© 2004 The American Genetic Association
Genetic Linkage Mapping of Allozyme Loci in Even- and Odd-year Pink Salmon (Oncorhynchus gorbuscha)
From the Juneau Center, School of Fisheries and Ocean Sciences, University of Alaska Fairbanks, 11120 Glacier Highway, Juneau, AK 99801 (Matsuoka, Gharrett, and Smoker), and the Auke Bay Laboratory, Alaska Fisheries Science Center, National Marine Fisheries Service, National Oceanographic and Atmospheric Administration, 11305 Glacier Highway, Juneau, AK 99801–8628 (Wilmot). M. P. Matsuoka is currently at the National Research Council, Institute for Marine Biosciences, 1411 Oxford St., Halifax, NS, B3H 3Z1, Canada.
Address correspondence to Makoto P. Matsuoka at the address above, or e-mail: makoto.matsuoka{at}nrc-cnrc.gc.ca.
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Abstract |
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We constructed genetic linkage maps of allozyme loci in even- and odd-year pink salmon (Oncorhynchus gorbuscha), using the total of 320 families (each female was crossed with two different males, and 80 females and 160 males were used for each of even year and odd year). The maps include eight linkage groups involving 22 loci. We observed substantial variation in recombination frequencies among different families within broodline and between sexes within broodlines. In the linkage analysis between sAAT-3* and sMDH-B1,2*, two even-year families and one odd-year family exhibited evidence of association, but two even-year and one odd-year families did not. Recombination rate tends to be reduced in males in pink salmon. The ratio of recombination rate (female/male), which ranged from 1.7 to infinity, averaged 2.8 in the even-year crosses and 3.2 in the odd-year crosses. The linkage groups (LG) I and II involving sAAT and mAH loci, which probably duplicated in the recent tetraploidization event, and the orders of loci in the LGs I (sAAT-3*
mAH-4*) and II (mAH-3* sAAT-4*) were reversed, suggesting the possible paracentric inversion during salmonid evolution after the duplication.
A linkage map can be constructed with information from joint segregation analysis and gene-centromere (G-C) distances. G-C distance can be estimated in gynogenetic progeny as the recombination frequency between a centromere and a locus on the same chromosome, and it determines the order of genes from centromere. We previously estimated G-C distances of 37 allozyme loci in pink salmon, Oncorhynchus gorbuscha (Matsuoka et al. 2004). Mating experiments are efficient methods to provide data for mapping in animal species such as fish and amphibians, which produce a large number of eggs and fertilize externally. Linkage maps have been constructed for a variety of allozyme loci in fish species, including the following: Oncorhynchus, Salmo, and Salvelinus spp. (e.g., May and Johnson 1993); Poecilia, Poecilopsis, and Xiphophorus spp. (e.g., Morizot et al. 1993); Fundulus heteroclitus (Brown et al. 1988); Lepomis spp. (Pasdar et al. 1984; Wheat et al. 1972; Wheat et al. 1973); and Ictalurus punctatus (Morizot et al. 1994). Comparison of linkage maps provides information about the evolution and rearrangement of syntenies. Although there are relatively few data for comparing linkage groups among different fish species, the comparisons that can be made exhibit extensive homology (Goodier and Davidson 1993). Moreover, comparisons of fish linkage maps with those of other vertebrates reveal chromosomal syntenies that have been conserved among widely divergent species. For example, PEP-B* and LDH-B* are syntenic in humans, many other mammals, salmonid fish, and ranid frogs (Ferguson and Allendorf 1991; Goodier and Davidson 1993; Morizot 1983).
