Consequences of the historical demography on the global population structure of two highly migratory cosmopolitan marine fishes: the yellowfin tuna (Thunnus albacares) and the skipjack tuna (Katsuwonus pelamis)
© Ely et al; licensee BioMed Central Ltd. 2005
Received: 28 October 2004
Accepted: 22 February 2005
Published: 22 February 2005
Yellowfin and skipjack tuna are globally distributed in the world's tropical and sub-tropical oceans. Since little, if any, migration of these fishes occurs between the Atlantic and Indo-Pacific Oceans, one might expect to see genetic differences between sub-populations in these ocean basins. However, yellowfin and skipjack tuna have extremely large population sizes. Thus, the rate of genetic drift should be slower than that observed for other tunas.
Low levels of genetic differentiation were observed between Atlantic and Pacific samples of yellowfin tuna. In contrast, no genetic differentiation was observed between Atlantic and Pacific samples of skipjack tuna.
Much lower levels of genetic differentiation were found among sub-populations of yellowfin tuna compared to those observed for other large tunas, probably due to the large population size of yellowfin tuna. Since skipjack tuna appear to have even larger population sizes, it is not surprising that no genetic differentiation was detected between Atlantic and Pacific samples of these fish.
The yellowfin tuna, Thunnus albacares, has a global distribution in tropical and sub-tropical oceans. Annual catches of yellowfin tuna have averaged 1.2 million metric tons since 1998 with sizes ranging from 5 to 20 kg . If the average size of a harvested fish is 10 kg, then the harvest of 1.3 million metric tons in 2002 represents approximately 130 million individual fish.
In an earlier study, Scoles and Graves  were unable to find evidence of genetic differentiation between small samples of yellowfin tuna (Thunnus albacares) from the Atlantic (n = 20) and Pacific Oceans (n = 100) using an RFLP analysis of whole mitochondrial DNA (mtDNA). Subsequently, Ward et al.  found significant differentiation at the GPI-A* allozyme locus but only weak evidence for genetic differentiation with an RFLP analysis of whole mtDNA. In the whole mtDNA study, much larger sample sizes were employed to increase the sensitivity of the mtDNA assay, but only two restriction enzymes were used and consequently, only a few restriction sites were analyzed. The GPI-A* data were consistent with earlier studies that demonstrated genetic differentiation between Eastern and Western Pacific samples [4, 5].
Skipjack tuna (Katsuwonus pelamis) are found in tropical and warm temperate waters of the world's oceans. They are present in the three major oceans in large numbers and comprise approximately 40% of the annual catch of the world's tunas. Annual catches are on the order of 2 million metric tons or approximately 670 million individuals per year . Despite their huge numbers, the skipjack tuna are not as well studied as most members of the genus Thunnus. Tagging studies have demonstrated limited seasonal movements, but not much transoceanic movement. Thus, they probably do not spawn at discrete locations .
In the Pacific, genetic studies using isozymes have demonstrated an East-West cline in a serum esterase allele [7–9]. Fujino et al.  also demonstrated differences in esterase allele frequencies in samples from the Atlantic, Indian, and Pacific Oceans. However, small samples of Atlantic (n = 7) and Pacific (n = 9) skipjack appeared identical when mtDNA was examined .
After the formation of the Isthmus of Panama, the potential contact between Atlantic and Indo-Pacific populations was limited to the waters around southern Africa. It appears that this separation of the Atlantic and Pacific Oceans resulted in significant genetic drift for many large pelagic fishes since these subpopulations are now genetically differentiated. Examples include bigeye tuna [12, 13], albacore [14, 15], swordfish [16, 17], blue marlin  and sailfish . In addition, even more pronounced differentiation produced species pairs of Atlantic and Pacific bluefin tunas and the Atlantic white marlin and the Pacific striped marlin [19–22].
To measure the degree of genetic differentiation between the Atlantic and Pacific sub-populations of either yellowfin or skipjack tuna, we examined the hypervariable control region I (CR-I) and a segment of a coding region gene of the respective mitochondrial DNAs. Genetic differences were observed between the Atlantic and Pacific yellowfin tuna samples with PCR-RFLP data of the ATCO gene region, but not with CR-I sequence data. In contrast, no differences between the Atlantic and Pacific skipjack tuna samples were detected with either type of data. Information contained in the CR-I reveals very different demographic histories for yellowfin tuna and skipjack tuna. However, very large long-term female effective population sizes (Ne) were estimated for both species, which may explain the observed levels of inter-oceanic genetic partitioning.
Control region nucleotide sequence analysis
Genetic diversity indices and demographic parameters of yellowfin tuna CR-I. N number of individuals; M, number of haplotypes; π, nucleotide diversity; h, haplotypic diversity. Tajima's D neutrality test and associated probability in parentheses. Mismatch distribution parameters τ, ΘO, Θ1.
0.035 ± 0.018
0.997 ± 0.001
0.027 ± 0.014
0.987 ± 0.012
0.029 ± 0.016
0.994 ± 0.009
0.033 ± 0.017
0.999 ± 0.006
0.032 ± 0.017
0.997 ± 0.006
Genetic diversity indices and demographic parameters of skipjack tuna CR-I. Abbreviations and notations as in Table 1.
