Polar Biology

, Volume 39, Issue 9, pp 1571–1579 | Cite as

Otolith variation in Pacific herring (Clupea pallasii) reflects mitogenomic variation rather than the subspecies classification

  • Lísa Anne Libungan
  • Aril Slotte
  • Edward O. Otis
  • Snæbjörn Pálsson
Original Paper
  • 222 Downloads

Abstract

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.

Keywords

Herring Subspecies Classification Otolith shape 

Introduction

Repeated trans-Arctic interchange of species from the Pacific and the Atlantic Ocean, following climate oscillations during the late Pliocene and Pleistocene, is considered to have played a large role in diversification and speciation among marine species at high latitudes (Vermeij 1991), e.g., in bivalves (Väinölä 2003) and gadoids (Carr et al. 1999). Several molecular studies have shown that some of this diversification is recent or has occurred after the last glacial period as in Theragra finnmarchica in northern Norway (Ursvik et al. 2007) and in Greenland cod, Gadus ogac (Carr et al. 1999). Due to the current changes in temperature, an increased number of trans-Arctic interchange may be expected to occur, resulting in greater connectivity and admixture between populations and species from the Atlantic and the Pacific.

Pacific herring (Clupea pallasii) provides one example of a trans-Arctic species, distributed in the coastal regions of the north Pacific Ocean and in the polar region of northeast Europe, from the Taymyr Peninsula, Russia in the east and west to Balsfjord in northern Norway. The geographic distribution and morphological characteristics within the Pacific herring have led to the description of three subspecies: the nominate subspecies C. pallasii pallasii in the Pacific, the White Sea herring (C. pallasii marisalbi) and the Chesha–Pechora herring (C. pallasii suworowi) of the southeast Barents and Kara Seas in Europe.

The Alaska Peninsula separates the Bering Sea from the northeast Pacific Ocean (Gulf of Alaska) and is considered to have been an obstacle for marine fauna and connectivity of populations in the region. Genetic divergence in mtDNA and microsatellites has been detected between herring occupying each side of the Alaska Peninsula, the northwest Pacific and the northeast Pacific lineages (O’Connell et al. 1998; Liu et al. 2012). Analysis of mtDNA variation by Laakkonen et al. (2013) on European C. pallasii showed that the European samples clustered within the northwest Pacific lineage defining the trans-Arctic group. The divergence between the herring in the northwest Pacific and Barents Sea within the group is recent or has occurred even after the last glacial period 10–15 kyr ago (Laakkonen et al. 2013), and signs of mixing have been reported to have occurred during the comparatively warm years of the 1930–1940s at several Arctic Siberian sites (Svetovidov 1952). The Arctic populations are characterized by low variation within areas, but genetic differentiation has been observed among the populations in the White Sea, in the Pechora Sea east of the White Sea and a strongly bottlenecked peripheral population in Balsfjord in northern Norway (Laakkonen et al. 2013; Semenova et al. 2015). A mixture of local Balsfjord herring and the highly migratory Norwegian spring spawners (Clupea harengus) based on allozymes and mitochondrial markers has also been observed (Jørstad and Pedersen 1986). Hybridization between the two species in northern Norway has been documented, where mitochondrial and nuclear introgression has occurred from Atlantic herring into Pacific herring in northern Norway; 21 % of the C. pallasii individuals in Balsfjord had variants of mtDNA from Atlantic herring (Laakkonen et al. 2015). Atlantic herring has been reported to penetrate the Barents Sea from the west, although they have not been found spawning there (Svetovidov 1952; Jørstad 2004).

Otolith shape has been used for decades as a population marker for Atlantic herring (Messieh 1972; Messieh et al. 1989; Turan 2000; Burke et al. 2008a, b) and more recently by Libungan et al. (2015a), which employed the same method as in this study. The otolith shape has been found to vary among populations in relation to spawning time of the year where the herring are experiencing different conditions during early developmental stages (Libungan et al. 2015a), despite lack of detectable genetic differentiation (Pampoulie et al. 2015). Otolith shape in Atlantic herring has furthermore been shown to vary among fjord populations along the coast of Norway where neighboring populations are more similar in shape than populations separated by larger distances (Libungan et al. 2015b), suggesting there might also be a genetic basis for the differentiation. The purpose of this study was to investigate whether the variation in otolith shape of herring in Balsfjord in northern Norway and southeast Barents Sea reflects their taxonomic classification into subspecies or the genetic affinities to the Pacific herring and the split between northwest and northeast Pacific known from the studies on mtDNA. If geographic patterns in otolith shape confirm the genetic patterns, a further support of the recent origin of the Arctic population is obtained. Furthermore, by including the Atlantic herring, we are able to analyze the differentiation between the two species and evaluate whether any signs of hybridization occur between them in Balsfjord.