In the evolutionary history of salmonid fish, a tetraploid origin and ongoing diploidization are widely accepted. Major chromosomal rearrangements during diploidization probably involved fusions of pairs of acrocentric chromosomes—in essence, Robertsonian translocations (Allendorf and Thorgaard 1984; Ohno 1970a,b). Researchers have studied linkage relationships of allozyme loci not only to determine whether homeologs, chromosomes that were duplicated during the tetraploidization event, have fused together to form single metacentric chromosomes, but also to construct linkage maps. In early studies of the inheritance of isoloci such as sAAT-1,2*, sIDHP-1,2*, LDH-A*, LDH-B*, and sMDH-B1,2*, an unusual result, termed pseudolinkage, showed an excess of recombinant progeny (Allendorf and Utter 1976; Aspinwall 1973, 1974; Kobayashi et al. 1984; May et al. 1975; May et al. 1979a,b; Morrison 1970; Stoneking et al. 1981; Wright et al. 1980). Pseudolinkage, which occurs only in males and appears to be unique in salmonids, has been interpreted as a form of residual tetrasomy resulting from pairing of multivalent homeologs (Johnson et al. 1987; Wright et al. 1983). To date, 18 classical linkage and five pseudolinkage groups have been found in hybrids of salmonid species, including cutbow trout (rainbow trout, Oncorhynchus mykiss, x cutthroat trout, Oncorhynchus clarki) and sparctic charr (brook trout, Salvelinus fontinalis, x arctic charr, Salvelinus alpinus; Johnson et al. 1987, May and Johnson 1993). Previous studies have also reported differences in recombination rate between sexes. Recombination rates tend to be reduced in male fish (Johnson et al. 1987; May and Johnson 1993), as well as in males of other species, such as Drosophila spp. (Morgan 1912), the palmate newt (Triturus helveticus; Callan and Perry 1977), and Japanese brown frogs (Rana japonica; Sumida and Nishioka 1994). Recent studies of molecular markers in fish have confirmed reduced recombination in male rainbow trout (Danzmann and Gharbi 2001; Sakamoto et al. 2000) and male zebrafish (Singer et al. 2002).
Previous analyses of linkage in pink salmon, O. gorbuscha, involved a small number of matings (Aspinwall 1973, 1974; Johnson 1979; McGregor 1982). Aspinwall (1974) studied inheritance of two isoloci, sMDH-A1,2* and sMDH-B1,2*, and found that sMDH-B1* and -B2* might be linked or pseudolinked. In this study, we conducted an intensive mating experiment and an inheritance study of allozyme loci in even- and odd-year pink salmon to construct linkage maps. The questions we addressed with these data include whether there is evidence for variation in linkage relationships within broodlines or between broodlines, whether recombination rates differ between sexes, and how the pink salmon linkage map compares to maps of other fish and vertebrate species.
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Materials and Methods |
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Fish and gametes used in this study were obtained from pink salmon returning to MaCaulay Hatchery, Douglas Island Pink and Chum, Inc., Juneau, Alaska. Families were produced in 1992 (even-year broodline) and 1993 (odd-year broodline). In each year, we used eggs from 80 females and semen from 160 males. Two batches of approximately 300 eggs from each female were crossed with two different males. In total, 160 bi-parental diploid families were produced each year. Families were designated E-1 to E-160 in the even year and O-1 to O-160 in the odd year. Fertilized embryos were incubated in F.A.L. HeathTM vertical incubators at ambient temperature (1.5–10.5°C). Dead embryos were removed as required.
Samples of muscle, heart, liver, and eye were taken from parental fish. Progeny families were sampled at the yolk absorption stage (7 to 8 months of age). Fish of some families for which heart and liver tissues expressed the enzymes of interest were transferred to aquaria and sampled when they were large enough for analysis (10 to 15 months of age). Two additional families were sampled to confirm linkage relationships between GPI-B1,2* and PEP-D2*. These latter crosses were made between one female from Auke Creek, Juneau, Alaska, and two males from Pillar Creek, Kodiak, Alaska, in 1997 (families K-23 and K-24). Tissue samples of adults, alevins, and fry were stored at –80°C until analysis.
