Genetic Discontinuity of Big Fish in a Small
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COMMENTARY Genetic discontinuity of big fish in a small sea Carol A. Reeb1 Hopkins Marine Station, Stanford University, Pacific Grove, CA 93950 here was a time not so long ago mictic model, one might assume that the straits of Sicily and Messina (7) as when geneticists might have depletion of one local population would shown in Fig. 1B. T branded the highly migratory be offset by the regular immigration or Bluefin are known to spawn in the Atlantic bluefin tuna (Thunnus ongoing larval recruitment from another, Balearic and Tyrrhenian seas on the thynnus) the quintessential panmictic both of which are enhanced by high fe- Mediterranean’s western side and in the population (1) of the marine world. Be- cundity. This has not always been the case Ionian and possibly Levantine seas to cause bluefin tuna are designed for mobi- and indicates that population structure the east (4, 5). Spawning in the Adriatic lity and capable of generating millions of could exist. However, analyses of neutrally is unknown. Plotted onto Fig. 1B are offspring per spawning pair (2), migration evolving markers (mitochondrial DNA or migration tracks from two Atlantic blue- and gene flow throughout their entire microsatellites) have often failed to reject fin (8, 9) tagged off North Carolina range seemed likely. This would homoge- the null hypothesis, leaving behind con- (roughly 7400 km away). After crossing nize regional subgroups and cause them to clusions that marine fish had little pop- the Atlantic Ocean, the bluefin pass behave, in a statistical sense, like one very ulation structure to manage (12) or that through the Straits of Gibraltar large, randomly mating population. In genetic techniques failed to resolve the where their tracks show remarkable other words, bluefin appeared to fit the structure that was there (13). salmon-like homing behavior to null hypothesis that population geneticists eastern and western Mediterranean make a living trying to reject. Hence, ge- Riccioni et al. note spawning grounds located less than netic discontinuities should have been 500 km apart. hard to find, especially within a small in- little loss Fig. 1B illustrates the challenge in land sea. In a study in PNAS, Riccioni accurately assessing stock sizes of et al. (3) examine microsatellite loci from of gene diversity distinct bluefin populations. Eastern contemporary and historical samples of Mediterranean fish must cross western T. thynnus and find remarkable evidence in the Mediterranean. Mediterranean waters to reach their (i) that the Mediterranean contains ge- spawning grounds; if caught en route, netically subdivided populations, (ii) that they will be counted as part of the this structure has persisted for nearly 100 To complicate matters more, evidence wrong population for stock assessments. years, and (iii) that gene diversity has re- of genetic differentiation was often suspect The same issue confronts the western mained surprisingly intact despite decades and considered an artifact of high Atlantic (Gulf of Mexico-spawning) of overexploitation and dramatic decline fecundity. Great reproductive success of stock. A proportion of T. thynnus in numbers. These results confirm pre- only a few individuals could cause genetic tagged off the coast of North Carolina ’ fl vious work (4, 5) hinting that T. thynnus in variance (FST s) to uctuate widely each belongs to the Mediterranean-spawning the Mediterranean is composed of multi- generation (commonly called “genetic stock, and their presence in the western ple breeding stocks and raises concern that sweepstakes”) (14) such that differences Atlantic catch can artificially inflate these newly recognized gene pools are at one year should not be expected the next. biomass estimates (16). One way to risk from overfishing. In the study in PNAS (3), the authors in- overcome this challenge is through the Atlantic bluefin tuna are migratory clude historical samples from juveniles and use of microsatellite markers. Multilocus giants. Weighing upwards of 600 kg, they adults—insightfully preserved by Masimo genetic profiles characterizing each traverse the North Atlantic and adjacent Sella in the early part of the last century— bluefin stock could make it possible to seas between feeding and spawning to confirm that the differences that they assign individuals to their population of grounds over a 30-year life span (6). Despite find in Atlantic bluefin tuna inhabiting the origin. Such work could enable better great historical abundance, spawning bio- Mediterranean Sea are temporally stable, accounting of migrating individuals cap- mass (Fig. 1A) has plummeted over the last and not a variable artifact. tured in regions of population overlap as four decades (2). The International Con- Riccioni et al. (3) show that spatial it has with salmonids (17). vention for the Conservation of Atlantic differences between Atlantic bluefin Finally, despite of lower biomass, Tunas, which coordinates management and sampled in the Adriatic and Tyrrhenian Riccioni et al. (3) note little loss of research of highly migratory