Materials and methods

Sampling

Herring were sampled during the period of 1996–2014 with purse seiners from Alaska, USA (C. p. pallasi) and Møre in western Norway (C. harengus) and research trawl vessels in Balsfjord in northern Norway (C. pallasi) and the southeast Barents Sea in Russia (C. p. suworowi) (Fig. 1; Table 1). Sampling areas and time of sampling were selected based on the knowledge of spawning behavior of the herring populations at each location, ensuring that individuals sampled belonged to the spawning population of that site, with the exception of sampling years 2005 and 2006 for Barents Sea herring, which were not sampled during their spawning season (Table 1). Balsfjord herring (C. pallasii) were sampled in Balsfjord and distinguished from possible mixture of Norwegian spring spawning herring based on allozymes according to Jørstad et al. (1994). Total length (cm) was recorded for each fish and maturity stage according to an 8-point scale: immature = 1 and 2, maturing = 3–5, running/spawning = 6, spent = 7, recovering/resting = 8 (Mjanger et al. 2011). The sagittal otoliths were washed in clean water and stored in paper bags. All fish were aged from their scales using standard aging techniques.
Fig. 1

Sampling areas and geographic distribution of Atlantic and Pacific herring analyzed for variation in otolith shape. Latitude is shown as 55–90°N (north), while longitude is shown as 0–360°E (east). NS Norwegian spring spawning Atlantic herring (C. harengus) and BA Balsfjord, Norway, an admixture zone of both species (C. harengus and C. pallasii) and Pacific herring from BS southeast Barents Sea (C. p. suworowi), BE Bering Sea (C. p. pallasii) and KA Kamishak Bay (C. p. pallasii) both in Alaska, USA. See further in Table 1

Table 1

Samples of Atlantic and Pacific herring (see also Fig. 1)

Area, location

Code

Date

Latitude (N)

Longitude (E, W)

n

Age (years)

Length (cm)

Alaska, USA

Bering Sea, Kuskokwim Bay (Nelson Island)

BE

09, 06, 2006

60°23.0′

165°45.0′ (W)

36

4–8

24.1 (21.1–29.4)

Gulf of Alaska, Kamishak Bay (Douglas Reef)

KA

01, 05, 2014

59°12.0′

154°01.0′ (W)

59

4–8

21.4 (19.2–23.9)

Norway

Balsfjord

BA

08, 08, 2012

69°22.1′

19°15.7′ (E)

8

3–5

22.7 (21.5–26.0)

23, 01, 2014

69°30.7′

19°36.7′

5

3–7

20.1 (17.5–26.0)

10, 03, 2014

69°52.1′

18°97.5′

9

3–7

21.7 (19.5–26.5)

11, 03, 2014

69°30.6′

19°36.6′

16

3–5

19.2 (18.0–20.0)

23, 04, 2014

69°25.6′

19°28.6′

45

4–7

25.3 (22.5–27.5)

Møre

NS

14, 02, 2010

62°51.6′

5°23.3′ (E)

12

5–8

32.8 (31.5–34.5)

19, 02, 2010

61°88.3′

4°58.3′

19

6–8

31.0 (29.0–34.0)

24, 02, 2010

62°53.3′

5°20.0′

23

6–8

32.5 (29.0–34.5)

24, 02, 2010

62°53.3′

5°25.0′

29

6–8

32.6 (29.0–34.5)

Russia

Barents Sea

BS1

10, 06, 1996

68°85.8′

45°50.0′ (E)

57

3–8

22.9 (15.0–27.5)

11, 06, 1996

69°26.3′

51°83.2′

35

3–8

20.8 (15.0–27.0)

11, 06, 1996

70°00.0′

46°85.0′

11

3–8

20.8 (15.0–27.0)

Barents Seaa

BS2

19, 02, 2005

71°04.2′

47°05.0′

30

4–5

21.8 (19.5–23.5)

Barents Seaa

19, 02, 2006

70°12.5′

43°59.5′

28

3–7

19.7 (15.5–24.0)

Barents Seaa

22, 02, 2006

72°13.8′

47°65.5′

14

4–8

23.6 (19.5–28.0)

