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Genetic Stock Structure of the Swordfish (Xiphias Gladius) Inferred

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Genetic Stock Structure of the Swordfish (Xiphias Gladius) Inferred Marine Biology (1997) 127: 359 – 367 Springer-Verlag 1997 S. Chow · H. Okamoto · Y. Uozumi · Y. Takeuchi H. Takeyama Genetic stock structure of the swordfish (Xiphias gladius ) inferred by PCR-RFLP analysis of the mitochondrial DNA control region Received: 28 August 1996 / Accepted: 2 October 1996 Abstract Restriction fragment length polymorphism Introduction (RFLP) analysis was performed on PCR amplified DNA fragments containing the control region of the swordfish (Xiphias gladius Linnaeus, 1758) mitochondrial DNA. A The swordfish (Xiphias gladius Linnaeus, 1758) is a re- total of 456 individuals comprising 13 local samples (six markable habitat generalist. It has a very wide range of Pacific, three Atlantic, the Mediterranean Sea, two In- occurrence from tropical to cold waters of all oceans, dian Ocean and the Cape of Good Hope) were surveyed including the Mediterranean Sea, and occasionally with four endonucleases (Alu I, Dde I, Hha IandRsa I), makes feeding excursions to the bottom (deepest re- yielding a total of 52 composite genotypes. Within- corded depth = 650 m) where the temperature may be sample genotypic diversity (H) was high ranging from as low as 5 °C (Nakamura 1985; Carey 1989). Because 0.702 to 0.962 with a value of 0.922 for the pooled of their cosmopolitan nature and the scarcity of physical sample. Significant geographic variation in the fre- barriers to prevent their migration, one might suppose quencies of genotypes and restriction patterns was re- the global swordfish population to be relatively homo- vealed. The Mediterranean sample was highly distinct geneous within or even among ocean basins. Yet the from all other samples. Further, Rsa I digestion revealed biological stock structure of this pelagic fish is con- high levels of polymorphism in all but the Mediterra- troversial. In the Atlantic Ocean, spawning seems nean samples, indicating that exogenous swordfishes widespread and continuous throughout the tropical rarely enter that body of water. Heterogeneity between area, and larvae are found in a wide area between 26°N the North and South Atlantic samples was significant, and 27°S (Nishikawa et al. 1985). The size composition both of which differed from those of the Pacific. In of swordfish caught by commercial fisheries and sea- contrast, the Indian Ocean samples were not sig- sonal trends are very similar on both sides of the North nificantly different from the samples of South Atlantic Atlantic (Farber 1988; Miyake and Rey 1989). On the and Pacific. Genetic differentiation among the Pacific other hand, tag and recapture data suggested north– samples was low. The results indicate that the world- south, but not east–west, movements in the North wide swordfish population is genetically structured not Atlantic (Farber 1988; Miyake and Rey 1989). only among, but also within ocean basins and suggest Using restriction fragment length polymorphism that gene flow is restricted despite the absence of geo- (RFLP) analysis of mitochondrial DNA (mtDNA), graphic barriers. Magoulas et al. (1992) compared the haplotype (geno- type) frequencies of swordfish samples collected in the Mediterranean, off Gibraltar (Tarifa) and in the Gulf of Guinea, and found that the Mediterranean and Tarifa samples were very similar to one another but con- siderably different from the Gulf of Guinea sample. However, they also noted Mediterranean swordfishes Communicated by T. Ikeda, Hakodate with bite marks of a dwarf shark Isistius brasiliensis,a species not found in the Mediterranean, suggesting that S. Chow (&) · H. Okamoto · Y. Uozumi · Y. Takeuchi National Research Institute of Far Seas Fisheries, the Mediterranean swordfishes may travel to the sub- Shimizu, Shizuoka 424, Japan tropical and tropical Atlantic and return to the Medi- H. Takeyama terranean Sea. Alvarado Bremer et al. (1995), using Tokyo University of Agriculture and Technology, Koganei, nucleotide sequencing analysis of a short DNA fragment Tokyo 184, Japan of the swordfish mitochondrial control region, found no 360 evidence of phylogeographic structuring within the Miyake and Rey 1989). However, the extent of popu- Atlantic nor even between the Atlantic and Pacific. lation mixing and movements of fishes are still un- Later, however, with much larger sample sizes, Alvarado known. On the other hand, the mtDNA analyses of the Bremer et al. (1996) reported significant heterogeneity in Pacific Ocean were performed among swordfish samples haplotype distributions among samples from the Medi- collected mostly in the North Pacific Ocean (Grijalva- terranean, North and South Atlantic and Pacific. Rosel Chon et al. 1994; Rosel and Block 1995; Chow 1996), and Block (1995) also sequenced the swordfish mi- and none showed evidence of population structuring. tochondrial control region and reported heterogeneity Hence, collection and comparison of samples collected among the Mediterranean, Atlantic and Pacific samples, over a wider