Chromosomal characterization of cultured populations of Chilean coho salmon (Oncorhynchus kistuch)

Chromosomal characterization of cultured populations of Chilean coho salmon (Oncorhynchus kistuch)

Nelson Colihueque V.

Departamento de Ciencias Básicas, Universidad de Los Lagos, Casilla 933, Osorno, Chile. E-mail: [e-mail]

ABSTRACT

Chromosomal characterization of coho salmon samples from three fish farms in southern Chile (Polcura, Castro and Coyhaique) was carried out in order to compare their chromosome constitutions. All populations had a 2n = 60; however, Polcura and Coyhaique had a different chromosome arm number (NF = 110; 40m + 10sm + 10st/t) than Castro (NF = 108; 40m + 8sm + 12st/t). Variation in NF was due to chromosome pair 25, which was submetacentric in Coyhaique and Polcura, but subtelocentric in Castro. In all karyotypes, a large submetacentric chromosome pair exhibited an interstitial secondary constriction in the short arm. The observed variability in chromosome arm number agrees with previous reports for O. kisutch, and in this particular case it seemed to be caused by a pericentric inversion of pair 25. Cultured populations of Chilean coho salmon are, therefore, likely to be cytogenetically variable.

INTRODUCTION

Salmonid cytogenetics is an interesting research area due to this fish's distinct genetic characteristics, such as tetraploid origin, diploidization process and high levels of chromosomal rearrangements (Ohno et al., 1969; Allendorf and Thorgaard, 1984; Hartley, 1987). Up to the middle of the past decade, the most cytogenetic information available for salmonids was diploid chromosome number, chromosome arm number, and some chromosome banding patterns (C, Q, NORs) (Hartley, 1987). However, the last ten years have introduced many other techniques, for example, fluorescent banding with base-specific fluorochromes, BrdU replication banding, and restriction enzyme banding. These advancements have provided detailed information on chromosome banding patterns in different salmonid species (Mayr et al., 1988; Inokkuchi et al., 1994; Abuín et al., 1994).

Coho salmon (Oncorhynchus kisutch) originates in the Pacific coast of North America and Asia. Its karyotype presents 2n = 60 and different chromosome arm numbers (NF) (NF = 106, NF = 108 or NF = 112) (Simon, 1963; Uyeno, 1972; Ueda, 1983). A single chromosome pair is the NOR carrier (Phillips et al., 1986), and the species does not exhibit sex chromosomes. Furthermore, constitutive heterochromatin in centromeric and telomeric regions as well as in complete chromosome arms has been described (Ueda, 1983).

In Chile, coho salmon along with rainbow trout (Oncorhynchus mykiss) and Atlantic salmon (Salmo salar) are important aquaculture species (Méndez, 1995). However, information on chromosomal characteristics of farmed and wild populations is only available in O. mykiss and S. salar (Veloso et al., 1990; Iturra et al., 1992). This study characterizes cytogenetically three farmed populations of coho salmon with the aim of describing the chromosome constitutions and the extent of karyotypic variability.

