Heterozygosity and morphological variability of pink ...

Heterozygosity and morphological variability of pink salmon (Oncorhynchus gorbuscha) from southern British Columbia and Puget Sound TERRY D. BEACHAMA N D RUTH E. WITHLER Department of Fisheries and Oceans, Fisheries Re.searc.h Branc.h, P(ic.iJi'c.Biolo,qic.ul St~ltion,Nanaimo, B.C., C ~ n u d uV9R 5K6 Can. J. Genet. Cytol. Downloaded from www.nrcresearchpress.com by Fisheries and Oceans on 08/14/15 For personal use only.

Corresponding Editor: A. J . F. Griffiths Received February 5. 1985 Accepted May 2 1 . 1985 BEACHAM, T. D., and R. E. WITHLER.1985. Heterozygosity and morphological variability of pink salmon (0nc.orhynchus gorbuscha) from southern British Columbia and Puget Sound. Can. J . Genet. Cytol. 27: 571 -579. We compared variability in gill raker number and four morphometric characters with heterozygosity at enzymatic loci within and among populations of pink salmon (Onc-orhynchusgorhu.sc.ha) in southern British Columbia and Puget Sound. Among individuals. there was no relationship between levels of heterozygosity at eight electrophoretic loci and degree of meristic or morphometric variation. Decreased phenotypic variance was not associated with increased heterozygosity. Among populations of pink salmon, increased levels of average heterozygosity were not associated with decreased phenotypic variation. Our results do not support the hypothesis that more heterozygous individuals are less phenotypically variable than more homozygous ones as a result of genetic homeostasis and a canalisation of morphology during development. Genetic distances between pairs of pink populations were significantly correlated with pairwise Mahalanobis distances derived from meristic characters (gill rakers) and less strongly correlated with distances derived from morphometric characters. Pink salmon are morphometrically adapted to the natal stream environment. whereas biochemical and meristic characters in these populations may be less affected differentially by local selective forces. Key words: salmon, electromorphs, homeostasis. genetic variability. heterozygosity. BEACHAM,T. D., et R. E. WITHLER.1985. Heterozygosity and morphological variability of pink salmon (One-orhynchus gorbuscha) from southern British Columbia and Puget Sound. Can. J . Genet. Cytol . 27: 57 1 - 579. Nous avons compare la variabilitd du nombre de peignes branchiaux et quatre traits morphomCtriques avec I'hCtCrozygositC sur des loci enzymatiques chez des populations de saumon a bosse (0nc.orhync.hu.s gorhu.sc.hcr) dans le sud de la Colombie britannique et a Puget Sound. Chez les individus on n'a pas trouvC de relation entre les niveaux d'hCtCrozygositC sur huit loci ClectrophorCtiques et le degrC de variation mCristique ou morphomCtrique. I1 n'y avait pas d'association entre la diminution de la variance phCnotypique et I'augmentation de I'hCtCrozygositC. Parmi les populations de saumon ri bosse, les niveaux plus ClevCs d'hCtCrozygositC moyenne ne corrklaient pas avec une diminution de la variation phCnotypique. Nos rCsultats ne supportent pas I'hypothese que les individus plus fortement hCtCrozygotes sont moins sujets a la variation phCnotypique que les individus plus fortement homozygotes a cause de I'homCostasie gCnCtique et d'une canalisation de la morphologie au cours du dCveloppement. Les distances gCnCtiques entre paires de populations de saumon i bosse Ctaient corrC1Ces significativement avec les distances de Mahalanobis par paires obtenues de traits miristiques (les peignes branchiaux) et moins fortement corrCICes avec les distances obtenues de traits morphomCtriques. Le saumon a bosse est morphomCtriquement adapt6 a I'environnement du cours d'eau ou il a vu le jour alors que les traits biochimiques et mCristiques chez ces populations sont peut-etre moins affect& diffCrentiellement par les forces de sClection locales. Mots clPs: saumon, Clectromorphes, homCostasie. variabilitC g6nCtique. hCtCrozygosit6. [Traduit par le journal]

