Corresponding author: Valerio Ketmaier (
Academic editor: Carsten Lüter
The Eastern Mediterranean land snails
In a study that appeared in the journal “Nature” on the 6th of April 1882, just a few days before his death, Charles Darwin returned to his lifelong fascination with mechanisms of passive long-distance dispersal in mollusks (
In the Eastern Mediterranean area,
Based on the above geographic occurrence of shell forms and on field observations, two alternative scenarios have been hypothesized to explain such a peculiar insular distribution (
Here we tested these two alternative scenarios by using sequences of two mitochondrial DNA (mtDNA) genes and the
The study is based on material collected by MG in April 1989 and May 1990 (
Taxa included in the study and their geographic origin. For each individual we detail the presence (O)/absence (C) of the umbilicus in the shell, the voucher number in the collections of the Zoological Museum Hamburg (ZMH) and the Museum für Naturkunde Berlin (ZMB) and the composite COI/16S haplotype identifier number.
Taxon | Umbilicus (O/C) | Location | Specimen voucher | mtDNA Haplotype |
---|---|---|---|---|
|
C | Greece, Karpathos, Mertonas, E Arhangells | ZMH.1555b | 1 |
|
C | Greece, Karpathos, Mertonas, E Arhangells | ZMH.1555c | 2 |
|
C | Greece, Karpathos, Mertonas, E Arhangells | ZMH.1555d | 2 |
|
C | Greece, Karpathos, Mertonas, E Arhangells | ZMH.1555e | 3 |
|
C | Greece, Karpathos, Mertonas, E Arhangells | ZMH.1555f | 4 |
|
C | Greece, Karpathos, Mertonas, E Arhangells | ZMH.1555g | 5 |
|
C | Greece, Karpathos, Mertonas, E Arhangells | ZMH.1555i/ j | 3 |
|
C | Greece, Rhodes, Moni Amos, Kap Ladiko | ZMH.1557a | 6 |
|
C | Greece, Rhodes, Moni Amos, Kap Ladiko | ZMH.1557b | 7 |
|
C | Greece, Rhodes, Moni Amos, Kap Ladiko | ZMH.1557d | 8 |
|
C | Greece, Rhodes, Charaki, Feraklos | ZMH.1557e | 9 |
|
C | Greece, Rhodes, Kamiros Castle | ZMH.1557f | 2 |
|
C | Greece, Rhodes, Kamiros Castle | ZMH.1557h | 3 |
|
C | Greece, Rhodes, Kamiros Castle | ZMH.1557i | 6 |
|
C | Greece, Rhodes, Profitis Ilias (900m) | ZMH.1557j | 1 |
|
C | Greece, Rhodes, Profitis Ilias (900m) | ZMH.1557k | 6 |
|
C | Greece, Rhodes, Monolithos Castle | ZMH.1557n | 10 |
|
C | Greece, Rhodes, Monolithos Castle | ZMH.1557o | 11 |
|
C | Greece, Symi, northern slope Vigala | ZMH.1558a | 5 |
|
C | Greece, Symi, NW Hariani harbor, Th. Sikidi | ZMH.1558c | 12 |
|
C | Greece, Symi, NW Hariani harbor, Th. Sikidi | ZMH.1558d | 13 |
|
C | Greece, Symi, NW Hariani harbor, Th. Sikidi | ZMH.1558e | 14 |
|
C | Greece, Symi, NW Hariani harbor, Th. Sikidi | ZMH.1558f | 13 |
|
C | Greece, Symi, NW Hariani harbor, Th. Sikidi | ZMH.1558g | 14 |
|
C | Greece, Symi, Panormitis, N monastery | ZMH.1561a | 24 |
|
C | Greece, Nimos | ZMH.1556a | 15 |
|
C | Turkey, Karaova, near Bodrum | ZMH. 1565 | 16 |
|
O | Greece, Karpathos, Larniotisa, near Kap Volakas | ZMH.1559a | 17 |
|
O | Greece, Karpathos, Pigadia, Patella mountain | ZMH.1559d | 17 |
|
O | Greece, Karpathos, Pigadia, Patella mountain | ZMH.1559e | 17 |
|
O | Greece, Karpathos, Pigadia, Patella mountain | ZMH.1559f | 18 |
|
O | Greece, Karpathos, Profitis Ilias, SE Aperi | ZMH.1559g | 19 |
|
O | Greece, Karpathos, E Mentes | ZMH.1559i | 20 |
|
O | Greece, Karpathos, E Mentes | ZMH.1559j | 20 |
|
O | Greece, Rhodes, Rampart d´Ambosie gate | ZMH.1560a | 21 |
|
O | Greece, Rhodes, Rampart d´Ambosie gate | ZMH.1560b | 21 |
|
O | Greece, Rhodes, Rampart d´Ambosie gate | ZMH.1560c | 21 |
|
O | Greece, Rhodes, Rampart d´Ambosie gate | ZMH.1560d | 22 |
|
O | Greece, Rhodes, Filerimos | ZMH.1560e | 23 |
|
O | Greece, SW Symi, Xisos | ZMH.1561b | 25 |
|
O | Greece, SW Symi, Xisos | ZMH.1561c | 23 |
|
O | Greece, SW Symi, Xisos | ZMH.1561d | 23 |
|
O | Greece, Symi, Skoumisa Bay, Kefala | ZMH.1561e | 23 |
|
O | Greece, Rhodes, Rampart d´Ambosie gate | ZMB 127533 | 27 |
|
O | Turkey, Datça | ZMH.1564 | 30 |
