The Splendour and Misery of European Pink Salmon, Oncorhynchus gorbuscha: Abundant Odd Lineage vs. Depressed Even Lineage—Insights from cytb Gene Analysis
by
,
Daria A. Zelenina
1,*,
Valeria A. Soshnina
1,
Ilya I. Gordeev
1,2,*, 
Maksim M. Alekseev
3,
Vladimir A. Zadelenov
4 and
Nikolai S. Mugue
1,5
1
Russian Federal Research Institute of Fisheries and Oceanography, Moscow 105187, Russia
2
Department of Invertebrate Zoology, Faculty of Biology, Lomonosov Moscow State University, Moscow 119234, Russia
3
Polar Branch of Russian Federal Research Institute of Fisheries and Oceanography (“PINRO”), Murmansk 183038, Russia
4
Krasnoyarsk Branch of Russian Federal Research Institute of Fisheries and Oceanography (“NIIERV”), Krasnoyarsk 660049, Russia
5
Koltzov Institute of Developmental Biology of the Russian Academy of Sciences (IDB RAS), Moscow 119334, Russia
*
Authors to whom correspondence should be addressed.
Diversity 2025, 17(8), 563; https://doi.org/10.3390/d17080563
Submission received: 30 June 2025
/
Revised: 4 August 2025
/
Accepted: 6 August 2025
/
Published: 11 August 2025
(This article belongs to the Special Issue Genetic and Morphological Diversity of Marine Fish Populations)
Abstract
Pink salmon, Oncorhynchus gorbuscha, introduced to the White Sea and expanded throughout the West Arctic and Northern Atlantics, represents a noteworthy example of a successful marine species introduction that has significantly impacted the local fish community. In our study, we analysed mitochondrial cytochrome b sequences from 635 individuals, representing both odd-year (n = 411) and even-year (n = 224) spawning lineages. These samples were collected from rivers in the White, Barents, Kara, and Northern seas, as well as from source populations in the Pacific. Fifteen cytb haplotypes were identified in the odd-year spawning lineage and twenty-six in the even-year lineage, with only ten haplotypes found in both lineages. The results demonstrated significant genetic differences between the native Pacific populations and the introduced Arctic populations in the odd-year lineage. In contrast, no genetic differentiation was found in the even-year lineage. This study describes the current haplotypic structure of European pink salmon in the Russian Arctic and provides insights into the genetic consequences of the species’ introductions.
1. Introduction
Pink salmon Oncorhynchus gorbuscha (Walbaum, 1792) is the most widespread and abundant species of Pacific salmon. Commercial fishing for pink salmon occurs throughout most of its range in the Northern Hemisphere. In the Russian Federation, pink salmon is a key species for fisheries, with catches in the Far Eastern fishery basin reaching 478,500 tons in 2023 and 136,200 tons in 2024.
Due to its strict two-year life cycle, pink salmon has two allochronic lineages: one that spawns in odd years and another that spawns in even years. These two lineages diverged a long time ago, with estimates of their reproductive isolation ranging from 0.9 to 1.1 million years [1] to as recently as 23,600 years [2]. This extended period of independent evolution has led to differences in both morphological [3,4] and ecological characteristics [5,6]. The most pronounced intraspecific genetic differences are also observed between the lineages. This conclusion is supported by mitochondrial [7,8,9], nuclear [10,11], and genomic research [12,13].
Pink salmon, a species not native to the North Atlantic, found a new home thanks to an ambitious experiment that began in 1956. This translocation program sought to enrich the commercial fish species and enhance the raw material base for regional fisheries. The introduction of pink salmon into the rivers of the White Sea proved to be a successful endeavour: this led not only to their thriving acclimatization but also to a striking increase in their populations throughout the European part of Russia [14]. As a result, this successful introduction transformed the region’s aquatic landscape and opened the door to the industrial development of pink salmon fishing.
Efforts to transport fertilised pink salmon eggs from the Far East hatcheries in the White Sea basin continued intermittently until 1998. During the first stage of introduction, from 1956 to 1980, over 200 million artificially fertilised pink salmon eggs, mostly from southern Sakhalin hatcheries, were brought to various salmon hatcheries in the White Sea [15,16]. Significant annual fluctuations in fish returns were observed, along with a rapid decline in the established population, particularly when no additional eggs were transported from their native range.
The second stage began in 1985, and this time, eggs were collected from the northern O. gorbuscha population from the Magadan Region, specifically from the Ola River. A single introduction of a small batch of pink salmon eggs from the odd-year spawning lineage in 1985 [15] sparked a natural reproduction process for pink salmon in the new area [17]. By 1989, a substantial pink salmon spawning run was noted in the rivers of the Kola Peninsula, and by 1993, the catch reached approximately 176,000 fish, totalling about 210 tons [14]. It is important to note that—as evidenced by various genetic markers, including allozymes [15], mtDNA restriction fragments [18], and microsatellites [17]—the introduction event resulted in a partial reduction in genetic diversity in the new area compared to the native range.
