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Variabilidad genetica en poblaciones chilenas de trucha arcoiris, Oncorhynchus mykiss.

Genetic diversity in Chilean populations of rainbow trout, Oncorhynchus mykiss

INTRODUCTION

The native distribution range of the rainbow trout Oncorhynchus mykiss (Walbaum, 1792), extends along the North American Pacific coast and the rivers that drain into it, from Alaska to the north of Mexico (MacCrimmon, 1971), and was introduced to the rest of the world from this zone (MacCrimmon, 1971; Hershberger, 1992; Crawford & Muir, 2008). In Europe, the rainbow trout was introduced at the end of the 19th century from an original stock from the McCloud River in Baird, California (Hershberger, 1992). Study of these populations has led to greater understanding of the effects of introductions and later translocations on their genetic diversity, as well as their offspring in captivity. Studies of allozymes in introduced or domesticated populations have revealed genetic differences between strains, showing fixation of alleles in normally polymorphic loci in wild populations and reduction in levels of heterozygosity (Currens et al., 1990). These changes are usually interpreted as reflecting the occurrence of the founder effect and genetic drift, both processes directly related with the effective population sizes (Quinn et al., 1996; 1998; Winkler et al., 1999). On the other hand, the historical isolation between different introduced stocks enables the observance of adaptive divergences between them (Moritz, 1999).

In Chile, the rainbow trout was originally introduced from Hamburg, Germany, between 1905 and 1910 (Hershberger, 1992; Soto et al., 2001, 2006; Crawford & Muir, 2008). Reproduction of these stocks was initially done in Blanco River (Los Andes; 32[degrees]55'S, 70[degrees]16'W) and later in Cautin River (Lautaro; 38[degrees]31'S, 72[degrees]27'W). From these stocks, young fish were seeded in central and southern rivers of the country, where wild populations were established in various bodies of water (Gosluda, 1927; Mann, 1954; Campos, 1970). Several varieties of rainbow trout from different origins have been imported for commercial purposes and have been released into water bodies deliberately or accidentally (Uribe, 1988; Mardones & Vega, 1993). Among the commercial strains introduced in Chile, one was recorded as being from Sulfur Spring River (North Carolina, USA), referred to locally as the "American" strain, as well as the Donaldson (Donaldson & Olsen, 1957); Cofradex, a variety developed in Denmark; Steelhead from the McCloud River (California, USA) and Kamloops from Kooteney Lake (British Columbia, Canada) (Colihueque et al., 2001). In Chile there is little information on the origin or lineage of populations spread in natural environments or their variability and genetic structure. Information is limited to cytogenetic studies of cultivated strains that indicate chromosomal heterogeneity (Colihueque et al., 2001), and allozyme variability analysis in three populations naturalized in the south of the country, showing levels of genetic diversity similar to trout in its native range of distribution (Gajardo et al., 1998). This species, along with other salmonid species, is naturalized in rivers and streams throughout the country, establishing itself as an important species for sport fishing and farming (Gajardo et al., 1998).

In Chile, the restocking and spreading of strains in wild environments and the policies followed to do this have not been accurately documented. Thus, the implementation of monitoring of genetic diversity of these wild and farmed populations is relevant given their influence on the fauna of local populations in the wild and the possibility of improving breeding (Gajardo et al., 1998; Farrington et al., 2004). In this context, the present study analyzed the genetic diversity of naturalized rainbow trout populations in two river basins in central-northern Chile, as well as six commercial strains introduced for cultivation.

MATERIALS AND METHODS

Sample collection

Elqui and Limari rivers are two main river basins located in a semi-arid climate in northern Chile, characterized by scarce rainfall and large inputs of water from snowmelts. River flows fluctuate dramatically depending on season and heavy rainfalls associated with the periodic occurrence of the El Nino event (Vila et al, 1999).

