Independent lineages in a common environment: the roles of determinism and contingency in shaping the migration timing of even‐ versus odd‐year pink salmon over broad spatial and temporal scales

Studies of parallel evolution are seldom able to disentangle the influence of cryptic environmental variation from that of evolutionary history; whereas the unique life history of pink salmon (Oncorhynchus gorbuscha) presents an opportunity to do so. All pink salmon mature at age two and die after breeding. Hence, pink salmon bred in even years are completely reproductively isolated from those bred in odd years, even if the two lineages bred in same location. We used time series (mean = 7 years, maximum = 74 years) of paired even‐ and odd‐year populations from 36 rivers spanning over 2000 km to explore parallelism in migration timing, a trait with a strong genetic basis. Migration timing was highly parallel, being determined almost entirely by local environmental differences among rivers. Interestingly, interannual changes in migration timing different somewhat between lineages. Overall, our findings indicate very strong determinism, with only a minor contribution of contingency.     

On possible re-distribution of pink salmon <Emphasis Type="Italic">Onchorhynchus gorbuscha</Emphasis> between the reproduction areas of different stocks in the Sakhalin-Kuril region

The scale structure of pink salmon Oncorhynchus gorbuscha inhabiting southern Sakhalin and Iturup Island were studied in 2014. These locations are characterized by the unusual dynamics of catches and biological parameters of the fish that come to spawn in different areas in the Sakhalin-Kuril region. The pink salmon that has originated from Iturup Island appeared en masse in the waters of southern Sakhalin, according to the analysis of the scleritogram fragments that reflect the fish growth during the first months of life. This is the first confirmation of the hypothesis of the fluctuating stocks of pink salmon approved by the ichthyological methods. It is suggested that wide-scale straying of pink salmon takes place in the years of dominance shift between the generations of even and odd spawning years.     

Evidence for competitive dominance of Pink salmon (<Emphasis Type="Italic">Oncorhynchus gorbuscha</Emphasis>) over other Salmonids in the North Pacific Ocean

Relatively little is known about fish species interactions in offshore areas of the world’s oceans because adequate experimental controls are typically unavailable in such vast areas. However, pink salmon (Oncorhynchus gorbuscha) are numerous and have an alternating-year pattern of abundance that provides a natural experimental control to test for interspecific competition in the North Pacific Ocean and Bering Sea. Since a number of studies have recently examined pink salmon interactions with other salmon, we reviewed them in an effort to describe patterns of interaction over broad regions of the ocean. Research consistently indicated that pink salmon significantly altered prey abundance of other salmon species (e.g., zooplankton, squid), leading to altered diet, reduced total prey consumption and growth, delayed maturation, and reduced survival, depending on species and locale. Reduced survival was observed in chum salmon (O. keta) and Chinook salmon (O. tshawytscha) originating from Puget Sound and in Bristol Bay sockeye salmon (O. nerka). Growth of pink salmon was not measurably affected by other salmon species, but their growth was sometimes inversely related to their own abundance. In all marine studies, pink salmon affected other species through exploitation of prey resources rather than interference. Interspecific competition was observed in nearshore and offshore waters of the North Pacific Ocean and Bering Sea, and one study documented competition between species originating from different continents. Climate change had variable effects on competition. In the North Pacific Ocean, competition was observed before and after the ocean regime shift in 1977 that significantly altered abundances of many marine species, whereas a study in the Pacific Northwest reported a shift from predation- to competition-based mortality in response to the 1982/1983 El Nino. Key traits of pink salmon that influenced competition with other salmonids included great abundance, high consumption rates and rapid growth, degree of diet overlap or consumption of lower trophic level prey, and early migration timing into the ocean. The consistent pattern of findings from multiple regions of the ocean provides evidence that interspecific competition can significantly influence salmon population dynamics and that pink salmon may be the dominant competitor among salmon in marine waters.     

