4, MDH-1, MDH-3, ME-2, PGI-1, and SDH-1. In most eases the alleles that were observed in the present study appeared to be the same alleles as have been reported from electrophoretic surveys of Scandinavian populations of Atlantic salmon. A more detailed eomparison of alleles in Euro~ean and North American populations of Atlantic salmon will be presented in a forthcoming paper. For the purpose of the present investi-.. gation, which only deals with Atlantic salmon from Canada, we have adopted the allele and locus designations earli.er reported from Scandinavian samples of Atlantic salmon, cf. Stahl (1981), Ryman and Stähl (1981), Ryman (1983), Stahl (1983). At the LDH-4 locus a variant not earlier reported allele, LDH-4(140), was observed in a low frequency in two of the present sampies, map code Band C. Two supernatant forms of the dimeric enzyme MDH have been described in J
6 6. salmonids; MDH-A (predomina~tly expressed in eye and liver tissue) and MDH-B (predominantly expressed in musele tissue)(bai1ey et a ; Allendorf et al. 1977; May et a ; Cross and Ward 1980; Andersson et < ). The MDH':"A form is eneoded by t~o loei, MDH-1 and -2, in Atlantie salmon. The MDH-l loeus is highly polymorphie in the present samples segregating for two alleles in all but one sample, map eode A. A variant allele, MDH-l(-200), with the same relative eleetrophoretic mobility has been observed among Atlantic salmon from Europe in a very low frequeney and only in two out of 32 populations analyzed (Ryman 1983). The muscle form of MDH (HDH-B) in Atlantic salrnon has previously been suggested to be eneoded by a pair of duplieated loei, MDH-3 and -4, with eommon alleles showing identieal eleetrophoretie mobility (Cross and Ward 1980). In the present samples three alleles were reeognized segregating at this pair of loei eoding for muscle MDH. Although it is impossible to assign an allele to a speeifie locus, i.e. MDH-3 or HDH-4, the suggested alleles were designated MDH-3(75), (100), and (115), respeetively, to correspond to earlier reported observations (Stahl 1981; Ryman and Stahl 1981; Ryman 1983; Stahl 1983). In the present samples only a single copy of the MDH-3(75) allele was observed, sample C. It was impossible to obtain any differences between the three banded phenotypes corresponding to homo- and heterozygotes for the variant MDH-3(115) allele. However, using fresh tissue samples it should be possible to obtain shifts in banding pattern intensity refleeting the dosage effects of one or two.copies of the variant allele eorresponding to the genotype MDH-3(100/115) MDH-4(100/100) as eompared to the genotype MDH-3(115/11S) MDH-4(100/100). At the HE-2 loeus two alleles, 100 and ~, were observed. Alleles with similar relative eleetrophoretic mobility differenees have been reported in samples of Atlantie salmon from Europe (Crossand Ward 1980; Stahl 1981; Ryman and Stahl 19~1; Ryman 1983; Stahl 1983). However, the eommon allele in the Canadian samples is the less eommon one in Europe.
