Evidence for Two Highly Differentiated Herring Groups at Goose Bank in the Barents Sea and the Genetic Relationship to Pacific Herring, Clupea pallasi

Genetic studies on Atlantic herring, Clupea harengus, have generally revealed a low level of genetic variation over large geographic areas. Genetically distinct herring populations in some of the Norwegian fjords are exceptions, and juvenile herring from the large oceanic herring, Norwegian Spring Spawners (NSS), are often found in mixture with local fjord populations as well as widely distributed in the Barents Sea. Research surveys in the eastern Barents Sea (Goose Bank) in 1993, 1994 and 2001 included collection of herring samples for allozyme analyses. As expected the results identified juveniles from NSS stock, but an additional unique group of herring (low vertebrae number), being almost fixed for alternative alleles at several allozyme loci, was detected. In some cases, the two groups of herring were taken in the same trawl catches as documented by highly significant departure from Hardy—Weinberg expectation with large excess of homozygotes providing evidence for population mixing. Large genetic differences (Nei's genetic distance = 1.53; F_ST = 0.754) were detected in pairwise comparisons based on five allozyme loci. The two herring groups were also compared with reference samples of Pacific herring, Clupea pallasi, including one sample from Japan Sea and three Alaskan samples. UPGMA dendrogram based on five allozyme loci revealed a close genetic relationship between the low vertebrae herring in the Barents Sea and the group of samples of Pacific herring. Although significant different in allele frequencies, one of the herring samples clustered together with the reference sample from Bering Sea with genetic distance of 0.008 and F_ST value of 0.032. The close genetic relationship found in this paper, suggest a re-evaluation of the taxonomic status of the Barents Sea herring populations investigated.     

Population structure and variability of Pacific herring (<Emphasis Type="Italic">Clupea pallasii</Emphasis>) in the White Sea,Barents and Kara Seas revealed by microsatellite DNA analyses

Pacific herring, Clupea pallasii, have recently colonised the northeast Atlantic and Arctic Oceans in the early Holocene. In a relatively short evolutionary time, the herring formed a community with a complex population structure. Previous genetic studies based on morphological, allozyme and mitochondrial DNA data have supported the existence of two herring subspecies from the White Sea and eastern Barents and Kara Seas (C. p. marisalbi and C. p. suworowi, respectively). However, the population structure of the White Sea herring has long been debated and remains controversial. The analyses of morphological and allozyme data have previously identified local spawning groups of herring in the White Sea, whereas mtDNA markers have not revealed any differentiation. We conducted one of the first studies of microsatellite variation for the purpose of investigating the genetic structure and relationship of Pacific herring among ten localities in the White Sea, the Barents Sea and the Kara Sea. Using classical genetic variance-based methods (hierarchical AMOVA, overall and pairwise F _ST comparisons), as well as the Bayesian clustering, we infer considerable genetic diversity and population structure in herring at ten microsatellite loci. Genetic differentiation was the most pronounced between the White Sea (C. p. marisalbi) versus the Barents and Kara seas (Chesha–Pechora herring, C. p. suworowi). While microsatellite variation in all C. pallasii was considerable, genetic diversity was significantly lower in C. p. suworowi, than in C. p. marisalbi. Also, tests of genetic differentiation were indicating significant differentiation within the White Sea herring between sympatric summer- and spring-spawning groups, in comparison with genetic homogeneity of the Chesha–Pechora herring.     

Analysis of microsatellite loci variations in herring (Clupea pallasii marisalbi) from the White Sea

The genetic diversity among spawning groups of herring from different parts of the White Sea was assessed using ten microsatellite loci. All loci were polymorphic with the expected heterozygosity estimates varying in the range of 12.7–94.1% (mean was 59.5%). The degree of genetic differentiation displayed by White Sea herring was statistically significant (θ = 2.03%). The level of pairwise genetic differentiation F _ST was 0–0.085, and it was statistically significant in most of the comparison pairs between the herring samples. A hierarchical analysis of molecular variance (AMOVA) revealed the statistically significant differentiation of White Sea herring. 96.59% genetic variation was found within the samples and 3.41% variation was found among the populations. The main component of interpopulation diversity (1.85%) falls at the differences between two ecological forms of herring, spring- and summer-spawning. Within the spring-spawning form, the presence of local stocks in Kandalaksha Bay, Onega Bay, and Dvina Bay was demonstrated.     

