Divergence of mitochondrial DNA in a population of sockeye salmon (Oncorhynchus nerka Walbaum) from Azabache'e lake (Kamchatka)

Variability of three PCR-amplified mtDNA regions was examined in five populations of sockeye salmon from Azabach'e Lake. Eighteen haplotypes were detected in 144 fish. Significant differences were found between seasonal races of sockeye salmon spawning in the lake. The short time of independent divergence between the seasonal races indicates that these races formed independently in each spawning region. No difference in mtDNA between lake samples of early sockeye salmon (subisolates) was revealed, which confirms the existence of gene flow between them. A high level of differences between the sockeye salmon spawning in the lake and spawning in the tributaries of the lake, the Bushuev and Lotnaya rivers, suggests that there were no migration between them during many generations and that the nature of spawning grounds (lake or river) is essential for within species differentiation in this species.     

The effect of reproduction biotopes on the genetic differentiation of populations of sockeye salmon Oncorhynchus nerka

Variation of mitochondrial DNA (mtDNA) was examined in nine populations from three lake-river systems of Chukotka and Kamchatka. Significant differences were found between most of the sockeye salmon samples studied. The genetic differences among populations were not high and often did not correlate with the geographical distances between them. The low population divergence is explained by a short time of existence of most of them, having been formed after the recession of the upper Pleistocene glacier. When the populations were grouped according to their spawning biotopes (river or lake), they in general appeared more genetically similar than upon their grouping by geographical location (the lake-river systems). The differences between the river and lake populations in the lake--river systems increased from north to south.     

Seasonal and interannual variations of sockeye salmon (Oncorhynchus nerka) microsatellite DNA in two Kamchatka lake-river systems

Seasonal and interannual variations in the sockeye salmon populations from two lake-river systems of the East and West Kamchatka were studied. Stability of allele and genotypic frequencies of six microsatellite DNA loci in the adjacent generations and spawning populations of the sockeye salmon of the Bol'shaya River was confirmed experimentally. The pairwise intersample differentiation (F(st)) of the local sockeye salmon populations from the southwestern Kamchatka coast (Ozernaya and Bol'shaya Rivers)was almost 7 times higher than the corresponding values for the spawning populations of the Bol'shaya River sockeye salmon of the adjacent years; 15 times, for the adjacent Bol'shaya River sockeye salmon generations; and four times, for the seasonal races within the Kamchatka River.     

MOLECULAR GENETIC EVIDENCE FOR PARALLEL LIFE-HISTORY EVOLUTION WITHIN A PACIFIC SALMON (SOCKEYE SALMON AND KOKANEE,ONCORHYNCHUS NERKA)

The Pacific salmon Oncorhynchus nerka typically occurs as a sea-run form (sockeye salmon) or may reside permanently in lakes (kokanee) thoughout its native North Pacific. We tested whether such geographically extensive ecotypic variation resulted from parallel evolutionary divergence thoughout the North Pacific or whether the two forms are monophyletic groups by examining allelic variation between sockeye salmon and kokanee at two minisatellite DNA repeat loci and in mitochondrial DNA (mtDNA) Bgl II restriction sites. Our examination of over 750 fish from 24 populations, ranging from Kamchatka to the Columbia River, identified two major genetic groups of North Pacific O. nerka: a “northwestern” group consisting of fish from Kamchatka, western Alaska, and northwestern British Columbia, and a “southern” group consisting of sockeye salmon and kokanee populations from the Fraser and Columbia River systems. Maximum-likelihood analysis accompanied by bootstrapping provided strong support for these two genetic groups of O. nerka; the populations did not cluster by migratory form, but genetic affinities were organized more strongly by geographic proximity. The two major genetic groups resolved in our study probably stem from historical isolation and dispersal of O. nerka from two major Wisconsinan glacial refugia in the North Pacific. There were significant minisatellite DNA allele frequency differences between sockeye salmon and kokanee populations from different parts of the same watershed, between populations spawning in different tributaries of the same lake, and also between sympatric populations spawning in the same stream at the same time. MtDNA Bgl II restriction site variation was significant between sockeye salmon and kokanee spawning in different parts of the same major watershed but not between forms spawning in closer degrees of reproductive sympatry. Patterns of genetic affinity and allele sharing suggested that kokanee have arisen from sea-run sockeye salmon several times independently in the North Pacific. We conclude that sockeye salmon and kokanee are para- and polyphyletic, respectively, and that the present geographic distribution of the ecotypes results from parallel evolutionary origins of kokanee from sockeye (divergences between them) thoughout the North Pacific.     