Sampling areas are shown in Fig. 1. Two populations were collected between September, 1994 and May, 1995 from La Laguna (30[degrees]02'S, 70[degrees]05'W) and Incaguas (29[degrees]30'S, 70[degrees]26'W) rivers, both belonging to the north-eastern branch of the Elqui River basin, and another sample from Claro River (30[degrees]02'S, 70[degrees]30'W), belonging to the south-eastern tributary of the Elqui River. Samples from Claro River were collected in late September, 1994 (one sample-RCL1) and in late May, 1995 (two samples-RCL2 and RCL3). Samples from the Limari River basin were collected in May, 1996, one from Hurtado River (30[degrees]17'S, 70[degrees]42'W) and another from Grande River (30[degrees]55'S, 70[degrees]46'W). Fishes were collected using electric fishing. The Donaldson, Cofradex and Steelhead strains were provided by the Lautaro fish farm, Lautaro (38[degrees]31'S, 72[degrees]26'W); the American and Scottish strains were provided by the Blanco River farm (32[degrees]55'S, 70[degrees]16'W) and the Kamloops strain was provided by a fish farm in the Macul stream (Santiago; 33[degrees]30'S, 70[degrees]30'W). Specimens were frozen in the field using dry ice or liquid nitrogen, and subsequently stored at -20[degrees]C until analysis. For data analysis, samples from La Laguna and Incaguas rivers were grouped and treated as from the same geographical origin. The same procedure was followed with samples from Claro River taking into account the geographical proximity and the absence of obvious barriers to migration between the sampling places.

Sample analysis

Muscle and liver tissue samples were obtained from each specimen. Each sample was homogenized in a grinding buffer (0.001M EDTA 2Na, 0.01M Tris). Electrophoresis was carried out on horizontal 10% starch gel following the general procedures described by Aebersold et al. (1987) and Hillis & Moritz (1990). The buffers and the 20 enzyme systems analyzed were; 1) Clayton & Tretiak (1972) buffer: Aspartate amino transferase (AAT; 2.6.1.1), Aconitate hydratase (ACO; 4.2.1.3), Malic enzyme (ME; 1.1.1.40), Glycerol-3phosphate dehydrogenase (G3PDH; 1.1.1.8), Isocitrate dehydrogenase (IDH; 1.1.1.42), Malate dehydrogenase (MDH; 1.1.1.37), Glucose-6-phosphate dehydrogenase (6PGD; 1.1.1.49), Phosphoglucomutase (PGM; 5.4. 2.2) and Superoxide dismutase (SOD; 1.15.1.1); and 2) Ridgway et al. (1970) buffer: Alcohol dehydrogenase (ADH; 1.1.1.1), Adenylate kinase (AK; 2.7.4.3), Creatine kinase (CK; 2.7.3.2), Diaphorase (DIA; 1.6.2.2) , Esterase (EST; 3.1.1.*), Glicerato dehidrogenasa (GLYDH; 1.1.1.29), Glucose-6-phosphate isomerase (GPI; 5.3.1.9), L-Iditol dehydrogenase (sIDDH; 1.1.1.14), Lactate dehydrogenase (LDH; 1.1.1.27), Transferrine (TF) and Xanthine dehydrogenase (XDH; 1.2.1.37).

Data analysis

Duplicate loci ([IDH-3,4.sup.*] and [MDH-3,4.sup.*]) were treated as two disomic loci with identical allele frequencies because allele variation could not be assigned to a specific locus (Allendorf & Thorgaard, 1984), although this treatment tends to give conservative estimates of heterozygosity and genetic differentiation (Krueger et al., 1989). Alleles for all enzymes were named according to their relative electrophoretic mobility, outlined by Krueger & May (1987).

Hardy-Weinberg equilibrium expectations for genotype frequencies at polymorphic loci were tested using a Chi-square test for goodness-of-fit, and the probability of the null hypothesis was estimated using a Monte Carlo simulation with 10,000 iterations. The genetic structure within and between populations was analyzed using the F-statistic (Wright, 1978; Nei, 1987). The F-statistic estimates were calculated following the method of Nei & Chesser (1983) and its statistical significance was tested using a Chi-square test for homogeneity of allele frequencies across samples, and the probability of the null hypothesis was estimated using a Monte Carlo simulation with 10,000 iterations. The sequential Bonferroni correction after Hochberg (1988) was applied to avoid the type I error resulting from multiple significance testing of the same null hypothesis (Rice, 1989). Estimates of genetic variability were calculated for each sample (Nei, 1987). The computer program Bottleneck v1.2.02 (Cornuet & Luikart, 1996) was used to detect whether there was a recent reduction in effective population size. In a bottleneck population, gene diversity will be higher than that expected at equilibrium. Gene diversity was estimated under three models: SMM, IAM and the two-phase model (TPM) of Di Rienzo et al. (1994) which may be closer to the true model of mutation for most loci. Recent bottleneck (heterozygosity excess) effects were tested using those three models with a Wilcoxon sign-rank test (Luikart et al., 1998).