MATERIAL AND METHODS

Samples studied were obtained from commercial fish farms located in Polcura (Region VIII, 37°17'S 71°44'W), Castro (Region X, 42°25'S 73°46'W) and Coyhaique (Region XI, 45°33'S 72°6'W). While Castro population is of unknown origin, Polcura and Coyhaique were established from imported eyed eggs (Oregon, USA). Thirty-three specimens (embryos, juveniles and adults) were studied: 18 from Polcura, 5 from Castro and 10 from Coyhaique. Chromosome slides were obtained from embryo and kidney tissues using the squash method according to Veloso et al. (1990), whereas adult chromosome spreads were obtained by lymphocyte cell culture (Colihueque, 1991). Chromosomes were stained in 4% Giemsa prepared in phosphate buffer, pH 7.2. Metaphase plates were chosen following Simon's (1963) criteria and chromosomes were counted with photographs. Chromosome morphology was established according to the centromeric index (CI) (Levan et al., 1964). In all populations, five suitable metaphase plates were used for CI determination. Chromosome measuring was done through a digital caliper (Max-Cal, Fowler & NSK, Japan). In replicated measurements (n = 10) of the same chromosome in different chromosome types, the experimental error (standard deviation) in CI determinations was < 1.45. For example, metacentrics, submetacentrics and subtelocentrics showed the following means and standard deviations: 48.42 ± 0.70; 31.18 ± 1.31; 16.48 ± 1.45, respectively. For NF determinations, it was assumed that metacentric-submetacentrics (m-sm) are two-armed chromosomes, and the subtelocentric-telocentrics (st-t) are one-armed chromosomes. Total chromosome relative length (RL), as a percentage, and the relative lengths of short arm (SA) and long arm (LA), over total length of haploid complement, were also obtained. SA and LA lengths were used to elaborate karyo-ideograms to analyze chromosomal differences within as well as between karyotypes (Spotorno et al., 1979).

RESULTS

Chromosome counts in the three analyzed populations are shown in Table I. All share a modal diploid chromosome number of 2n = 60. Two specimens, however, exhibited triploid karyotypes with chromosome number near 90 (36-172 in Polcura; 110 in Coyhaique).

Table I
- Chromosomal counts in coho salmon populations from Chile.

Population/ Fish	Chromosome number																			No. of cells observed
	Sex	<55	55	56	57	58	59	60	61	62	>62		<86	86	87	88	89	90	>90
Polcura (1)
36-11	?							2												2
36-12	?						1	1												2
36-21	?	1				5		1												7
36-51	?	2	1	1	4	1	1	2												12
36-61	?							2												2
36-71	?	7				1	1	1	1											7
36-72	?					1	1	1		1										4
36-81	?				1	3	1	4	1											10
36-101	?	1	2		1		2	1		1										8
36-121	?	1			2	1	2	1	1											8
36-122	?							1	1											2
36-131	?	1			2	2	1	2	1	1										10
36-141	?	1				1		4												6
36-151	?		1	1				2												4
36-161	?	2	2	1	3		1	1												10
36-172	?												4	3						7
100	F (2)	1	1		3	2	1	2												10
107	F	1				2	1	1												5
Total		14	7	3	16	19	13	29	5	3			4	3
Castro
19	F	1		1		2		3												7
21	F	1				1		3												5
42	?						1	3												4
46	?	3			1		1	2												7
124	M (3)			1	1	3	3	8	2	1										19
Total		5		2	2	6	5	19	2	1
Coyhaique
1	F	5				1	1	3	1											11
2	M					1	1	2	1											5
109	?					2	1	3												6
110	M												5		1	1	4	1		12
111	F				2		5	6		1										14
112	M	1	1	1		1	2	4												10
113	M	2	1		4	1	3	5	1											17
114	M	2				2	2	4			1									11
115	M				2		1	1	1											5
118	F	1				2	1	2	1											7
Total		11	2	1	8	10	17	30	5	1	1		5		1	1	4	1

(1) Samples between 36-11 and 36-172 are embryos; (2) F = female; (3) M = male. Underlined number is the modal chromosome number.

Relative length and centromeric index mean values for the 30 chromosome pairs of a diploid karyotype are shown in Table II. The centromeric index reveals that Coyhaique and Polcura have similar chromosome constitutions: 40m + 10sm + 10st/t, with an NF of 110, whereas Castro's karyotype formula was 40m + 8sm + 12st/t, with NF being 108. Different chromosome arm numbers occurred as a consequence of pair 25 (ANOVA test, F = 13.58, P < 0.05), which was sm in Coyhaique and Polcura, but st in Castro. Significant differences in CI were also observed in chromosome pair 2 (ANOVA test, F = 47.98, P < 0.05), though this did not affect its metacentric morphology. Likewise, all populations showed high CI variability (coefficient of variation (CV) > 0.59) in small one-armed chromosomes (pairs 29 and 30).