spatial range throughout the entire Pacific but they did not consider the North and South Atlantic is necessary. Although highly significant differences have to be separable stocks. Despite less biological informa- been reported among the Atlantic, Mediterranean and tion for the Pacific swordfish, several hypotheses re- Pacific swordfish samples (Rosel and Block 1995; Al- garding from one to four stocks have been proposed varado Bremer et al. 1996; Chow 1996), genetic re- based on the distributions of swordfish larvae and lationships among the ‘‘stocks’’ of these ocean basins are spawners, and longline catch rates (Nishikawa et al. poorly understood and no swordfish sample from the 1985; Bartoo and Coan 1989; Sakagawa 1989; Skillman Indian Ocean has been investigated so far. 1989; Sosa-Nishizaki and Shimizu 1991). However, We have collected swordfish samples from the Med- mtDNA analyses supplied no evidence of genetic dif- iterranean Sea, North and South Atlantic, Indian, and ferentiation between samples collected from the western, North and South Pacific Oceans for mtDNA analysis. central and eastern North Pacific, and suggested that Here, we present the results of our analysis on genetic there may be sufficient gene flow across the North Pacific variation within and among these samples and discuss to prevent genetic differentiation (Grijalva-Chon et al. the global population structure, gene flow and move- 1994; Rosel and Block 1995; Chow 1996). ment of individuals. For the Atlantic and Mediterranean swordfishes, the molecular data provided by Alvarado Bremer et al. (1996) seems to support the three separate management Materials and methods units (the Mediterranean Sea, North and South Atlantic Ocean) proposed by the International Commission for Collection information on the 13 swordfish samples used in this the Conservation of Atlantic Tunas (ICCAT) (see study are presented in Table 1. Muscle tissues of swordfish collected Table 1 Xiphias gladius. Descriptions for the swordfish samples Tuna Commission, USA; IP–SP Instituto de Pesca Sao Paulo, used in this study. Sri Lanka sample was caught by artisanal fishery Brazil; IPTP Indo Pacific Tuna Development and Management around the Islands; Medit. sample was an adult or subadult caught Programme, Sri Lanka; NIWA National Institute of Water & At- by harpoon fishery around the Sisily Island (AQUASTUDIO Italy; mospheric Research Ltd. New Zealand; NMFS National Marine CICESE Centro de Investigacion Cientifica y de Educacion Su- Fisheries Service, USA; NRIFSF National Research Institute of perior de Ensenada, Mexico; BRS Bureau of Resources Sciences, Far Seas Fisheries, Japan; USC University of South Carolina, Australia; CSIRO Commonwealth Scientific and Industrial Re- USA; n/a not available) search Organization, Australia; IATTC Inter-American Tropical Area, Latitude Longitude Date Collaborating Size range Sample sample code organization of fish size Pacific Ocean Japan 24–35°N 144–154°E November 1991–February 1992 NRIFSF 13–90 kga 45 Hawaii 0–12°N 165°W October 1994 NMFS 62–175 cmb 51 Mexico 24–27°N 113–115°W January–March 1992 CICESE 89–231 cmb 35 Ecuador 1°N79°W October 1994 IATTC 90–173 cmb 21 Peru 8–18°S 84–124°W June–July 1994 NRIFSF 61–186 cmb 53 SWPO 30–38°S 154–179°E June 1994, July–September 1995 NRIFSF, NIWA 62–285 cmb 31 Indian Ocean SriLanka n/a n/a March–April 1992 IPTP 57–144 cmb 28 SJava 16–17°S 118–119°E February 1995 BRS, CSIRO 57–214 cmb 35 South Africa Cape 38°S25°E June 1992 NRIFSF 120–178 cmb 11 Atlantic Ocean NWA90 38–40°N 59–72°W June–October 1990 USC 48–175 cmc 27 NWA93 20–30°N 57–90°W January–April 1993 USC 120–227 cmc 29 Brazil 20–30°S 35–50°W October 1994–January 1995 IP-SP 83–249 cmb 63 Mediterranean Sea Medit. n/a n/a 1994 AQUASTUDIO n/a 34 aDressed weight bEye to fork length cLower jaw to fork length 361 by foreign organizations were preserved in ethanol prior to mailing analysis was conducted using the Monte Carlo simulation of Roff to the laboratory in Japan. Fresh or frozen tissue samples were and Bentzen (1989) with 1000 randomizations of the data to test collected by the Japanese longliners and transferred to the lab- heterogeneity of the frequency distributions of the genotypes be- oratory. Procedures for total DNA extraction from fresh, frozen or tween and among samples. ethanol-preserved muscle tissues and PCR amplification followed by RFLP analysis are described elsewhere (Chow et al. 1993; Chow and Inoue 1993; Chow and Ushiama 1995). Primer sequences for amplifying the mtDNA segment containing the flanking tRNAs, Results parts of the cytochrome b and 12S rRNA genes and the control region are from Palumbi et al. (1991), and the nucleotide sequences are as follows: CB3R-L, 5′-CATATTAAACCCGAATG A single fragment of approximately 1900 base pairs ATATTT-3′ and 12SAR-H, 5′-ATAGTGGGGTATCTAATCC- was amplified in all individuals and no apparent size ′ CAGTT-3 . Without further purification the amplified fragments difference among individuals was observed. Restriction were digested using four-base cutters, electrophoresed on a 2% agarose gel, and stained with ethidium bromide for photographing.
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