7 7. At the PGI-1 loeus a single eopy of a new allele PGI-1(140) was observed in the sampie from Taxis River (D). At the SDH-l loeus twe> phenotypes were observed eorresponding to two alleles with the same relative eleetrophoretie mobility differenees as have been reported for the Atlantie salmon in Europe (Stähl 1981). As for the HE-2 loeus the eommon allel'e in Canada appears to eörrespond to the less e~mmon one in Europe. The remaining 36 loei were monomorphie in the present study. Allele frequeneies (Table 2) were ealeulated by allele eounting for all loei exeept for MDH-3 and SDH-1 where the frequeney of the 100-allele was eomputed from the square root of the proportion of tod/tod homozygotes. Tests of signifieanee for genetie heterogeneity among sampies at individual loei are presented in Table 2. Among sampies representing different tributaries within the Miramichi River drainage system there is an overall statistically significant allele frequency heterogeneity at one of the six genetically variable loei (MDH-3). At this loeus there is also a statistieally signifieant allele frequeney differenee between sampie A and B <X 2 e = 5.07, P<0.05) representing Atlantie salmon at two loealities whieh are only 10 km apart within the same tributary The total sum of chi-squares over all loei and loealities (X = 51.13, P<O.Ol) is also highly statistieally signifieant and further indieates that the Atlantie salmon is subdivided into genetieally different loeal populations between as weh as within tributaries of the Hiramichi River system. Aeeepting that the phenotypic variation of the museie form of MDH refleets the expression of two alleles at one of a pair of disomic loei, MDH-j and -4, there are no deviations from the expeeted Hardy-Weinberg phenotypic proportion at any loeus in any sampie. The ave:rage amount of genetie variation in terms of
8 average heterozygosity (H = 0.016) and the proportion of polymorphie loei (P = 0.086) over all populations are elose to what has been reported in Seandinavian sampies of Atlantie salmon (Ryman 1983; St5hl 1983). The present estimates from the Hiramichi River are within the range of estimates of the amount of genetic variation reported for other salmonids in North America (Allendorf and Utter 1979). The small average genetic distance (D = ); Nei 1972) between the present Canadian sampies is only about one third of the genetie distance typieally observed among natural populations of Atlantic salmon in Scandinavia (Stähl 1981; Ryman 1983). The genetie distanees among the present samplesare graphieally summarized in a dendrogram. Fig~ 2 (eonstrueted using the UPGMA algorithm; Sneath and Sokal 1973). In spite of the small genetie distanees observed between the populations ln this survey these populations have previously been described to navedir'ferentiated with respect to body shape and migratory behavior (Riddell and Leggett 1981; Riddell et al. 1981). In brown trout (Salmo trutta) significant differenees in growth rates have been reported betljeen sympatrically living populations. However. those populations show a genetie distance (D c 0.025; Ryman et al.1979) which 1s 4It almost30 times greater than the present estimates among Atlantie salmon in the ~tiramichi River. The present results reinforee the eoncept that minor genetie differences may be eoupled with morphologieal eharacteristies of great eeonomical and management importance. These observations stress the importance of a detailed genetic analysis of the population Btructure prior to any management activities. tje are indepted to Drs. Nils Ryman and Olof Leimar for helpful comments on the paper. Thc invcstigation was supported by grants from The National Swedish Environment Protcction Board and the Swedish Natural Science R~search Council.
9 ". 9. RefHrences Allendorf. F.W. and F.M. Utter Population genetics. p In: W.S. Hoar. D.J. Randall. emd J.R. Brett (eds.) Fi.sh Physiology. Vol. 8. Academic Press. New York. Allendorf. F.W. N. Mitehell. N. Ryman. and G. Stähl Isozyme loci in brown trout (Salmo salar L.): detection and interpretation from e' population data. Hereditas 86: Andersson. L N. Ryman. and G. Stähle Protein loci in the Aretie char (Salvelinus aplinus L.): Electrophoretic expression and genetic variability patterns. J. Fish Biology (in press). Bailey. G.S A.C. Wilson. J. Halver. and C.L. Johnson Multiple forms of supernatant malate de!hydrogenase in salmonid fishes.. J. Bio!. Chem. 245: Clayton. J.W. and D.N. Tretiak Amine-citrate bufferfor pr control in starch gel electrophoresis. J. Fisheries Res. Board Can. 29: Cross. T.F. and R.D. Ward Protein variation and duplieate loci in the Atlantic salmon. Salmo sal~ L. Genet. Res. 36: Grant. S Biochemical genetie variation. population structures. and evolution of Atlantic and Pacific herring. Ph.D. thesis. Univ. Washington. Seattle. USA.