Since the introduction of “Magadan” pink salmon, their population and spawning range in the new area have increased significantly. Pink salmon have successfully adapted to the rivers of the White and Barents Seas and have expanded their distribution both westward into the North Atlantic [19,20,21] and eastward into the rivers of the Kara Sea [22]. Pink salmon spawning has also been observed in the rivers of the British Isles [23].
The information above pertains specifically to the odd-year spawning lineage. In contrast, the situation for the pink salmon of the even lineage is quite different. Despite multiple introduction attempts in 1984, 1986, 1996, and 1998, the “even” O. gorbuscha population experienced a sharp decline in the following generation. Interestingly, genetic analyses of two generations after the introduction did not show a significant reduction in the genetic diversity of the even pink salmon in their new habitat [17].
The depressed state of native Atlantic salmon Salmo salar populations, whose catches in Russia are steadily declining (Section 4), makes assessing the population stability and genetic structure of pink salmon important for fisheries in the region. Numerous studies have explored the potential interaction and competition between Atlantic salmon and pink salmon [24,25,26,27,28]. The most significant concerns are associated with the competition of these two species for food resources during migration. Much remains unknown about the interaction between them; however, long-term observations have shown no correlation between pink salmon and Atlantic salmon catches. The potential threat that pink salmon pose to the commercially valuable Atlantic salmon is a key reason for the heightened interest in understanding the population dynamics and distribution of pink salmon.
In this study, we examined the polymorphism of the mitochondrial gene cytb, a genetic marker commonly used in salmonid research. We focused on odd-year spawning and even-year spawning populations of pink salmon from both the European and Asian parts of their range. This approach allowed us to explore subtle differences for the first time at various levels: (1) between native and introduced areas within each lineage, (2) among different regions within the introduced area (only for the odd lineage), and (3) between odd-year and even-year spawning lineages in the new range.
2. Materials and Methods
2.1. Sampling
Samples of pink salmon were collected by the staff of the Russian Federal Research Institute of Fisheries and Oceanography (“VNIRO”) and local fisheries authorities during the spawning run in the rivers of the Arctic coast of Russia and in the Magadan area (Figure 1). A total of 635 genetic specimens were analysed in this study: 411 were collected in odd years and 224 were collected in even years (Table 1). Among these, four samples (203 fish), including a sample from Scotland, of odd-year spawning pink salmon were previously utilized in our earlier study (Table 1). A detailed description of the sampling sites in Scotland can be found in that study [29]. Fin tissues were fixed in 96% ethanol and stored at −20 °C until DNA extraction.
2.2. Genetic Analysis
The isolation and purification of total DNA were performed by adsorption onto AcroPrep™ 96 filter plates, 1 mL–1.0 mm, glass fibre media microcolumns (PALL, Port Washington, NY, USA), as described earlier [30]. Complete Cytb gene sequences (1141 bp) were amplified and sequenced in accordance with [31]. Sequencing was performed on an ABI Prism Genetic Analyzer 3500 (Applied Biosystems, Waltham, MA, USA).
2.3. Data Analysis
Cytochrome B sequences were analysed using the Geneious 6.0.5 software package [32]. We used data from our previous study (see Table 1), which included 203 sequences, each 1018 bp in length. Therefore, prior to building multiple sequence alignments, all sequences were trimmed to 1018 bp. TCS haplotype networks were constructed in the PopArt (https://popart.maths.otago.ac.nz, accessed on 1 June 2025) software [33]. We calculated nucleotide and haplotype diversity and conducted Tajima’s test for selective neutrality, along with hierarchical AMOVA, using the Arlequin v3.5.1.3 software program [34]. For pairwise differentiation, we applied a probabilistic exact test [35] and computed pairwise ΦST using the Kimura 2-Parameter model [34].
3. Results
Cytb sequences were obtained for 635 pink salmon individuals, resulting in 31 haplotypes (Table 2). In 224 fish from the even-year spawning lineage, we identified 26 haplotypes, whereas in 411 fish from the odd-year spawning lineage, 15 haplotypes were found, and only 10 were common to both lineages (Table 2 and Table 3). Because these lineages diverged thousands of years ago and evolved and reproduced independently, we first made comparisons within each. We analysed samples from the artificially introduced area for both lineages and compared them to the source populations.
3.1. Odd-Year Spawning Lineage
Samples of odd-year spawning pink salmon were collected outside their native range in several regions. Samples from the White Sea (KER17, UMBA21, VARZ23, MEZ23), the Barents Sea (KOLA19), the Kara Sea (PYAS17 from the Pyasina River), and the North Sea (SCOT17 from Scotland) exhibited genetic similarities (see Table 3 and Table 4). The PYAS17 sample is confirmed to be of White Sea (WS) origin, as it contains the identical six haplotypes found in most populations of this group and shows no significant differences from other samples based on pairwise comparisons.