Introduction The relationship between genetic and phenotypic variability has been a topic of interest for several decades. Lerner (1954) suggested that in animals decreased morphological variability is associated with increased heterozygosity. This general hypothesis is based on the suggestion that the increased genetic variance within heterozygotes may increase their genetic homeostasis, i.e., the ability to buffer the effects of environmental variability on morphological development and growth rate. More specifically, individuals heterozygous at a single or many loci may be better able than homozygotes to maintain near optimal levels of

enzyme activity under varying environmental conditions (Koehn 1970; Johnson 1977) and throughout a succession of developmental stages which impose varying enzymatic demands (Mitton and Grant 1984). However, Chakraborty and Ryman (1983) have shown for phenotypic traits with large components of additive genetic variance that decreased phenotypic variance may be associated with increased genomic heterozygosity as a result of the decreased genetic variance among highly heterozygous individuals. The decreased levels of genetic variation among heterozygotes do not, however, account for the decreased levels of phenotypic variation observed within individuals (as mea-

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sured by asymmetry in bilateral traits) or for the increased growth rates that are often associated with increased heterozygosity. Mitton and Grant ( 1984.) have reviewed extensive experimental results obtained from a wide range of organisms that suggest, regardless of the mechanism, that the degree of heterozygosity of individuals and of populations is related both to morphological variation and to growth rate. Morphological variance has been shown to be inversely related to heterozygosity for a number of invertebrate (Eanes 1978; Kat 1982) and vertebrate species (Soule 1979; Fleischer et al. 1983). In fishes, increased levels of heterozygosity are associated with decreased morphological variance among individuals of a poeciliid, Poeciliopsis lucida (Angus and Schultz 1983), of killifish, Fundulus heteroclitus (Mitton 1978), and of Poecilia reticulata (Beardmore and Shami 1979). However, morphological variation among individuals has been found to be unrelated to heterozygosity in the plaice, Pleuronectes platessa (McAndrew et al. 1982), the crested blenny, Anoplarchus purpurescens (Yoshiyama and Sassaman 1983), the Atlantic herring, Clupea harengus (Ryman et al. I984), and the chum salmon, Oncorhynchus keta (Beacham and Withler 1985). A high degree of heterozygosity was associated with decreased variation within individuals, as measured by asymmetry, among rainbow trout, Salmo gairdneri (Leary et al. 1983) and populations of Poeciliopsis monacha (Vrijenhoek and Lerman 1982). Growth rate has been positively correlated with heterozygosity in invertebrates (Zouros et al. 1980; Fujio 1982), vertebrates (Pierce and Mitton 1982; Johns et al. 1977; Makaveev et al. 1978), and plants (Mitton and Grant 1980; Ledig et al. 1983). In some coniferous species, increased heterozygosity was not associated with increased growth rate, but with a decreased variance in growth rate (Mitton 1983). In the present study, we have compared enzymatic variability with morphological variance and growth rates among individuals and populations of pink salmon (Oncorhynchus gorbuscha) in southern British Columbia. We also examined the relationship between biochemical and morphological divergence among populations by comparing genetic distance with Mahalanobis distances for morphometric and meristic traits.

Materials and Methods Pink salmon were sampled on the spawning grounds from four rivers in 1982 and 20 rivers in 1983 (Fig. 1 ). Pink salmon from three rivers (Glendale, Quinsam, and Puntledge) were sampled in both 1982 and 1983. All samples were taken during the latter portion of the spawning period when all individuals were fully mature. Salmon were collected either with beach seines or by sampling fresh dead fish. One hundred fish were usually sampled from each river, although 200

fish were sampled from the Fraser River and four of its tributaries. Exact sample sizes for each stock were outlined by Beacham ( 1985). The only meristic character recorded was the number of gill rakers on the left anterior gill arch. Morphometric characters recorded were postorbital-hypural length (Vladykov 1962), postorbital head length (Vladykov 1962). caudal peduncle depth, and length of the base of anal and dorsal fins (Hubbs and Lagler 1958). All meristic and morphometric measurements were recorded in the field. All morphometric characters were measured to the nearest millimetre with either a hypural stick (postorbital-hypural length) or calipers (other morphometric characters). The sex of each individual was confirmed by internal inspection. We used horizontal starch gel electrophoresis following Utter et al. (1974) to determine the genotype of individuals at five single and three pairs of duplicated loci. It was not possible to assign allelic variation to individual loci of a duplicate pair. We considered each pair of duplicated loci as a single locus in our analysis, and at these loci any individual possessing two or more different alleles was considered a heterozygote. Loci scored from muscle were as follows: malate dehydrogenase (Mdh-3,4), malic enzyme (Me), 6-phosphogluconate dehydrogenase (6-Pg), alphaglycerophosphate dehydrogenase (Agp), phosphoglucomutase (Pgm), and phosphoglucoisomerase (Pgi-l,2). Aspartate aminotransferase (Aat) was scored from the eye and Mdh-l,2 was scored from the liver. Preliminary analysis indicated that there were significantly different allometric growth regressions (log, character length = log, a + b log, body length) for each morphometric measurement. All such measurements were standardized for each individual to the overall mean postorbital-hypural length of all spawning ground samples (419 mm) by the method outlined by Ihssen et al. (198 1). The standardization of all morphometric measurements to the length of the overall sample mean minimizes variability resulting from allometric growth and differences in mean size of individuals among stocks (Gould 1966; Thorpe 1 976). We conducted analyses of variance to determine if the means of the phenotypic characters differed among populations, between sexes, and between individuals homozygous and heterozygous at each locus. The model used for the analysis was