Table II
- Mean values of karyological parameters in coho salmon populations from Chile.

Chromosome pairs	Population
	Polcura			Castro			Coyhaique
	RL%(1)	CI ±SD(2)	Types	RL%	CI ±SD	Types	RL%	CI ±SD	Types
1	5.06	46.90 ± 1.63	m(3)	5.12	47.48 ± 0.72	m	5.48	43.44 ± 3.27	m
2	4.76	45.05 ± 0.25 NS	m	4.69	47.18 ± 0.74 a	m	4.79	43.07 ± 0.96b	m
3	4.37	45.41 ± 0.35	m	4.57	44.67 ± 2.43	m	4.68	45.32 ± 0.97	m
4	4.32	45.55 ± 1.26	m	4.45	44.21 ± 1.85	m	4.53	45.84 ± 2.37	m
5	4.21	46.45 ± 1.11	m	4.28	45.41 ± 0.65	m	4.42	47.38 ± 1.38	m
6	4.11	47.98 ± 0.62	m	4.19	46.60 ± 1.87	m	4.28	45.29 ± 2.35	m
7	4.06	46.48 ± 1.72	m	4.10	46.94 ± 1.82	m	4.19	46.80 ± 1.39	m
8	3.99	46.28 ± 1.22	m	4.00	45.87 ± 1.01	m	4.06	45.88 ± 2.12	m
9	3.93	45.79 ± 2.80	m	3.92	43.71 ± 3.46	m	3.95	45.94 ± 2.78	m
10	3.87	42.35 ± 3.18	m	3.86	44.87 ± 2.00	m	3.84	45.92 ± 2.96	m
11	3.82	45.22 ± 4.43	m	3.79	46.38 ± 1.51	m	3.76	44.25 ± 3.37	m
12	3.77	44.53 ± 3.34	m	3.74	47.23 ± 1.22	m	3.65	43.68 ± 2.31	m
13	3.70	45.93 ± 0.54	m	3.67	47.03 ± 0.99	m	3.55	45.84 ± 1.61	m
14	3.57	45.46 ± 2.47	m	3.55	45.15 ± 0.86	m	3.47	45.23 ± 1.54	m
15	3.47	45.94 ± 1.42	m	3.43	45.44 ± 2.97	m	3.36	46.22 ± 2.36	m
16	3.38	43.43 ± 1.71	m	3.31	46.04 ± 1.31	m	3.24	45.91 ± 1.77	m
17	3.31	44.65 ± 1.99	m	3.17	45.16 ± 3.53	m	3.11	44.54 ± 1.17	m
18	3.13	45.83 ± 0.36	m	3.07	45.80 ± 2.37	m	2.97	45.56 ± 3.34	m
19	2.86	41.70 ± 1.13	m	2.77	44.50 ± 1.67	m	2.76	44.52 ± 2.40	m
20	2.36	41.19 ± 3.37	m	2.35	46.39 ± 2.48	m	2.33	42.03 ± 2.95	m
21	4.03	33.43 ± 2.42	sm(4)	3.77	35.03 ± 1.22	sm	3.79	36.13 ± 1.68	sm
22	2.92	34.40 ± 4.66	sm	2.81	29.21 ± 4.51	sm	2.88	33.10 ± 1.97	sm
23	2.36	30.46 ± 2.19	sm	2.40	29.47 ± 1.98	sm	2.32	30.32 ± 0.98	sm
24	2.15	28.87 ± 0.93	sm	2.03	31.13 ± 3.54	sm	2.08	29.65 ± 1.75	sm
25	1.96	29.82 ± 1.26a	sm	2.69	16.79 ± 5.97 b	st	1.83	30.06 ± 1.13 a	sm
26	2.32	21.28 ± 1.21	st(5)	2.31	14.07 ± 8.51	st	2.61	20.28 ± 3.40	st
27	2.07	19.70 ± 3.91	st	2.17	13.36 ± 7.97	st	2.19	22.82 ± 2.71	st
28	2.30	9.54 ± 7.58	t(6)	2.06	11.99 ± 7.25	t	1.96	20.59 ± 1.53	st
29	2.01	7.54 ± 10.66	t	1.93	15.04 ± 8.88	st	1.98	11.69 ± 10.93	t
30	1.84	7.70 ± 8.44	t	1.65	7.08 ± 8.44	t	1.80	8.60 ± 10.56	t