For the odd-year lineage, we compared 274 individuals from seven Atlantic and Arctic populations with 137 individuals from two rivers in the Pacific basin: the Ola River (source river for translocation, sample OLA09) and the Taui River (samples TAUI11 and TAUI17), which also flows into Magadan Bay. In the populations from the native range, we identified 13 haplotypes, while, after the introduction, the number of haplotypes decreased to 8 (Table 2, Figure 1). Notably, two of these were singletons, so only six haplotypes were common across most populations of WS origin (Table 3, Figure 1a).
The computations of pairwise ΦST and the exact test for pairwise population differentiation, as shown in Table 4, reveal highly significant differences between odd-year spawning pink salmon from their native range and those from introduced regions. In contrast, all intra-regional tests, with two minor exceptions, yielded non-significant results. Furthermore, the AMOVA analysis indicated significant differentiation between Pacific and Atlantic groups (Table 5a), although no significant differences were found among samples within these groups (see Table 5b).
3.2. Even-Year Spawning Lineage
In contrast to the odd-year pink salmon, the even-year lineage is notably less abundant in the Atlantic part of its range. In this study, we analysed 96 individuals from the Umba River (UMBA18), the site of the pink salmon introduction to this new area, and compared them with 128 fish from the Ola (OLA16, OLA22) and Taui (TAUI12, TAUI16) Rivers from the source area. Following the translocation, the number of haplotypes decreased by nearly half (Table 2). However, the frequencies of the dominant haplotypes changed very little (Table 3, Figure 1b). Three statistical approaches—pairwise ΦST, Fisher’s exact test (Table 4), and AMOVA (Table 5c)—found no significant differences among the samples within the Pacific group or between the Atlantic and Pacific basins.
3.3. Odd-Year Versus Even-Year Pink Salmon Lineages
In both lineages, nucleotide and haplotype diversity values were higher in the native part of the range compared to the introduced part. Among the two lineages, all even-year spawning populations exhibited greater polymorphism than those sampled in odd years (Table 2, Figure 2c). Following the introduction, the total number of haplotypes was reduced by nearly half (Figure 1 and Figure 2, Table 3).
In even-year lineages, the frequencies of most mass haplotypes in both native and introduced areas were similar (Figure 2a). In contrast, among odd-year lineages, two haplotypes, A1-13 and B1-15, which were very rare in the native range, became prevalent after their introduction (Figure 2b). Haplotype B1-59 was found at a significant frequency in both lineages but only in the introduced area (see Figure 2c). Notably, we did not detect this haplotype in over 4000 individuals collected from across the Pacific Rim (Zelenina et al., unpublished [36]).
4. Discussion
The odd-year spawning pink salmon became an important biological resource in the White Sea, exploited by both industrial fishing companies and numerous amateur fishermen. From 2000 to 2024, the total catch varied between 98.3 and 714.7 tons in odd-numbered years, with an average of 263 ± 50.63 tons. In contrast, during even-numbered years, the total catch ranged from 0.1 to 11.1 tons, averaging 3.3 ± 0.99 tons (Figure 3). In 2023, the primary catch was concentrated along the northern coast of the White Sea in the Murmansk region, particularly in the Varzuga and Umba rivers, using fixed seines and fish-counting barriers. The most successful even-numbered year recorded to date is 2021, when 714.7 tons were caught across the regions of Murmansk and Arkhangelsk, the Republic of Karelia, and the Nenets Autonomous Region.
In the new range of pink salmon, odd-year spawning fish are notably more numerous. Generally, one lineage of pink salmon is more abundant than the other in their natural habitats, although this pattern can vary by region. In the United States and Canada, the odd-year lineage is predominant in the southern part of their range, particularly in Washington and southern British Columbia. Conversely, the even-year lineage is more numerous in the northern regions, specifically in northern British Columbia and Alaska. It has been suggested that modern-day lineages originated from different glacial refuges [37]. Consequently, each lineage seems to be better adapted to either warmer or colder environments, respectively [11].
It is generally accepted that Asian pink salmon stocks primarily originate from the northern glacial refuge in Beringia [12]. However, their numbers vary between odd and even years in different regions of the northwestern Pacific. In some areas, odd-year spawners are more prevalent, while in others, even-year spawners dominate. Interestingly, the dominance of a specific lineage in a region is not static; it tends to shift approximately once every few decades [38]. During years of high abundance for the dominant lineage, pink salmon catches can exceed those of adjacent years by tenfold or more [38,39]. In the White and Barents Seas, the number of pink salmon spawning runs in odd years is several dozen times greater than in even years. This phenomenon likely results from the more successful introduction of the odd-spawning lineage, which probably has better adaptability [17]. However, it is also possible that we may witness a future switch in dominance, similarly to what occurs in the northern Pacific.
Except for the European North, another notable case of successful pink salmon adaptation occurred in 1956. This began with a single accidental introduction of an odd-year spawning lineage to the Great Lakes [40]. Since then, the species has established a stable population, spreading throughout the lake–river system, and can now be found in every Great Lake. This species, which is typically considered obligately anadromous, has successfully formed a reproducing freshwater stock. Furthermore, spawning now occurs in both odd and even years, and both stocks have the odd-year source [41,42]. Numerous records of three-year-old fish explain this phenomenon [43].