Area, location: sampling sites, code: area abbreviation, date: date of sampling (day, month, year), latitude (N: north), longitude (E: east, W: west), n sample size, age: range in years, length: average and range in cm

aNon-spawning herring

Image and data analysis

A digital image of each otolith was captured using either a Leica M60 stereomicroscope with a Leica DFC450 camera and the software Leica Application Suite (LAS Version 4.5) (Leica Micro-systems, Wetzlar, Germany, http://www.leica-microsystems.com) or a Leica MZ95 stereomicroscope (Leica Micro-systems, Wetzlar, Germany) with an Evolution LC-PL A662 camera (MediaCybernetics, Maryland, USA) using the software PixeLINK 3.2 (www.pixelink.com). All statistical analyses were conducted with R (R Core Team 2015) using the R packages ade4 (Dray and Dufour 2007), shapeR (Libungan and Pálsson 2015) and vegan (Oksanen et al. 2013).

Shape analysis

Following a method by Libungan et al. (2015a), the variation in otolith shape was examined by plotting the mean shape of each population using the shapeR package (Libungan and Pálsson 2015). The wavelet coefficients, which were 64 in total and represent the otolith shape, were obtained from the digital images using the wavethresh package (Nason 2012) and scaled by adjusting for allometric relationships with fish length as in Lleonart et al. (2000) and Reist (1985), implemented in the shapeR package (Libungan and Pálsson 2015). To inspect the variation in shape within herring groups, the mean and standard deviation of the coefficients was plotted against the angle using plotCI from the gplots package (Warnes et al. 2014). The proportion of variation within groups along the outline was summarized with intraclass correlation (ICC). Temporal stability in otolith shape was analyzed within the Barents Sea sample since there existed samples from 3 years (see Table 1) by applying canonical analysis of principal coordinates (CAP) (Anderson and Willis 2003) and an ANOVA-like permutation test to assess the significance of constraints using 2000 permutations with the vegan package (Oksanen et al. 2013). Otolith shape was then compared among populations with an overall test and also by applying comparisons between all populations to test for regional differences, using the CAP and the ANOVA-like permutation test. The same analyses were used to evaluate differences between age classes and the interaction of age and geographic origin since age is known to have confounding effects on otolith shape (Castonguay et al. 1991).

Ordination of the population averages along the first three canonical axes (CAP1, CAP2 and CAP3) was examined graphically with the shape descriptors. Variance within locations was calculated on the shape distances (CAP1 and CAP2) between each individual within each area. To compare the fit of the otolith shape variation to the previous taxonomic classification and to the divergence observed by genetic analyses, the CAP was conducted by partitioning the variation with respect to classification based firstly on the taxonomic split of species: the Norwegian spring spawners (C. harengus) with herring populations within C. pallasii and secondly between the two subspecies C. p. pallasii in the Pacific (Kamishak Bay and Bering Sea herring) with C. p. suworowi in the southeast Barents Sea. Thirdly, the northeast Pacific herring (C. p. pallasii from Kamishak Bay in the Gulf of Alaska) was compared with the trans-Arctic group as described by Laakkonen et al. (2013), comprised of the Bering Sea herring (C. p. pallasii) in the northeast Pacific and Barents Sea herring (C. p. suworowi) in Russia. Lastly, the Balsfjord herring (C. pallasii) in northern Norway, known to have introgressed genetic markers from C. harengus, was compared to its neighboring populations from C. harengus in Norway (NS) and C. p. suworowi from the Barents Sea (BS). Euclidean distances were calculated between the coordinates of the averages of the different population samples for the first four axes, weighted by the contribution of each axis to the overall variation and presented with boxplots.

Results

Main shape features

Otolith shape differed among all populations in the study, mainly at the excisura (Bird et al. 1986), rostrum, posterior tip and notch at the posterior rim (Fig. 2), which was further confirmed by examining variability in the mean wavelet coefficients and the proportion of variation within groups summarized with the ICC (Fig. 3a). Comparison of the otolith shape between the two species showed (Fig. 3b) similar patterns as among all samples, except at the angle close to 120°, where a large differentiation was found among samples within C. pallasii, especially between the trans-Arctic groups and the northeast Pacific sample KA (Fig. 3b). The ICC for comparisons of BA with the other samples showed that the largest split was around the angle of 200°, and in comparison with NS, it was about 0.25, and in comparison with the other, C. pallasii it was 0.17–0.18. The population from the northeast Pacific (Kamishak Bay in the Gulf of Alaska) showed a clear separation from all other populations at the excisura area (Fig. 2).
Fig. 2