Preliminary data on variation of four microsatellite loci in Pacific herring Clupea pallasii

Variation of microsatellite loci Cpa 10, Cpa 113, Cpa4, and Cpa7 was for the first time examined in Pacific-type herring Clupea pallasii from the White Sea (CI. pallasii marisalbi), the Kara Sea (CI. pallasii suworowi), the Sea of Okhotsk, and Lake Nerpich'e, Kamchatka Bay, northwestern Pacific (CI. pallasiipallasii). All loci exhibitedhigh genetic diversity. The estimates of expected heterozygosity varied from 41.5 to 95.6% (mean, 82%). The level of pairwise genetic differentiation Fst at all microsatellite loci varied from 0.005 to 0.076 (0.019, on average) and t was statistically significant (P < 0.05) in most of the pairs of herring samples. Estimates of genetic differentiation among the herring of one subspecies were lower than between the groups belonging to different subspecies.     

Otolith variation in Pacific herring (<Emphasis Type="Italic">Clupea pallasii</Emphasis>) reflects mitogenomic variation rather than the subspecies classification

Pacific herring (Clupea pallasii) is divided into three subspecies: two in northeast Europe and one in the north Pacific Ocean. Genetic studies have indicated that the populations in northeast Europe have derived from the northwest Pacific herring recently, or during the last 10–15 kyr, and that they are distinct from the population in the northeast Pacific. In addition, hybridization between the Pacific herring and the Atlantic herring has been documented. Otolith variation has been considered to be largely affected by environmental variation, but here we evaluate whether the genetic differentiation is reflected in otolith shape differences. A clear difference in otolith shape was observed between the genetically differentiated herring species Clupea harengus from the Atlantic and C. pallasii. The otolith shape of C. p. suworowi in the Barents Sea was different from the shape of C. pallasii in northern Norway and C. p. pallasii from the Pacific. Populations of C. p. pallasii, sampled east and west of the Alaska Peninsula, which belong to two genetically different clades of the C. p. pallasii in the Pacific Ocean, show a clear difference in otolith shape. C. p. suworowi and the local C. pallasii peripheral population in Balsfjord in northern Norway are more similar to the northwest Pacific herring (C. p. pallasii) than to the northeast Pacific herring (C. p. pallasii), both genetically and in otolith shape. The Balsfjord population, known to be influenced by introgression of mtDNA from the Atlantic herring, does not show any sign of admixture in otolith shape between the two species. A revised classification, considering the observed genetic and morphological evidence, should rather group the northwest Pacific herring in the Bering Sea together with the European populations of C. pallasii than with the northeast Pacific herring in the Gulf of Alaska.     

Phylogeography of Bivalve Cyclina sinensis: Testing the Historical Glaciations and Changjiang River Outflow Hypotheses in Northwestern Pacific

Background

The marginal seas of northwestern Pacific are characterized by unique topography and intricate hydrology. Two hypotheses have been proposed to explain genetic patterns of marine species inhabiting the region: the historical glaciations hypothesis suggests population genetic divergence between sea basins, whereas the Changjiang River outflow hypothesis suggests genetic break in line with the Changjiang Estuary. Here the phylogeography of bivalve Cyclina sinensis was investigated to test the validity of these two hypotheses for intertidal species in three marginal seas—the East China Sea (ECS), the South China Sea (SCS), and the Japan Sea (JPS).

Methodology/Principal Findings

Fragments of two markers (mitochondrial COI and nuclear ITS-1) were sequenced for 335 individuals collected from 21 populations. Significant pairwise Φ_ST were observed between different marginal sea populations. Network analyses illustrated restricted distribution of haplogroups/sub-haplogroups to sea basins, with a narrow secondary contact zone between the ECS and SCS. Demographic expansion was inferred for ECS and SCS lineages using mismatch distributions, neutral tests, and extended Bayesian Skyline Plots. Based on a molecular clock method, the divergence times among COI lineages were estimated dating from the Pleistocene.