Seasonal and interannual variations of sockeye salmon (<Emphasis Type="Italic">Oncorhynchus nerka</Emphasis>) microsatellite DNA in two Kamchatka lake-river systems

Seasonal and interannual variations in the sockeye salmon populations from two lake-river systems of the East and West Kamchatka were studied. Stability of allele and genotypic frequencies of six microsatellite DNA loci in the adjacent generations and spawning populations of the sockeye salmon of the Bol’shaya River was confirmed experimentally. The pairwise intersample differentiation (F _st) of the local sockeye salmon populations from the southwestern Kamchatka coast (Ozernaya and Bol’shaya Rivers) was almost 7 times higher than the corresponding values for the spawning populations of the Bol’shaya River sockeye salmon of the adjacent years; 15 times, for the adjacent Bol’shaya River sockeye salmon generations; and four times, for the seasonal races within the Kamchatka River.     

The Effect of Reproduction Biotopes on the Genetic Differentiation of Populations of Sockeye Salmon <Emphasis Type="Italic">Oncorhynchus nerka</Emphasis>

Variation of mitochondrial DNA (mtDNA) was examined in nine populations from three lake-river systems of Chukotka and Kamchatka. Significant differences were found between most of the sockeye salmon samples studied. The genetic differences among populations were not high and often did not correlate with the geographical distances between them. The low population divergence is explained by a short time of existence of most of them, having been formed after the recession of the upper Pleistocene glacier. When the populations were grouped according to their spawning biotopes (river or lake), they in general appeared more genetically similar than upon their grouping by geographical location (the lake-river systems). The differences between the river and lake populations in the lake-river systems increased from north to south.__________Translated from Genetika, Vol. 41, No. 5, 2005, pp. 635–645.Original Russian Text Copyright © 2005 by Brykov, Polyakova, Podlesnykh, E. Golub’, A. Golub’, Zhdanova.     

The variability in chum salmon Oncorhynchus keta (Walbaum) mitochondrial DNA and its connection with the paleogeological events in the northwest Pacific

The results of examining mtDNA variability in populations of chum salmon Oncorhynchus keta from the rivers of the basins of the seas of Japan and Okhotsk and in the chum salmon seasonal races of the Amur River are presented. A significant level of polymorphism between the majority of the populations studied was detected. The groups of chum salmon from the seas of Japan and Okhotsk displayed the most pronounced differences. Analysis of genetic variability demonstrated that periodic paleontologic and climatic changes in the past of this region were the most probable factor that caused the divergence of these populations. The advances and retreats of glaciers and the accompanying regressions and transgressions of the ocean level caused isolation of chum salmon in the refugia belonging hypothetically to the paleo-Shuifen and paleo-Amur regions. These population groups diverged presumably 350–450 thousand years ago. Differences between the seasonal races of the Amur chum salmon are insignificant, and their emergence dates back to the period of the last Wisconsinian glaciation. Probably, the main isolation factor now is the genetically determined time of spawning.     

The variation in chum salmon Oncorhynchus keta (Walbaum) mitochondrial DNA and its connection with the paleogeographic events in the Northwest Pacific

The results of examining mtDNA variation in populations of chum salmon Oncorhynchus keta from the rivers of the basins of the seas of Japan and Okhotsk and in the chum salmon seasonal races of the Amur River are presented. A significant level of polymorphism between the majority of the populations studied was detected. The groups of chum salmon from the Japan and Okhotsk Seas displayed the most pronounced differences. Analysis of genetic variation demonstrated that periodic paleontologic and climatic changes in the past of this region were the most probable factor that caused the divergence of these populations. The advances and retreats of glaciers and the accompanying regressions and transgressions of the ocean level caused isolation of chum salmon in the refugia belonging hypothetically to the paleo-Suifun and paleo-Amur regions. These population groups diverged presumably 350-450 thousand years ago. Differences between the seasonal races of the Amur chum salmon are insignificant, and their emergence dates back to the period of the last Wisconsin glaciation. Probably, the main isolation factor now is the genetically determined time of spawning.     