Horizontal starch gel electrophoresis and histochemical stain techniques (Utter et al. 1986) were used to resolve allozyme bands. Locus nomenclature was according to Shaklee et al. (1990). Using stains for 32 enzymes described in Matsuoka et al. (2004), we detected 61 loci. Tissues of parental fish were screened to identify the most useful families for analysis. Of 61 loci screened, 25 loci in maternal parents and 21 loci in paternal parents were informative in the even year, and 21 loci in maternal parents and 23 loci in paternal parents were informative in the odd year. In total, we examined 7,927 progeny from 91 even-year families and 5,144 progeny from 73 odd-year families by starch gel electrophoresis to obtain genotype data.
Two types of crosses were analyzed statistically. First is the double backcrosses, in which one of the parents was a double heterozygote: AaBb x aabb. The hypothesis for the statistical test was that the progeny would have equal frequencies of the genotypes AaBb, Aabb, aaBb, and aabb. The second is the single backcrosses as AaBb x Aabb. The statistical hypothesis tested was that the progeny with genotypes AABb, aaBb, Aabb, and aabb would be equally abundant. The data for the genotypes AaBb and Aabb expected in the single backcross were omitted from the test because the origin of alleles cannot be identified. To test the joint segregation statistically, we calculated the likelihood of odds (LOD) score, using the formula
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is the recombination fraction, n is the sample size, and r is the number of recombinant progeny. We included pairs of loci with LOD scores greater than 3 in our linkage map. We also included the map pairs for which the LOD score was between 2 and 3 as possible linkage. Since linkage phases were unknown in this study, the number of progeny with parental (nonrecombinant) genotypes was assumed to exceed those of recombinant genotypes in estimates of recombination frequency; that is, recombination rate is no greater than 0.5. Distances were measured in centi-Morgans (cM). Homogeneity was tested with use of log-likelihood ratios (G tests: Sokal and Rohlf 1981). An adjustment of significance level for multiple tests was made according to the sequential Bonferroni method (Rice 1989). |
Results |
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We statistically analyzed joint segregation for 220 locus pairs in even-year and 187 locus pairs in odd-year families. Nonrandom assortment was observed at 19 locus pairs. Using information from these 19 locus pairs, we constructed eight linkage groups, which involved 22 loci in pink salmon (Figure 1 and Appendix Table A). The loci in each linkage group were ordered according to the G-C distances estimated in our previous study (Matsuoka et al. 2004).
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Homogeneity in Recombination Rate Among Families
Homogeneity in recombination rates among families was tested separately for each informative sex for each broodline for each locus pair (Table 1). Heterogeneity was observed in three out of 17 tests in females at a significance level of.05. One test was still significant after the Bonferroni correction for multiple tests. In contrast, seven of 15 tests in males showed heterogeneity. The result was still significant in three tests after the correction for multiple tests.
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Homogeneity in recombination rates between broodlines was tested for each locus pair for each informative sex. Heterogeneity was observed at one out of six locus pairs tested in females at 0.05, but it was not significant after the correction. In males, two out of the eight locus pairs tested were significant, and one of them was significant after the correction (Table 1).
We observed contradictory results among families in the linkage relationship between sAAT-3* and sMDH-B1,2*. Two even-year families, E-231 and E-232, and one odd-year family, O-151 (O-118 showed possible linkage), exhibited evidence of association between two loci. In contrast, two even-year families (E-223 and E-224) and one odd-year family (O-199) failed to show evidence of association (Table 2).
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Recombination Rates Between Sexes
Homogeneity in recombination rates between sexes within broodline in classical linkage groups was tested using the pooled recombination rates (Table 1). Heterogeneity was observed in 16 out of 18 instances, and 12 tests remained significant after the Bonferroni correction. The pooled recombination rates in females always exceeded those of males in all comparisons (Table 1).
The ratios of recombination rates (female/male) between sexes were calculated in five linkage groups (Table 3). The ratios, which ranged from 1.7 to infinity, averaged 2.8 in the even-year data and 3.2 in the odd-year data. The ratios between broodlines (even year versus odd year) within a region were inconsistent, and the ratios were 18 versus 2.9 between ADA-2* and PGDH*, and 2.6 versus 13.5 between mMEP-1* and sIDHP-1,2*.
