Vol 439|26 January 2006 BRIEF COMMUNICATIONS

Molecular trails from hitch-hiking snails Migrating birds may have transported the Balealand snail across vast distances to remote islands.

Darwin was fascinated by the transportation of to Balea, a genus of Clausiliidae thought to be land snails across great swathes of open ocean restricted to the Palaearctic region, which by birds — he even immersed snails in sea includes northern Africa and Eurasia to the water to see how long they would survive1. north of the Himalayas5. The Tristan archi- Here we follow a molecular phylogenetic trail pelago consists of three main islands situated that reveals the incredible transequatorial dis- midway between South Africa and South persal of the land snail Baleafrom Europe to America at about 37 S, with lying the and the islands, about 350 km to the south-southeast (Fig. 2a). and back again. This long-distance dispersal is It lies 9,000 km and 8,500 km from the Azores unexpected for what are proverbially consid- and continental Europe, respectively. ered the most pedestrian of creatures. On the basis of their extreme biogeographi- An allegorical picture2from the sixteenth cal disjunction, these Tristan land-snail century shows a bird carrying a snail (Fig. 1), species were subsequently transferred to a new but it was not until 1921 that the possibility of genus, Tristania6. Additional species of Trista- Figure 1 | Etching from Marcus Gheeraerts’ fable land-snail dispersal by birds was discussed for niawere later described from other islands in ‘Pride comes before a fall’2.An eagle is depicted Balea3. It was suggested that the exceptionally the Tristan/Gough group7,8. To reach Tristan here, but is unlikely to be the bird that transported tenacious slime and arboreal habit of Balea from either Europe or the Azores, where two Balea(see supplementary information). Waders or perversa,an ovoviviparous hermaphrodite, Baleaspecies occur9, a hostile gap of nearly other migratory birds, which are regular vagrants on mid-Atlantic islands, are more likely vectors. could aid passive dispersal by birds3. As land 9,000 km has to be bridged, which hardly snails occur on even the most remote islands, seems possible for a vulnerable pulmonate. Europe, where it exists as a distinct species this must be a frequent event, despite the lim- Despite renewed claims for the generic dis- only recently distinguished from B. perversa13 ited number of well documented cases4. tinctness of Tristania, including the erection (the European B. perversareached Iceland rel- In 1824, John Gray assigned two new species of the subfamily Tristaniinae10, anatomical atively late and remains indistinguishable from of land snail from the Tristan da Cunha islands evidence indicates that Tristaniaand Balea conspecific European populations). belong to the same genus8. We have analysed Edmund Gittenberger*†, Dick S. J. Groenenberg*, a Iceland mitochondrial DNA sequence data for sub- Bas Kokshoorn†, Richard C. Preece‡ unit I of cytochrome oxidase for different *National Museum of Natural History Naturalis, Balea species and find that they confirm this PO Box 9517, and †Institute of Biology, Leiden Azores view: our neighbour-joining phylogenetic tree University, PO Box 9516, 2300 RA Leiden, (Fig. 2b, and see supplementary information) The Netherlands indicates that Azorean and Tristan groups of ‡Department of Zoology, University of Cambridge, Baleaarose from a single ancestral species. Downing Street, Cambridge CB2 3EJ, UK Tristan da Cunha As the Baleinae originally radiated in the e-mail: [email protected] Gough Island western Palaearctic region11,12, the most parsi- b monious scenario is that first the ancestral 1. Darwin, C. On the Origin of Species(Murray, London, 1859). Balea biplicata Netherlands species reached the Azores, then, after addi- 2. Gheeraerts, M. De Warachtighe Fabulen der Dieren(Pieter 99 Balea perversa Italy de Clerck, Brugge, 1567). 97 Balea perversa Slovakia tional long-distance dispersal, radiations 3. Cockerell, T. D. A. Nature108,496–497 (1921). 4. Rees, W. J. Proc. Malac. Soc. Lond.36,269–282 (1965). 72 Balea perversa UK resulted in two species in the Azores and at 5. Gray, J. E. Zool. J.1,61–62 (1824). 100 least eight in the Tristan/Gough archipelago. Balea perversa Iceland 6. Boettger, O. Ber. Thät. Offenb. Ver. Naturk.17/18,18–104 99 Balea perversa Spain One of the Azorean species, B. heydeni, reached (1878). Balea perversa Netherlands Madeira and then ‘returned’ to western 7. Odhner, N. H. Proc. Malac. Soc. Lond.34,168–173 (1960). Balea nitida Azores 8. Preece, R. C. & Gittenberger, E. J. Moll. Stud.69,329–348 Figure 2 |Distribution of Baleaspecies. a, Areas (2003). Balea heydeni Denmark where the snails are found.b, Neighbour-joining 9. Backhuys, W. Land and Freshwater Molluscs of the Azores Balea heydeni Netherlands tree for DNA sequences of cytochrome oxidase (Backhuys & Meesters, Amsterdam, 1975). Balea heydeni Ireland 10. Schileyko, A. A. Ruthenica2(suppl.), 437–564 (1999). 96 subunit I in selected species, with bootstrap 100 Balea heydeni UK 11. Nordsieck, H. Arch. Molluskenk.109,67–89 (1978). support values (1,000 replicates). A smaller 12. Nordsieck, H. Arch. Molluskenk.109,249–275 (1979). Balea heydeni UK International Transcribed Spacer 1 data set 13. Gittenberger, E., Preece, R. C. & Ripken, T. E. J. J. Conch. 80 Balea heydeni Portugal corroborates these results (see supplementary (submitted). Balea heydeni Madeira information). Lineages from mid-Atlantic islands Balea heydeni Azores are in red. The extent of sequence divergence Supplementary informationaccompanies this communication on Nature’s website. Balea swalesi Tristan between B. perversaand its sister clade, together 52 Received 2 August; accepted 22 December 2005. Balea ventricosa Tristan with the occurrence of at least eight Baleaspecies Competing financial interests:declared none. Balea costellata Tristan on Tristan/Gough8, rule out human introduction doi:10.1038/439409a 68 60 Balea tristensis Gough of the snails. The sequences of populations of Balea tristensis Gough B. heydenifrom mainland Europe are extremely BRIEF COMMUNICATIONS ARISINGonline similar, suggesting a recent return to the continent. ➧www.nature.com/bca see Naturecontents.

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