Our study also investigates the evolution of the same species in a recently inhabited area. Both lineages were introduced here; however, only the odd-year spawning lineage has successfully established itself and dispersed widely to neighbouring regions. In contrast, the other lineage reproduces in the European North but in significantly smaller numbers. This creates opportunities for pink salmon spawning in even-numbered years. If the even-year lineage proves to be less adaptive, it might be supplemented or partially replaced by fish from the odd-year spawning lineage. At first glance, our results seem to contradict this hypothesis. According to our previous research [9], the two pink salmon lineages in their native range exhibit significant differences in cytb haplotype content. In the Arctic–Atlantic basin, the haplotype composition for each lineage reflects their respective source populations (Figure 1), indicating the even-year spawning lineage’s origin of the depressed lineage.
When comparing genetic diversity between the source and introduced populations, we found that a significant founder event resulted in notable differences between the two groups for the odd-year spawning lineage. The translocation also decreased genetic diversity in the even-year spawning lineage due to the partial loss of rare haplotypes. However, the frequencies of major haplotypes remained nearly the same, and no significant differences were observed within the even-year spawning lineage. We can propose two hypotheses to explain this discrepancy. First, there was only one introduction event of odd-year spawning pink salmon, resulting in a relatively low number of individuals and limited genetic polymorphism in the new area. In contrast, the translocations of even-year spawners occurred repeatedly, which significantly increased their original genetic diversity. Additionally, some adaptive alleles for the new environment may have been present in the introduced odd-year pink salmon eggs but absent in other lineages. In the new area, directional selection occurred within the odd-year spawning lineage, which greatly enhanced the founder effect. This process contributed to increased fitness for the odd-year pink salmon in the White Sea, leading to a rapid rise in their population.
When we compare odd-year spawning populations from native and introduced ranges, the effects of a pronounced founder event become apparent. In the Arctic–Atlantic basin, we identified only six haplotypes (plus two singletons that we do not consider in our analysis), all commonly found across almost every population in this area. Three of these haplotypes were predominant in the source population, while two were recorded as singletons in several populations from the Far East. The origin of one haplotype, OG-B1-59, remains unclear.
We sequenced the cytb gene in over 4000 pink salmon from both lineages and did not find OG-B1-59 haplotype. There are two possible explanations for its presence in the introduced area: either it was introduced as a very rare haplotype, or it is a new variant (separated by two substitutions from the closest known haplotype) that emerged after the introduction. The high level of polymorphism in the cytb gene among Pacific salmon, combined with the limited size of our analysed samples, suggests that we may have missed this haplotype in the native range.
Haplotype OG-B1-59 was found in four even-year spawners from the White Sea. This haplotype, which is unique to the introduced range, is unlikely to have emerged independently in both lineages. Therefore, its presence suggests that there has been an exchange of genetic material between the lineages. Previous observations of three-year-old spawners in the native range [44,45] support the possibility of this exchange. We hope that future WGS studies will provide clarity on this issue.
Author Contributions
Conceptualization, D.A.Z., I.I.G. and N.S.M.; Methodology, D.A.Z.; validation, D.A.Z. and N.S.M.; formal analysis, D.A.Z.; investigation, D.A.Z., V.A.S., M.M.A., and V.A.Z.; resources, V.A.S., I.I.G., M.M.A., and V.A.Z.; data curation, D.A.Z.; writing—original draft, D.A.Z., I.I.G., and N.S.M.; writing—review and editing, D.A.Z., and N.S.M.; visualization, D.A.Z. and I.I.G.; supervision, D.A.Z., N.S.M., and I.I.G.; project administration, N.S.M.; funding acquisition, N.S.M. All authors have read and agreed to the published version of the manuscript.
Funding
This research was supported by a grant from the Ministry of Science and Higher Education of the Russian Federation (agreement No. 075-15-2025-479).
Institutional Review Board Statement
Not applicable.
Data Availability Statement
The original contributions presented in this study are included in the article. Further inquiries can be directed to the corresponding authors.
Acknowledgments
Authors wish to thank the staff members of the Polar and North branches of the Russian Federal Research Institute of Fisheries and Oceanography, in particular Alexey Tortsev, Artem Tkachenko, Sergey Prusov and Dmitry Kuzmin. Molecular analysis was carried out on the basis of Core Shared Research Facilities “Fisheries Genomics”, registration number 3579654 (https://ckp-rf.ru/catalog/ckp/3579654, accessed on 5 August 2025). Samples for research belong to Large-Scale Research Facility “Bioresource collection of water biological resources”, registration number 3990221, (https://ckp-rf.ru/catalog/ckp/3990221, accessed on 5 August 2025).
Conflicts of Interest
The authors declare no conflicts of interest.
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Figure 1.
Sampling locations for odd-year spawning (a) and even-year spawning (b) lineages. Pie charts indicate cytb haplotype compositions of the samples.
Figure 1.
Sampling locations for odd-year spawning (a) and even-year spawning (b) lineages. Pie charts indicate cytb haplotype compositions of the samples.