Average shape of otoliths for the five sampling areas in the study. From Norway: Balsfjord (BA) and Møre (NS), from Russia: Barents Sea (BS1, BS2) and USA: Alaska [Bering Sea (BE) and Kamishak Bay (KA)]. The most variable areas on the otolith outline, the excisura (E), rostrum (R), posterior tip (P) and the notch at the posterior rim (N) are marked. The numbers 0, 90, 180 and 270 represent angle in degrees (°) on the outline which correspond to Fig. 3

Fig. 3

a Mean and standard deviation (SD) of the wavelet coefficients (gray) for all combined otoliths and the proportion of variance within groups or the intraclass correlation (ICC, black solid line), and b ICC for comparisons between species (NS vs. BA + BS1 + BS2 + BE + KA, solid line), between subspecies (KA + BE vs. BS1 + BS2, coarse dotted line) and between northeast Pacific and the trans-Arctic lineages (KA vs. BE + BS1 + BS2 + BA, fine dotted line) (see Table 1 for area codes and Table 2). The horizontal axis shows angle in degrees (°) based on polar coordinates where the centroid of the otolith is the center point of the polar coordinates (see also Fig. 2)

Multivariate analysis of otolith shape

No differences in otolith shape were detected within areas with more than one sampling event (F < 0.82, P > 0.12) with the exception of the Barents Sea sample, and samples were thus pooled (Table 1). The samples from the Barents Sea were from three sampling years (1996, 2005 and 2006), and the samples from years 2005 and 2006 were similar (F = 0.87, P = 0.51) and were therefore pooled. Significant differences were, however, observed between the 1996 sample and the 2005 and 2006 samples pooled (F = 4.53, P < 0.0001). The samples from the Barents Sea were therefore divided into two samples, with BS1 representing the 1996 year sample and BS2 representing the 2005 and 2006 samples (Table 1). No interactions were observed for age and populations in an overall test for ages 3–8 years (F = 1.13, P = 0.28). Age also resulted nonsignificant (F = 0.43, P = 0.90) and therefore excluded from the model and samples pooled and used in all comparisons. Significant differences in otolith shape were observed among populations and in tests contrasting different regions (F = 20.14, P = 5 × 10−4, Table 2). Also, significant differences (P = 5 × 10−4) were found between all population pairs in the study, even after applying a Bonferroni correction for multiple comparisons (P adjusted = 0.008).
Table 2

Otolith shape compared among all herring populations in the present study, between species, subspecies and the genetically distinct groups within C. pallasii

 

df

Var

F

All populations

5

0.22

24.03

Residual

433

  

Between species

NS versus (BA + BS1 + BS2 + BE + KA)

1

0.11

53.83

Residual

437

0.89

 

Between subspecies

KA + BE versus BS1 + BS2

1

15.16

21.31

Residual

268

190.67

 

Between northeast Pacific and the trans-Arctic lineages

KA versus (BE + BS1 + BS2 + BA)

1

19.50

27.17

Residual

378

251.92

 

Results from ANOVA-like permutation tests based on 2000 permutations. All tests were highly significant with P values 5 × 10−4. See Table 1 for population ID codes

Df degrees of freedom, Var variance, FF value

Examining the canonical scores for the populations revealed the largest differences between species (Fig. 4). Barents Sea and Bering Sea herring were similar in otolith shape, although statistically different, and clustered with Balsfjord herring along the first axis (Fig. 4a) intermediate between the distinct Norwegian spring spawning herring from Møre and the herring from Kamishak Bay in the Gulf of Alaska (Fig. 5). The first two canonical axes explained most of the variation between populations (CAP 1: 57.5, CAP1: 21.5 %), but the third and fourth axis also contributed to the differences observed (CAP3: 12.9 and CAP4: 7.2 %). The CAP1 and the CAP3 scores (Fig. 4b) showed that Balsfjord herring were intermediate in shape between the Norwegian spring spawners and the Pacific herring from the other samples of the trans-Arctic group (Barents Sea and Bering Sea). Otherwise, a similar pattern was observed as with CAP1 and CAP2 (Fig. 4a). The canonical distances representing shape differences between populations showed that the variation in otolith shape between species (C. harengus vs. C. pallasii) was large, but similar differentiation was observed between C. p. pallasii in the northeast Pacific (Kamishak Bay in the Gulf of Alaska) and the trans-Arctic group (Bering Sea, Barents Sea and Balsfjord) (Fig. 6). Balsfjord herring (C. pallasii) in northern Norway, in comparison with all other C. pallasii populations (Barents Sea, Bering Sea and Kamishak Bay in the Gulf of Alaska), revealed large differences, while similar shape was observed among subspecies occupying the Barents Sea (C. p. suworowi) and around Alaska (C. p. pallasii). The lowest variation among samples was observed within the trans-Arctic group as described by Laakkonen et al. (2013). Within-group variance based on shape distances between individuals revealed the highest values for Norwegian spring spawning herring (1.02) and second highest for the population in the northeast Pacific from Kamishak Bay (0.50). For the other populations, the values were Barents Sea (BS1) = 0.43, Balsfjord = 0.29, Bering Sea = 0.27 and Barents Sea (BS2) = 0.21.
Fig. 4