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Discussion |
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Pink Salmon Genetic Linkage Map
We detected eight linkage groups that included 22 loci in this study. Explanations are necessary for some assignments. In LG VI, we assigned classical linkage for LDH-B1* and PEP-B*, though we did not have a family for examining segregation in females. Two families showed strong evidence of nonrandom assortment in males. In addition, the loci are classically linked in other salmonid fish, as well as in vertebrate species including humans, many mammals, and amphibians (Ferguson and Allendorf 1991; Goodier and Davidson 1993; Morizot 1983). The order of loci is unknown, because we did not have a family for estimating the G-C distance of LDH-B1* in our previous study (Matsuoka et al. 2004). LG VII includes three loci, GDA*, GPI-B1,2*, and PEP-D2*. In even-year families, map distances between GPI-B1,2* and GDA* (41.7 cM), and between GDA* and PEP-D2* (43.7 cM), suggest GDA* and each of the other two loci are distal to one another. We assigned GDA* to the opposite arm of a metacentric chromosome. DIA-1* and FDHG* showed nonrandom assortment only in males. They are on different chromosome arms of the same metacentric chromosome (distal to each other), or they may be pseudolinked. We tentatively assigned them as LG VIII. Possible pseudolinkage relationships were found in LGs IV and VIII, including G3PDH-1* and sMDH-A1,2*, which are pseudolinked in splake charr and in sparctic charr (May and Johnson 1993). Pseudolinkage was defined as an excess of nonparental male gamete types relative to parental ones (Johnson et al. 1987); the linkage phase of parental fish must be known to examine this matter. In this study, the linkage phase was unknown. Since pseudolinkage is observed only in males, we interpreted a locus pair that showed linkage only in males as possible pseudolinkge.
Johnson (1979) examined joint segregation of four locus pairs (G3PDH-1* with sMDH-B1,2*, G3PDH-1* with mMEP-1*, G3PDH-1* with PGM-2*, and sMDH-B1,2* with mMEP-1*) in odd-year pink salmon (BY1977) and found no linkage relationships in these four pairs. We tested the first three of the four pairs Johnson tested, and did not find any significant relationship. We did not have a family to test for the last locus pair (sMDH-B1,2* with mMEP-1*). McGregor (1982) examined 17 locus pairs and found strong nonrandom assortment between GPI-B1,2* and PEP-D2*, and weak nonrandom assortments between mAH-4* and PGDH* in males and between sAAT-3* and PEP-D2* in females. This study confirmed the previous observations of association between GPI-B1,2* and PEP-D2*. However, no evidence of linkage was found for two other locus pairs. For 14 other locus pairs of random assortment in McGregor's study, our result agreed with his result, except for GPI-B1,2* and mMEP-1*, for which we did not have a family to test.
The pink salmon LGs I (including mAH-4* and sAAT-3*) and II (including mAH-3* and sAAT-4*) may have been derived from a single ancestral linkage group and duplicated during the tetraploidization event. In our map, the orders of mAH* and sAAT* in the two linkage groups are reversed (at least in odd-year pink salmon). mAH-4* is distal in LG I, and sAAT-4* is distal in LG II. This indicates that at least one paracentric inversion occurred after the duplication. Major chromosomal rearrangements, which occurred in salmonid species after the tetraploidization event (25–100 million years ago), generally involved centric fusions, in which pairs of acrocentric chromosomes form metacentric chromosomes (e.g., Allendorf and Thorgaard 1984).
