© 2005 International Council for the Exploration of the Sea
Genetic differentiation of blue whiting (Micromesistius poutassou Risso) populations at the extremes of the species range and at the Hebrides–Porcupine Bank spawning grounds
a NTNU – Norwegian University of Science and Technology, Trondhjem Biological Station N-7493 Trondheim, Norway
b Aquaculture Development Centre, Department of Zoology and Animal Ecology Lee Maltings, Prospect Row, National University of Ireland, Cork, Ireland
*Correspondence to A. W. Ryan: Institute of Molecular Medicine, Trinity Centre for Health Sciences, St James's Hospital, Dublin 8, Ireland; tel: +353 1 608 3273/3292; fax: +353 1 454 2043. e-mail: aryan12{at}tcd.ie.
The blue whiting, Micromesistius poutassou (Teleostei, Gadidae) is found between latitudes 26° and 82°N along the continental margin of the Northeast Atlantic, with smaller populations in the Northwest Atlantic and the Mediterranean. There is an annual spawning aggregation on the Porcupine Bank and Hebridean Shelf (west of Ireland and Scotland, respectively), where most of the blue whiting population of the Northeast Atlantic spawns. Analysis of samples from the Barents Sea, the Northeast Atlantic, and the Mediterranean (n = 850, 11 samples) using one minisatellite and five microsatellite loci revealed significant geographic heterogeneity and isolated populations at the extremes of the species range in the Barents Sea and the Mediterranean. Furthermore, there was evidence of genetic heterogeneity among samples taken during the spawning season on the Porcupine Bank and Hebridean Shelf, with highly significant differentiation between the samples taken in the Hebrides in 1992 and 1998.
Keywords: genetic differentiation, marine species, Micromesistius, microsatellites, minisatellites
Received 28 November 2004; accepted 5 March 2005.
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Introduction |
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Marine fish species often have large population sizes, considerable migratory capabilities, and pelagic eggs and larvae that may drift passively for long distances in ocean currents. This dispersal, coupled with the relative lack of barriers to gene flow in the marine environment, is consistent with the observation that the level of inter-population differentiation in marine fish is considerably lower than that observed in freshwater and anadromous species (Gyllensten, 1985; Ward et al., 1994; DeWoody and Avise, 2000).
From a fisheries perspective, a local population may be largely self-recruiting, and thus react independently to exploitation, but still not be genetically distinguishable since a relatively low level of gene flow is sufficient to genetically homogenize populations. Where genetic differentiation can be demonstrated, a strong case can be made for stock separation into genetically meaningful management units (Carvalho and Hauser, 1995).
The blue whiting, Micromesistius poutassou Risso, a pelagic gadoid of commercial importance, is found between latitudes 26° and 82°N along the continental shelf in the Northeast Atlantic, with smaller populations in the Northwest Atlantic and in the Mediterranean (Bailey, 1982). A single juvenile specimen has been recorded in the Black Sea (Boltachev et al., 1999). A sister species, Micromesistius australis Norman, occurs in the southern hemisphere in two geographically distinct areas, with probable genetic differentiation between these populations (Ryan et al., 2002).
There is a large annual M. poutassou spawning aggregation during April and May along the Hebridean Shelf and Porcupine Bank, west of Scotland and Ireland, respectively, with a corresponding spawning migration from the Norwegian Sea feeding grounds. Local spawning has been recorded in the Mediterranean and may also occur in the Barents Sea (Bailey, 1982).
ICES (The International Council for the Exploration of the Sea) suggested that blue whiting in the Northeast Atlantic be managed as two stocks: a northern stock which spawns on the Hebridean shelf and feeds in the Norwegian Sea, and a southern stock with a nursery area off Spain and Portugal. The southern stock is thought to spawn on the continental shelf further north, as far as the Porcupine Bank, which has also been considered a transitional area between the northern and the southern stocks (Skogen et al., 1999 and references therein).
Population genetic studies on blue whiting were first performed by Mork and Giæver (1995), who screened 25-tissue-allozyme loci and reported three useful loci. Allele frequencies at two loci (IDHP-2* and PGM-1*) from 65 samples in the East Atlantic and Mediterranean revealed significant geographic heterogeneity and pointed to a genetically distinct population in the Barents Sea, with potentially isolated populations (not statistically significant) in the Mediterranean and Romsdalsfjord, Norway (Giæver and Stien, 1998). There was also evidence of temporal differentiation among some Barents Sea samples taken in 1992 and 1995.
In the Northeast Atlantic, part of the North Atlantic Current meets the continental slope in the vicinity of the Porcupine Bank and splits into two branches, heading north and south. Simulations of ocean currents on the continental shelf suggest that blue whiting eggs and larvae deposited north of the Porcupine Bank will be carried northwards, while those deposited to the south will be carried further south (Skogen et al., 1999). The authors proposed a separation line at approximately 54.5°N, between the Porcupine Bank and the Hebrides. However, the simulations pointed to considerable interannual variation, with the "line of separation" occurring as much as 200 km further north in some years.