Conclusions

The phylogeographical break revealed for C. sinensis populations is congruent with the historical isolation of sea basins rather than the putative Changjiang River outflow barrier. The large land bridges extending between seas during glaciation allowed accumulation of mutations and subsequently gave rise to deep divergent lineages. The low-dispersal capacity of the clam and coastal oceanography may facilitate the maintenance of the historical patterns as barriers shift. Our study supports the historical glaciations hypothesis for interpreting present-day phylogeographical patterns of C. sinensis, and highlights the importance of historical glaciations for generating genetic structure of marine coastal species especially those with low-dispersal abilities in northwestern Pacific.     

What Maintains the Central North Pacific Genetic Discontinuity in Pacific Herring?

Pacific herring show an abrupt genetic discontinuity in the central North Pacific that represents secondary contact between refuge populations previously isolated during Pleistocene glaciations. Paradoxically, high levels of gene flow produce genetic homogeneity among ocean-type populations within each group. Here, we surveyed variability in mtDNA control-region sequences (463 bp) and nine microsatellite loci in Pacific herring from sites across the North Pacific to further explore the nature of the genetic discontinuity around the Alaska Peninsula. Consistent with previous studies, little divergence (Φ_ST  = 0.011) was detected between ocean-type populations of Pacific herring in the North West Pacific, except for a population in the Yellow Sea (Φ_ST  = 0.065). A moderate reduction in genetic diversity for both mtDNA and microsatellites in the Yellow Sea likely reflects founder effects during the last colonization of this sea. Reciprocal monophyly between divergent mtDNA lineages (Φ_ST  = 0.391) across the Alaska Peninsula defines the discontinuity across the North Pacific. However, microsatellites did not show a strong break, as eastern Bering Sea (EBS) herring were more closely related to NE Pacific than to NW Pacific herring. This discordance between mtDNA and microsatellites may be due to microsatellite allelic convergence or to sex-biased dispersal across the secondary contact zone. The sharp discontinuity between Pacific herring populations may be maintained by high-density blocking, competitive exclusion or hybrid inferiority.     

Preliminary data on variation of four microsatellite loci in Pacific herring <Emphasis Type="Italic">Clupea pallasii</Emphasis>

Variation of microsatellite loci Cpa110, Cpa113, Cpa4, and Cpa7 was for the first time examined in Pacific-type herring Clupea pallasii from the White Sea (Cl. pallasii marisalbi), the Kara Sea (Cl. pallasii suworowi), the Sea of Okhotsk, and Lake Nerpich’e, Kamchatka Bay, northwestern Pacific (Cl. pallasii pallasii). All loci exhibitedhigh genetic diversity. The estimates of expected heterozygosity varied from 41.5 to 95.6% (mean, 82%). The level of pairwise genetic differentiation F _st at all microsatellite loci varied from 0.005 to 0.076 (0.019, on average) and t was statistically significant (p < 0.05) in most of the pairs of herring samples. Estimates of genetic differentiation among the herring of one subspecies were lower than between the groups belonging to different subspecies.     

Roseobacter-Like Bacteria in Red and Mediterranean Sea Aerobic Anoxygenic Photosynthetic Populations

Bacteriochlorophyll a-containing aerobic anoxygenic phototrophs (AAnP) have been proposed to account for up to 11% of the total surface water microbial community and to potentially have great ecological importance in the world's oceans. Recently, environmental and genomic data based on analysis of the pufM gene identified the existence of α-proteobacteria as well as possible γ-like proteobacteria among AAnP in the Pacific Ocean. Here we report on analyses of environmental samples from the Red and Mediterranean Seas by using pufM as well as the bchX and bchL genes as molecular markers. The majority of photosynthesis genes retrieved from these seas were related to Roseobacter-like AAnP sequences. Furthermore, the sequence of a novel photosynthetic operon organization from an uncultured Roseobacter-like bacterial artificial chromosome retrieved from the Red Sea is described. The data show the presence of Roseobacter-like bacteria in Red and Mediterranean Sea AAnP populations in the seasons analyzed.     