We found possible variation in the position of one locus of sMDH-B1,2* between broodlines. G-C distances at sMDH-B1,2* from five even-year families ranged from 31 to 50 cM, with significant heterogeneity (though no such variation in 11 odd-year families ranged from 46 to 50 cM), suggesting the variation at sMDH-B1,2* may be occurring at both of the isoloci (Matsuoka et al. 2004). In the study we observed that one locus of sMDH-B1,2* linked with sAAT-3* showed G-C distance of 50 cM, and another locus not linked with sAAT-3* showed an intermediate level of 34 cM in the even broodyear. This supports our previous observation in G-C distances, which is one cross involved variants at one of the loci and the other cross had the same variants at the other locus. In the odd-year fish, both loci are distal (50 cM), regardless of the linkage with sAAT-3*. Because sMDH-B1,2* is not sufficiently variable to lend itself to desirable mating studies, an additional inheritance study would be necessary to address this question.
The cause of the variation we observed among families through this experiment is unknown. The possible factors are chromosomal rearrangements such as translocation, inversion, insertion, and deletion, as well as differences in DNA structure (sequence), genetic control mechanisms, and environmental factors such as temperature (Lichten and Goldman 1995; Wright et al. 1983).
Reduced Recombination Rate in Males
Suppression of recombination rate in males, which has been reported in rainbow trout and Salvelinus species (Johnson et al. 1987; May and Johnson 1993), was observed in this study in pink salmon. The average ratio of recombination rates in pink salmon in this study was 2.8:1 in the even year and 3.2:1 in the odd year. The ratios of female:male recombination rates among adjacent markers ranged from 1.7 to infinity. Recently, sex-associated differences in recombination rate have been examined with use of higher density linkage maps with DNA markers such as microsatellite loci in rainbow trout (Sakamoto et al. 2000) and zebrafish (Singer et al. 2002). The ratio of female:male recombination rates among all adjacent markers in rainbow trout averaged 3.25:1, varying from infinity to 0.00 (Sakamoto et al. 2000), and 2.74:1 in zebrafish (Singer et al. 2002). Sakamoto et al. (2000) also observed that rainbow trout female recombination rates near the centromere were much higher than those of males, and, conversely, male recombination rates appeared to be higher in telomeric regions. The same tendency was observed in zebrafish (Singer et al. 2002). We observed no recombination in male pink salmon in the region including the centromere in LG I (Figure 1 and Appendix Table A). This is consistent with the observations in the previous studies that the female recombination rate is much higher near the centromere. The mechanism that reduces recombination in males has been proposed in terms of chiasmata distributions. In mice and human males, a strong telomeric/subtelomeric localization of chiasmata has been observed. In female mice, the tendency toward subtelomeric localization is significantly reduced and chiasmata are more broadly distributed (Lichten and Goldman 1995). This observation suggests that chiasmata in male pink salmon might share telomeric/subtelomeric localization with mice and humans.
Comparisons of the Pink Salmon Map with Fish and Other Vertebrate Maps
Comparisons of linkage groups of pink salmon to those of other fish species are summarized in Table 4. Three linkage groups (VIII, IX, and X) detected in pink salmon were previously reported in the maps of other salmonids (May and Johnson 1993). The pink salmon LG VIII (sIDHP-1,2* and mMEP-1*) would be homologous with linkage group 5L (Idh-3 and Me-2). The linkage between these loci seems to be tighter in Salvelinus than in Oncorhynchus. G-C maps revealed that mMEP-1* is distal in these species: 48 cM in pink salmon (Matsuoka et al. 2004), 49 cM in splake trout, and 48 cM in rainbow trout (May and Johnson 1993). The intergeneric difference in recombination frequencies for this locus pair might reflect a difference in the physical position of sIDHP-1,2* (Idh-3*) or in the location of sites at which recombination occurs frequently. LDH-B1* and PEP-B* are tightly linked in cutbow trout (7 cM) and splake trout (8 cM), and each of the two loci is proximal to the centromere. In pink salmon, although PEP-B* is proximal (5 in even year and 10.5 cM in odd year), no informative family was available for our examination of recombination in females for this locus pair or for our estimation of G-C distance for LDH-B1*. GPI-B2* and PEP-D2* are also tightly linked in splake trout, and the G-C distance at PEP-D2* is distal (48 cM). In pink salmon, the two loci are also tightly linked, and the G-C distance indicates that they are at 47 cM for GPI-B1,2* and 46 cM for PEP-D2*. In Xiphophorus (Poeciliidae), 80 polymorphic biochemical loci have been assigned to 14 multipoint linkage groups (e.g., Morizot et al. 1991; Morizot et al. 1993). ADA* and PGD* (PGDH*) are linked in Xiphophorus (41 cM). ADA-2* and PGDH* are classically linked in this study. Linkage between GPI-1* (presumably homologous with GPI-B1,2* in pink salmon) and PEP-D* was also observed in Xiphophorus and Poeciliopsis. Linkages between LDH-B1* and PEP-B*, and between sIDHP-1,2* and sMEP-1*, detected in this study have not been not tested in Poeciliids.
