© 2004 International Council for the Exploration of the Sea
Population genetic structure and history of the long-tailed hake, Macruronus magellanicus, in the SW Atlantic as revealed by mtDNA RFLP analysis
a University of Hull, Molecular Ecology and Fisheries Genetics Laboratory Hull HU6 7RX, UK
b Consejo Nacional de Investigaciones Científicas Argentina
*Correspondence to M. E. D'Amato: Present address: Stellenbosch University, Department of Genetics, Aquaculture Division, Stellenbosch, South Africa. tel: +27 21 808 5832; fax: +27 21 8085833. e-mail: damato{at}sun.ac.za.
The long-tailed hake, Macruronus magellanicus, is widely distributed in the SW Atlantic, and although it is commercially exploited, the extent of genetic structuring remains unclear. The hypothesis of a separate inshore stock as suggested by past biological data in northern Patagonia was tested with RFLP profiles of the mtDNA region ND5/6, in a total of 160 animals from eight locations. Sequence divergence between populations was nil, and all diversity is contained within populations. Despite the lack of geographic structuring in the distribution of haplotypes, the inference of population homogeneity should be taken cautiously owing to the skewed frequency distribution of haplotypes, with one allele accounting for 63% of individuals. A phylogenetic analysis of haplotypes reveals a star-shaped pattern with the presence of two lineages that may represent a population expansion. A rapid turnover of lineages, sweepstake recruitment, rapid expansion, or vulnerability to environmental conditions is not only suggested by the network pattern, but also by the departure from neutrality expectations. However, the role of selection cannot be ruled out until more loci or markers are examined.
Keywords: Macruronus magellanicus, mtDNA, population history, population structure
Received 28 January 2004; accepted 5 November 2004.
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Introduction |
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The long-tailed hake, Macruronus magellanicus (Lönnberg, 1907) (Pisces, Gadiformes, Merlucciidae), also known as blue grenadier, is widely distributed in the SW Atlantic from 35°S to 55°S, as well as in the SE Pacific (south of Chile). In the SW Atlantic it inhabits waters at depths between 60 and 600 m, where it appears to be associated with the Falklands (Malvinas) Current (reviewed in Giussi, 1996). The differential seasonal aggregations of the species on the Patagonian platform and platform edge were attributed to the fluctuating influence of this cold-temperate mass of water (Giussi, 1996). Fish aggregations display higher densities below 45°S, where it represents the most abundant fish resource.
M. magellanicus is similar to other demersal-pelagic species in that it undergoes diurnal vertical migrations from pelagic to deeper waters by day, and the opposite by night, a behavioural characteristics that could account for a high potential for dispersal and gene flow. Juveniles are pelagic, reach sexual maturity at between 2.9 and 4 years old (Giussi and Wöhler, 2001), and can live until 16 years old (Giussi, 1996). Spawning sites and times are indirectly derived from spent fish, maturity indices, and the presence of larvae. Based on gonad maturity, it is likely that spawning grounds occur widely in winter in shallow waters such as the San Matías Gulf, San Jorge Gulf, and Bahia Grande and also in the platform edge eastern to Falkland Islands in spring (Giussi, 1996). The presence of different breeding areas is also suggested by the presence of larvae and juveniles in autumn in San Matías Gulf (Giussi, 1996), in spring at Isla de los Estados, Tierra del Fuego (Machinandiarena and Ehrlich, 1999), and the eastern Falkland Islands (Giussi, 1996).
Stock structure remains controversial. The differential spatial and temporal presence of juveniles and mature or post-spawned fish does not appear to show a clear pattern. However, data from Giussi (1996), Perier and Di Giacomo (1999), and Giussi et al. (1999) indicate that a group of fish overwinters inshore in San Matías Gulf waters, exhibiting consistent differences from proximate populations in age distribution and differential growth. The hypothesis of a separate stock in San Matías Gulf is also suggested by the absence of fish in the intervening area between the Gulf and the platform at 42°S (Giussi, 1996; Perier and Di Giacomo, 1999).
Historically, the main fishing target in the S W Atlantic has been the hake Merluccius hubbsi. Its decline as a result of overexploitation resulted in imposition of strict quotas and the subsequent severe reduction of commercial activities during the 1990s. As a consequence, recommendations to diversify the fisheries targets (Wöhler et al., 1999) suggested M. magellanicus as a major alternative. The exploitation of Macruronus magellanicus was low during the 1980s, reached a peak of 145 000 t in 1988, and then declined to values between 28 000 and 65 000 t. Since 1998 the catch has reached values similar to those of 1988, and showed a progressive increase.