where Y;,k/ is the observed phenotypic character; p is the mean; A, is the effect of the ith population (i = 1.24); S, is the effect of sex ( j = 1,2), Hk is the effect of heterozygosity (k = 1,2) (homozygous or heterozygous);ASl,, AHih,SHjk,and ASHijkare the interactions among the main effects; and e,,klis the error term of the lth observation in subgroup ijk. Pink salmon are anadromous and return from the ocean to spawn and die in their natal stream at 2 years of age (Bilton and Ricker 1965; Aspinwall 1974). As pink salmon in the Pacific Ocean mature at 2 years of age, body length is an estimate of growth rate. We examined whether or not homozygous fish (those homozygous at all loci) matured at different sizes than heterozygous fish (those heterozygous at one or more loci) by using Eq. I outlined previously for each brood

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FIG. 1. Locations of pink salmon stocks sampled during 1982 and 1983. Listed in ascending order are ( 1 ) Thompson R., (2) Portage Cr., (3) Seton Cr., (4) Coquihalla R., (5) Jones Cr., ( 6 )Fraser R.. (7) Harrison R., (8) Vedder R., (9) Skagit R., (10) Stillaguamish R., (I I) Snohomish R., ( 12) Puntledge R., (13) Quinsam R . , ( 14) Adam R., ( 15) Cluxewe R., ( 16) Keogh R., (17) Indian R., (18) Phillips R., (19) Glendale R . , (20) Kakweiken R . , and (21) Wakeman R. line separately. We estimated the within-stock variance of each phenotypic character and of body length for homozygous and heterozygous individuals at each locus separately. Variance was estimated as the residual mean square for the linear model incorporating population and sex as the main effects, along with their interaction: [2]

Y,, = p

+ A, + SJ + AS, + e,,~

with the variables defined as in Eq. 1. If two groups of observations have the same population mean but different variances, the average distance between an individual and the population mean must differ between the two groups. We calculated Mahalanobis distance (d) (Kendall 1975) between each individual and its own stock and sex centroid for the meristic and morphometric variables. Analyses of variance were then conducted to determine if mean Mahalanobis distance differed among fish homozygous or heterozygous at each locus or if it varied among fish with

different numbers of heterozygous loci. Preliminary analyses using Eq. I indicated that there were no significant stock or sex effects for Mahalanobis distance, so the model used was [3]

Y, = p

+ H, + e,

where Y,, is the Mahalanobis distance, p is the mean, H, is the effect of number of heterozygous loci ( i = 0,5), and el, is the residual variance. We compared variability in morphometric and meristic characters among populations with heterozygosity by comparing the mean coefficient of variation for each set of characters averaged over all characters in the set with mean heterozygosity. We used the original unstandardized morphometric measurements in the analysis of the coefficients of variation. The morphometric characters measured have been previously shown to be sexually dimorphic in pink salmon (Beacham 1985) and thus males and females were analyzed separately. There was no sexual dimorphism in the meristic character

CAN. J . GENET. CYTOL. VOL. 27, 1985

TABLE1 . Within-stock variances of gill rakers and four morphometric characters for homozygous (homo) and heterozygous (hetero) pink salmon at eight loci

Locus


Me Mdh-1,2 Mdh-3,4

Pgm 6-Pg Pgi-I ,2 Aat A ~ P

State

N

Gill rakers

Head length

Caudal peduncle depth

Anal fin base

Dorsal fin base

Homo Hetero F Homo Hetero F Homo Hetero F Homo Hetero F Homo Hetero F Homo Hetero F Homo Hetero F Homo Hetero F

counted and thus sexes were combined in this analysis. We calculated genetic distances between pairs of populations by the method of Nei (1978). We then compared genetic distance between all pairwise combinations of populations with Mahalanobis distance based upon all morphometric characters (sexes separate, standardized measurements) and gill raker number (sexes combined).