Nei's (1978) unbiased genetic distances (D) among population pairs were estimated. The resulting pairwise genetic distance matrices were used to build NeighborJoining (NJ) trees (Saitou & Nei, 1987). To assess the confidence of the obtained trees, 1,000 bootstrap replicates of each data matrix were generated (Felsenstein, 1985). A Neighbor-Joining analysis was done using the 10 allozymic loci shared between the present study and that reported by Gajardo et al. (1998) in southern Chile, Gregg et al. (2001) in England, and Farrington et al. (2004) in Australia, ([ADH-1.sup.*], [G3PDH.sup.*], [GPI-1,2.sup.*], [GPI-3.sup.*] [IDH3-4.sup.*], [MDH -1,2.sup.*], [MDH3-4.sup.*], [ME-1.sup.*], [ME-2.sup.*] and [SOD.sup.*]) (Table 1 for alleles comparison).

The samples were also ordered with a nonmetric multidimensional scaling (MDS) of the pairwise [F.sub.ST] matrix, and the final stress was calculated (Dunn & Everitt, 1982). The genetic data were analyzed using the FSTAT v2.9.3 (Goudet, 2002), GeDis v1.8 (Pena et al., 2009), GENEPOP v4.1.1 (Raymond & Rousset, 2000), Bottleneck v1.2.02 (Cornuet & Luikart, 1996) and Phylip v3.69c computer programs.

RESULTS

Of the 20 enzyme systems analyzed, a total of 38 presumptive loci were resolved, 9 were found to be polymorphic in at least one of the populations in the study ([ACO.sup.*], [DIA.sup.*], [GLYDH.sup.*], [G3PDH-3.sup.*], [PGM-2.sup.*], [SOD.sup.*], [TF.sup.*]) and the duplicate loci [IDH-3,4.sup.*] and [MDH3,4.sup.*] (Table 2).

Alleles per locus and allele frequencies at each population are showed in Table 2. Samples from the Limari river basins did not show variation for the [ACO.sup.*], [DIA.sup.*], [GLYDH.sup.*], [G3PDH.sup.*] and [TF.sup.*] locus, but in these populations an exclusive [PGM-2.sup.*]60 allele was observed with significant differences in frequency among them (P < 0.05). Samples from the Elqui basin did not show variation for [ACO.sup.*] and [GLYDH.sup.*]. In the La Laguna sample an allele ([DIA.sup.*]95) was only shared with the Cofradex strain. The Claro River sample was the only wild population that showed the allele ([G3PDH.sup.*]120), which was also observed in the cultured Steelhead and Donaldson strains. The allele [IDH-3,4.sup.*]70 in the La Laguna sample was also observed only in cultured strains, except for Steelhead, but the allele [IDH-3,4.sup.*]90 was exclusive to the Cofradex strain. In both basins, Elqui and Limari, F-values for the locus [IDH-3,4.sup.*] were significantly different from zero (P < 0.01), and also [PGM-2.sup.*] in the Limari basin populations and in the Kamloops strain (Table 2).

Wild rainbow trout populations showed a similar range of variation in heterocigosity, polymorphism (P%) and number of alleles per locus than commercial strains (Table 2). In turn, wild populations from the Elqui basin showed higher genetic variability than populations from the Limari River basin (Table 2). Only the sample from Claro River showed a significant departure from Hardy-Weinberg equilibrium in genotype frequencies (P < 0.05), having an excess of observed homozygotes. This population was built by pooling three subsamples from the same river with different size distributions (Fig.4).

The [F.sub.ST] value of all populations was 0.222, ranging between 0.014 for locus [DIA.sup.*] to 0.361 for locus [TF.sup.*], with all values being different from zero (P < 0.05), except for [DIA.sup.*] (P > 0.05). Fst between the wild populations was 0.155 and for between hatchery samples it was 0.213, both highly significant (P < 0.001). Similarly, pair-wise comparisons between populations were highly significant (P < 0.001), and only the comparisons between rivers within the Limari basin, and between the Limari basin and the Steelhead strain did not show differences (P > 0.05; Table 3). The analysis to detect recent effective population size reductions from allele data frequencies showed a significant departure from the IAM model only for the Grande River samples (P < 0.05).