Figure 2.
TCS networks of pink salmon cytb haplotypes include: (a) the even-year spawning fish, (b) the odd-year spawning fish, and (c) the overall group of fish. For each haplotype, the proportion of fish from different samples or regional groups is displayed. Samples collected from the native range are marked in yellow or orange, whereas those from the introduced range are marked in blue or green.
Figure 2.
TCS networks of pink salmon cytb haplotypes include: (a) the even-year spawning fish, (b) the odd-year spawning fish, and (c) the overall group of fish. For each haplotype, the proportion of fish from different samples or regional groups is displayed. Samples collected from the native range are marked in yellow or orange, whereas those from the introduced range are marked in blue or green.
Figure 3.
The pink salmon and Atlantic salmon catches in the European part of Russia from 2000 to 2024.
Figure 3.
The pink salmon and Atlantic salmon catches in the European part of Russia from 2000 to 2024.
Table 1.
Sampling information.
| Sea Basin | Sampling Location | Odd-Year Spawning Lineage | Even-Year Spawning Lineage | ||||
|---|---|---|---|---|---|---|---|
| Abbr. | Date of Collection | Sample Size | Abbr. | Date of Collection | Sample Size | ||
| North Sea | Scotland | SCOT17 * | Summer 2017 | 48 | |||
| Barents Sea | Kola River | KOLA19 | July 2019 | 30 | |||
| White Sea | Varzuga River | VARZ23 | July 2023 | 50 | |||
| Umba River | UMBA21 | Summer 2021 | 30 | UMBA18 | August–September 2018 | 96 | |
| Keret River | KER17 * | Summer 2017 | 50 | ||||
| Mezen River | MEZ23 | August 2023 | 25 | ||||
| Kara Sea | Pyasina River | PYAS17 | Summer 2017 | 41 | |||
| Okhotsk Sea | Ola River | OLA09 * | July 2009 | 60 | OLA16 | July 2016 | 45 |
| OLA22 | July–August 2022 | 27 | |||||
| Taui River | TAUI11 * | July 2011 | 45 | TAUI12 | July 2012 | 27 | |
| TAUI17 | July 2017 | 32 | TAUI16 | July 2016 | 29 | ||
* Samples analysed in the previous study [29].
Table 2.
Cytb gene haplotype and nucleotide diversity in populations and regions. The names of the samples are given in Table 1.
Table 2.
Cytb gene haplotype and nucleotide diversity in populations and regions. The names of the samples are given in Table 1.
| Odd-Lineage Samples | |||||||
| Sample | Ocean Basin | N | H | S | π × 100 | h | D |
| SCOT17 | A | 48 | 6 | 6 | 0.1604 | 0.7872 | 0.5336 |
| KOLA19 | A | 30 | 7 | 7 | 0.1545 | 0.8414 | −0.3253 |
| VARZ23 | A | 50 | 6 | 6 | 0.1539 | 0.7845 | 0.4314 |
| UMBA21 | A | 30 | 5 | 6 | 0.1235 | 0.7241 | −0.4843 |
| KER17 | A | 50 | 6 | 6 | 0.149 | 0.7829 | 0.3368 |
| MEZ23 | A | 25 | 6 | 6 | 0.1336 | 0.78 | −0.4311 |
| PYAS17 | A | 41 | 6 | 6 | 0.1356 | 0.8073 | −0.0414 |
| OLA09 | P | 60 | 9 | 10 | 0.145 | 0.7757 | −0.8629 |
| TAUI11 | P | 45 | 10 | 12 | 0.184 | 0.8182 | −0.9571 |
| TAUI17 | P | 32 | 7 | 8 | 0.1767 | 0.8226 | −0.2834 |
| ODD ATLANTIC/ARCTIC | A | 274 | 8 | 9 | 0.1471 | 0.7899 | 0.0656 |
| ODD PACIFIC | P | 137 | 13 | 15 | 0.1664 | 0.8102 | −1.0098 |
| ALL ODD | 411 | 15 | 18 | 0.1576 | 0.8157 | −1.0118 | |
| Even-Lineage Samples | |||||||
| Sample | Ocean Basin | N | H | S | π × 100 | h | D |
| UMBA18 | A | 96 | 13 | 12 | 0.1846 | 0.8498 | −0.5223 |
| OLA16 | P | 45 | 14 | 16 | 0.2147 | 0.8788 | −1.2687 |
| OLA22 | P | 27 | 11 | 11 | 0.1959 | 0.886 | −0.9923 |
| TAUI12 | P | 27 | 12 | 10 | 0.2228 | 0.9088 | −0.4084 |
| TAUI16 | P | 29 | 8 | 7 | 0.1669 | 0.8498 | −0.1386 |
| EVEN ATLANTIC/ARCTIC | A | 96 | 13 | 12 | 0.1846 | 0.8498 | −0.5223 |
| EVEN PACIFIC | P | 128 | 23 | 21 | 0.2017 | 0.8761 | −1.3291 |
| ALL EVEN | 224 | 26 | 23 | 0.1942 | 0.8646 | −1.3118 | |
| ALL | 635 | 31 | 29 | 0.1817 | 0.8812 | −1.4119 | |
Ocean basin: A = Atlantic/Arctic; P = Pacific; N = individuals sequenced; H = number of haplotypes; S = number of variable sites; π = nucleotide diversity; h = haplotype diversity; D = Tajima test coefficient.