|
O | Jerusalem | ZMB.74072 | 27 |
|
O | Jerusalem | ZMB.9126 | 27 |
|
O | Jerusalem, Givat Ram Campus, Hebrew Univ. | ZMH.1562 | 27 |
|
O | Jerusalem, Givat Ram Campus, Hebrew Univ. | ZMH.1563a | 27 |
|
O | Jerusalem, Givat Ram Campus, Hebrew Univ. | ZMH.1563b | 29 |
|
C | Arbell Cliff, Lake Tiberias | ZMH.1568 | 27 |
|
C | Arbell Cliff, Lake Tiberias | ZMH.1569d | 31 |
|
O | Arbell Cliff, Lake Tiberias | ZMH.1569e | 27 |
|
C | Arbell Cliff, Lake Tiberias | ZMH.1569g | 32 |
|
C | Arbell Cliff, Lake Tiberias | ZMH.1569h/i | 33 |
|
- | Greece, Peloponnese, Marathopolis village, Messina | ZMB 107155 | N/A |
|
- | - |
|
N/A |
|
- | - |
|
N/A |
|
- | - |
|
N/A |
|
- | - |
|
N/A |
|
C | Turkey, Harput near Elazig | ZMB 127531 | 26 |
|
C | Turkey, Anatolia, 3 km SE Mardin | ZMB 127532 | 28 |
|
- | Lybia,Tripoli, Djebel Garim | ZMB 86612-1 | N/A |
|
- | Lybia,Tripoli, | ZMB 86612-2 | N/A |
|
- | - |
|
N/A |
Sequences were edited and aligned in SEQUENCHER 4.1 (Gene Code Corporation, Ann Arbor, MI, USA); the alignment was further checked by eye. We included a selection of
The robustness of the ML hypothesis was tested by 1,000 bootstrap replicates; MrBAYES was run two times independently for 2,000,000 generations with a sampling frequency of 100 generations. We ran one cold and three heated Markov chains and two independent runs. To establish if the Markov chains had reached stationarity, we plotted the likelihood scores of the sampled trees against generation time. Trees generated before stationarity were discarded as burn-in (first 10% of the sampled trees) and posterior probability values for each node were calculated on the basis of the remaining 90% of sampled trees. We applied coalescence as implemented in the BEAST 1.7.2 package (
The final alignment including all samples amplified by nested PCR was 482 base pair (bp) long, with 281 bp for COI and 201 for 16S and defined a total of 33 unique haplotypes (GenBank accession numbers
Evolutionary relationships in
Historical biogeography in
We could not retrieve two reciprocally monophyletic clades for
The biogeographic reconstruction presented in Fig.
Even though the hypothesis of the non-umbilicate clade being of insular origin is appealing from an evolutionary perspective, we should not overlook the fact that this result could be an artifact due our limited sampling. In particular, we cannot completely rule out the hypothesis that the non-umbilicate clade originated in the Levant and subsequently reached the Dodecanese. We indeed identified a non-umbilicate clade grouping haplotypes from both the Levant and the Dodecanese (haplotypes 12, 16, 31, and 33). The non-umbilicate samples from the Levant are genetically close to a few samples from Symi. The other non-umbilicate individuals from that island are spread in the upper part of the tree of Fig.
Rhodes, the largest island of the Dodecanese and the closest to the mainland, is identified as the first colonized by the two
We are aware that the scenario presented in here – although fascinating – is not the only possible one. Due to the sub-optimal quality of most of the samples at our disposal, we were able to sequence short gene fragments. This implies that we could have easily missed out on rare genetic variants. In addition,
The data presented in here, along with the similar evidence existing for the area mentioned in the previous paragraph, suggest that two different layers of complexity (natural colonization vs. historical human activities) should be considered when addressing puzzling distributions in an area interested by intense human activities since historical times. Also, this study represents a starting point for further investigations based on a more extensive sampling in terms of geographic and taxon coverage as well as molecular markers.
We wish to thank Binia De Cahsan for producing the shell drawings in Figs