The Neighbor-Joining tree (Fig. 2a) grouped rainbow trout populations from the Limari basin in a cluster together with the Steelhead strain. Populations from the Elqui basin are enclosed in a broader cluster that includes the Donaldson and Cofradex commercial strains, the cluster of Limari basin populations and the Steelhead strain. The next Neighbor-Joining tree and MDS, including data of populations from southern Chile, England and Australia (Fig. 2b, 3) showed that, with the exception of the American, Kamloop and Scottish commercial strains, the remaining populations are grouped in a large cluster that include all the rainbow trout populations studied at present in Chile, and also strains from England and Australia (75%). Within this group, samples from southern Chile and Australia (70%) are clearly distinct from the stocks of the Limari basin and Steelhead (56%).

DISCUSSION

The results show that rainbow trout populations in the basins of the Limari and Elqui rivers in north-central Chile retain relatively high levels of genetic variability, demonstrating genetic differences among them and with southern populations. However, rainbow trout populations from Elqui basin had higher genetic variability than those from the Limary basin, as shown heterozygosity levels. They also show genetic associations with different cultured strains.

Intrapopulation analysis showed a private allele in populations in the Limari basin ([PGM-2.sup.*]60), and rare alleles in the Elqui basin were not detected in Limari, but in cultured strains they were. This, coupled with the absence of statistically detectable bottlenecks, indicates that populations have retained similar levels of variability compared to the original populations (Allendorf & Phelps, 1981; Hershberger, 1992; Krueger et al., 1994).

Only the population of Claro River showed a significant departure from Hardy-Weinberg equilibrium (excess homozygotes). This could be due to the "Wahlund effect" caused by mixing of different year-class individuals with different allele frequencies in the same sample, as suggested by the differences in size distribution between subsamples from the river (Fig. 4). This type of phenomenon has been previously reported as being associated with the movement of older groups across the gradient of the inflowing waters, creating cohorts or spatial-temporal segregation between juveniles and adults (Biette et al., 1981; Moran et al., 1995). By contrast, southern feral populations analyzed by Gajardo et al. (1998) showed four out of the 10 loci with excess heterozygotes, three of them in the Huillin population. Taking into account the presence of rare alleles in Pilmaiquen trouts, they propose the existence of reproductive isolation between both populations.

Another way to assess the genetic diversity within populations is through heterozygosity, polymorphism and mean number of alleles. In our study, average values for wild and hatchery populations were He = 0.040 and 0.049, P = 13% and 14% and An = 1.15 and 1.21, respectively, without significant differences among them (P < 0.05). Wild rainbow trout populations from southern Chile showed values of P = 21.8% and An = 1.26 (Gajardo et al., 1998). Their average He estimations (0.07) were higher than those observed in the present study. This is a consequence of differences in allele frequency at polymorphic loci. Northern Chile populations showed higher frequency of rare alleles, which inflate polymorphism and the number of alleles per locus, but not heterozygosity to the same extent (Currens et al., 1990). In Australia, wild rainbow trout introduced over 100 years ago and hatchery strains showed values of He between 0.020 and 0.042 and P from 16% to 22%, respectively, without significant differences between hatchery and wild naturalized populations (Farrigton et al., 2004). These results are very close to our findings in northern Chilean populations of rainbow trout.