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A synteny, which is presumably homologous with LG IX (LDH-B1* and PEP-B*) in pink salmon, has been observed in 10 vertebrate species (listed in O'Brien 1993) from Xenopus to human. As well, a synteny homologous with LG X (GPI-B1,2* and PEP-D2*) has been observed in 12 vertebrates. However, these two loci are not linked and belong to different linkage groups in mouse (Mus musculus), rat (Rattus norvegicus), and rabbit (Oryctolagus cuniculus). In contrast, no linkage relationships of presumably homologous loci of LGs IV (ADA-2* and PGDH*) and VIII (sIDHP-1,2* and mMEP-1*) have been reported in any other vertebrates (O'Brien 1993). In mouse, mink, and cow, the loci presumably homologous to sIDHP-1,2* and sMEP-1* are on different chromosomes, and ADA-2* and PGDH* belong to different syntenies in mink, rat, mouse, cotton-topped marmoset, and humans. The biological meaning of conserved linkage groups over divergent species is unknown. Morizot (1983) suggested that inversions and translocations might have occurred infrequently and even rather loose linkage might persist for millions of years. However, comparisons of pink salmon linkage maps to other species suggest that linkage of two conserved groups, X and IX, was tighter than one of two unconserved groups, IV and VIII. In addition, two loci of the linkage group X are on different chromosomes in some species, as described above. This information suggests that conservation of a synteny may be more affected by the physical nature of linkage (tight or loose) than as yet undefined functional or structural constraints, such as that a synteny must be conserved to make genes function properly.
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Acknowledgments |
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We gratefully acknowledge DIPAC (Douglas Island Pink and Chum, Inc., Juneau, Alaska) for providing materials and facility to incubate eggs; and C. Kondzela, S. Hawkins, X. Luan, H. Nguyen, C. Guthrie, and C. Russell (Auke Bay Lab, NMFS, NOAA) for their technical support for starch gel electrophoresis. We also thank Dr. Katsutoshi Arai (Hokkaido University, Japan) and Dr. Patricia Crandell (University of Alaska Fairbanks) for their suggestions and help with this experiment. This study was supported by a research grant from the Alaska Science and Technology Foundation to W.W.S. (90-1-040). Complementary research and publication charges were supported by Alaska Sea Grant with funds from the National Oceanic and Atmospheric Administration Office of Sea Grant, Department of Commerce, under grant no. NA16RG2321 (project nos. R/31-06 and RR/03-05), and by the University of Alaska with funds appropriated by the state.
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Footnotes |
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Corresponding Editor: William Modi
Received September 15, 2003
Accepted April 9, 2004
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References |
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Allendorf FW, Thorgaard GH, 1984. Tetraploidy and the evolution of salmonid fishes. In: Evolutionary genetics of fishes (Turner B, ed). New York: Plenum Press; 1–53.
Allendorf FW, Utter FM, 1976. Gene duplication in the family Salmonidae. III. Linkage between two duplicated loci coding for aspartate aminotransferase in the cutthroat trout (Salmo clarki). Hereditas. 82:19-24.[Web of Science][Medline]
Aspinwall N, 1973. Inheritance of alpha-glycerophosphate dehydrogenase in the pink salmon, Oncorhynchus gorbuscha (Walbaum). Genetics. 73:639-643.