tunas, recog- seas have persisted for nearly a century. gene diversity in the Mediterranean. nizes two populations (Western and East- Genetic differences between these two However, even in fish populations that ern Atlantic stocks) that spawn in the Gulf regions have been reported in other have undergone more extensive declines of Mexico and the Mediterranean Sea and species (15), including red mullet than those documented here (e.g., manages them along a line bisecting the (Mullus barbatus,), anchovies (Engraulis Newfoundland cod, 75–99%), it is not mid-Atlantic at the 45th meridian (6). Re- encrasicolus), and striped sea bream always possible to observe bottlenecks cently, the nation of Monaco requested that (Lithognathus mormyrus). Given the in genetic data (18). T. thynnus be listed under appendix I of the Atlantic bluefin’s reputation for wander- Atlantic bluefintunahavelongbeena Convention on International Trade of En- lust, it is odd that it would join a list of challenge for population geneticists. At first dangered Species, citing the alarming drop lesser vagile species with a similar geno- in the Mediterranean stock by 60% in the geographic pattern. However, the past 10 years (10). eastern and western basins of the Author contributions: C.R. wrote the paper. Marine fish species had once been con- Mediterranean differ in temperature, The author declares no conflict of interest. sidered resilient to overexploitation, yet salinity, and circulation. Oceano- See companion article on page 2102 in issue 5 of volume today marine fishery stocks worldwide are graphically speaking, these basins are 107. in precipitous decline (11). Under a pan- considered partially isolated along the 1E-mail: [email protected]. www.pnas.org/cgi/doi/10.1073/pnas.0914639107 PNAS | February 9, 2010 | vol. 107 | no. 6 | 2377–2378 Downloaded by guest on October 2, 2021 Fig. 1.(A) Decline over time of Atlantic bluefin tuna biomass in the Mediterranean- and Gulf of Mexico-spawning stocks (2). MT, metric tons. (B) Map of the Mediterranean Sea divided into eastern (yellow) and western (orange) basins with relevant subseas labeled (7). Blue (8) and red (9) lines are tracks of T. thynnus migrating into the Mediterranean Sea carrying electronic tags deployed off North Carolina. glance, they appear to be unproductive tags, otolith microchemistry) combined their whole range...” But he added, research choices. But a closer looks reveals with genetics will soon rewrite the dogma “This is probably unusual.” fi a ne-scale structure. Although develop- surrounding highly migratory marine fish ment of faster-evolving markers such as and pave the way for geneticists to finally ACKNOWLEDGMENTS. Electronic tag data for microsatellites has undoubtedly helped to Fig. 1B were kindly provided by B. Block and make significant contributions to the resolve population structure in highly plotted by M. Castleton. Genetic research of migratory fishes, better experimental management and conservation of these migratory marine fishery species is funded by the fi design and elimination of mixed samples sheries. Decades ago, Sewall Wright (19) Lenfest Foundation, Monterey Bay Aquarium, have played a more important role. Addi- wrote, “There are species which appear to and National Oceanic and Atmospheric tional technologies (forensics, electronic breed so nearly at random throughout Administration. 1. Wright S (1940) Breeding structure of populations in Ocean Sciences, eds Steele JH, Turekian KK, Thorpe SA 15. Maggio T, Brutto SL, Garoia F, Tinti F, Arculeo M (2009) relation to speciation. Am Nat 74:232–248. (Academic Press, London), pp 1689–1706. Microsatellite analysis of red mullet Mullus barbatus 2. International Commission for the Conservation of 8. Block BA, et al. (2005) Electronic tagging and popula- (Perciformes, Mullidae) reveals the isolation of the fi fi Atlantic Tunas. Report of the 2008 Atlantic Blue n tion structure of Atlantic blue n tuna. Nature 434: Adriatic Basin in the Mediterranean Sea. ICES J Mar 1121–1127. Stock Assessment Session (SCRS/2008/019). (Interna- Sci 66:1883–1891. 9. Walli A, et al. (2009) Seasonal movements, aggrega- tional Commission for the Conservation of Atlantic 16. Kurota H, et al. (2009) A sequential Bayesian method- tions and diving behavior of Atlantic bluefin tuna Tunas, Madrid). ology to estimate movement and exploitation rates 3. Riccioni G, et al. (2010) Spatio-temporal population (Thunnus thynnus) revealed with archival tags. PLoS One 4:e6151. using electronic and conventional tag data: Applica- structuring and genetic diversity retention in depleted fi 10. Silfvergrip, A. (2009) Supplementary information to tion to Atlantic blue n tuna (Thunnus thynnus). Can Atlantic bluefin tuna of the Mediterranean. Proc Natl the draft proposal to CoP15 to include bluefin tuna J Fish Aquat Sci 66:321–342. Acad Sci USA 107:2102–2107. Thunnus thynnus on Appendix I of CITES as proposed 17. Tonteri A, Veselov AJ, Zubchenko AV, Lumme J, 4. Carlsson J, et al. (2004) Microsatellite and mitochon- at Monaco 18 September 2009. Primmer CR (2009) Microsatellites reveal clear genetic drial DNA analyses of Atlantic bluefin tuna (Thunnus 11.