Average expected heterozygosity values (He) described in the literature in cultured strains of rainbow trout range from 0.012 and 0.096, which is not an extremely wide range if we consider the large number of studied strains (Thompson, 1985; Paaver, 1988; Ferguson et al, 1993; Gregg et al, 2001; Farrington et al, 2004). The He observed in almost all commercial strains in the present study were close to the upper limit of variability described for the species, consistent with the previous reports for all forms of O. mykiss (Ryman, 1983; Krueger & May, 1987; Berg & Gall, 1988; Hershberger, 1992). However, in the present study He in the Donaldson strain was almost double the value reported for the same strain in Russia (Ho = 0.023, Paaver, 1988) and close to values observed in Steelhead (Ho = 0.040, Paaver, 1988). Paaver (1988) did not detect variability at the [PGM-2.sup.*] locus in Steelhead nor in Donaldson strains, but in the present study both strains (20 individual in each sample) show an undescribed low frequency allele (80), a phenomenon that suggests that in Chile these strains could receive genes from other commercial lines. On the other hand, the retention of high levels of enzyme heterozygosity in rainbow trout culture strains has been associated with mixture of origins during its founding and subsequent propagation or balanced selection followed by a population bottleneck and artificial selection (Busack et al., 1979; Thompson, 1985; Ferguson et al., 1993).

The relative genetic diversity estimated among all samples was 22%. This is the largest genetic diversity reported in studies in rainbow trout populations. Relative genetic diversity between wild populations was much lower (15%). However, it is larger than that observed between wild populations from eastern North America (3.6-5.5%; Krueger & May, 1987; Krueger et al., 1994), western North America (1.8%-13.2%; Allendorf & Phelps, 1981; Berg & Gall, 1988; Reisenbichler & Phelps, 1989), between interior and coastal regions of Scandinavia and northern North America (15%; Gyllensten, 1985), or between wild stocks from southern Chile lakes (5.2%; Gajardo et al., 1998). Limari and Elqui basins are well separated by their geographic and hydrographic characteristics, and both are affected by strong seasonal and inter-annual flow variations. Water flow variations over 6,000% and 10,000% have been registered within one year in Elqui and Limari basins, respectively, during the El Nino event (Direccion General de Aguas, Chile). Altered environmental conditions that accompany demographic expansion could shift fitness and survival patterns within and among populations creating a variety of effects on the gene pool (Nielsen, 1999). So, changes in effective population size (Ardren & Kapuscinski, 2003), gene flow among surviving groups and possible reintroductions must be considered to understand the population genetic structure within the basins (Avise, 1994; Allendorf & Waples, 1996). This could explain the high levels of genetic differentiation among populations accompanied with the retention of high levels of within-population genetic variation in the rainbow trout populations from northern Chile.

The cultivated strains of this species, as wild populations, normally retain high levels of within-population genetic variation (Milner et al., 1979; Thompson, 1985; Paaver, 1988; Winkler, 1994; Carcamo, 1999). In our study, the average genetic differentiation (Fst) among the six strains reaches 21%, close to the 23% obtained by Gregg et al. (2001) from the analysis of 12 strains, and higher than those described by Thompson (1985) from 5 strains (10%).

Allozyme analysis of rainbow trout populations from the different river basins in Chile showed genetic differences that could be caused by the source of trout used to first seed some river basins, but also by subsequent reseeding of the rivers with rainbow trout of different origins. As an example, Neighbor-Joining analyses with 38 and 8 loci, as well as the multidimensional scaling analysis strongly suggest that the rainbow trout populations of Limari basin could originate from the Steelhead strain with unsuccessful or non-subsequent reseeding of the rivers with trout of different origins. On the other hand, the Elqui basin populations like to be closely related with Donaldson (Washington, USA; Donaldson & Olson, 1957), Cofradex, (Denmark; Mardones & Vega, 1993), and London strains (UK; Gregg et al., 2001). The latter strain was developed in London, but was obtained by interbreeding rainbow trout from Bowden Ohio, West Virginia, the Shepherd of the Hills Hatchery in Missouri and the Manchester Hatchery in Iowa (Gregg et al., 2001). This situation involves two different scenarios, one in which there is a mixture in the origin of the introduction and subsequent naturalization or, a second option, where an initial introduction was followed by subsequent successful reintroductions of trout from different origins. Given the high levels of genetic variability, similar to its native range, we think the second option is the most feasible. By contrast, brown trout (Salmo trutta), another salmonid species introduced at the beginnings of the 20th century, shows lower genetic divergence for allozyme markers (9.5-12.64%) among Chilean populations (Faundez et al., 1997; Colihueque et al., 2003), suggesting a more homogeneous origin.