Aspinwall N, 1974. Genetic analysis of duplicate malate dehydrogenase loci in the pink salmon, Oncorhynchus gorbuscha. Genetics. 76:65-72.[Abstract]
Brown DC, Ropson IJ, Powers DA, 1988. Biochemical genetics of Fundulus heteroclitus (L.): V. Inheritance of 10 biochemical loci. J Hered. 79:359-365.
Callan HG, Perry PE, 1977. Recombination in male and female meiocytes contrasted. Phil Trans R Soc Lond B Biol Sci. 277:227-233.[CrossRef][Web of Science][Medline]
Danzmann RG, Gharbi K, 2001. Gene mapping in fishes: a means to an end. Genetica. 111:3-23.[CrossRef][Web of Science][Medline]
Ferguson MM, Allendorf FW, 1991. Evolution of the fish genome. In: Biochemistry and molecular biology of fishes, vol.1 (Hochachka PW and Mommsen TP, eds). New York: Elsevier; 25–42.
Goodier JL, Davidson WS, 1993. Gene mapping in fish. In Biochemistry and molecular biology of fishes, vol.1 (Hochachka PW and Mommsen TP, eds). New York, Elsevier, 93–112.
Johnson KR, 1979. Genetic variation in populations of pink salmon (Oncorhynchus gorbuscha) from Kodiak Island, Alaska (MSc thesis). Seattle, Washington: University of Washington.
Johnson KR, Wright JE, Jr, May B, 1987. Linkage relationships reflecting ancestral tetraploidy in salmonid fish. Genetics. 116:579-591.
Kobayashi K, Milner GB, Teel DJ, Utter FM, 1984. Genetic basis for electrophoretic variation of adenosine deaminase in chinook salmon. Trans Am Fish Soc. 113:86-89.[CrossRef]
Lichten M, Goldman ASH, 1995. Meiotic recombination hotspots. Annu Rev Genetics. 29:423-444.[CrossRef][Web of Science][Medline]
Matsuoka MP, Gharrett AJ, Wilmot RL, Smoker WW, 2004. Gene-centromere mapping of allozyme loci in even- and odd-year pink salmon (Oncorhynchus gorbuscha). Genetica. 121:1-11.[CrossRef][Web of Science][Medline]
May B, Johnson KR, 1993. Composite linkage map of salmonid fishes (Salvelinus, Salmo, Oncorhynchus). In: Genetic maps: locus maps of complex genomes, book 4, nonhuman vertebrates, 6th ed. (O'Brien SJ, ed). Cold Spring Harbor, NY: Cold Spring Harbor Laboratory; 309–317.
May B, Stoneking M, Wright JE, Jr, 1979a. Joint segregation of malate dehydrogenase and diaphorase loci in brown trout (Salmo trutta). Trans Am Fish Soc. 108:373-377.[CrossRef]
May B, Utter FM, Allendorf FW, 1975. Biochemical genetic variation in pink and chum salmon. J Hered. 66:227-232.
May B, Wright JE, Stoneking M, 1979b. Joint segregation of biochemical loci in Salmonidae: results from experiments with Salvelinus and review of the literature on other species. J Fish Res Board Can. 36:1114-1128.
McGregor AJ, 1982. A biochemical genetic analysis of pink salmon (Oncorhynchus gorbuscha) from selected streams in northern Southeast Alaska (MSc thesis). Juneau, Alaska: University of Alaska–Juneau.
Morgan TH, 1912. Complete linkage in the second chromosome of the male of Drosophila. Science. 36:719-720.
Morizot DC, 1983. Tracking linkage groups from fishes to mammals. J Hered. 74:413-416.
Morizot DC, Harless J, Nairn RS, Kallman KD, Walter RB, 1993. Linkage maps of non-salmonid fishes. In: Genetic maps: locus maps of complex genomes, book 4, nonhuman vertebrates, 6th ed. (O'Brien SJ, ed). Cold Spring Harbor, NY: Cold Spring Harbor Laboratory; 318–325.