(1) RL = Relative length; (2) CI = centromeric index; (3) m = metacentric; (4) sm = submetacentric; (5) st = subtelocentric; (6) t = telocentric. Distinct letters between means for CI indicate that these are significantly different from each other (ANOVA test, P < 0.05).

The karyo-ideogram (Figure 1) revealed that chromosome classes of studied population karyotypes (m, sm and st/t) tended to decrease in size (groups positioned in a diagonal line) as follows: m > sm > st/t. On the other hand, Figure 1 also shows that various chromosome pairs could be easily identified (large 1 and 2, and small 17, 18, 19, 20 pairs in metacentrics; large 21 and 22, and small 23, 24 and 25 pairs in submetacentrics), due to their characteristic size and morphology. However, various chromosome pairs within the metacentric group, which appear as a cluster in Figure 1, exhibited similar size (pairs 3 to 16). Interpopulation chromosomal differences in CI (Table II) were also revealed for chromosome pairs 2 and 25.

Figure 1
- Karyo-ideogram of cultured coho salmon populations (Coyhaique, Castro and Polcura) from Chile. Relative lengths of short chromosome arms (SA) and long chromosome arms (LA) of each chromosome pairs are shown in the abscissa and ordinate, respectively. Diagonal lines separate the chromosome morphologies in metacentrics (m), submetacentrics (sm), subtelocentrics (st) and telocentrics (t). Dotted lines show the same chromosome pairs of studied populations (the number identifies each pair) that are easily distinguished from the rest of the chromosome pairs in the karyotype, except pairs 3 to 16 in metacentrics (asterisk). Arrows show the different morphology of pair 25 in Castro (st) with regard to Coyhaique and Polcura (sm). SC indicates the chromosome pair that exhibits the secondary constriction in the karyotype.

Figures 2a and 2b show the two different karyotypes found in the studied populations. The Coyhaique karyotype with 2n = 60 and NF = 110 (Figure 2a) had 40m (1-20 p.), 10sm (21-25 p.) and 10st/t (26-30 p.), whereas Castro's karyotype with 2n = 60 and NF = 108 (Figure 2b) exhibited 40m (1-20 p.), 8sm (21-24 p.) and 12st/t (25-30 p.). Both karyotypes showed one large submetacentric chromosome pair with a clear interstitial secondary constriction in the short arm (pair 22 in Figure 2a and b). Likewise, those chromosomes, that were classified as one armed (st/t), showed a characteristic minor arm (e.g., pairs 26 and 27 in Coyhaique, Figure 2a). In Castro, chromosome pair 21 exhibited more variability in relative length than Coyhaique (CV = 0.15 vs. CV = 0.09). So, in the same karyotypes of Castro population this chromosome pair presented a big size (Figure 2b).

Figure 2
- Representative karyotypes of coho salmon populations from Chile. Karyotypes of Coyhaique with 2n = 60 (NF = 110) and Castro with 2n = 60 (NF = 108) are shown in a and b, respectively. Morphology of chromosome pairs is indicated at bottom right of each karyotype. SC indicates the chromosome pair that exhibits secondary constriction. Bar represents 10 mm.

No karyotype chromosome heteromorphism was clearly observed, though chromosome pair 20 in some males exhibited slight heteromorphism.