The above discussed result shows that rainbow trout stocks from different river basins in Chile have substantive within and between genetic variations at allozyme loci. Rivers along Chile exhibit strong environmental variation in a north to south climatic cline (Miloslavich et al., 2011). After 100 years of the presence of this introduced species, and assuming both selective and non-selective processes affecting the rainbow trout populations in the wild, it is possible that feral populations of rainbow trout in Chile can be a promising source of gene variability that can be exploited for aquaculture and/or conservation proposes. More detailed studies are necessary to map the amount and distribution of these resources in Chile.

DOI: 10.3856/vol43-issue1-fulltext-6

ACKNOWLEDGEMENTS

The authors thank Mr. Luis Perez and Ms. Ninoska Silva for collaboration during the electrophoretic analysis of the samples. This research was partially financed by Grant 1940259-94 from the Chilean National Foundation for Science and Technology (FONDECYT).

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Received: 19 March 2014; Accepted 12 September 2014

Claudia B. Carcamo (1), Nelson F. Diaz (3) & Federico M. Winkler (1,2)

(1) Departamento Biologia Marina, Facultad de Ciencias del Mar, Universidad Catolica del Norte Larrondo 1281, Coquimbo, Chile

(2) Centro de Estudios Avanzados en Zonas Aridas (CEAZA), Universidad Catolica del Norte Larrondo 1281, Coquimbo, Chile

(3) Departamento de Produccion Animal, Facultad de Ciencias Agronomicas, Universidad de Chile P.O. Box 1004, Santiago, Chile

Corresponding author: Federico M. Winkler (fwinkler@ucn.cl)

Corresponding editor: Sergio Palma

Caption: Figure 1. Location of sampling sites for rainbow trout in the Elqui and Limari River basins, Coquimbo Region, Chile.

Caption: Figure 2. Neighbor Joining based on Nei's distances. a) Samples from Elqui basin, Limari basin and strain culture, b) The samples from this study and samples from AUS (Australia wild; Farrigton et al, 2004), CHL (Southern Chile; Gajardo et al, 1998) and OIN (Ohio-Indiana; Gregg et al, 2001).

Caption: Figure 3. Multidimensional scaling (MDS) from the matrix Fst by Reynolds et al. (1983) of the population from Elqui and Limari basins, culture strain and samples from Gajardo et al. (1998) (Huillin, Pescadero and Pilmaiquen), Farrington et al. (2004) (Lightning and Still) and Gregg et al. (2001) (London).

Caption: Figure 4. Size (total length) frequency distribution of rainbow trout sampled in the Claro River.
Table 1. Approximate size and size inferred from allele frequencies
of loci in O. mykiss analyzed by different authors.

Loci                Alleles     Gajardo et
                                al. (1998)

ADH-1             Monomorphic   Monomorphic
G3PDH                 120       Monomorphic
                      100
[GPI-1,2.sup.*]   Monomorphic   Monomorphic
[GPI-3.sup.*]     Monomorphic   Monomorphic
[IDH-3,4.sup.*]       120           110
                      100           100
                      90            90
                      70            --
                      40            --
[MDH-1,2.sup.*]   Monomorphic   Monomorphic
[MDH-3,4.sup.*]       125           --
                      100           100
                      --            95
                      60            90
[ME-1.sup.*]      Monomorphic       105
                                    100
[ME-2.sup.*]      Monomorphic       100
                                    95
[SOD-1.sup.*]         140           115
                      100           100
                      40            ---

Loci               Gregg et     Farrington et
                  al. (2001)     al. (2004)

ADH-1             Monomorphic    Monomorphic
G3PDH             Monomorphic        120
                                     100
[GPI-1,2.sup.*]   Monomorphic    Monomorphic
[GPI-3.sup.*]     Monomorphic    Monomorphic
[IDH-3,4.sup.*]       --             120
                      100            100
                      --             --
                      70             80
                      40             60
[MDH-1,2.sup.*]   Monomorphic    Monomorphic
[MDH-3,4.sup.*]   Monomorphic        --
                                     100
                                     80
                                     60
[ME-1.sup.*]          110        Monomorphic
                      100
[ME-2.sup.*]      Monomorphic    Monomorphic

[SOD-1.sup.*]         150            150
                      100            100
                      50             ---

Table 2. Allele frequencies of rainbow trout for 9 polymorphic loci
in four naturalized populations from northern Chile and six fanned
stock. Nmnber of individuals (N), and Heterozygote deficiency (F) by
locus in each population. The superscripts indicate those significant
[chi square] test values after a Bonferroni's conection ((a): P <
0.05, (b) :P< 0.01).