Recent local adaptation of sockeye salmon to glacial spawning habitats

Salmonids spawn in highly diverse habitats, exhibit strong genetic population structuring, and can quickly colonize newly created habitats with few founders. Spawning traits often differ among populations, but it is largely unknown if these differences are adaptive or due to genetic drift. To test if sockeye salmon (Oncorhynchus nerka) populations are adapted to glacial, beach, and tributary spawning habitats, we examined variation in heritable phenotypic traits associated with spawning in 13 populations of wild sockeye salmon in Lake Clark, Alaska. These populations were commonly founded between 100 and 400 hundred sockeye salmon generations ago and exhibit low genetic divergence at 11 microsatellite loci (F _ST < 0.024) that is uncorrelated with spawning habitat type. We found that mean P _ST (phenotypic divergence among populations) exceeded neutral F _ST for most phenotypic traits measured, indicating that phenotypic differences among populations could not be explained by genetic drift alone. Phenotypic divergence among populations was associated with spawning habitat differences, but not with neutral genetic divergence. For example, female body color was lighter and egg color was darker in glacial than non-glacial habitats. This may be due to reduced sexual selection for red spawning color in glacial habitats and an apparent trade-off in carotenoid allocation to body and egg color in females. Phenotypic plasticity is an unlikely source of phenotypic differences because Lake Clark sockeye salmon spend nearly all their lives in a common environment. Our data suggest that Lake Clark sockeye salmon populations are adapted to spawning in glacial, beach and tributary habitats and provide the first evidence of a glacial spawning ecotype in salmonids. Glacial spawning habitats are often young (i.e., <200 years old) and ephemeral. Thus, local adaptation of sockeye salmon to glacial habitats appears to have occurred recently.     

Divergence of the seasonal races of chum salmon, <Emphasis Type="Italic">Oncorhynchus keta</Emphasis> Walbaum, 1792, in the Amur and Poronai rivers: Ecology,genetics, and morphology

The chum salmon of the Amur River (the mainland part of the Far East) and the Poronai River (Terpeniya Bay, Sakhalin Island) are historically related to one another, as the drainage basins of these rivers are the remnants of a formerly single river system, the Paleoamur, which existed when Sakhalin Island was a part of the continent. Both river populations of chum salmon consist of the early-run and late-run ecological forms (seasonal races), which are also referred to as the summer and autumn races. They are reproductively isolated from each other due to their spawning at different times and in different types of spawning grounds. To assess the direction, pattern, and degree of divergence between these chum salmon races in the both river fragments since the Paleoamur, it is necessary to compare them using two types of traits: selectively neutral DNA markers and morphological and physiological traits, variations in which may have an adaptive value. For this, we have studied chum salmon from both rivers in terms of microsatellite DNA markers, body counts and measurements, body weight, and fecundity. Both in the Amur River and in the Poronai River, the autumn race of chum salmon prevails over the summer race in body length and weight, fecundity, number of pyloric caeca, and several other meristic traits. The intra-basin differences between the races are much more pronounced in the Amur chum salmon. The inter-race differences in microsatellites are also greater in the Amur chum salmon compared to the Poronai chum salmon. Using microsatellites, three levels of differentiation have been revealed: (1) between the basins of the Amur and Poronai rivers, (2) between the races within each of the river basins, (3) and between population samples within each race of each basin. A hypothesis is proposed that the currently existing races of chum salmon in the Amur and Poronai rivers have evolved since the breakup of the Paleoamur, and the intra-basin divergence of the races started in the Amur River earlier than in the Poronai River. An analysis of our own data and the published data suggests that the adaptation of the seasonal races of chum salmon to the conditions of their spawning grounds is determined by a complex of morphological and physiological traits, including the number of pyloric caeca, which is an adaptive and highly heritable trait associated with the incubation temperature of the water.     

Asynchrony in population dynamics of sockeye salmon in southwest Alaska

Ecologists have examined the synchronization of population dynamics across space as a means to understand how populations respond to climate variation. However, response diversity may reflect important variation among local population dynamics driven by population‐specific responses to regional environmental change. We used long‐term data on sockeye salmon Oncorhynchus nerka from pristine watersheds of southwestern Alaska to show that populations spawning in close proximity (<40 km) to one another have a limited degree of synchrony in their dynamics, even after accounting for density‐dependent processes. In fact, the dynamics of local populations of stream‐spawning sockeye salmon were no more coherent than those of stocks at a much coarser resolution across this region of Alaska. We examined four hypotheses to explain the observed patterns of asynchrony among stream‐spawning populations, and found that populations spawning in dissimilar habitats, and using different nursery lakes were less synchronized in their productivity. Similarity in the age structure of spawning adults was less correlated with synchrony in productivity. These results emphasize the importance of maintaining diverse spawning and rearing habitat for the conservation of Pacific salmon, and should guide conservation planning for Pacific salmon populations in regions where natural dynamics have been altered by habitat loss, hatchery practices, and over‐fishing.     