Canonical scores on discriminating axes a 1 and 2 and b 1 and 3 for each herring group. The first axis contributed most to the variation observed among the species/populations (57.5 %), while the second axis explained 21.5 % and third 12.9 %. From Norway: Balsfjord (BA) and Møre (NS), from Russia (BS1, BS2) and Alaska, USA (BE, KA) (see Table 1). Black letters represent the mean canonical value for each herring population. Intervals represent mean ± SE

Fig. 5

a Example of herring otoliths used for the shape analysis from Alaska, USA (KA) and b Møre Norway (NS) (see Table 1). Individuals of NS herring had the lowest canonical 1 scores representing shape differences among groups, while KA herring had the highest scores (see Fig. 4). The otolith shape differed mainly at the excisura, rostrum, the posterior tip and notch at the posterior rim (see Fig. 2)

Fig. 6

Boxplots of canonical score distances (see also Fig. 4) with respect to variation among herring species and subspecies. The comparisons are h–p: C. harengus versus C. pallasii, p-BA: Balsfjord herring (C. pallasii) in northern Norway, in comparison with all other C. pallasii populations (Barents Sea, Bering Sea, Kamishak Bay in the Gulf of Alaska). p.p–p.s: C. p. pallasii from the Pacific (Kamishak Bay and Bering Sea) versus C. pallasii suworowi from the Barents Sea. W: comparisons within the trans-Arctic group (Laakkonen et al. 2013) including the Bering Sea herring C. p. pallasii, the Barents Sea herring (C. p. suworowi) and Balsfjord herring (C. pallasii). W–E: comparisons between C. p. pallasii in the northeast Pacific (Kamishak Bay in the Gulf of Alaska) and the trans-Arctic group (Bering Sea, Barents Sea and Balsfjord)

Discussion

The results of this study show that otolith shape differs among the Atlantic and Pacific herring species, and variation between the species is larger than within Pacific herring. The C. pallasii herring occupying Balsfjord in northern Norway, C. pallasii suworowi in the Barents Sea and C. p. pallasii from the Bering Sea in the northwest Pacific are more similar to each other than to C. p. pallasii in the Gulf of Alaska in the northeast Pacific. These results are in accordance with previous studies based on genetic variation (Jørstad and Nævdal 1981; Jørstad and Pedersen 1986; Laakkonen et al. 2013, 2015). The Bering Sea herring and the European branch of the Pacific herring are intermediate in otolith shape between the Atlantic herring and the Pacific herring from the Gulf of Alaska.

The difference in the mean otolith shape for the herring populations was different from the patterns observed in previous studies on Atlantic herring (Eggers et al. 2014; Libungan et al. 2015a, b). At the excisura, around the 200° angle, which had the largest variation among Atlantic herring populations (Libungan et al. 2015a), the Norwegian spring spawners at Møre had the inner most shape in this study. A very distinct pattern at the excisura was found, where the Kamishak Bay herring from the Gulf of Alaska had the outermost otolith shape.