A major objective of fisheries genetics is the identification of discrete populations or groups with more or less restricted gene flow (reviewed in Carvalho and Hauser, 1995; Hauser and Ward, 1998). The amount and distribution of genetic diversity is determined not only by contemporary levels of gene flow, but also by demographic processes, population history, and selection. Separating the effects of migration from long-term population history or selection can be difficult, especially in marine organisms where high fecundity, high variance in reproductive success, and environmental instability seem to be frequent. The insight into historical processes can enhance the understanding of population structure and underlying evolutionary processes (Grant and Bowen, 1998; Árnason et al., 2000; Pogson et al., 2001). Such information is especially important in exploited species where interactions between exploitation and natural global and local climatic change may intensify such vulnerability (O'Brien et al., 2000) The absence of existing data on the genetic structure of M. magellanicus populations renders the design of an appropriate programme of conservation and long-term management extremely difficult.
In this paper, the population genetic structure, in particular the extent of differentiation of the San Matías samples, and recent history of M. magellanicus in its Atlantic distribution encompassing 2000 km was examined using mtDNA RFLPs of the ND5/6 2.5 Kb region. This fragment has been applied successfully for detecting population structuring in clupeids (Bembo et al., 1995; Hauser et al., 1995; Hauser et al., 2001) and salmonids (Bernatchez and Osinov, 1995; Apostolidis et al., 1996).
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Samples
Samples were collected between April 1997 and December 1998 (Figure 1). Owing to logistical constraints, none of our samples consisted of spawning individuals. To examine regional and local patterns of genetic structure we collected samples over the whole distribution range in the Atlantic and in the major gulfs of Patagonia. San Matías samples (samples 1 and 2) were taken out of the spawning season to ensure the capture of the hypothetical resident fish. The possibility of collecting a mixed sample composed of resident fish and individuals that migrate to the spawning ground is thus excluded. Sample 3 was taken in late winter in San Jorge Gulf (a hypothetical winter spawning area). The rest of the samples were collected on the shelf edge, where major aggregations occur. Collection dates and sample sizes (n) are as follows: 1 (March 1997), n = 12; 2 (April 1997), n = 34; 3 (September 1998), n = 11; 4 (September 1998), n = 24; 5 (April 1997), n = 6; 6 (March 1997), n = 7; 7 (September 1998), n = 45; 8 (April 1997), n = 21. Samples 1, 2 and 3 are referred to as inshore samples in the Results section.
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DNA extraction
DNA was extracted from fresh spleen, heart, or gonads using a CTAB method (Corach, 1991), or from muscle and fin clips preserved in 96% ethanol, a general proteinase K/phenol–chloroform procedure (modified from Sambrook et al., 1989).
RFLP analysis of mtDNA
The 2.5 Kb mtDNA region containing ND5 and ND6 genes of the NADH–dehydrogenase complex (Cronin et al., 1993) was amplified in a final volume of 20 µl, with 20–100 ng DNA, 1x NH4 buffer, 3 mM MgCl2, 500 µM dNTPs, 0.1 µM each primer, 0.1 U Taq polymerase, BioTaqTM BIOLINE, London, UK in an Omni Gene Hybaid cycler. PCR conditions were 94°C for 3 min, followed by 35 cycles at 94°C for 1 min, 47°C for 1 min, 72°C for 1 min, and a final extension at 72°C for 3 min.
PCR products were digested with DraI, EcoRI, HaeIII, MspI, PstI, PvuII, RsaI, TaqI, and XbaI (Promega Corporation, UK) overnight in a final volume of 10–15 µl using 1 µl of PCR and 3 U of restriction enzyme following manufacturer's recommendation. Restriction fragments were size-separated on 6% acrylamide (acrylamide:bisacrylamide 30% w/v 37, 5:1, NBL Gene Science Limited, Northumberland, UK) gels in 1x TBE buffer (Sambrook et al., 1989) at 200 V, 30 mA/gel, during 2–2:30 h, and silver stained (Sambrook et al., 1989). Fragment sizes were estimated with the program DNAFRAG (Schaffer and Sederoff, 1981) using pGEM® as a molecular marker.