DISCUSSION

Diploid chromosome number observed in farmed Chilean coho populations (2n = 60) agrees with previous reports for the species (Simon, 1963; Uyeno, 1972; Ueda, 1983). Likewise, variation in NF (NF = 108 in Castro vs. NF = 110 in Polcura and Coyahique, Figure 2) agrees with interpopulation polymorphism found by other authors. For example, Simon (1963) and Uyeno (1972) reported NF = 112 and NF = 106, respectively, for American populations of O. kisutch. Although the NF = 110 of Coyhaique and Polcura (Figure 2) has not been previously described in the literature, it is close to those reported by Simon (1963). The NF = 108 of Castro has been observed in Japanese populations by Ueda (1983). Interpopulation differences regarding chromomosome arm number are likely to reflect the distinct origin of the population studied.

In addition to robertsonian polymorphism, structural rearrangements are also important in salmonids. For example, in O. keta (2n = 74), Kulinova (1971) observed two races with distinct chromosome arm number (NF = 94 or NF = 102), and Hartley and Horne (1984) showed NF = 101 or NF = 102 in a population of Salmo trutta (2n = 80). If more chromosomal analysis confirms the NF variation observed in our study, between 108 and 110, this variability could be explained by a pericentric inversion involving pair 25. Sm or st chromosomes were seen for this pair in the karyotypes of analyzed populations (Figure 1). Likewise, differences in heterochromatic composition for the short arms of those chromosome pairs could not be ruled out.

Significant interpopulational variation of the centromeric index for chromosome pair 2 is worth noting (Table II), although its metacentric type did not change. As a result, CI variability was probably related to polymorphism in the amount and/or distribution of this chromosome telomeric constitutive heterochromatin. In coho salmon as in Salvelinus leucomaenis, telomeric C-bands are present (Ueda, 1983; Ueda and Ojima, 1983). In this latter species, Ueda and Ojima (1983) observed a chromosome polymorphism that was due to unequal distribution of telomeric C-bands. Likewise, the heteromorphism observed in pair 1 of Figure 2b probably represents an apparent heteromorphism due to technical errors in chromosome spreads as it was only seen in the karyotype selected for the picture. Different factors such as the position of a particular chromosome in the metaphase spread, mechanical distortions involved in preparation, etc., are responsible for this type of error. This class of heteromorphism in homomorphic pairs has been reported for human chromosomes (Mark et al., 1993).

The chromosome formula of coho salmon (48m + 8 - 10sm + 10 - 12st/t; Table II) corresponds to the B-karyotype category for salmonids (Hartley, 1987), i.e., it has more two-armed chromosomes than one-armed chromosomes with 2n and NF around 60 and 104, respectively. This type of karyotype, common in Pacific salmons and trouts, involves a high number of chromosome rearrangements: if one assumes that the salmonid tetraploid's ancestor had 96 acrocentric chromosomes (Ohno et al., 1969), in fact, to obtain such a karyotype, 72 centric fusions and 8 pericentric inversions would be required. NF = 108 and NF = 110 observed in the current study, which are in the upper limit of variation observed for Oncorhynchus, would require the occurrence of 4 to 6 additional structural rearrangements from the standard B karyotype. Two to three subtelocentric chromosome pairs, that clearly appear in this study (Figure 2), could also reflect this type of chromosome rearrangement.

One-armed chromosomes with small short arms seen in the coho karyotype (Figure 2) are similar to those observed in O. masou and O. tshawytscha (Ueda, 1983; Phillips et al., 1985). Despite the fact that these cytogenetic similarities need to be more carefully studied, they are well correlated with morphological and/or molecular observations, particularly between coho salmon and chinook salmon (Smith and Stearly, 1989; Phillips et al., 1992).

This study found a secondary constriction in pair 22 (Figure 2), which agrees with reported evidence that only one chromosome pair carries NOR in the coho salmon karyotype as well as in other Oncorhynchus species (Phillips et al., 1986). The NOR carrier observed in Chilean samples is submetacentric (Figure 1). Its shape is similar to the chromosome pair with satellites described by Ueda (1983) in coho salmon. The shape of this pair can, however, vary as Phillips et al. (1986) observed in acrocentric chromosomes with NOR. So, it is clear that further studies are required to know the exact morphology of the chromosome pair that carries NOR in O. kisutch. With this in mind, our preliminary results with silver and chromomycin A3 stains indicate that it is located in the short arm of a two-armed chromosome.