Locus             Allele          Populations

                                Elqui Basin

                             Laguna         Claro

                    N          22            58
[ACO.sup.*]        100        1.000         1.000
                    83         --            --
                    67         --            --
                    F
[DIA.sup.*]        100        0.977         1.000
                    95        0.023          --
                    F        -0.02.3
[GLYDH.sup.*]      100        1.000         1.000
                    78         --            --
                    F
[G3PDH-3.sup.*]    120         --           0.008
                   100        1.000         0.992
                    F                      -0.008
[IDH-3,4.sup.*]    120        0.023         0.043
                   100        0.523         0.448
                    90         --            --
                    70        0.023          --
                    40        0.431         0.509
                    F      -0.673  (b)   -0.757  (b)
[MDH-3,4.sup.*]    125         --            --
                   100        0.409         0.552
                    60        0.591         0.448
                    F         0.083        -0.106
[PGM-2.sup.*]      200         --            --
                   100        0.955         0.888
                    80        0.045         0.112
                    60         --            --
                    F        -0.034        -0.117
[SOD.sup.*]        140        0.386         0.009
                   100        0.614         0.991
                    40         --            --
                    F        -0.055        -0.117
[TF.sup.*]         100        0.675         0.632
                    95        0.325         0.368
                    F        -0.254         0.333
He                            0.057         0.046
Ho                            0.065         0.056
Allele/locus                  1.21          1.18
[P.sub.99]                    15.79         15.79

Locus             Allele         Populations

                               Limari Basin

                             Grande      Hurtado

                    N          30           30
[ACO.sup.*]        100       1.000        1.000
                    83         --           --
                    67         --           --
                    F
[DIA.sup.*]        100       1.000        1.000
                    95         --           --
                    F
[GLYDH.sup.*]      100       1.000        1.000
                    78         --           --
                    F
[G3PDH-3.sup.*]    120         --           --
                   100       1.000        1.000
                    F
[IDH-3,4.sup.*]    120       0.167        0.033
                   100         --           --
                    90         --           --
                    70         --           --
                    40       0.833        0.967
                    F      0.532  (b)   1.000  (b)
[MDH-3,4.sup.*]    125         --           --
                   100       0.533        0.500
                    60       0.467        0.500
                    F        -0.054       -0.049
[PGM-2.sup.*]      200         --           --
                   100       0.867        0.967
                    80         --           --
                    60       0.133        0.033
                    F        -0.137       -0.178
[SOD.sup.*]        140       0.121        0.150
                   100       0.879        0.850
                    40         --           --
                    F        -0.120       0.361
[TF.sup.*]         100       1.000        1.000
                    95         --           --
                    F
He                           0.033        0.024
Ho                           0.031        0.020
Allele/locus                  1.11         1.11
[P.sub.99]                   10.53        10.53

Locus             Allele             Populations

                                  Commercial strains

                           Steelhead   Donaldson   Cofradex

                    N         20          20          20
[ACO.sup.*]        100       1.000       1.000      1.000
                    83        --          --          --
                    67        --          --          --
                    F
[DIA.sup.*]        100       1.000       1.000      0.975
                    95        --          --        0.025
                    F                               -0.026
[GLYDH.sup.*]      100       1.000       1.000      1.000
                    78        --          --          --
                    F
[G3PDH-3.sup.*]    120       0.025       0.225        --
                   100       0.975       0.775      1.000
                    F       -0.025      -0.290
[IDH-3,4.sup.*]    120       0.250       0.100        --
                   100        --         0.150      0.200
                    90        --          --        0.075
                    70        --         0.200      0.150
                    40       0.750       0.550      0.575
                    F       -0.310      -0.256      -0.223
[MDH-3,4.sup.*]    125        --          --          --
                   100       0.650       0.850      0.400
                    60       0.350       0.150      0.600
                    F       -0.295      -0.151      0.191
[PGM-2.sup.*]      200        --          --          --
                   100       0.975       0.975      0.700
                    80       0.025       0.025      0.300
                    60        --          --          --
                    F       -0.026      -0.026      -0.407
[SOD.sup.*]        140       0.150       0.200      0.375
                   100       0.850       0.800      0.625
                    40        --          --          --
                    F       -0.151       0.088      0.277
[TF.sup.*]         100       1.000       0.500      0.650
                    95        --         0.500      0.350
                    F                   -0.115      0.146
He                           0.033       0.058      0.068
Ho                           0.039       0.066      0.067
Allele/locus                 1.13        1.21        1.21
[P.sub.99]                   15.16       15.79      15.79