Ancient Divergence in the Trans-Oceanic Deep-Sea Shark Centroscymnus crepidater

Unravelling the genetic structure and phylogeographic patterns of deep-sea sharks is particularly challenging given the inherent difficulty in obtaining samples. The deep-sea shark Centroscymnus crepidater is a medium-sized benthopelagic species that exhibits a circumglobal distribution occurring both in the Atlantic and Indo-Pacific Oceans. Contrary to the wealth of phylogeographic studies focused on coastal sharks, the genetic structure of bathyal species remains largely unexplored. We used a fragment of the mitochondrial DNA control region, and microsatellite data, to examine genetic structure in C. crepidater collected from the Atlantic Ocean, Tasman Sea, and southern Pacific Ocean (Chatham Rise). Two deeply divergent (3.1%) mtDNA clades were recovered, with one clade including both Atlantic and Pacific specimens, and the other composed of Atlantic samples with a single specimen from the Pacific (Chatham Rise). Bayesian analyses estimated this splitting in the Miocene at about 15 million years ago. The ancestral C. crepidater lineage was probably widely distributed in the Atlantic and Indo-Pacific Oceans. The oceanic cooling observed during the Miocene due to an Antarctic glaciation and the Tethys closure caused changes in environmental conditions that presumably restricted gene flow between basins. Fluctuations in food resources in the Southern Ocean might have promoted the dispersal of C. crepidater throughout the northern Atlantic where habitat conditions were more suitable during the Miocene. The significant genetic structure revealed by microsatellite data suggests the existence of present-day barriers to gene flow between the Atlantic and Pacific populations most likely due to the influence of the Agulhas Current retroflection on prey movements.     

Comparative analysis of alternative statistical models for differentiation of herring stocks based on meristic characters

A basic stock assessment problem is the mixing and separation of herring populations in their specific areas. Within the transition zone between the North and the Baltic seas (Skagerrak, Kattegat, The Sound) a mixing of two herring populations ( Clupea harengus L.) temporarily takes place. One major component stems from the Baltic Sea (spring spawner), and the other from the North Sea (autumn spawner); each stock exhibits different meristic characteristics. In order to separate the two herring populations, 'pure' learning samples of meristic characters were created in 1995 as differential variables. Mainly gained during two research surveys at two geographically remote areas where a mixing of herring components was relatively unlikely, these learning samples were considered as representative for one or the other herring population. This paper compares the current (ICES) separation approach for herring stock assessment with two alternative methods wherein vertebra counts (vc) are used as meristic characters. The two proposed methods are (a) an inverted variance weighted linear model, and (b) a separation rule based on a quadratic discriminant analysis. The paper summarizes and discusses the results of predicting fractions of the two herring components derived from all three separation models. The underlying example data set stems from a 1991–97 routine Swedish survey in the transition zone. In comparison, the quadratic discriminant analysis separation model was identified as superior to the two other methods. Furthermore, the model suggests a higher degree of mixing of the two herring stocks in the transition area than was previously thought; inter-annual changes in the geographical distribution of the two populations are suggested as being less variable than previously assumed.     

Outlier Loci Detect Intraspecific Biodiversity amongst Spring and Autumn Spawning Herring across Local Scales

Herring, Clupea harengus, is one of the ecologically and commercially most important species in European northern seas, where two distinct ecotypes have been described based on spawning time; spring and autumn. To date, it is unknown if these spring and autumn spawning herring constitute genetically distinct units. We assessed levels of genetic divergence between spring and autumn spawning herring in the Baltic Sea using two types of DNA markers, microsatellites and Single Nucleotide Polymorphisms, and compared the results with data for autumn spawning North Sea herring. Temporally replicated analyses reveal clear genetic differences between ecotypes and hence support reproductive isolation. Loci showing non-neutral behaviour, so-called outlier loci, show convergence between autumn spawning herring from demographically disjoint populations, potentially reflecting selective processes associated with autumn spawning ecotypes. The abundance and exploitation of the two ecotypes have varied strongly over space and time in the Baltic Sea, where autumn spawners have faced strong depression for decades. The results therefore have practical implications by highlighting the need for specific management of these co-occurring ecotypes to meet requirements for sustainable exploitation and ensure optimal livelihood for coastal communities.     