Therefore, biological and oceanographic data point towards stock heterogeneity in the spawning areas to the west of Scotland and Ireland, i.e. a Hebridean spawning stock with a summer feeding migration into the Norwegian Sea, and a Porcupine spawning stock with feeding migrations to the south, northwest, or in both directions. The question remains, however, as to whether historical hydrographic and biological conditions have resulted in genetic differentiation between the putative stocks in this area.
The present study had two main objectives. First, to explore the overall level and pattern of genetic differentiation in Northeast Atlantic and Mediterranean blue whiting by means of a newly developed set of DNA mini- and microsatellite markers (Rico et al., 1997; Moran et al., 1999; Mattiangeli et al., 2002; Ryan et al., 2002), and to compare the picture obtained with that revealed by former allozyme studies (Mork and Giæver, 1995; Giæver and Stien, 1998). The second aim of the study was to use these new DNA markers to explore the genetic relationships among blue whiting spawning samples from the Porcupine Bank and Hebridean Shelf during the annual spawning aggregation.
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Material and methods |
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Eleven samples of blue whiting (n = 50–100) were taken from the Barents Sea, Iceland, the Northeast Atlantic, and the western Mediterranean (Figure 1). This sampling regime covers most of the species range in the East Atlantic. For convenience, each sample was allocated a three-character code. The availability of two separate samples (spring 1992, 1HS and 1PB, and spring 1998, 2HS and 2PB) from the Hebrides–Porcupine Bank areas afforded some comparison between samples taken in different years in the same approximate area.
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Details of the samples collected are given in Table 1. Gonad condition was determined by the individual collectors, and age was determined at the CEFAS laboratories, Lowestoft, UK, for those samples for which otoliths were available.
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DNA was prepared from frozen or alcohol-preserved muscle or, preferably, gill tissue by standard phenol/chloroform extraction and precipitation in ethanol (Sambrook et al., 1989). A single locus PCRable minisatellite, MmerAmpIB, was amplified using primers designed for whiting Merlangius merlangus L. (McGregor et al., 1996; Mattiangeli et al., 2002). PCR conditions consisted of a hot-start step of 95°C for 10 min, after which polymerase was added, followed by 30 cycles of 95°C, 60°C annealing, and 72°C for 1 min each, and a final elongation step of 72°C for 10 min. Four microsatellite loci isolated from blue whiting (MpouBW07, MpouBW08, MpouBW09, and MpouBW13; Moran et al., 1999), and one microsatellite locus isolated from whiting (MmerUEAW01; Rico et al., 1997), were amplified using 95°C for 3 min, 7 cycles of 94°C, 52°C, and 72°C for 30 s each, 24 cycles of 90°C, 52°C, and 72°C for 30 s each, and a final elongation step at 72°C for 5 min. Further details of the loci used are given in Ryan et al. (2002).
Amplification products for the minisatellite locus MmerAmpIB were resolved on 1% agarose gels and visualized by staining with ethidium bromide. For microsatellite loci, PCR fragments were diluted (1:10–1:30, experimentally determined to give optimal resolution) and loaded onto a Li-COR 4000 automated sequencer with formamide loading dye (formamide and bromophenol blue) in the ratio 1:2 PCR dilution to loading dye. Molecular-weight ladder (LI-COR 4000) and locus-specific standard amplification products (individuals of known genotype) were loaded onto every gel.
Allele frequencies were calculated from spreadsheet data using Genepop v3.2 (Raymond and Rousset, 1995; updated version 3.2a, May 2000). Deviation from Hardy–Weinberg equilibrium (HWE), allele-frequency heterogeneity tests, and FST (Weir and Cockerham, 1984) were also performed using Genepop. A Bonferroni correction (0.05/number of tests) was used to correct for multiple testing. Hierarchical analysis of molecular variance (AMOVA) and RST (Slatkin, 1995) calculations were performed using Arlequin (Schneider et al., 2000). Microchecker (van Oosterhout et al., 2004) was used to check for the presence of null alleles (microsatellite alleles that always fail to amplify) and large allele dropout (failure to amplify the larger of two alleles in a heterozygote due to the preferential amplification of the smaller allele).
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Results |
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Allele frequencies obtained for all loci and other supplementary information are available online1. Two loci (MpouBW09 and MpouBW13) showed significant deviation from HWE in multiple samples. Because of this deviation, all the results are presented for the total data set (i.e. all six loci, including MpouBW09 and MpouBW13), and only for those four loci that showed good fit to HWE. Microchecker analysis suggested the presence of null alleles at MpouBW09 (all samples except Portugal), MpouBW13 (all samples except Portugal and Trondheimsfjord), MpouBW07 in the Celtic Sea (CsA), and MmerUEAW01 in the Barents Sea. There was no indication of large allele dropout at any locus in any sample.