Results Individual variability If pink salmon homozygous at a given locus have the same mean but greater variance for any phenotypic character than heterozygous individuals, then the average Mahalanobis distance from the individual's phenotypic characters to the population centroid will be greater for homozygotes than for heterozygotes. We first determined if homozygous and heterozygous fish for each locus had the same mean values for each phenotypic character. Of 40 (8 loci by 5 characters) analyses of variance conducted (Eq. I), two (5.0%) were statistically significant ( P < 0.05), about the level expected by chance. Homozygous and heterozygous pink salmon have the same mean value for the five phenotypic characters investigated. We next tested the hypothesis that homozygous and

heterozygous fish at each locus had equal variance for the individual meristic and morphometric characters investigated. Of the 40 comparisons of within-stock variance (Eq. 2), the F-statistic was < 1.00 in 19 cases, equal to 1.00 in 1 case, and > I .OO in 20 cases (Table 1). Homozygous and heterozygous pink salmon have similar phenotypic variability when compared on a locus by locus and character by character basis. We used Mahalanobis distance to compare the variability in gill raker number and the combined phenotypic variance of the four morphometric characters in pink salmon homozygous and heterozygous at each of the eight loci investigated. When the loci were considered separately, variability in the meristic character (number of gill rakers) was similar for homozygous and heterozygous pink salmon (Table 2) (F-values range from 0.09 to 2.24, all P > 0.10). Variability of the morphometric characters combined was similar for homozygous and heterozygous pink salmon for all loci except Me (Table 2). At this locus, heterozygous pink salmon were less variable than homozygous ones for the combined morphometric characters ( F = 4.82; df = 1, 2776; P < 0.05) and for all traits when gill raker number was included in the analysis (F = 4.35; df = 1, 2776; P < 0.05).

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TABLE2. Mean Mahalanobis distance from population centroid for pink salmon homozygous and heterozygous at eight loci. Five phenotypic characters (one meristic, four morphometric) were included in the determination of Mahalanobis distance. Standard deviations are in parentheses Gill rakers


Locus

Me Mdh-1,2 Mdh-3,4 Pgm 6-Pg Pgi-1,2 Aat A ~ P

N

Homozygous

2703 2736 2623 2076 2008 254 1 1852 2327

1.08(0.84) 1.09(0.84) 1.08(0.84) 1 . I O(0.86) 1.08(0.85) 1.09(0.85) 1.09(0.84) 1.09(0.84)

N

Morphometrics

Heterozygous

Homozygous

Heterozygous

All characters Homozygous

Heterozygous

TABLE3. Mean Mahalanobis distance from population centroid for pink salmon with different numbers of heterozygous loci for four morphometric and five characters in total. Standard deviations are in parentheses. N is sample size Morphometrics No. of heterozygous loci

N

Gill rakers

Head length

Caudal peduncle depth

Finally, we used Mahalanobis distances to compare the mean levels of variability for meristic and morphometric characters among pink salmon with different numbers of heterozygous loci (Eq. 3). Pink salmon with more heterozygous loci were not less variable phenotypically than more homozygous pink salmon (Table 3) (F-values range from 0.35 to 1.11; df = 5, 2788; P > 0.05). We found no evidence for a relationship between heterozygosity at individual or multiple loci (except Me) and the degree of phenotypic variability for the pink salmon examined in this study. Population variability Aat was not scored in the 1982 Puntledge River sample, and this stock was not included in the comparison of average heterozygosity with phenotypic variation by population. Populations that had higher levels of heterozygosity had greater phenotypic variability for gill raker number ( r = 0.58, df = 21, P < 0.05) (Fig. 2), but not for the combined morphometric characters in either males ( r = 0.07, P > 0.10) or females ( r = 0.3 1, P > 0.10). Morphometric characters, with coefficients of variation generally greater than 6%, were more variable than the gill raker count, with coef-