Postglacial Colonization of the North European Seas by Pacific Fishes and Lamprey

A critical analysis of literature data on the distribution, morphology, and phylogeography of the Arctic lamprey (Lethenteron camtschaticum) and five species of marine and anadromous fish such as navaga (Eleginus navaga), pollock (Theragra chalcogramma), rainbow smelt (Osmerus mordax dentex), Pacific herring (Clupea pallasii), and pond smelt (Hypomesus olidus) has been performed. The results show that all these species have colonized Northern European seas, distributing along the Arctic coastline of Eurasia after the glacier retreat. The reasons that the dispersal of these species in the Atlantic Ocean may be impeded (preference for a cold environment, competition, and decrease of the evolutionary potential) are discussed.     

Variability in the Correlation between Asian Dust Storms and Chlorophyll a Concentration from the North to Equatorial Pacific

A long-term record of Asian dust storms showed seven high-occurrence-frequency centers in China. The intrusion of Asian dust into the downwind seas, including the China seas, the Sea of Japan, the subarctic North Pacific, the North Pacific subtropical gyre, and the western and eastern Equatorial Pacific, has been shown to add nutrients to ocean ecosystems and enhance their biological activities. To explore the relationship between the transported dust from various sources to the six seas and oceanic biological activities with different nutrient conditions, the correlation between monthly chlorophyll a concentration in each sea and monthly dust storm occurrence frequencies reaching the sea during 1997–2007 was examined in this study. No correlations were observed between dust and chlorophyll a concentration in the <50 m China seas because atmospheric deposition is commonly believed to exert less impact on coastal seas. Significant correlations existed between dust sources and many sea areas, suggesting a link between dust and chlorophyll a concentration in those seas. However, the correlation coefficients were highly variable. In general, the correlation coefficients (0.54–0.63) for the Sea of Japan were highest, except for that between the subarctic Pacific and the Taklimakan Desert, where it was as high as 0.7. For the >50 m China seas and the North Pacific subtropical gyre, the correlation coefficients were in the range 0.32–0.57. The correlation coefficients for the western and eastern Equatorial Pacific were relatively low (<0.36). These correlation coefficients were further interpreted in terms of the geographical distributions of dust sources, the transport pathways, the dust deposition, the nutrient conditions of oceans, and the probability of dust storms reaching the seas.     

Microsatellite Variability of Pacific Herring <Emphasis Type="Italic">Clupea pallasii</Emphasis> Valenciennes, 1847 from the Sea of Okhotsk and Bering Sea

The genetic variability of ten microsatellite loci was examined in samples of the herring from the Sea of Okhotsk and the Bering Sea. All loci were polymorphic; the expected heterozygosity estimates varied in the range of 0.3–94.3% (mean 66.7%). The degree of genetic differentiation of the herring was statistically significant (θ = 1.38%). The level of pairwise genetic differentiation F_ST was–0.002–0.046; R_ST was–0.003–0.166. Genetic differentiation of the herring from the Sea of Okhotsk and the Bering Sea correlated with the spatial-geographic structure of the species in the studied range on the basis of F_ST (P = 0.001).     

Little population structuring and recent evolution of the Pacific saury (Cololabis saira) as indicated by mitochondrial and nuclear DNA sequence data

Genetic population structure of the Pacific saury (Cololabis saira) was investigated using nucleotide sequence analysis on the mitochondrial DNA control region (355-361 bp). Although the left domain of the control region is known to be highly variable in many species, extremely low nucleotide and haplotype diversities (π = 0.17% and h = 0.418, respectively) were observed in a total of 141 individuals collected from five distant locales (East China Sea, Sea of Okhotsk, northwest Pacific, central North Pacific and northeast Pacific). No significant haplotype frequency differences were detected among widely separated samples, therefore we were unable to reject the null hypothesis of no genetic structuring in the Pacific saury population. Moderate levels of nucleotide substitution (p-distance) were observed between the Pacific saury and its Atlantic counterpart (Scomberesox saurus) in the control region (7.44%), cytochrome b gene (4.64%), and internal transcribed spacer (ITS1) (11.49%), indicating that the low sequence diversity of the control region in the Pacific saury is not due to the slow mutation rate. The molecular data suggest the Pacific saury may be a relatively recent offshoot among the extant members in the family Scomberesocidae.     