Two separate trawl hauls were taken in Icelandic waters. These were pooled into a single sample, as there was no allele-frequency heterogeneity between them, and there was no departure from HWE in the pooled sample, apart from the loci MpouBW09 and MpouBW13, which do not conform to HWE in many samples (Supplementary information downloadable).
Summary statistics (RST or FST and allele-frequency heterogeneity) for all loci are presented in Table 2. The test data show that there is significant allele-frequency heterogeneity among the populations sampled, in both the total data and the Hebrides–Porcupine Bank spawning aggregation. The greatest differentiation is found at the MmerUEAW01 locus.
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Pairwise FST and allele-frequency heterogeneity are presented in Table 3 for all loci combined (Fishers method, Genepop). The greatest population differentiation occurs between the Barents Sea and all other samples, and the Mediterranean and all other samples. Furthermore, even with a Bonferroni correction for multiple tests (all loci combined, 55 pairwise tests, p < 0.05/55 = 0.000909 is equivalent to significance at the 5% level), there is significant differentiation between the 1992 and 1998 Hebridean samples. Because the 1992 and 1998 Hebridean and Porcupine Bank sampling was a priori planned to test for temporal and spatial genetic heterogeneity within the main spawning area, the required Bonferroni correction is in this case 0.05/6 = 0.0083 for significance at the 5% level for pairwise comparisons. The 1998 Hebrides sample is also differentiated from at least one of the Celtic Sea samples (Table 3, pairwise p values).
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These results strongly indicate genetically differentiated populations at the latitudinal extremes of the range (i.e. in the Barents Sea and in the Mediterranean). Furthermore, there is robust indication of heterogeneity in the Porcupine–Hebridean spawning area, although this is stronger between years (1992 vs. 1998) than between geographical areas.
The results of the hierarchical analysis of molecular variance (AMOVA) are shown in Table 4. There is significant differentiation between years within regions, while the analysis does not suggest significant differentiation between the Hebridean Shelf and the Porcupine Bank. So, while the results clearly show genetic differentiation within the spawning grounds (Table 2, spawning aggregation and Table 3, pairwise comparisons), AMOVA suggests that this differentiation is largely temporal in nature.
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Discussion |
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Departures from HWE
Two of the loci, MpouBW09 and MpouBW13, used in the present study showed departure from HWE, owing to a deficit of heterozygotes. While a biological explanation is possible (Wahlund effect, selection), it is perhaps more likely that this is an artefact of the PCR amplification of allelic fragments. Deficiency of heterozygotes may be due to null alleles, which do not amplify because of mutations in the primer annealing site, or to allelic dropout, where the larger allele in a heterozygote fails to amplify to detectable levels following the more efficient amplification of the smaller allele. Analyses using Microchecker suggest the former. In addition, 68 alleles were detected at MpouBW09, and a sample size of 50–100 individuals is perhaps not sufficient to determine whether the samples are in HWE. Our main conclusions are largely unaffected by whether the analyses are performed on all loci, or whether MpouBW09 and MpouBW13 are excluded from the analyses (four loci only). However, if all loci are included in the analysis, there is an additional indication of differentiation between the 1992 Hebrides and Porcupine Bank samples (1HS vs. 1PB, p = 0.00209, Table 3a). Caution is required in this case, however, because the conclusion depends on the inference of population differentiation using loci with significant departures from HWE.
The Mediterranean and Barents Seas
These mini- and microsatellite data are compatible with results from allozyme studies on blue whiting (Giæver and Stien, 1998), in that the strongest differentiation is found for populations at the extremes of the species range, a pattern also seen in Atlantic cod Gadus morhua L. (Mork et al., 1985). While allozyme analysis has shown significant differentiation of the Barents Sea blue whiting sample, statistically significant differentiation of the Mediterranean blue whiting population was not reported by Giæver and Stien (1998).
Both the Corsica and Barents Sea samples contain a high proportion of presumably immature 2-year-olds (Table 1, gonad information was not available for either sample), and, in the case of the Barents Sea, were taken at a time not associated with spawning (September). It could then be argued that, as these samples represent migrating and immature individuals, they may not be representative of the local spawning populations in these areas. However, both samples show differentiation from almost all others, including the geographically nearest (Portugal and Trondheimfjord, Table 3), and other samples with high proportions of juveniles or sampled outside the spawning season (Portugal, Celtic Sea, Iceland) were not similarly affected.
The Hebrides–Porcupine Bank spawning aggregation
Comparable levels of differentiation were revealed at all loci (Table 2), with the greatest differentiation at MpouBW07 in the spawning aggregation.
