Research Group 2: Evolutionary Genetics

When the American sea sturgeon swam east

Ludwig A, Debus L, Lieckfeldt D, Wirgin I, Benecke N, Jenneckens I, Williot P, Waldman JR, Pitra C (2002): NATURE 419, 447-448.

North- and Baltic Sea sturgeon populations became extinct during the last century mainly caused by overfishing and river damming in North and Baltic Sea (poster). However, their large public interest resulting from their long life cycles and their well known product - black caviar - renders these fishes an international flagship species for nature conservation. Therefore, several international projects were launched to restore sturgeon in Baltic waters. These efforts were complicated by the fact that only very limited information is available about the historic populations. Trans-Atlantic colonization and founding of a self-sustaining population in Baltic waters by North American sea sturgeon during the Middle Ages was demonstrated in this study for the first time. The historic presence allows the re-introduction of A. oxyrinchus in Baltic waters.

The two species of Atlantic sea sturgeon on either shore of the North Atlantic, Acipenser sturio in Europe and A. oxyrinchus in North America, probably diverged with closure of the Tethys Sea and onset of the North Atlantic Gyre 15-20 million years ago, and contact between them was then presumably precluded by geographic distance. Here we present genetic, morphological, and archaeological evidence indicating that the North American sturgeon colonized the Baltic during the Middle Ages and replaced the native sturgeon there, before recently becoming extinct itself in Europe as a result of human activities. In addition to representing a unique transatlantic colonization event by a fish that swims upriver to spawn, our findings have important implications for projects aimed at restocking Baltic waters with the European sturgeon.

A. sturio, once occurred abundantly in rivers in regions from the Black Sea right up to the Baltic, but is now reduced to a relict population in southern France. A. oxyrinchus, however, is still found in rivers that run into the Atlantic from the Gulf of Mexico to Quebec. We studied centuries-old museum specimens (n=53) and contemporary specimens of A. sturio (n=67) and A. oxyrinchus (n=351) from almost all known populations. To investigate their molecular genetics, we compared the same two DNA fragments, one of about 200 base pairs from the mitochondrial D-loop and the other from about 230 base pairs fragment of nuclear DNA flanking microsatellite Aox-23.  Two A. sturio and 39 A. oxyrinchus mitochondrial DNA-haplotypes were found that had 22 fixed differences between species. Fourteen archived specimens from the European Atlantic and the North, Adriatic, and Mediterranean seas showed the expected A. sturio-haplotypes. But surprisingly, ten archived specimens from the Baltic and one from the Oste River (North Sea) carried the A. oxyrinchus-haplotype-A.

In the nuclear DNA, three consistent differences distinguished each species. Archived specimens with haplotype A carried A. oxyrinchus genotypes, whereas all other archived specimens had A. sturio genotypes. Nuclear sequences revealed no evidence of hybridisation. Estimations based on a molecular clock indicate that the Baltic A. oxyrinchus originated from a single founding matrilineage (haplotype A) during the past 1,910 years (50% confidence interval).

Examination of morphological differences associated with the two species revealed that archived Baltic sturgeon had a closer affinity with A. oxyrinchus than with A. sturio (table). In addition, achieved Baltic specimens showed alveolar sculpting on their scutes - as seen in A. oxyrinchus - and not the tubercular-radial sculpting displayed by A. sturio.

Re-examination of 972 scutes from nine archaeological sites indicated that A. sturio colonized Baltic waters some time after the Pleistocene (about 3,000 years ago), followed by A. oxyrinchus about 1,800 years later. Both species were found in deposits in Ralswiek, Island of Rugia, suggesting that there had been a remarkable species shift from A. sturio to A. oxyrinchus between 1,200 and 800 years ago in the Baltic.  The subsequent decline of A. sturio and the establishment of a sustained A. oxyrinchus population in European waters during the Little Ice Age might have been due to selection for the hypothermal conditions that characterize their likely Canadian sources: A. oxyrinchus spawns between 13.3°C and 17.8°C in the Delaware River, whereas A. sturio did not spawn below 20°C in the Oste River (Elbe system) or in the Gironde River, France.

Our findings have conservation implications for restocking the Baltic Sea with sturgeon (HELCOM-Decision 18/97), an endeavour that has so far stagnated owing to the very limited availability of A. sturio. Attempts to reintroduce the North American A. oxyrinchus could also be hindered because this cold-water-tolerant species might no longer flourish in today's warmer Baltic waters, which would better suit the thermal tolerance of the European sturgeon.

Acknowledgements

We thank the many people who provided samples, and for helpful comments V. J. Birstein, J. Fickel, J. Gessner, F. Kirschbaum, A. Ludwig and T. Mehner, for drawing the maps H. Behrendt, for translation of Russian articles K. Zeller as well as for technical assistance A. Schmidt, J. Spamer and S. Rautenberg. This study was supported by grants from the Deutsche Forschungsgemeinschaft, the Bundesamt für Naturschutz and the New York Sea Grant and the U.S. National Institute of Environmental Health Sciences Center Grant ES00260. Arne Ludwig started these analyses on the Institute of Freshwater Ecology and Inland Fisheries in 1997 and finished it on the IZW in 2002.