Morizot DC, Schmidt ME, Carmichael GJ, 1994. Joint segregation of allozymes in catfish genetic crosses: designation of Ictalurus punctatus linkage group I. Trans Am Fish Soc. 123:22-27.[CrossRef]
Morizot DC, Slaugenhaupt SA, Kallman KD, Chakravarti A, 1991. Genetic linkage map of fish of the genus Xiphophorus (Teleostei: Poeciliidae). Genetics. 127:399-410.[Abstract]
Morrison WJ, 1970. Nonrandom segregation of two lactate dehydrogenase subunit loci in trout. Trans Am Fish Soc. 99:193-206.[CrossRef]
O'Brien SJ, 1993. Genetic maps: locus maps of complex genomes, book 4, nonhuman vertebrates, 6th ed. Cold Spring Harbor NY: Cold Spring Harbor Laboratory.
Ohno S, 1970a. The enormous diversity in genome sizes of fish as a reflection of nature's extensive experiments with gene duplication. Trans Am Fish Soc. 99:120-130.
Ohno S, 1970b. Evolution by gene duplication. New York: Springer-Verlag.
Pasdar M, Philipp DP, Whitt GS, 1984. Linkage relationships of nine enzyme loci in sunfishes (Lepomis; Centrarchidae). Genetics. 107:435-446.
Rice WR, 1989. Analyzing tables of statistical tests. Evolution. 43:223-225.[CrossRef][Web of Science]
Sakamoto T, Danzmann RG, Gharbi K, Howard P, Ozaki A, Khoo SK, Woram RA, Okamoto N, Ferguson MM, Holm LE, et al., 2000. A microsatellite linkage map of rainbow trout (Oncorhynchus mykiss) characterized by large sex-specific differences in recombination rates. Genetics. 155:1331-1345.
Shaklee JB, Allendorf FW, Morizot DC, Whitt GS, 1990. Gene nomenclature for protein-coding loci in fish. Trans Am Fish Soc. 119:2-15.[CrossRef]
Singer A, Perlman H, Yan Y, Walker C, Corley-Smith G, Brandhorst B, Postlethwait J, 2002. Sex-specific recombination rates in zebrafish (Danio rerio). Genetics. 160:649-657.
Sokal RR, Rohlf FJ, 1981. Biometry, 2nd ed. New York: Freeman.
Stoneking M, May B, Wright JE, 1981. Loss of duplicate gene expression in salmonids: evidence for a null allele polymorphism at the duplicate aspartate aminotransferase loci in brook trout (Salvelinus fontinalis). Biochem Genet. 19:1063-1077.[CrossRef][Web of Science][Medline]
Sumida M, Nishioka M, 1994. A pronounced sex difference when two linked loci of the Japanese brown frog Rana japonica are recombined. Biochem Genet. 32:361-369.[CrossRef][Web of Science][Medline]
Utter F, Aebersold P, Winans G, 1986. Interpreting genetic variation detected by electrophoresis. In: Population genetics and fishery management (Ryman N and Utter F, eds). Seattle: University of Washington Press; 21–45.
Wheat TE, Whitt GS, Childers WF, 1972. Linkage relationships between the homologous malate dehydrogenase loci in teleosts. Genetics. 70:337-340.
Wheat TE, Whitt GS, Childers WF, 1973. Linkage relationships of six loci in interspecific sunfish hybrids (genus Lepomis). Genetics. 74:343-350.
Wright JE, Jr, Johnson K, Hollister A, May B, 1983. Meiotic models to explain classical linkage, pseudolinkage, and chromosome pairing in tetraploid derivative salmonid genomes. Isozymes Curr Top Biol Med Res. 10:239-260.[Web of Science][Medline]
Wright JE, Jr, May B, Stoneking M, Lee GM, 1980. Pseudolinkage of the duplicate loci for supernatant aspartate aminotransferase in brook trout, Salvelinus fontinalis. J Hered. 71:223-238.
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