The samples from the Barents Sea (C. p. suworowi) were collected at different times of the year, the 1996 sample in June and the 2005–2006 samples were both from February. Shape differences were detected in a comparison between the 1996 sample and the 2005–2006 samples pooled. Herring in the southeast Barents Sea are reported to spawn on average in July (Semenova et al. 2015). Herring occupying nearby oceans, from the White Sea (C. p. marisalbi), southwest of the sampling area in the Barents Sea spawns in spring/early summer in March–June (Semenova et al. 2013, 2015), while herring occupying the Kara Sea (C. p. suworowi), east of the Barents Sea, spawns in late summer in August (Semenova et al. 2015). Even though the samples from the Barents Sea were sampled in different seasons (February and June), the majority of the herring from each sample were maturing (stage 4), which indicates a mixture of herring populations occupying this region, with one population spawning in spring and the other during late summer. Since the herring were close to spawning, the population sampled in February might have been White Sea herring migrating to their respective spawning grounds during the time of sampling. Since genetic variation exists between spawning groups of White Sea and Barents Sea herring at four allozyme loci (Semenova et al. 2009), further investigations are needed to see whether the same pattern of divergence is observed with otolith shape. Comparisons of the species C. harengus (Norwegian spring spawners from W-Norway) and C. pallasii from Balsfjord, Barents Sea, Bering Sea and Kamishak Bay in the Gulf of Alaska yielded the highest F value (53.83, Table 2), while a comparison of Kamishak Bay herring in the Gulf of Alaska with the trans-Arctic group of herring from the Barents Sea, Balsfjord and Bering Sea (Laakkonen et al. 2013) had a considerably lower F value (27.17) and thus more divergence in otolith shape, as might be expected, at the species level than intraspecies level. Differentiation in otolith shape between the C. pallasii subspecies was less than among populations within C. pallasii based on the genetic lineages of the northeast and the trans-Arctic group (Laakkonen et al. 2013).

Studies on genetic variation have shown that the more southerly distributed herring groups, such as the large Norwegian spring spawners and herring in the northeast Pacific, harbor more genetic variation than the northern populations in accordance with their population sizes and even bottlenecks in populations following the colonization of the Barents Sea and northern Norway (Laakkonen et al. 2013). In otolith variation, we observe a similar pattern, where the smallest variation was in the Bering Sea and Barents Sea herring. Higher variance could be expected in the Balsfjord population as a result of hybridization (Laakkonen et al. 2015), but this was not the case in the present study.

Similar amphiboreal distribution as in the Pacific herring is known for other species which may reflect emigration of Pacific herring into the Atlantic after the last glacial period of the Ice Age. The two gadoid genera, Eleginus and Theragra, E. navaga and T. finnmarchica species are known in the northeast Atlantic and E. gracilis and T. chalcogramma in the north Pacific (Christiansen et al. 2005), where the Theragra species have been classified as a single species based on mtDNA variation (Ursvik et al. 2007). Pacific cod (Gadus macrocephalus) and Greenland cod (G. ogac) are also closely related and may be classified as a single species (Carr et al. 1999), and the circumpolar capelin (Mallotus villosus) (Vilhjálmsson 1994) shows signs of trans-Arctic migration (Præbel et al. 2013). For Atlantic and Pacific herring, the diversification between the species is clear both genetically and in the morphology of the otoliths despite introgression. Also, populations of Pacific herring which are separated both by large geographic distances and barriers along the coast of northern Norway and the Alaska Peninsula are clearly distinguishable genetically and in otolith shape.

Further studies are needed to resolve the patterns within C. pallasii from northern Europe. The Barents Sea sample, which was intermediate in shape between the two herring samples from the Pacific, did not contain spawning fish and could therefore be a mixture of populations. Thus, analysis of samples from spawning populations of C. p. suworowi and also from C. p. marisalbi in the White Sea is warranted. Additional samples from the coast between Balsfjord and the Barents Sea might also be needed to evaluate whether the Balsfjord population has been shaped by the known genetic introgression and/or its small effective population size (Laakkonen et al. 2015).

It is apparent, as pointed out by Laakkonen et al. (2013), that the pattern does not comply with the current subspecies division within C. pallasii. A revised classification, considering the observed genetic and morphological evidence, should rather distinguish the northwest Pacific population occupying the Bering Sea together with the European populations of C. pallasii than with the northeast Pacific herring, occupying the Gulf of Alaska.

Notes

Acknowledgments

Torstein Pedersen at the University of Tromsø is thanked for providing the samples from Balsfjord in Norway. Ole Ingar Paulsen at the Institute of Marine Research in Norway is thanked for allozyme analysis, splitting out Norwegian spring spawning herring (C. harengus) from Balsfjord herring (C. pallasii) in Balsfjord. This work was funded by the Assistant teacher’s grant of the University of Iceland.

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Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Lísa Anne Libungan
    • 1
  • Aril Slotte
    • 2
    • 3
  • Edward O. Otis
    • 4
  • Snæbjörn Pálsson
    • 1
  1. 1.Department of Life and Environmental SciencesUniversity of IcelandReykjavíkIceland
  2. 2.Institute of Marine ResearchBergenNorway
  3. 3.Hjort Centre for Marine Ecosystem DynamicsBergenNorway
  4. 4.Alaska Department of Fish and GameHomerUSA

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