Data analysis
MtDNA haplotype patterns for each enzyme were given an alphabetical (A, B, etc.) code, with haplotype A being the most common, and the remainder ranked in the order in which they were found for each restriction enzyme. Composite restriction enzyme patterns were then given a numerical code (1–24) to facilitate data handling. Data were converted into a binary format, coding restriction sites as presence/absence (1.0). Restriction sites were derived from fragment data by both direct observation and partial digestions.
Variation within samples was estimated by nucleotide diversity (p) and haplotype diversity (h) (Nei, 1987, equation 10.11); variation among samples was estimated by nucleotide divergence (dai Nei, 1987;option DA in REAP; McElroy et al., 1992). Heterogeneity in haplotype frequency distribution was tested using a
2 Monte Carlo randomization test for small samples (Roff and Bentzen, 1989).
Haplotype frequencies and nucleotide divergence between haplotypes were used to estimate the partitioning of variance components among sampling sites and the haplotypic correlation measures, the Fst analogs of Excoffier et al. (1992) (WINAMOVA ver. 1.53, Excoffier, 1993). Significance of the 
-statistics is calculated using randomization tests: for st (within populations), haplotypes are permuted across populations; for sc (among populations), permutations are performed within groups; and for ct (among groups) populations are randomized across groups. The hierarchical analysis was performed among (i) eight separate populations, (ii) between inshore and offshore samples, and (iii) between San Matías samples and all others. The last two were carried out to test the possibility of two stocks: San Matías residents and migrants from the platform edge, or coastal residents and migrants.
Deviation from equilibrium expectations were tested with Tajima's (Tajima, 1989) and Fu's Fs (Fu, 1997) neutrality tests, based on the infinite-site model without recombination. Tajima's test is based on the difference between expected segregating (S) sites and nucleotide differences (k) between DNA sequences, and simulation studies strongly suggest it is more powerful than other similar tests when alternative hypotheses are selective sweeps and population bottleneck (Simonsen et al., 1995). Fu's test detects an excess of new (rare) alleles, and it is more powerful than other tests in cases of population expansion and genetic hitchhiking (Fu, 1997). These tests were performed with Arlequin ver. 2000 (Schneider et al., 2000).
The number of restriction site differences between haplotypes was used to construct a minimum spanning network (MINSPNET, Excoffier and Smouse, 1994). This method results in networks, rather than bifurcating dichotomies, that have the smallest possible total length.
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Restriction fragment variation
PCR amplification resulted in a product of approximately 2.5 Kb. The restriction enzymes (RE) that showed polymorphic patterns, DraI, HaeIII, MspI, PvuII, RsaI, and TaqI, were used to define haplotypes. The resultant restriction patterns are listed in the Appendix. The minimal number of mutations (sites) scored to configure the restriction patterns was 31. The estimated total number of bases analysed was 138. A total of 24 composite haplotypes was found for 160 individuals (Table 1).
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Haplotype 1 (AAAAAA) was the most common, present in 63.12% of individuals, while the next most frequent (haplotype 2) was present in only 6.87% of individuals. In all, 12 haplotypes occurred only once.
Average haplotype diversity within populations was high (h = 0.62), and nucleotide diversity was low (average p = 0.0104 ± 0.003) (Table 1).
Variation among samples
Heterogeneity in haplotype frequency distribution among samples was tested by Monte Carlo 2 simulation and AMOVA. The Monte Carlo 2 simulation found no significant heterogeneity among all samples (p = 0.35 ± 0.015), between inshore and offshore (p = 0.70 +/– 0.0144) or between the Santa Matías fish and the rest (p = 0.71 ± 0.0143).
Variance components and F-statistics analogs (st, ct and sc) were calculated with AMOVA ver. 1.53 (Excoffier, 1993). No significant differences among samples or between regions were found, and the negative values for the variance components among samples indicated that all variance can be attributed to within sample variation (Table 2). A further estimate of variation among samples, nucleotide divergence between samples revealed no structuring (average da = –0.00027).
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Phylogenetic relationship between haplotypes
The network of Figure 2 shows phylogenetic relationships among haplotypes. All connections between haplotypes represent a single mutational event, with types 5 and 7 the most distantly connected (seven mutational events). The resultant network shows a star-shaped group centralized on the most common type 1 (AAAAAA), connected to other more distantly related haplotypes, centralized on type 3 (BBAAA). The alternative connections between types 1 and 3 suggest the presence of homoplasies.