Introgressive hybridization between the Atlantic and Pacific herring (<Emphasis Type="Italic">Clupea harengus</Emphasis> and <Emphasis Type="Italic">Clupea pallasii</Emphasis>) in the White Sea,Barents and Kara Seas evidenced by microsatellites

In the North of Europe two sister species of herring—the Atlantic Clupea harengus and Pacific Clupea pallasii have post-glacially come into secondary contact. Although the breeding areas of the two species are thought to be separate, previous genetic studies based on allozyme and mitochondrial DNA data have supported the existence of introgression from the Atlantic herring to the Pacific herring. In this study, we employed microsatellite markers to explore the extent of introgressive hybridization between these fishes. Bayesian methods for assigning individuals to populations and identifying admixture proportions were applied to the genetic data based on ten microsatellites. Results indicated that 18 out of 464 Pacific herring (3.88%) were likely admixed. Some of the hybrid individuals contained genotypes suggesting that introgressive hybridization is an ongoing process. Despite some admixture, the Atlantic and Pacific herring gene pools remain sharply distinct (the average proportions of membership to “Atlantic” and “Pacific” clusters were Q_A = 0.998 and Q_P = 0.974, respectively), suggesting that hybridization was not frequent. The discovery of introgression among herring species opens new questions about the mechanisms underlying the observed pattern of genetic population differentiation in the North European Pacific herring.     

Biological features of the common fish species in Olyutorsky-Navarin region and the adjacent waters of the Bering Sea: 2. Families Macrouridae,Clupeidae, and Osmeridae

Biological features of the four common fish species, giant grenadier Albatrossia pectoralis (Macrouridae), Pacific herring Clupea pallasii (Clupeidae), Pacific rainbow smelt Osmerus mordax dentex, and Pacific capelin Mallotus villosus catervarius (Osmeridae), were studied under the 20-year dataset (1995?2015). These species inhabit the northwestern Bering Sea in the summer–autumn period and form the schoolings in the Olyutorsky-Navarin region. The size–age parameters of the fish caught by different sampling gear, as well as the peculiarities of the body length and body weight dynamics, spawning periods, spawning range, and conditions, were analyzed. The largest specimens of giant grenadier, Pacific herring, and Pacific rainbow smelt were observed in the catches performed by the bottom setline and the gill nets; the smallest fish were found in the trawl catches. The body length and body weight of Pacific herring were larger in the pelagic trawls compared to the bottom trawls; an opposite pattern was observed for the Pacific capelin. The abundant year-class in the species with short life cycle (capelin and herring) is well tracked on the longterm plots of the fish body size; this is accompanied by the decrease of their biological parameters. Herring stock covers large growing grounds; smaller body size was observed for the herring grazing in the coastal waters; young specimens dominate here.     

Genetic structuring among Alaskan Pacific herring populations identified using microsatellite variation

Five highly variable microsatellite loci were used to investigate population structuring in Pacific herring Clupea pallasi collected from Kodiak Island, two sites in the Bering Sea and four sites within Prince William Sound, Alaska. All loci revealed high levels of variability with heterozygosity estimates ranging from 86 to 97% (mean heterozygosity: 89%). The variation was structured significantly among sites suggesting that the samples investigated were genetically distinct from each other. Genetic divergence was greatest between populations from the Bering Sea and those from Prince William Sound. The Kodiak Island and Point Chalmers samples appeared to be distinct from the Prince William Sound and Bering Sea populations. The observed genetic distance relationships among samples could be explained largely in terms of geographical separation.     

Roseobacter-like bacteria in red and mediterranean sea aerobic anoxygenic photosynthetic populations

Bacteriochlorophyll a-containing aerobic anoxygenic phototrophs (AAnP) have been proposed to account for up to 11% of the total surface water microbial community and to potentially have great ecological importance in the world's oceans. Recently, environmental and genomic data based on analysis of the pufM gene identified the existence of alpha-proteobacteria as well as possible gamma-like proteobacteria among AAnP in the Pacific Ocean. Here we report on analyses of environmental samples from the Red and Mediterranean Seas by using pufM as well as the bchX and bchL genes as molecular markers. The majority of photosynthesis genes retrieved from these seas were related to Roseobacter-like AAnP sequences. Furthermore, the sequence of a novel photosynthetic operon organization from an uncultured Roseobacter-like bacterial artificial chromosome retrieved from the Red Sea is described. The data show the presence of Roseobacter-like bacteria in Red and Mediterranean Sea AAnP populations in the seasons analyzed.