Genetic variability and population structure of sockeye salmon from the Asian Coast of Pacific Ocean

Variability of six microsatellite loci and 45 single nucleotide polymorphism (SNP) loci was analyzed in 17 samples of sockeye salmon from 10 major spawning watersheds on the Asian coast of the Pacific Ocean. On the basis of the analysis of SNP loci variability of sockeye salmon in the examined part of the range, five population groups were identified, including local stocks from the Palana, Okhota, and Kamchatka rivers, as well as the population groups of Southwestern Kamchatka, and Northeastern Kamchatka and Chukotka. Rather different pattern of samples differentiation was obtained by estimating variability of six microsatellite DNA loci. Regional complexes of the eastern and western coasts of Kamchatka were identified. Moreover, sockeye salmon from the Palana River fell into the cluster of Western Kamchatka populations, while the population from the Okhota River and Meynypilgin lake–river system (Chukotka), confined to the subperiphery of the range, where the most differentiated from the others. The possible reasons for the discrepancies and high divergence of the Palana River and the Okhota River sockeye salmon populations, inferred from the SNP markers analysis, are discussed.     

Structure of spawning school of chum salmon Oncorhynchus keta from Olutorsky Bay of the Bering Sea (Northeastern Kamchatka)

Results of studies of spawning chum salmon Oncorhynchus keta (Walbaum) in Olutorsky Bay and the Apuka River—the largest river in northeast Kamchatka—inflowing Olutorsky Bay of the Bering Sea are presented. It was established that the first individuals of the chum salmon enter the river together with early sockeye salmon and chinook salmon in the first ten-day period of June, and mass-spawning run takes place in July–August. Analysis of biological characteristics of chum salmon caught in the Apuka River and Olutorsky Bay of the Bering Sea enabled us to reveal the inhomogeneity of its spawning school represented by two seasonal forms.     

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.     

Disturbance of freshwater habitats by anadromous salmon in Alaska

High densities of habitat modifiers can dramatically alter the structure of ecosystems. Whereas spawning sockeye salmon (Oncorhynchus nerka) dig nests that cover over 2 m² and are at least 20 cm deep, and can spawn at high densities, relatively little attention has been devoted to investigating the impacts of this disturbance. We hypothesized that this temporally and spatially predictable bioturbation has large impacts on the coastal aquatic habitats used by sockeye. We experimentally investigated the impacts of disturbance caused by spawning sockeye in two streams and two lakes in Alaska by excluding salmon from 2.25 m² plots where they traditionally spawn. We sampled exclusions and control plots before, during, and after spawning. During sockeye spawning, fine sediment accumulated in areas where sockeye were excluded from spawning. In addition, sockeye spawning significantly decreased algal biomass by 80% compared to exclusion plots. We found mixed effects of spawning on the invertebrate assemblage. Tricladida and Chironomidae densities increased by 3x in exclusion plots relative to control plots in one creek site. However, for most taxa and sites, invertebrate densities declined substantially as spawning progressed, regardless of experimental treatment. Habitat modification by spawning salmon alters both community organization and ecosystem processes.     

Founding events influence genetic population structure of sockeye salmon (Oncorhynchus nerka) in Lake Clark, Alaska

Bottlenecks can have lasting effects on genetic population structure that obscure patterns of contemporary gene flow and drift. Sockeye salmon are vulnerable to bottleneck effects because they are a highly structured species with excellent colonizing abilities and often occupy geologically young habitats. We describe genetic divergence among and genetic variation within spawning populations of sockeye salmon throughout the Lake Clark area of Alaska. Fin tissue was collected from sockeye salmon representing 15 spawning populations of Lake Clark, Six-mile Lake, and Lake Iliamna. Allele frequencies differed significantly at 11 microsatellite loci in 96 of 105 pairwise population comparisons. Pairwise estimates of FST ranged from zero to 0.089. Six-mile Lake and Lake Clark populations have historically been grouped together for management purposes and are geographically proximate. However, Six-mile Lake populations are genetically similar to Lake Iliamna populations and are divergent from Lake Clark populations. The reduced allelic diversity and strong divergence of Lake Clark populations relative to Six-mile Lake and Lake Iliamna populations suggest a bottleneck associated with the colonization of Lake Clark by sockeye salmon. Geographic distance and spawning habitat differences apparently do not contribute to isolation and divergence among populations. However, temporal isolation based on spawning time and founder effects associated with ongoing glacial retreat and colonization of new spawning habitats contribute to the genetic population structure of Lake Clark sockeye salmon. Nonequilibrium conditions and the strong influence of genetic drift caution against using estimates of divergence to estimate gene flow among populations of Lake Clark sockeye salmon.     