0.084 ± 0.041
0.999 ± 0.001
0.082 ± 0.041
0.998 ± 0.009
0.084 ± 0.043
1.000 ± 0.020
E. Pacific Ocean
0.077 ± 0.038
0.998 ± 0.008
0.083 ± 0.041
0.998 ± 0.007
AMOVA of the patterns of sequence variation contained in the CR-I of yellowfin tuna. Localities were assigned into three regional groupings: Atlantic, Pacific and Indian. The Atlantic region included two samples, NW Atlantic and Ivory Coast, whereas the Pacific and Indian regions included only one sample each.
Source of Variation
ΦCT : 0.003
0.17 ± 0.01
Among populations within groups
ΦSC : -0.001
0.51 ± 0.01
ΦST : 0.002
0.038 ± 0.006
AMOVA of the patterns of sequence variation contained in the CR-I of skipjack tuna. Localities were assigned into three regional groupings: Atlantic, Pacific and Indian. The Atlantic region included two samples, NW Atlantic and Brazil, whereas the eastern Pacific and Indian Ocean (Solomon Islands) regions included only one sample each.
Source of Variation
ΦCT : 0.019
0.16 ± 0.00
Among populations within groups
ΦSC : -0.023
0.72 ± 0.01
ΦST : -0.003
0.72 ± 0.01
RFLP analysis of the mitochondrial ATCO gene region
Allele frequencies at the yellowfin tuna mtDNA ATPase6 locus
Analysis of molecular variance between Atlantic and Pacific yellowfin tuna samples
Source of Variation
Sum of Squares
Percentage of Variation
Allele frequencies at the skipjack mtDNA cytB locus
Demographic history and effective population size
Compared to other scombroid species with cosmopolitan distributions, we found substantially less genetic differentiation between Atlantic and Pacific sub-populations of yellowfin tuna and no inter-oceanic genetic differentiation of skipjack tuna. For instance, in bigeye tuna, there are two highly divergent mtDNA clades, one is cosmopolitan and the other is endemic to the Atlantic [12, 13]. This asymmetric distribution of Atlantic and Pacific clades has been observed in other large pelagic fishes as well, including swordfish [16, 17], blue marlin , and sailfish [19, 26]. Similarly, the striped marlin (Pacific) and white marlin (Atlantic) and the Atlantic bluefin tuna and the Pacific bluefin tuna are considered to be pairs of sister species [19–21, 26]. Thus, significant differentiation has occurred between the Atlantic and Pacific populations of many large pelagic species. Why are skipjack and yellowfin tuna populations different? One possibility is that in contrast to other large pelagic species, sufficient gene flow occurs to prevent inter-oceanic genetic differentiation. However, this explanation is contrary to the distribution patterns of tunas and billfish [27, 28]. For instance, bigeye tuna has a distribution of catches that would suggest a population continuum from the Indian Ocean to South Atlantic waters along the east and west coasts of Africa. However, bigeye samples show a marked inter-oceanic differentiation [12, 13]. In the Indian Ocean, the presence of skipjack and yellowfin tuna south of 20° S, is confined to the warm waters associated with the Agulhas currents. Seasonal movements do occur around the Cape of Good Hope via the Agulhas current, but it appears that the migrant tuna and other pelagic species return to the Indian Ocean as the seasons change [13, 29]. In fact, the distribution patterns of these two species in the South Atlantic along the African coast of are remarkably similar to both blue marlin and sailfish, two species that show a pronounced differentiation between Indo-Pacific and Atlantic populations. It should be noted, however, that the presence of "Pacific" mitochondrial DNA clades in Atlantic subpopulations of many tuna species indicates that inter-oceanic migration has occurred in the past. However, contemporary levels of inter-oceanic genetic differentiation for these species indicate that current levels of gene flow are absent or severely reduced. Thus, current distribution patterns of skipjack tuna and yellowfin tuna are not consistent with substantial levels of inter-oceanic gene flow. Certainly, there is no evidence to suggest that gene flow is occurring or has occurred at levels higher in these two species than in any of the other pelagic species where interoceanic differentiation has been demonstrated.
An alternative explanation to account for the lack of inter-oceanic differentiation in skipjack tuna and yellowfin tuna, is that the time since population expansion began has not been sufficient to allow for the populations to become differentiated. Assuming the very conservative mutation rate for CR-I of 4.9% per million years, a generation time 3.5 years, and the tau value 8.52, expansion of yellowfin tuna occurred about 522 Ky ago. By comparison, the estimated time for genetic differentiation of the Atlantic and Pacific populations of swordfish and of the Atlantic and Pacific bluefin tunas, using the same mutation rate, is very similar (450–470 Ky), and an even shorter time (170 Ky) is sufficient to explain the substantial genetic differentiation between the Atlantic and Mediterranean swordfish populations . Thus, time since expansion cannot explain the absence of inter-oceanic differentiation in these species. Therefore, we propose that much larger effective population sizes are the primary factor responsible for the similarity of the Atlantic and Pacific sub-populations of skipjack and yellowfin tuna.