Comparative anatomy of the dorsal hump in mature Pacific salmon

Mature male Pacific salmon (Genus Oncorhynchus ) demonstrate prominent morphological changes, such as the development of a dorsal hump. The degree of dorsal hump formation depends on the species in Pacific salmon. It is generally accepted that mature males of sockeye (O. nerka ) and pink (O. gorbuscha ) salmon develop most pronounced dorsal humps. The internal structure of the dorsal hump in pink salmon has been confirmed in detail. In this study, the dorsal hump morphologies were analyzed in four Pacific salmon species inhabiting Japan, masu (O. masou ), sockeye, chum (O. keta ), and pink salmon. The internal structure of the dorsal humps also depended on the species; sockeye and pink salmon showed conspicuous development of connective tissue and growth of bone tissues in the dorsal tissues. Masu and chum salmon exhibited less‐pronounced increases in connective tissues and bone growth. Hyaluronic acid was clearly detected in dorsal hump connective tissue by histochemistry, except for in masu salmon. The lipid content in dorsal hump connective tissue was richer in masu and chum salmon than in sockeye and pink salmon. These results revealed that the patterns of dorsal hump formation differed among species, and especially sockeye and pink salmon develop pronounced dorsal humps through both increases in the amount of connective tissue and the growth of bone tissues. In contrast, masu and chum salmon develop their dorsal humps by the growth of bone tissues, rather than the development of connective tissue.     

Identification of the sex chromosome pair in chum salmon (Oncorhynchus keta) and pink salmon (Oncorhynchus gorbuscha)

Fluorescence in situ hybridization (FISH) using a probe to the male-specific GH-Y (growth hormone pseudogene) was used to identify the Y chromosome in the karyotypes of chum salmon (Oncorhynchus keta) and pink salmon (Oncorhynchus gorbuscha). The sex chromosome pair is a small acrocentric chromosome pair in chum salmon and the smallest metacentric chromosome pair in pink salmon. Both of these chromosome pairs are morphologically different from the sex chromosome pairs in chinook salmon (Oncorhynchus tshawytscha) and coho salmon (Oncorhynchus kisutch). The 5S rRNA genes are on multiple chromosome pairs including the sex chromosome pair in chum salmon, but at the centromeres of two autosomal metacentric pairs in pink salmon. The sex chromosome pairs and the chromosomal locations of the 5S rDNA appear to be different in all five of the North American Pacific salmon species and rainbow trout. The implications of these results for evolution of sex chromosomes in salmonids are discussed.     

Physiological consequences of the salmon louse (Lepeophtheirus salmonis) on juvenile pink salmon (Oncorhynchus gorbuscha): implications for wild salmon ecology and management, and for salmon aquaculture

Pink salmon, Oncorhynchus gorbuscha, are the most abundant wild salmon species and are thought of as an indicator of ecosystem health. The salmon louse, Lepeophtheirus salmonis, is endemic to pink salmon habitat but these ectoparasites have been implicated in reducing local pink salmon populations in the Broughton Archipelago, British Columbia. This allegation arose largely because juvenile pink salmon migrate past commercial open net salmon farms, which are known to incubate the salmon louse. Juvenile pink salmon are thought to be especially sensitive to this ectoparasite because they enter the sea at such a small size (approx. 0.2 g). Here, we describe how 'no effect' thresholds for salmon louse sublethal impacts on juvenile pink salmon were determined using physiological principles. These data were accepted by environmental managers and are being used to minimize the impact of salmon aquaculture on wild pink salmon populations.     

Influence of Extreme Environmental Factors on the Dynamics of Abundance of the Pink Salmon <Emphasis Type="Italic">Oncorhynchus gorbuscha</Emphasis>

The correlation between the number of returned fish and the spawners of the parent generation recorded in the rivers (the reproduction index) has been analyzed in a series of generations of the five largest stocks of pink salmon Oncorhynchus gorbuscha in the Sakhalin-Kuril region. The hypothesis that the appearance of low-yielding generations of pink salmon was mainly due to the impact of typhoons as extreme environmental factors has been confirmed. Low values of the reproduction index of pink salmon generations that have been exposed to typhoons during embryonic development in the rivers (redds) or during the feeding period of juveniles in the coastal region of the sea (the next few days after downstream migration) allow for a conclusion on their significant importance for the formation of the abundance of this species. During some adjacent year groups, the frequency of typhoons attributable to the indicated periods of the pink salmon’s life cycle increases, this causes a number of low-yielding generations. At the same time, the strength of the typhoons and the limits of their impact are constantly changing, which explains the lack of synchronism in the sharp changes in the pink salmon population of all the stocks in the region.     