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Neutrality tests were used to detect displacement from equilibrium. Tajima's neutrality test value D was not significant (D = –1.2348, p = 0.08), whereas Fu's Fs was highly significant (Fs = –16.54, p < 0.001), indicating displacement from equilibrium due to excess of rare alleles.
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Discussion |
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Genetic diversity
Levels of ND5/6 RFLP diversity observed in long-tailed hake (h = 0.61) are lower than in marine and freshwater species. For example, 0.88 is reported, for European anchovy (Bembo et al., 1995), 0.89 for Atlantic herring (Turan et al., 1998), 0.834 for walleye pollock (Olsen et al., 2002), and 0.88 in kapenta (Hauser et al., 1998). Values are similar to those for anadromous fish: 047–0.79 in eulachon (McLean et al., 1999). Different mtDNA markers used for Macruronus novaezelandiae (Smith et al., 1996), Atlantic cod (Carr and Marshall, 1991; Carr et al., 1995), shallow-water Cape hake Merluccius capensis, and deep-water Cape hake M. paradoxus (Becker et al., 1988), European anchovy (Bembo et al., 1995), jackass morwong (Grewe et al., 1994), walleye pollock Theragra chalcogramma (Shields and Gust, 1995), several species of sardine and anchovy (Bowen and Grant, 1997; Grant and Bowen, 1998), and Atlantic herring (Turan et al., 1998; Hauser et al., 2001), show a skewed haplotype frequency pattern similar to that of M. magellanicus: a common haplotype accompanied by numerous rare haplotypes. The main consequence of such a pattern is that it reduces the statistical power of tests to detect differentiation (Hauser et al., 2001).
Population structure in open ocean
Unlike terrestrial environments, the marine realm is usually regarded as lacking major geographical barriers to dispersal and gene flow. Species with high dispersal and large population size such as pelagic fish often result in shallow or no genetic structuring across large geographic scales (see Ovenden, 1990; Palumbi, 1994; Graves, 1998; Waples, 1998), though there are an increasing number of cases showing the converse (Ruzzante et al., 1996; Lundy et al., 1999; Shaw et al., 1999).
The presence of fish with distinct growth patterns and migratory behaviour in San Matías Gulf (Giussi et al., 1999; Perier and Di Giacomo, 1999) suggests a certain degree of isolation. Our data here, however, provided no genetic evidence of such subdivision between samples overall or between inshore and offshore samples. All genetic variation appears to be present within samples, and nucleotide divergence among samples was absent. Such population homogeneity is in accordance with previous studies on the sister species Macruronus novaezelandiae, using cytb sequence information (Baker et al., 1995) and whole mtDNA RFLP (Smith et al., 1996).
The interpretation of indirect estimates of gene flow often presents difficulties (Bossart and Prowell, 1998), as well as the use of different sets of molecular markers that vary in their sensitivity to detecting gene flow (reviewed in Hauser and Ward, 1998). Using microsatellite markers, population structuring was detected in cod (Ruzzante et al., 1996, 1998; Hutchinson et al., 2001) and European hake Merluccius merluccius (Lundy et al., 1999), where previous studies using mtDNA did not (e.g. Smith et al., 1989; Carr and Marshall, 1991; Lundy et al., 2000). However, similar (Scribner et al., 1998; Gold and Turner, 2002) and higher discriminatory power of mtDNA over nuclear markers was observed in Atlantic salmon (Tessier et al., 1995), Spanish mackerel (Scomberomorus maculatus) (Buonaccorsi et al., 2001b), and blue marlin (Makaira nigricans) (Buonaccorsi et al., 2001a), while structuring was detected only with mtDNA in walleye pollock (Olsen et al., 2002).
Sampling design is also of crucial importance in identifying stocks. Unfortunately, as stated before, spawning sites were not clearly identified in M. magellanicus, and it is unknown whether this species displays homing behaviour. Other technical difficulties in detecting population structure arise when assumptions of the population genetics models are violated, as for example, in cases of demographic instability (Bossart and Prowell, 1998). Another limitation of molecular markers to detect population structure may result from low genetic drift when population sizes are in the order 103–106 individuals.