Observations of spontaneous triploid individuals are common in fish, in general (Al-Sabti, 1983; Arai et al., 1991), and in rainbow trout, in particular (Thorgaard and Gall, 1979). In this species, spontaneous chromosome abnormalities seem to occur in association with other numerical rearrangements (Colihueque et al., 1996). Therefore, the observation of two individuals with triploid chromosome constitutions in the coho populations studied (Table I) confirms that this is not an uncommon event in salmonid fish. Although it is actually difficult to explain the appearance of these individuals, the spontaneous retention of the second polar body is probable.

Information produced in this study contributes to characterization of both diploid chromosome number and chromosome arm number in cultured coho salmon currently available in Chilean salmon farms. Similarly, relative lengths and centromeric index of 30 chromosome pairs, that composed the karyotype of this species, provide a base line for further karyotype variability studies, either within or among salmonid species.

ACKNOWLEDGMENTS

Research partially supported by DI-ULA No. 3070/1995 from Dirección de Investigación y Postgrado de la Universidad de Los Lagos. We wish to thank Piscícola Huililco Ltda. and Cía. Pesquera Camanchaca S.A. We are also indebted to Edmundo Pérez for his technical assistance, and Dr. Gonzalo Gajardo for critically reading the manuscript.

RESUMO

A caracterização cromossômica de amostras de salmon tipo coho de três criações de peixes do sul do Chile (Polcura, Castro e Coyhaique) foi feita com a intenção de comparar suas constituições cromossômicas. Todas as populações apresentaram 2n = 60; contudo, Polcura e Coyhaique tiveram um número de braços cromossômicos (NF = 110; 40m + 10sm + 10st/t) diferente de Castro (NF = 108; 40m + 8sm + 12st/t). A variação no NF deveu-se ao par cromossômico 25, que era submetacêntrico em Coyhaique e Polcura e subtelocêntrico em Castro. Em todos os cariótipos, um grande par cromossômico submetacêntrico exibiu uma constrição secundária intersticial no braço curto. A variabilidade observada no número de braços cromossômicos concorda com relatos prévios para O. kisutch e, neste caso particular, parece ter sido causada por uma inversão pericêntrica no par 25. Portanto, populações cultivadas de salmão chileno do tipo coho provavelmente são citogeneticamente variáveis.

(Received May 26, 1997)