Table 3.
Haplotype composition of population and regional samples. The names of the samples are given in Table 1. In the left column, black colour is applied for haplotypes common to both lineages, and grey colour and white colour for haplotypes typical only for the “even” and “odd” lineages, respectively.
Table 3.
Haplotype composition of population and regional samples. The names of the samples are given in Table 1. In the left column, black colour is applied for haplotypes common to both lineages, and grey colour and white colour for haplotypes typical only for the “even” and “odd” lineages, respectively.
| Lineage | Even-Year Spawning Lineage | Odd-Year Spawning Lineage | |||||||||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
| Ocean Basin * | A | P | P | P | P | A | A | A | A | A | A | A | P | P | P | ||
| Haplotype | GenBank Acc. Number (1018 bp) | GenBank Acc. Number (1141 bp) | UMBA18 | OLA16 | OLA22 | TAUI12 | TAUI16 | SCOT17 | KOLA19 | VARZ23 | UMBA21 | KER17 | MEZ23 | PYAS17 | TAUI11 | TAUI17 | OLA09 |
| A1 | MT328254 | PQ817431 | 25 | 10 | 5 | 5 | 7 | 1 | 4 | 2 | - | 2 | 1 | 6 | 12 | 5 | 7 |
| A1-8 | MT328262 | PQ817432 | 2 | 1 | - | - | - | - | - | - | - | - | - | - | - | - | - |
| A1-9 | MT328263 | PQ817433 | - | - | 1 | 1 | - | - | - | - | - | - | - | - | - | - | - |
| A1-13 | MT328267 | PQ817434 | 2 | 1 | - | - | - | 13 | 3 | 12 | 4 | 6 | 3 | 3 | - | - | - |
| A2 | MT328278 | PQ817435 | 13 | 8 | 3 | 1 | 4 | - | - | - | - | - | - | - | - | - | 1 |
| A2-1 | MT328279 | PQ817436 | - | - | 1 | - | - | - | - | - | - | - | - | - | - | - | - |
| A2-5 | MT328283 | - | - | 1 | - | - | - | - | - | - | - | - | - | - | - | - | - |
| A3 | MT328285 | PQ817437 | 8 | 3 | - | 1 | 1 | - | - | - | - | - | - | - | - | - | - |
| A3-1 | MT328286 | PQ817438 | - | 1 | - | - | - | - | - | - | - | - | - | - | 1 | - | - |
| A4 | MT328290 | PQ817439 | - | 1 | - | - | - | - | 1 | - | - | - | - | - | 4 | - | 2 |
| A4-1 | MT328291 | - | - | - | - | - | - | - | - | - | - | - | - | - | 1 | - | - |
| A5 | MT328292 | PQ817440 | 1 | 2 | - | 1 | 1 | - | - | 1 | - | - | - | - | 2 | 4 | 3 |
| A5-3 | MT328295 | - | - | 1 | - | - | - | - | - | - | - | - | - | - | - | - | - |
| A6 | MT328297 | PQ817441 | 1 | - | 1 | 3 | 1 | - | - | - | - | - | - | - | - | - | - |
| A6-2 | MT328299 | - | - | 1 | - | - | - | - | - | - | - | - | - | - | - | - | - |
| B1 | MT328300 | PQ817442 | 7 | - | 3 | 5 | 5 | 13 | 8 | 13 | 12 | 15 | 9 | 12 | 5 | 10 | 21 |
| B1-1 | MT328301 | PQ817443 | - | - | 1 | 1 | - | - | - | - | - | - | - | - | - | 1 | - |
| B1-13 | MT328313 | PQ817445 | - | - | 1 | - | - | - | - | - | - | - | - | - | - | - | - |
| B1-15 | MT328315 | PQ817446 | - | - | - | - | - | 8 | 7 | 14 | 3 | 6 | 7 | 8 | 1 | - | - |
| B1-33 | MT328333 | - | - | - | - | 1 | - | - | - | - | - | - | - | - | - | - | - |
| B1-42 | MT328342 | - | - | 1 | - | - | - | - | - | - | - | - | - | - | - | - | - |
| B1-45 | MT328345 | PQ817447 | 2 | - | - | - | - | - | - | - | - | - | - | - | - | - | - |
| B1-59 | MT328359 | PQ817448 | 4 | - | - | - | - | 2 | 2 | - | 1 | 5 | 1 | 2 | - | - | - |
| B2 | MT328360 | PQ817449 | 22 | 8 | 7 | 4 | 7 | - | - | - | - | - | - | - | 1 | 1 | 4 |
| B2-9 | MT328369 | PQ817450 | - | - | - | - | - | - | - | - | - | - | - | - | - | - | 1 |
| B3 | MT328373 | PQ817451 | 6 | 6 | 3 | 3 | 3 | - | - | - | - | - | - | - | - | - | - |
| B3-1 | MT328374 | PQ817452 | - | - | - | 1 | - | - | - | - | - | - | - | - | - | - | - |
| B3-9 | - | PQ817453 | - | - | 1 | - | - | - | - | - | - | - | - | - | - | - | - |
| B4 | MT328382 | PQ817454 | - | - | - | - | - | 11 | 5 | 8 | 10 | 16 | 4 | 10 | 14 | 7 | 18 |
| B5 | MT328389 | PQ817455 | - | - | - | - | - | - | - | - | - | - | - | - | 4 | 4 | 3 |
| B6 | MT328390 | PQ817456 | 3 | - | - | - | - | - | - | - | - | - | - | - | - | - | - |
* Ocean basin: A—Atlantic/Arctic; P—Pacific.