Sex Determination Model in Pink Salmon <Emphasis Type="Italic">Oncorhynchus gorbuscha</Emphasis> (Walbaum, 1792) (Salmonidae,Osteichthyes) Controlled by Multi-Copy Genes Located in Sex Chromosomes

This article is devoted to presenting the hypothesis explaining the fact of a considerable prevalence of phenotypic males among the triploid pink salmon as well as the regular occurrence of intersexes, which were revealed by us. This hypothesis also explains the large proportion (in some cases) in pink salmon populations of the individuals whose genetic sex does not match the phenotypic sex. We assume that the genes encoding the factors that contribute to the transformation of individuals into males (but not the marker sequences of the Y chromosome) are present not only in the Y chromosome of pink salmon but also in the X chromosome, although in smaller quantities.     

Sex and proximity to reproductive maturity influence the survival, final maturation, and blood physiology of Pacific salmon when exposed to high temperature during a simulated migration

Some Pacific salmon populations have been experiencing increasingly warmer river temperatures during their once-in-a-lifetime spawning migration, which has been associated with en route and prespawn mortality. The mechanisms underlying such temperature-mediated mortality are poorly understood. Wild adult pink (Oncorhynchus gorbuscha) and sockeye (Oncorhynchus nerka) salmon were used in this study. The objectives were to investigate the effects of elevated water temperature on mortality, final maturation, and blood properties under controlled conditions that simulated a "cool" (13°C) and "warm" (19°C) freshwater spawning migration. After 10 d at 13°C, observed mortality was 50%-80% in all groups, which suggested that there was likely some mortality associated with handling and confinement. Observed mortality after 10 d at 19°C was higher, reaching ≥98% in male pink salmon and female pink and sockeye salmon. Thus, male sockeye salmon were the most thermally tolerant (54% observed mortality). Model selection supported the temperature- and sex-specific mortality patterns. The pink salmon were closer to reproductive maturation and farther along the senescence trajectory than sockeye salmon, which likely influenced their survival and physiological responses throughout the experiment. Females of both species held at 19°C had reduced plasma sex steroids compared with those held at 13°C, and female pink salmon were less likely to become fully mature at 19° than at 13°C. Male and female sockeye salmon held at 19°C had higher plasma chloride and osmolality than those held at 13°C, indicative of a thermally related stress response. These findings suggest that sex differences and proximity to reproductive maturity must be considered when predicting thermal tolerance and the magnitude of en route and prespawn mortality for Pacific salmon.     

Genetic changes in pink salmon Oncorhynchus gorbuscha Walbaum during acclimatization in the White sea basin

Genetic parameters of pink salmon introduced into the White Sea basin in 1985 and 1998 were compared to the corresponding parameters of the donor population from the Ola River (Magadan oblast). The detected genetic differences indicate that colonization of a new area is accompanied by impoverishment of the gene pool of the native population. This effect was particularly marked in the odd-year line of pink salmon introduced in 1985. The probable causes of these genetic changes are discussed.     

Genetic Changes in Pink Salmon Oncorhynchus gorbuscha Walbaum during Acclimatization in the White Sea Basin

Genetic parameters of pink salmon introduced into the White Sea basin in 1985 and 1998 were compared to the corresponding parameters of the donor population from the Ola River (Magadan oblast). The detected genetic differences indicate that colonization of a new area is accompanied by impoverishment of the gene pool of the native population. This effect was particularly marked in the odd-year broodline of pink salmon introduced in 1985. The probable causes of these genetic changes are discussed.     

Incomplete congruence between morphobiological characters and sex-specific molecular markers in Pacific salmons: 1. Analysis of discrepancy in five species of the genus <Emphasis Type="Italic">Oncorhynchus</Emphasis>

The congruence between molecular markers, identifying the presence of the Y chromosome, and secondary sexual characters was examined in Asian populations of five Pacific salmon species: pink salmon (Oncorhynchus gorbuscha), chum salmon (O. keta), sockeye salmon (O. nerka), chinook salmon (O. tschawytscha), and sima (O. masou). It was demonstrated that in all species examined, the presence or absence of sex-specific molecular markers was to a considerable degree congruent with secondary sexual characters, but in some cases, an incongruence was found. These findings suggested that the mechanism underlying this phenomenon was similar or identical in all species examined. Possible genetic and physiological explanations of this phenomenon are discussed.     