• Abuín, M., Amaro,R. and Sánchez, L. (1994). Improving Salmo salar karyotype: restriction enzyme and replication banding. Cytobios 78: 143-152.
• Al-Sabti, K. (1983). Spontaneous triploidy and tetraploidy in the common carp (Cyprinus carpio L.). Vet. Arch. 53: 217-223.
• Allendorf, F.W. and Thorgaard, G.H. (1984). Tetraploidy and the evolution of salmonid fishes. In: Evolutionary Genetics of Fishes (Turner, B.J., ed.). Plenum Press, New York and London, pp. 1-53.
• Arai, K., Matsubara, K. and Suzuki, R. (1991). Karyotype and erythrocyte size of spontaneous tetraploidy and triploidy in the loach Misgurnus anguillicaudatus Nippon Suisan Gakkaishi 57: 2167-2172.
• Colihueque, N. (1991). Estudio familiar y meiótico de la variación cromosómica en trucha arcoiris, Oncorhynchus mykiss (Walbaum). Master's thesis, Ciencias Biológicas, Universidad de Chile, Santiago, Chile.
• Colihueque, N., Iturra, P., Díaz, N.F. and Veloso, A. (1996). Further evidence of chromosome abnormalities in normal and haploid progenies of rainbow trout, Oncorhynchus mykiss J. Exp. Zool. 276: 70-75.
• Hartley, S.E. (1987). The chromosome of salmonid fishes. Biol. Rev. 62: 197-214.
• Hartley, S.E. and Horne, M.T. (1984). Chromosome relationships in the genus Salmo Chromosoma 90: 229-237.
• Inokkuchi, T., Abe, S., Yamaha, E., Yamasaki, F. and Yoshida, M.C. (1994). BrdU replication banding studies on the chromosomes in early embryos of salmonid fishes. Hereditas 121: 255-265.
• Iturra, P., Veloso, A., Díaz, N.F., Colihueque, N. and Estay, F. (1992). Citogenética de salmonídeos. Rev. Bras. Genet. 15 (Suppl. 1): 218-221.
• Kulinova, N.F. (1971). Intraspecific variability of karyotypes of chum salmon (Oncorhynchus keta (Walb)). J. Ichthyol. II: 977-983.
• Levan, A., Fredga, K. and Sandberg, A.A. (1964). Nomenclature for centromeric position on chromosome. Hereditas 52: 201-220.
• Mark, H.F.L, Wyandt, H.E., Pan, T., Mark, R., Parmenter, M.,Campbell, W. and Mark, Y. (1993). A study of homologous chromosomes using a morphometric approach. Genome 36: 1003-1006.
• Mayr, B., Kalat, M. and Rab, P. (1988). Heterochromatins and band karyotypes in three species of salmonids. Theor. Appl. Genet. 76: 45-53.
• Méndez, R. (1995). Compendium of Chilean aquaculture. Editec Ltda., Santiago, Chile, pp. 226.
• Ohno, S., Muramoto, J., Klein, J. and Atkin, N.B. (1969). Diploid tetraploid relationship in Clupeoid and Salmonid fishes. Chromosomes Today II: 139-147.
• Phillips, R.B., Zajicek, K.D. and Utter, F.M. (1985). Q band chromosomal polymorphism in chinook salmon (Oncorhynchus tshawytscha). Copeia (2): 273-278.
• Phillips, R.B., Zajicek, K.D. and Utter, F.M. (1986). Chromosome banding in salmonid fishes: nucleolar organizer regions in Oncorhynchus Can. J. Genet. Cytol. 28: 502-510.
• Phillips, R.B., Pleyte, K.A. and Brown, M.R. (1992). Salmonid phylogeny inferred from ribosomal DNA restriction maps. Can. J. Fish. Aquat. Sci. 49: 2345-2353.
• Simon, R.C. (1963). Chromosome morphology and species evolution in the five North American species of Pacific salmon (Oncorhynchus). J. Morphol. 112: 77-95.
• Smith, G.R. and Stearly, R.F. (1989). The classification and scientific names of rainbow and cutthroat trouts. Fisheries 14: 4-10.
• Spotorno, A., Fernández-Donoso, R. and Pincheira, J. (1979). Similitud cromosómica: un nuevo método cuantitativo de descripción y comparación. Arch. Biol. Med. Exp. 12: 233 (Abstract).
• Thorgaard, G.H. and Gall, G.A.E. (1979). Adult triploids in a rainbow trout family. Genetics 93: 961-973.
• Ueda, T. (1983). Cytogenetical characters of 4 species in the salmonid fishes. Bull. Fac. Educ. Utsunomiya Univ. 34: 53-61.
• Ueda, T. and Ojima, Y. (1983). Geographic and chromosomal polymorphism in the Iwana (Salvelinus leucomaenis). Proc. Jpn. Acad. B59: 259-262.
• Uyeno, T. (1972). Chromosome offspring resulting from crossing coho salmon and brook trout. Jpn. J. Ichthyol. 19: 166-171.
• Veloso, A., Iturra, P., Colihueque, N., Díaz, N. and Estay, F. (1990). Polimorfismo cromosómico en dos poblaciones de la trucha arcoiris, Oncorhynchus mykiss (Walbaum), de la zona central de Chile. Biol. Pesq. 19: 3-8.

Publication Dates

• Publication in this collection
  02 June 1999
• Date of issue
  Mar 1999

History

• Received
  26 May 1997