Table 4.
The values below the diagonal represent pairwise genetic differentiation (ΦST) for pink salmon samples, with statistically significant differences highlighted in bold italics (* α ≤ 0.05). The values above the diagonal indicate the levels of significance from the probabilistic test (exact test) for pairwise differentiation. These are classified as follows: * p < 0.05, *** p < 0.001; and NS indicates that the differences are not statistically significant.
Table 4.
The values below the diagonal represent pairwise genetic differentiation (ΦST) for pink salmon samples, with statistically significant differences highlighted in bold italics (* α ≤ 0.05). The values above the diagonal indicate the levels of significance from the probabilistic test (exact test) for pairwise differentiation. These are classified as follows: * p < 0.05, *** p < 0.001; and NS indicates that the differences are not statistically significant.
| Lineage | Odd-Year Spawning Lineage | Even-Year Spawning Lineage | |||||||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
| Ocean Basin * | P | P | P | A | A | A | A | A | A | A | P | P | P | P | A |
| TAUI11 | TAUI17 | OLA09 | SCOT17 | KOLA19 | VARZ23 | UMBA21 | KER17 | MEZ23 | PYAS17 | TAUI12 | TAUI16 | OLA16 | OLA22 | UMBA18 | |
| TAUI11 | NS | * | *** | *** | *** | *** | *** | *** | *** | *** | *** | *** | *** | *** | |
| TAUI17 | 0.009 | NS | *** | *** | *** | *** | *** | *** | *** | *** | *** | *** | *** | *** | |
| OLA09 | 0.021 | 0.000 | *** | *** | *** | *** | *** | *** | *** | *** | *** | *** | *** | *** | |
| SCOT17 | 0.066 * | 0.069 * | 0.065 * | NS | NS | NS | NS | NS | NS | *** | *** | *** | *** | *** | |
| KOLA19 | 0.051 * | 0.049 * | 0.048 * | 0.000 | NS | NS | NS | NS | NS | *** | *** | *** | *** | *** | |
| VARZ23 | 0.087 * | 0.084 * | 0.091 * | 0.000 | 0.000 | NS | * | NS | NS | *** | *** | *** | *** | *** | |
| UMBA21 | 0.064 * | 0.049 * | 0.016 | 0.013 | 0.014 | 0.043 | NS | NS | NS | *** | *** | *** | *** | *** | |
| KER17 | 0.068 * | 0.056 * | 0.03 * | 0.016 | 0.007 | 0.047 * | 0.000 | NS | NS | *** | *** | *** | *** | *** | |
| MEZ23 | 0.091 * | 0.07 * | 0.064 * | 0.007 | 0.000 | 0.000 | 0.012 | 0.01 | NS | *** | *** | *** | *** | *** | |
| PYAS17 | 0.053 * | 0.045 * | 0.029 * | 0.007 | 0.000 | 0.014 | 0.000 | 0.000 | 0.000 | *** | *** | *** | *** | *** | |
| TAUI12 | 0.072 * | 0.036 * | 0.097 * | 0.127 * | 0.096 * | 0.13 * | 0.157 * | 0.147 * | 0.131 * | 0.124 * | NS | * | NS | * | |
| TAUI16 | 0.075 * | 0.056 * | 0.102 * | 0.137 * | 0.113 * | 0.139 * | 0.183 * | 0.17 * | 0.158 * | 0.141 * | 0.000 | NS | NS | NS | |
| OLA16 | 0.095 * | 0.098 * | 0.16 * | 0.173 * | 0.154 * | 0.172 * | 0.223 * | 0.219 * | 0.197 * | 0.187 * | 0.011 | 0.000 | NS | NS | |
| OLA22 | 0.073 * | 0.043 * | 0.084 * | 0.124 * | 0.096 * | 0.127 * | 0.153 * | 0.147 * | 0.128 * | 0.121 * | 0.000 | 0.000 | 0.021 | NS | |
| UMBA18 | 0.084 * | 0.079 * | 0.117 * | 0.136 * | 0.114 * | 0.139 * | 0.175 * | 0.169 * | 0.153 * | 0.139 * | 0.009 | 0.000 | 0.005 | 0.000 | |
Table 5.