AMOVA of the 1992 and 1998 temporal samples from the Hebrides–Porcupine Bank spawning aggregation shows that the greatest differentiation in this area is between years within regions (Table 4). Temporal population differentiation in blue whiting has previously been observed in allozyme frequencies in the Barents Sea (Giæver and Stien, 1998), where samples taken from 1992 and 1995 were genetically distinct.
Temporal population differentiation has also been observed in the European hake Merluccius merluccius L. (Lundy et al., 2000), another commercially important gadoid, on the basis of multiple samples from the north and south of the Bay of Biscay. The authors concluded that such temporal differentiation might be indicative of a metapopulation structure, where genetic differentiation may persist for some generations, only to be obliterated in the years when stocks are larger and mix genetically.
In the case of the blue whiting, it is not possible to draw such a conclusion based on the limited samples available. However, this is the second time that temporal differentiation has been demonstrated in areas where spawning occurs (Barents Sea and Hebrides–Porcupine Bank). It is also interesting that surveys of the spawning aggregation in 1986 and 1987 assigned some of the Porcupine Bank biomass to the southern stock, while this was not evident from 1988 surveys (Skogen et al., 1999 and references therein).
Waples (1997) outlined three possible explanations for temporal instability in the allele frequencies of marine species: first, an imperfect understanding of the biology of the species; second, unrecognized complexities in the processes involved; and third, flawed data. While the third possibility may be applicable to MpouBW09 and MpouBW13, due to heterozygote deficiencies and the possibility of null alleles, this does not appear to be the case for the other loci investigated. In addition, both the 1HS and 2HS samples were composed overwhelmingly of mature individuals, albeit with many specimens exhibiting spent gonads. These latter individuals could represent a component of the population that was actively undertaking a feeding migration, and did not spawn in the area where they were captured. However, only further sampling of mature, actively spawning individuals can shed light on this.
There was some indication of within-year differentiation between the Hebrides–Porcupine Bank samples in 1992. If all loci are included in the analysis, including two loci that show significant departure from HWE, this might appear to be the case (1HS vs. 1PB, p = 0.00209, Table 3a). However, departure from HWE at two loci is a cause for concern.
A considerable proportion of the between-year differentiation stems from the 1998 Hebrides sample 2HS which is composed of mature, predominantly 3-year-old specimens, and is strongly differentiated from the 1992 Hebrides sample. Whether this represents a genuine change in allele frequencies over time, or a component of the population that has not previously been sampled (a southern or western stock?), cannot be answered using the present data.
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Conclusions |
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TopIntroductionMaterial and methodsResultsDiscussionConclusionsReferences |
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Our data confirm the presence of a differentiated population of blue whiting in the Barents Sea, and provide a statistically significant confirmation of the existence of a distinct genetic stock in the Mediterranean, as previously indicated by allozyme results (Giæver and Stien, 1998). However, these data are not sufficient for us to identify explicitly boundaries that can then be translated into concrete assumptions about the geographical ranges of putative stocks in the Barents Sea and the Hebrides–Porcupine Bank area.
In the case of the Hebrides–Porcupine Bank spawning aggregation, it may be argued that the a priori two-population hypothesis is an oversimplification. On the other hand, there is now a preponderance of evidence in favour of genetic heterogeneity in the region. Whether the difficulty in reconciling the present genetic information with a specific geographic stock structure is due to an oversimplified stock model, difficulty interpreting the results obtained from some genetic markers, or an inadequate sampling grid, can perhaps only be elucidated by more extensive temporal and spatial studies.
The observation of temporal differentiation, for the second time in this species and the first time in the Hebrides–Porcupine Bank spawning aggregation, is intriguing. The implications for the use of genetics in stock identification are far reaching, and point to large-scale temporal sampling as a productive avenue of future research.
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Acknowledgements |
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The authors thank Terje Monstad (Institute of Marine Research, Bergen), Richard Millner (CEFAS, Lowestoft, UK), Margarida Castro (Univ. do Algarve, Faro, Portugal), Marianne Giæver, and Per Pedersen (Trondhjem biologiske stasjon) for the collection of samples, local information, and useful discussion. Jo Forthun (Trondhjem biologiske stasjon) provided the digital map shown in Figure 1. The contributions of The Norwegian Fisheries Research Board (NFFR), grant number I.3000.309.018, The Norwegian Research Council, grant number 108093/110, and The Directorate for Nature Management (DN), Norway, grant number 610.93/104, to the collection of samples are gratefully acknowledged. Thanks are due to Mari-Ann Østensen and Olav Vaagan (Trondhjem biologiske stasjon) for technical assistance. This work was funded by the European Union, grant FAIR CT95 0282.
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Footnotes |
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1 Supplementary information for this manuscript can be downloaded at doi: 10.1016/j.icesjms.2005.03.006.
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References |
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