Anal fin base

Dorsal fin base

All morphometrics

All characters

ficients of variation generally less than 6%. Genetic distances determined from the electrophoretic data (Nei 1978) between all pairwise combinations of populations were compared with pairwise Mahalanobis distances calculated using the meristic or the four morphometric characters. There was a significant positive relationship between genetic distance and Mahalanobis distance among populations for gill rakers ( r = 0.74, df = 251, P < 0.01) (Fig. 3) and for the morphometric characters of males ( r = 0.27, df = 25 1 , P < 0.01) (Fig. 4) and females ( r = 0.51, df = 251, P < 0.01) (Fig. 5). Patterns of variability among populations in gill raker number were more similar to the genetic differences among the populations than was variability in the morphometric characters. Growth Body length in pink salmon is an estimate of growth rate, and after stock and sex differences had been accounted for (Eq. 1 ), homozygous and heterozygous individuals matured at similar lengths in both the evenyear (F = 2.40, P > 0.05) and odd-year (F = 2.82, P > 0.05) brood lines. Thus, no differences in growth rates to adult size were detected between homozygous

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576

31 0.090

I

0.100

I

I

0.110 0.120 HETEROZYGOSITY

1

0.130

1

0.140

FIG.2. Relationship between the coefficient of variation (CV) for gill raker number and average heterozygosity at enzymatic loci among populations of pink salmon in southern British Columbia and Puget Sound ( r = 0.58, P < 0.05). and heterozygous fish. The within-stock variances of growth rates (Eq. 2) of heterozygous fish were less than those of homozygous ones in both the even-year (740.5 vs. 858.8) and odd-year brood lines (624.9 vs. 674.4), but the differences were not significant (both F < 1 .16, P > 0.05).

Discussion No relationship between phenotypic variability and heterozygosity for individual pink salmon in our study was found. There was no reduction in phenotypic variance that could be attributed to genetic homeostasis or to reduced genetic variance (Chakraborty and Ryman 1983) among pink salmon with comparatively more heterozygous loci. Heterozygotes were not larger at maturity (2 years of age) than homozygotes, and there was only a weak indication that the variance in size of heterozygotes was less than that in homozygotes. The absence of a relationship between morphological variability and heterozygosity for individuals is not surprising in view of our small sample of the thousands of loci that constitute the pink salmon genome. Phenotypic variance may be strongly affected by regulatory loci that control gene expression and exert a strong influence upon morphology by affecting development (Johnson 1977; Wilson 1977). Levels of heterozygosity over the entire genome may affect phenotypic vari-

FIG.3. Mahalanobis distance (based on gill rakers) versus genetic distance for pink salmon in sou them British Columbia and Puget Sound ( r = 0.74, P < 0.01). ability for many traits less than the level of heterozygosity at a relatively few, but important, loci that control gene expression. Allelic variation at the Pgrnl-t regulatory locus in another salmonid species, the rainbow trout (Salmo gairdneri), has been shown to influence developmental rate, meristic symmetry, and age of maturity (Allendorf et al. 1983). Moreover, rainbow trout of differing Pgml-t genotypes also differed in eight meristic characters, presumably as a result of the inlluence of Pgml-t on development rate (Leary et al. 1984). However, in spite of this demonstration of the effects that may be associated with variation at a single regulatory locus, Leary et al. (1983) also found that average heterozygosity over 42 structural (enzyme) loci was associated with greater developmental stability, as measured by meristic symmetry among individual rainbow trout from a single population. The rainbow trout results are consistent with the finding for numerous organisms that the level of heterozygosity at loci coding for catabolic enzymes is associated with the degree of morphological variation within and among individuals. However, McAndrew et al. (1982) reported no relationship between levels of heterozygosity and morphological variability among individual plaice (P1euronec.te.s platessu). There was no


BEACHAM AND WITHLER

F I G . 4. Mahalanobis distance (based on morphometric characters) versus genetic distance for male pink salmon populations in southern British Columbia and Puget Sound (r = 0.27, P < 0.01).

F I G . 5 . Mahalanobis distance (based on morphometric characters) versus genetic distance for female pink salmon populations in southern British Columbia and Puget Sound ( r = 0 . 5 1 , P < 0.01).