Conditions of reproduction and population dynamics of Pacific salmons (<Emphasis Type="Italic">Oncorhynchus</Emphasis>): The northeast of Sakhalin Island

The efficiency of reproduction of Pacific salmon (Oncorhynchus) in the rivers of the northeastern Sakhalin coast is characterized based on long-term observations. The rivers of the northern, central, and southern parts differ in the type of their channel, faunistic composition of aquatic biota, and prevalent salmon species. The northern rivers have a plain type of channel with rather low spawning efficiency of salmons and relatively poor freshwater ichthyofauna. The central area houses the largest rivers (Tym’ and Nabil’ Rivers) running to the Nyiskii and Nabil’skii Gulfs; the rivers there have developed channels of a plain type, high diversity of resident ichthyofauna, low spawning efficiency of the pink salmon Oncorhynchus gorbuscha, and high (in the past) abundance of the fall chum salmon O. keta. Characteristic of the southern rivers with their prevalently mountain–foothill type of channels are poor fish population and high spawning efficiency of the pink salmon. The population dynamics of the salmonids in the northeastern coast of Sakhalin is described. The total number of breeders entering the rivers of the northeastern coast that provides an efficient reproduction is estimated as 3.5?9.0 million individuals for the pink salmon and 0.04–0.60 million individuals for the chum salmon (fall race).     

Preferences of invasive Ponto-Caspian and native European gammarids for zebra mussel (<Emphasis Type="Italic">Dreissena polymorpha</Emphasis>, Bivalvia) shell habitat

The migratory behavior and swimming patterns of anadromous upstream migratory fish have been poorly described in the Shibetsu River in eastern Hokkaido, Japan. In this 2004 study, we used electromyogram (EMG) transmitters and depth/ temperature (DT) loggers to compare the upstream migratory behavior of adult male chum salmon (Oncorhynchus keta) and pink salmon (O. gorbuscha) in the canalized and reconstructed segments of the Shibetsu River, where a part of canalized section was preliminary reconstructed meander to restore a more natural section. The EMG transmitter and DT logger were externally attached to the left side of the body, below the front edge of the dorsal fin. Fish of both species often migrated along the riverbanks and near the bottom of the water column, sometimes engaged in holding behavior, which was defined as cessation of swimming during their upstream migration for 5 minutes. Modal swimming depth calculated by DT loggers for chum salmon (0.2–0.4 m) was shallower than pink salmon (0.6–0.8 m). Further, modal swimming speeds measured by calibrated EMG for chum salmon (0.2–0.4 BL s⁻¹) were slower than pink salmon (1.2–1.4 BL s⁻¹). Pink salmon swam faster as well as in relatively deeper than chum salmon, suggesting that they expend more energy than chum salmon in the reconstructed segment. Based on these results, it seemed likely that the upstream migration behavior of chum and pink salmon was different with species-specific strategies.     

Straying of hatchery salmon in Prince William Sound,Alaska

The straying of hatchery salmon may harm wild salmon populations through a variety of ecological and genetic mechanisms. Surveys of pink (Oncorhynchus gorbuscha), chum (O. keta) and sockeye (O. nerka) salmon in wild salmon spawning locations in Prince William Sound (PWS), Alaska since 1997 show a wide range of hatchery straying. The analysis of thermally marked otoliths collected from carcasses indicate that 0–98% of pink salmon, 0–63% of chum salmon and 0–93% of sockeye salmon in spawning areas are hatchery fish, producing an unknown number of hatchery-wild hybrids. Most spawning locations sampled (77%) had hatchery pink salmon from three or more hatcheries, and 51% had annual escapements consisting of more than 10% hatchery pink salmon during at least one of the years surveyed. An exponential decay model of the percentage of hatchery pink salmon strays with distance from hatcheries indicated that streams throughout PWS contain more than 10% hatchery pink salmon. The prevalence of hatchery pink salmon strays in streams increased throughout the spawning season, while the prevalence of hatchery chum salmon decreased. The level of hatchery salmon strays in many areas of PWS are beyond all proposed thresholds (2–10%), which confounds wild salmon escapement goals and may harm the productivity, genetic diversity and fitness of wild salmon in this region     

Polymorphism of smolts of pink salmon <Emphasis Type="Italic">Oncorhynchs gorbuscha</Emphasis> in the Indera River (Kola Peninsula)

Pink salmon introduced into the White Sea started to exploit as spawning grounds middle and upper reaches of the river 20 years after its appearance in the Indera River. As a result of this, the migration pathway of smolts and late smolts appeared in addition to early smolts. The intraspecies polymorphism of smolts is confirmed by differences of early and late smolts by body length and weight, migration dates, food spectrum, and indices of stomach fullness. The food spectra of late juveniles of pink salmon coincide with those of parr of Atlantic salmon Salmo salar and of brown trout S. trutta. Greater abundance of late migrants of pink salmon may cause competition of these species for food.     