Worldwide Tuna Catch Data for the Year 2002 
Catch (metric tons)
Ave. Wt. (kg)
Est. Number Fish Harvested*
2.0 × 106
670 × 106
1.3 × 106
130 × 106
0.43 × 106
24 × 106
0.24 × 106
16 × 106
0.125 × 106
6.9 × 106
0.024 × 106
3.4 × 106
0.036 × 106
2.1 × 106
Bigeye tuna, and bluefin tuna have much greater levels of genetic differentiation between Atlantic and Pacific subpopulations when mitochondrial DNA control region sequences are compared [12, 31]. However, their population sizes are 6 and 15 times lower than that of yellowfin and 30 and 75 times lower than that of skipjack, respectively. Furthermore, since bluefin tuna are a more temperate species, their effective population sizes may have been significantly lower than those observed in recent times whenever the northern hemisphere experienced glacial maxima. Thus, the relative differentiation of the Atlantic and Pacific subpopulations is consistent with the demographics of these species of tuna.
One exception to the patterns described above is albacore tuna. The distribution of albacore tuna mitochondrial DNAs does not appear to fit the patterns described above for the other temperate tuna species. Albacore abundance is similar to that of bigeye tuna and both species have two mtDNA clades. However, in albacore the two clades are not as well differentiated nor do they display the phylogeographic association observed for the bigeye tuna clades . Instead, the bimodal mismatch distribution of pairwise differences in albacore mtDNA is concordant with very large long-term effective population sizes in contrast to the contemporary population size.
Much lower levels of genetic differentiation were found among sub-populations of yellowfin tuna compared to those observed for other large tunas, probably due to the large population size of yellowfin tuna. Since skipjack tuna appear to have even larger population sizes than yellowfin tuna, it is not surprising that no genetic differentiation was observed between Atlantic and Pacific samples of these fish.
Samples of yellowfin tuna were obtained from the eastern Pacific Ocean (near the equator at 110° W; n = 41), the Indian Ocean (n = 63), the Gulf of Mexico and the East Coast of Florida (n = 38) and the Gulf of Guinea (n = 100). Samples of skipjack tuna were obtained from the Northwest Atlantic (n = 31), off the coast of Brazil (n = 19), the eastern Pacific Ocean (n = 43), and the south Pacific near the Solomon Islands (n = 37). DNA isolation, mitochondrial DNA D-loop region amplification, and nucleotide sequence analyses have been described previously [12, 32]. The number of segregating sites (S) was estimated with MEGA. Values of haplotypic diversity (h) , nucleotide diversity (π)  and the mean number of pairwise differences (K) were computed in ARLEQUIN ver. 2.0 . Mitochondrial DNA haplotype phylogenies were estimated using neighbour-joining analyses  with Tamura-Nei distances (α = 0.5)) in MEGA . The pair-deletion option was used when missing data, insertions, or deletions were present. Maximum-Parsimony (MP) [38, 39] was carried using heuristic searches with the default options in PAUP* 4.0b10 . Statistical support for the nodes was estimated with 1000 non-parametric bootstrap replicates . All trees were rooted at midpoint. Analyses of molecular variance (AMOVA)  were performed to estimate the partitioning of genetic variation in regional hierarchical arrangements using ARLEQUIN.
The demographic history contained in the mtDNA CR-I sequence data was inferred using two approaches. First, the null hypothesis of neutrality may be rejected when a population has experienced population expansion . Accordingly, Tajima's D test of neutrality [43, 44] and its significance levels were estimated using DnaSP 4.00  based on 1000 simulated re-samplings replicates. Alternatively, a population that has experienced a rapid expansion in the recent past shows smooth wave-like mismatch distribution [46, 47]. Thus, mismatch distribution analyses, under the assumption of selective neutrality, were also used to evaluate possible historical events of population growth and decline [47, 48]. Past demographic parameters, including τ , θ0 and θ1 and their probabilities  were estimated in ARLEQUIN taking into account the heterogeneity of mutation rates .
For the analysis of the mitochondrial cytochrome b gene, a 650 bp fragment of the skipjack tuna cytochrome b gene was amplified using primers CB3 (GGCAAATAGGAARTATCATTC) and GLUDG (TGACTTGAARAACCAYCGTTG) . Alleles were identified by determining the nucleotide sequence of the amplified fragment. For yellowfin tuna, the ATCO gene region was amplified using primers H9342 (GCCATATCGTAGCCCTTTTTG) and L8562 (CTTCGACCAATTTATGAGCCC) . The amplified fragments were digested with either Dde I or Hpy CH4III and the digestion products were resolved by electrophoresis in a 1.2% agarose gel.
We thank Bernard Stequert, Peter Sharples, the National Marine Fisheries Service, and the Inter-American Tropical Tuna Commission (IATTC) for providing the samples used in this study. Kurt Schaefer of IATTC graciously provided estimates of age at maturity for skipjack and yellowfin tunas and valuable information on the regional heterogeneity of these estimates. This study was funded in part by grant RT/F-1 to the Cooperative Institute for Fisheries Molecular Biology (FISHTEC) from NOAA.
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