Countergradient variation in carotenoid use between sympatric morphs of sockeye salmon (Oncorhynchus nerka) exposes nonanadromous hybrids in the wild by their mismatched spawning colour

Understanding the mechanisms that decrease gene flow between diverging populations is critical to understanding speciation. Anadromous (sockeye) and nonanadromous (kokanee) morphs of the Pacific sockeye salmon Oncorhynchus nerka spawn sympatrically and interbreed, yet allele frequency differences at neutral loci indicate restricted gene flow. Disruptive natural selection associated with strong selective differences between anadromous and nonanadromous life histories is thought to maintain the genetic differentiation of the morphs. Recently, a putative third morph of O. nerka exhibiting green rather than red breeding colour has been found on the spawning grounds sympatric with sockeye and kokanee. We investigated the ancestry of these green fish in a 2‐year controlled breeding study by using previously documented heritable, countergradient variation in red breeding colour to distinguish pure and hybrid morphs. Stabilizing sexual selection for similar red breeding colour in sockeye and kokanee has led to adaptive differences in the efficiency of carotenoid uptake between the morphs given differences in carotenoid availability between marine and lacustrine habitats. On the same diet, offspring parented by the green fish were intermediate in colour and in the concentration of dietary carotenoid pigments in their flesh and skin to those parented by either sockeye or kokanee; they were most similar to those parented by known kokanee × sockeye hybrids. This countergradient variation in carotenoid use results in a genotype‐environment mismatch in nonanadromous hybrids that exposes them by their breeding colour on the spawning grounds. Given that red colour is important in mate choice, sexual selection will almost certainly reduce reproductive opportunities for these hybrids and promote sympatric divergence of these incipient species. © 2005 The Linnean Society of London, Biological Journal of the Linnean Society, 2005, 84 , 287–305.     

The distribution of juvenile Pacific salmon and associated fish species in Lake Sopochnoye,Iturup Island

A single survey using a minnow seine net showed that juvenile chum and sockeye salmon are distributed extremely unevenly along the shoreline of Lake Sopochnoye, on Iturup Island. Young-of-the-year chum salmon aggregate mainly near the estuaries of the rivers that flow into the lake; young-of-the-year and 2-year-old sockeye salmon aggregate closer to the central part of the lake. The distribution of associated fish species is also very uneven, but none of them dominates within the zone of catches; the abundance of each of these species is comparable to that of the juvenile Pacific salmon.     

Seasonal races of chum salmon <Emphasis Type="Italic">Oncorhynchus keta</Emphasis> and their interrelations in Kamchatka Rivers

Dates of migration and spawning, size-age structure, and fecundity of seasonal races of chum salmon Oncorhynchus keta from the Kol River are reviewed, those of early summer, late summer, and autumn races, as well as localization and structure of their spawning grounds, bed-sediment particle size in the redds, hydrological and thermal conditions on spawning grounds, and meristic characters of races. Special traits of reproduction of seasonal races within the species range and in Kamchatka in particular are discussed. The number of seasonal races in rivers depends on the presence of various habitats suitable for spawning. In rivers with complicated hydrogeomorphological structure, the number of seasonal races increases. Variations of types of seasonal races in a particular river and in the whole species area are epigenetic, i.e., they depend on the hereditary genetic program and presence of conditions providing its realization via various channels.     

The genetic population structure of lacustrine sockeye salmon, <Emphasis Type="Italic">Oncorhynchus nerka,</Emphasis> in Japan as the endangered species

Lacustrine sockeye salmon (Oncorhynchus nerka) are listed as an endangered species in Japan despite little genetic information on their population structure. In order to clarify the genetic diversity and structure of Japanese populations for evaluating on the bottleneck effect and an endangered species, we analyzed the ND5 region of mitochondrial DNA (mtDNA) and 45 single nucleotide polymorphisms (SNPs) in 640 lacustrine sockeye salmon in Japan and 80 anadromous sockeye salmon in Iliamna Lake of Alaska. The genetic diversity of the Japanese population in both mtDNA and SNPs was significantly less than that of the Iliamna Lake population. Moreover, all Japanese populations had SNP loci deviating from the HWE. In spite of low genetic diversity, the SNP analyses resulted that the Japanese population was significantly divided into three groups. These suggest that Japanese sockeye salmon populations should be protected as an endangered species and genetically disturbed by the hatchery program and transplantations.