Sex ratio control in pink salmon (<Emphasis Type="Italic">Oncorhynchus gorbuscha</Emphasis> and chum salmon (<Emphasis Type="Italic">O. keta</Emphasis>) populations: The possible causes and mechanisms of changes in the sex ratio

Long-term changes in the sex ratio have been studied in pink salmon (Oncorhynchus gorbuscha and chum salmon (O. keta) populations of Kamchatka and Sakhalin. It has been demonstrated that these changes are an adaptation to population dynamics: an increase in the population size is accompanied by a shift towards a higher proportion of males; a decrease in population size, by a shift towards a higher proportion of females. The correspondence between morphological and molecular characters in populations of the two species has been analyzed in order to determine the mechanism of sex ratio control. In some pink salmon and chum salmon populations, there is a discrepancy between sex identifications based on morphological characters and molecular markers. This discrepancy is assumed to be accounted for by sex inversion mechanisms, which may be population-or region-specific. In two cases, it has been found that the sex ratio discrepancy in populations is related to the numbers of fish in subsequent generations. These findings suggest that sex inversion may be related to population size control.     

High estimates of differentiation between pink salmon, <Emphasis Type="Italic">Oncorhynchus gorbuscha</Emphasis>, populations at locus of major histocompatibility complex MHC-I <Emphasis Type="Italic">A1</Emphasis> support the “local stock” hypothesis

Variability at the locus of major histocompatibility complex MHC-I A1 in 20 populations of pink salmon Oncorhynchus gorbuscha from the five major geographical regions of the Russian Far East was studied. Indices of genetic differentiation at all levels of the hierarchy were unexpectedly high and comparable with the corresponding estimates in related species of Pacific salmon. The data obtained allow us to revise the existing hypotheses concerning intraspecific structure of pink salmon, in particular, to reject the “fluctuating stock” hypothesis. Good resolution of the detected marker will find application in the problems of identification of populations in mixed catches.     

Genetic monitoring of northern sea of Okhotsk populations of pink salmon (<Emphasis Type="Italic">Oncorhynchus gorbuscha</Emphasis>)

Results from the 1993–2004 genetic monitoring of pink salmon populations reproducing in the rivers of Tauy Bay on the Sea of Okhotsk are analyzed. A statistically significant heterogeneity of samples as determined by gene frequencies is found only in the pink salmon generations of even years. The genetic differentiation of samples from even years (G_ST = 1.39 ± 0.41) is higher than that of odd years (G_ST = 0.740.09). The pattern for the indicator of genetic variability (heterozygosity) is exactly the opposite (0.076 ± 0.02564 vs. 0.8760 ± 0.01950). Consequently, the lower-heterozygosity samples of lines from even years are on average more genetically distinct than the analogous indicator for odd years. In addition, the interpopulation ratio in the general value of genetic diversity is almost always smaller than both the intraannual and interannual ratios, leading to a low level of interpopulation genetic differences. Cluster analysis reveals that most 2001–2004 samples are grouped separately from samples collected prior to 2000. In our opinion, the reason for this could be the turnover of a numerically dominant generation of northern Sea of Okhtosk pink salmon and the change in gene frequencies accompanying it.     

The Salmon Smai Family of Short Interspersed Repetitive Elements (Sines): Interspecific and Intraspecific Variation of the Insertion of Sines in the Genomes of Chum and Pink Salmon

The genomes of chum salmon and pink salmon contain a family of short interspersed repetitive elements (SINEs), designated the salmon SmaI family. It is restricted to these two species, a distribution that suggests that this SINE family might have been generated in their common ancestor. When insertions of the SmaI SINEs at 10 orthologous loci of these species were analyzed, however, it was found that there were no shared insertion sites between chum and pink salmon. Furthermore, at six loci where SmaI SINEs have been species-specifically inserted in chum salmon, insertions of SINEs were polymorphic among populations of chum salmon. By contrast, at four loci where SmaI SINEs had been species-specifically inserted in pink salmon, the SINEs were fixed among all populations of pink salmon. The interspecific and intraspecific variation of the SmaI SINEs cannot be explained by the assumption that the SmaI family was amplified in a common ancestor of these two species. To interpret these observations, we propose several possible models, including introgression and the horizontal transfer of SINEs from pink salmon to chum salmon during evolution.