The results of hierarchical AMOVA. The significance levels for the p-value: * 0.01–0.05; ** 0.001–0.01; *** <0.001.
Table 5.
The results of hierarchical AMOVA. The significance levels for the p-value: * 0.01–0.05; ** 0.001–0.01; *** <0.001.
| (a) Among all samples (4 groups: EVEN-A, EVEN-P, ODD-A, ODD-P). | ||||
| Source of variation | d.f. | Sum of squares | Variance composition (%) | Fixation indexes |
| Among groups | 3 | 47.221 | 0.09824 (10.27%) | FCT: 0.10274 *** |
| Among populations within groups | 11 | 11.233 | 0.00444 (0.46%) | FSC: 0.00518 ns |
| Within populations | 620 | 529.163 | 0.85349 (99.26%) | FST: 0.10739 *** |
| Total | 634 | 587.617 | 0.95618 | |
| (b) Among odd-year spawning populations and groups (2 groups: ODD-A, ODD-P). | ||||
| Source of variation | d.f. | Sum of squares | Variance composition | Fixation indexes |
| Among groups | 1 | 9.222 | 0.04471 (5.39%) | FCT: 0.05394 ** |
| Among populations within groups | 8 | 8.141 | 0.00597 (0.72%) | FSC: 0.00761 ns |
| Within populations | 401 | 312.115 | 0.77834 (93.89%) | FST: 0.06113 *** |
| Total | 410 | 329.478 | 0.82902 | |
| (c) Among even-year spawning populations and groups (2 groups: EVEN-A, EVEN-P). | ||||
| Source of variation | d.f. | Sum of squares | Variance composition | Fixation indexes |
| Among groups | 1 | 0.829 | −0.00228 (−0.13%) | FCT: −0.00230 ns |
| Among populations within groups | 3 | 3.092 | 0.00126 (0.13%) | FSC: 0.00127 ns |
| Within populations | 219 | 217.048 | 0.99109 (100.10%) | FST: −0.00103 ns |
| Total | 223 | 220.968 | 0.99007 | |
| (d) Among Atlantic populations and groups (2 groups: ATL-ODD, ATL-EVEN). | ||||
| Source of variation | d.f. | Sum of squares | Variance composition | Fixation indexes |
| Among groups | 1 | 22.415 | 0.15004 (15.78%) | FCT: 0.15776 ns |
| Among populations within groups | 6 | 5.593 | 0.00348 (0.37%) | FSC: 0.00434 ns |
| Within populations | 362 | 288.704 | 0.79752 (83.86%) | FST: 0.16142 *** |
| Total | 369 | 316.712 | 0.95104 | |
| (e) Among Pacific populations and groups (2 groups: PAC-ODD, PAC-EVEN). | ||||
| Source of variation | d.f. | Sum of squares | Variance composition | Fixation indexes |
| Among groups | 1 | 12.94 | 0.08907 (8.68%) | FCT: 0.08678 * |
| Among populations within groups | 5 | 5.64 | 0.00536 (0.52%) | FSC: 0.00572 ns |
| Within populations | 258 | 240.459 | 0.93201 (90.80%) | FST: 0.09200 *** |
| Total | 264 | 259.038 | 1.02644 | |
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Zelenina, D.A.; Soshnina, V.A.; Gordeev, I.I.; Alekseev, M.M.; Zadelenov, V.A.; Mugue, N.S. The Splendour and Misery of European Pink Salmon, Oncorhynchus gorbuscha: Abundant Odd Lineage vs. Depressed Even Lineage—Insights from cytb Gene Analysis. Diversity 2025, 17, 563. https://doi.org/10.3390/d17080563
AMA Style
Zelenina DA, Soshnina VA, Gordeev II, Alekseev MM, Zadelenov VA, Mugue NS. The Splendour and Misery of European Pink Salmon, Oncorhynchus gorbuscha: Abundant Odd Lineage vs. Depressed Even Lineage—Insights from cytb Gene Analysis. Diversity. 2025; 17(8):563. https://doi.org/10.3390/d17080563
Chicago/Turabian StyleZelenina, Daria A., Valeria A. Soshnina, Ilya I. Gordeev, Maksim M. Alekseev, Vladimir A. Zadelenov, and Nikolai S. Mugue. 2025. "The Splendour and Misery of European Pink Salmon, Oncorhynchus gorbuscha: Abundant Odd Lineage vs. Depressed Even Lineage—Insights from cytb Gene Analysis" Diversity 17, no. 8: 563. https://doi.org/10.3390/d17080563
APA StyleZelenina, D. A., Soshnina, V. A., Gordeev, I. I., Alekseev, M. M., Zadelenov, V. A., & Mugue, N. S. (2025). The Splendour and Misery of European Pink Salmon, Oncorhynchus gorbuscha: Abundant Odd Lineage vs. Depressed Even Lineage—Insights from cytb Gene Analysis. Diversity, 17(8), 563. https://doi.org/10.3390/d17080563
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