strong evidence for the action of stabilizing selection on plaice morphology over the age-groups examined, and the authors suggested that an association between heterozygosity and morphological variance may be more likely apparent when selection can be shown to be operating on phenotypic characters. Soule (1982) suggested that the relationship between heterozygosity and developmental stability may not be apparent in phenotypic characters with strong canalization or large coefficients of variation. Mitton and Grant (1984) have suggested that this hypothesis may explain the lack of correlation between heterozygosity and variability in fin ray numbers in plaice. It may also account for the negative results reported for individual chum salmon (Beacham and Withler 1985) and for pink salmon in this study. Among pink salmon populations, variability of gill rakers increased in more heterozygous populations. This increase in meristic variability may indicate that variability at electrophoretic loci is an index of variability over the entire genome. The increased phenotypic variability in more heterozygous populations could be due to increased additive genetic variation at loci which determine meristic traits. If average heterozygosity is related to effective population size in pink salmon as it appears to be in chum

salmon (Kijima and Fujio 1984), the positive correlation between biochemical and meristic variation may simply result from decreased genetic drift, and therefore increased genetic variance, in populations with large effective sizes. Bryant (1984) attributed a correlation between levels of biochemical and morphological variability in the face fly (Musca autumnalis) to genetic drift during a population bottleneck. We found a significant correlation between pairwise genetic distance and pairwise Mahalanobis distance based on meristic and morphometric characters for the pink salmon populations surveyed in this study. In a survey of electrophoretic, meristic, and morphometric characters in lake whitefish Coregonus clupeaformiu, Ihssen et al. (1981) also found a positive correlation between meristic divergence (Mahalanobis distance) and electrophoretic divergence (genetic distance). The morphometric characters surveyed in our study have previously been shown to be adapted to environmental conditions that the returning adult pink salmon encounter in their natal streams (Beacham 1985). The correlation between genetic distance and Mahalanobis distance based on gill raker number was greater than that based on morphometric characters. This is consistent with the finding that electrophoretic and meristic vari-

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ation in pink salmon was greater between genetically isolated brood lines than among populations within each brood line, whereas morphological variation was greater within than between brood lines (Beacham 1985). In pink salmon, allelic frequencies and meristic frequencies may be less affected by differential selection among habitats than morphometric characters.

Acknowledgments The field sampling undertaken for this study would not have been possible without the assistance of many people. Among those involved were Terry Calvin. Al Gould, Clyde Murray, Alvin Sewid, and Alf Stefanson. Dr. James Woodey of the International Pacific Salmon Fisheries Commission supervised most of the collections of the Fraser River stocks. Mr. Jim Ames and Harry McBride of the Washington Department of Fisheries supervised the collections of the Puget Sound stocks. The electrophoretic analysis was conducted by Helix Biotech Ltd. of Richmond, British Columbia, under contract to the Department of Fisheries and Oceans. Two referees suggested significant improvements to the manuscript. ALLENDORF, F. W., K. 1, KNIJDSEN. and R. F. LEARY. 1983. Adaptive significance of differences in the tissue-specific expression of a phosphogluco-mutase gene in rainbow trout. Proc. Natl. Acad. Sci. U.S. A. 80: 1397- 1400. ANGUS,R. A.. and R. J. SCHULTZ. 1983. Meristic variation in homozygous and heterozygous fish. Copeia. 1983(2): 287 - 299. ASPINWALL, N. 1974. Genetic analysis of North American populations of the pink salmon. Oncor hync.hus ,gorbusc.hn, possible evidence for the neutral mutation - random drift hypothesis. Evolution (Lawrence, Kansas), 28: 295 - 305. BEACHAM, T. D. 1985. Meristic and morphornetric variation in pink salmon (Ont.orh!~nchus gorbusc.hn) in southern British Columbia and Puget Sound. Can. J. Zool. 63: 366-372. BEACHAM. T. D., and R. E. WITHLER. 1985. Hetero~ygosity and morphological variability of chum salmon (0nc.orhvnchus keta) in southern British Columb~a.Heredity. 54: 313-322. BEARDMORE, J. A , and S. A. SHAMI.1979. Hetero~ygosity and the optimum phenotype under stabilizing selection. Aquilo Ser. Zool. 10: 100- 1 10. BILTON,H. T., and W. E. RICKER.1965. Supplementary checks on the scales of pink salmon (0ncorhynchu.s gorbuscha) and chum salmon ( 0 . keta). J. Fish. Res. Board Can. 22: 1477- 1489. BRYANT,E. H. 1984. A cornparlson of electrophoretic and morphometric variability in the face fly, Micscn nuturnnalis. Evolution (Lawrence, Kansas), 38: 455-458. CHAKRABORTY, R., and N. RYMAN.1983. Relationship of mean and variance of genotypic values with heterozygosity per individual in a natural population. Genetics, 103: 149- 152. EANES,W. F. 1978. Morphological variance and enzyme

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