Although the current data do support high levels of gene flow, additional comparative work should be undertaken using microsatellite markers to discount the effects of sampling and marker variability. However, despite the above points, mtDNA markers can be particularly informative in inferring historical changes by reconstructing intraspecific genealogies and in estimating population shifts from equilibrium (Avise et al., 1984; Rand, 1996).
Levels of diversity: demographic and historical perspectives
A pattern of dominant haplotypes and numerous rare ones may indicate selection (differential survival of fish, probably during early stages of life), demographical traits such as high reproductive success of a few females, suggested to be a factor among species with high fecundity (Avise et al., 1984; Hedgecock, 1994), or historical stochastic population events, such as a founder effect or bottleneck followed by population expansion. All these factors determine departures from mutation-drift equilibrium that can be detected analytically in neutrality tests and visualized graphically in networks. The characteristic out-of-equilibrium signature left in the genetic composition of the populations is usually detected as a star-like mtDNA network (e.g. Figure 2), that has been reported for other pelagic fish (Shields and Gust, 1995; Magoulas et al., 1996; Bowen and Grant, 1997; Grant and Bowen, 1998; McLean et al., 1999).
Also, the relationship between h (haplotype diversity) and 
(nucleotide diversity) is informative about population demographic history. Taking into account the levels of diversity detected by these two indices, Grant and Bowen (1998) defined four categories of fish, using either whole mtDNA RFLP or cytb sequence data. Low h and are interpreted as recent bottlenecks or a founder event, for example, M. novaezelandiae. In rapidly expanding conditions, h increases more rapidly than , so resulting in a large number of closely related haplotypes. In comparison with other ND5/6 cases, M. magellanicus appears to have high to moderate levels of haplotype diversity, which, along with low nucleotide diversity, would imply a past population bottleneck followed by rapid population expansion and accumulation of mutations. Such a case would indicate that the population is not in mutation-drift equilibrium.
Fu's Fs test (Fu, 1997), which is particularly sensitive to cases of population expansion and genetic hitchhiking, indicates a departure from equilibrium, though it is not possible to identify the cause from current data.
If patterns observed here in M. magellanicus are explained within a demographic-stochastic context, then an increase in population size must have occurred mainly from the two lineages represented by the central haplotypes 1 and 3 and its derivatives. Alternatively, a selective advantage of a few mitochondrial lineages can be postulated, though based on the neutrality tests, demographic instability seems more likely.
Besides the estimated historical changes, M. magellanicus populations appear to be subjected to fluctuations at shorter time-scales. Total biomass estimates indicate a constant increase in population size during the last three decades: e.g. 680 000 t in 1969, 1 544 440 t in 1992, 4 000 000 t in 1998 (Giussi, 1996 and references therein; Wöhler et al., 2000).
Current evidence and patterns taken from the literature (Magoulas et al., 1996; Bowen and Grant, 1997; Grant and Bowen, 1998; Árnason et al., 2000) indicate that the demographic instability hypothesis is more likely than selection in explaining the patterns observed in M. magellanicus. To confirm any of the two possible alternatives of population expansion or selection, other loci (see Rand, 1996 and references therein), such as nuclear markers, should be analysed. Selection would affect only a limited number of loci, but demographic factors such as bottlenecks would show a major effect at numerous loci.
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Appendix |
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Polymorphic restriction patterns of the 2.5Kb mtDNA PCR fragment ND5/6. Haplotypes were named in order of frequency, with A being the most common type. Restriction enzymes PstI and XbaI generated monomorphic patterns of two fragments each (1312 and 1153 bp; and 2045 and 422 bp, respectively).
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Acknowledgements |
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We are grateful to Daniel Corach (Universidad de Buenos Aires), Fernando Dulout (Universidad Nacional de La Plata), Marta Lizarralde (Centro Austral de Investigaciones Científicas), Lorenzo Lamatina (Universidad de Mar del Plata), and Atila Gostonyi (Centro Nacional Patagónico) for providing laboratory facilities for DNA extraction; to Alejandro Pettovello (Centro de Investigaciones Puerto Deseado), Raúl González (Instituto de Biología Marina y Pesquera Almte. Storni), and Bruno Pre
ski (formerly Instituto Nacional de Investigación y Desarrollo Pesquero) for collection of samples, and to Lorenz Hauser for his insightful comments on the manuscript. The work was funded by the Fisheries Society of the British Isles. |
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