Locus             Allele            Populations

                                  Commercial strains

                           Escocesa   Kamloops    Americana

                    N         56         89          102
[ACO.sup.*]        100      0.920       0.956       1.000
                    83      0.043       0.031        --
                    67      0.036       0.013        --
                    F       -0.063     -0.036
[DIA.sup.*]        100      1.000       1.000       1.000
                    95        --         --          --
                    F
[GLYDH.sup.*]      100      0.889       0.871       1.000
                    78      0.111       0.129        --
                    F       -0.029     -0.140
[G3PDH-3.sup.*]    120        --         --          --
                   100      1.000       1.000       1.000
                    F
[IDH-3,4.sup.*]    120        --        0.026        --
                   100      0.818       0.647       0.599
                    90        -           -           -
                    70      0.100       0.064       0.156
                    40      0.082       0.263       0.245
                    F       0.073      -0.074      -0.178
[MDH-3,4.sup.*]    125      0.058       0.067        --
                   100      0.558       0.762       1.000
                    60      0.384       0.171        --
                    F       0.005      -0.013
[PGM-2.sup.*]      200      0.042       0.236       0.250
                   100      0.958       0.768       0.750
                    80        --         --          --
                    60        --         --          --
                    F       -0.043    0.252 (a)    -0.072
[SOD.sup.*]        140      0.170       0.104       0.338
                   100      0.688       0.813       0.662
                    40      0.143       0.083        --
                    F       -0.120     -0.164      -0.160
[TF.sup.*]         100      1.000       1.000       1.000
                    95        --         --          --
                    F
He                          0.052       0.045       0.037
Ho                          0.040       0.037       0.041
Allele/locus                 1.30       1.30        1.11
[P.sub.99]                  15.79       15.79       7.90

Table 3. [F.sub.ST] values for 38 allozyme loci between population
pairs of four naturalized populations of rainbow trout in northern
Chile and six farmed stock. The superscripts indicate those
significant [chi square] test values after a Bonferroni's correction
((b): P < 0.01).

Populations    Laguna       Claro      Grande      Hurtado

Laguna           --
Claro         0.080 (b)      --
Grande        0.200 (b)   0.161 (b)      --
Hurtado       0.232 (b)   0.198 (b)   0.010          --
Steelhead     0.144 (b)   0.137       0.026       0.047
Donaldson     0.101 (b)   0.147 (b)   0.241 (b)   0.271 (b)
Cofradex      0.038       0.101 (b)   0.152 (b)   0.181 (b)
Escosesa      0.130 (b)   0.185 (b)   0.316 (b)   0.360 (b)
Kamloops      0.177 (b)   0.162 (b)   0.272 (b)   0.318 (b)
Americana     0.254 (b)   0.261 (b)   0.334 (b)   0.379 (b)

Populations   Steelhead   Donaldson   Cofradex    Escosesa

Laguna
Claro
Grande
Hurtado
Steelhead        --
Donaldson     0.081 (b)      --
Cofradex      0.093 (b)   0.079 (b)      --
Escosesa      0.303 (b)   0.319 (b)   0.233 (b)      --
Kamloops      0.296 (b)   0.358 (b)   0.246 (b)   0.055 (b)
Americana     0.384 (b)   0.450 (b)   0.301 (b)   0.154 (b)

Populations   Kamloops    Americana

Laguna
Claro
Grande
Hurtado
Steelhead
Donaldson
Cofradex
Escosesa
Kamloops         --
Americana     0.064 (b)      --
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Title Annotation:Research Article
Author:Carcamo, Claudia B.; Diaz, Nelson F.; Winkler, Federico M.
Publication:Latin American Journal of Aquatic Research
Date:Mar 1, 2015
Words:6790
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