10 10~ Markert, C.L. and I. Faulhaber Lactate dehydrogenease isozyme patterns of fish. J. Exp. Zool. 159: May, B., J.E. Wright, and M. Stoneking Joint segregation of bioehemieal laei in Salmonidae; Results from experiments with Salvelinus and review of the litterature on other species. J. Fish. Res. Board Can. 36: Nei, ~ Genetic distance bl~tween populations. The Ameriean Naturalist 106: Riddell, B.E. and W.L. Leggett Evidenee of an adaptive basis for geographie variation in body morphology and time of downstream migration of juvenile Atlantie salmen (Salloo salar). Can. J. Fish. Aquat. Sei. 38: Riddell, B.E., W.C. Leggett, and R.L. Saunders Evidenee of adaptive polygenie variation between two populations of Atlantie salmon (Salme salar) native to tributaries of the S.W. Miramichi River, N.B. Can. J. Fish. Aquat. Sei. 38: Ridgway, G.J., S.W. Sherburne, and R.D. Lewis Polymorphisms ln esterases of Atlantic herring. Trans. Am. Fisheries Soe. 99: Ryman, N~ Patterns of distribution of biochemical genetie,variation in salmonids: differences between species. Aquaculture (in press). Ryman, N. and G. Stähl Genetic perspeetives of the identifieation and conservation of Scandinavian stocks of fish. Can. J. Fish. Aquat. Sei. 38:
11 11. Ryman, N. F.W. Allendorf. and G. Stähl Reproduetive isolation with little genetie divergenee in sympatrie populations of brown trout (Salmo trutta). Geneties 92: Sneath. P.H.A. and R.R. Sokal Numerieal taxonomy. 573 pp. W.H. Freeman and Co. San Fransiseo. Stählt G Genetie differentiation among natural populations of Atlantie salmon (Salmo salar) in northern Sweden. In: N. Ryman (ed.) Fish Gene Pools. Ecol. Bull. (Stoekholm) 34: Utter. F.M. H.O. Hodgins. and F.W. Allendorf Bioehemieal genetie studies of fishes: Potentialities and limitations. In: D.C. Malins and J.R. Sargent (eds.) Bioehemieal and Biophysieal Perspeetives in Marine Biology. pp Academie Press. New York.
12 12... Table 1. Combination of buffer system and tissue u~ed for scoring a totalof 42 loci. Descriptions of buffer systems are given in the iext. Buffer system MuseIe Liver Eye I AGP-l,2 DIA CPK-3 CPK-l GVS GAPDH-2 LDH-l.2,J,4 HK-l G-6-PDH PGI-l.2 6-PGDH-2 LDH-5 PGM-l,2 SDH-l.2' SOD XDH --- Il AK-3 ACON FVM ADH IDH-l GDH ME-l,2,3 IDH-2,3 MDH-3,4 MDH-l,2 6-PGDH-l III ADA GPT PMI
13 Table 2. Allele frequeneies at six genetieally variable loei in five sampies of Atlantie salmon from the Miramichi River, Canada, colleeted in the fall Estimates of the proportion of polymorphie loei ( P; 0.99 eriterion) and average heterozygosity (H) were based on a total of 42 loei. The eontingeney chi-squares for hornogeneity between samples (df=4) at eaeh loeus have been based on the numberof alleles for all loei exeept for MDH-3 and SDH-l where the numberof fish of eaeh phenotype have been eompared. io'~* means P<O.OOl and n is the nurnber of individuals. Map LDH-4 MDH-l MDH-3 ME-2 PGI-l SDH-1 code Locality n öO 1öö :so P H -- A Silliker's Bridge B Mouth of Otter Brook C Rocky Brook D Taxis River E Sabbies River X 2 *** =
14 '... Miramichi Rlver System J ~------_ _._ Figure 1. Map of Miramichi River system (New Brunswick, Canada) showing four- tributaries from which samp1es were co11ected for e1ectrophoretic study. GENETIC DISTANCE (Nei ) I I I J o B o c E A otter Brook Taxis River Rocky Brook Sabbies River Silliker's Bridge Figure 2. Dendrogram summar1z1ng the genetic relationships among populations of Atlantic salmon in the Miramichi River. Genetic distances were based on the allele frequency distributions at 42 loci
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