Proceedings of the Royal Society B: Biological Sciences

    The insular dwarfism seen in Pleistocene elephants has come to epitomize the island rule; yet our understanding of this phenomenon is hampered by poor taxonomy. For Mediterranean dwarf elephants, where the most extreme cases of insular dwarfism are observed, a key systematic question remains unresolved: are all taxa phyletic dwarfs of a single mainland species Palaeoloxodon antiquus (straight-tusked elephant), or are some referable to Mammuthus (mammoths)? Ancient DNA and geochronological evidence have been used to support a Mammuthus origin for the Cretan ‘Palaeoloxodon’ creticus, but these studies have been shown to be flawed. On the basis of existing collections and recent field discoveries, we present new, morphological evidence for the taxonomic status of ‘P’. creticus, and show that it is indeed a mammoth, most probably derived from Early Pleistocene Mammuthus meridionalis or possibly Late Pliocene Mammuthus rumanus. We also show that Mammuthus creticus is smaller than other known insular dwarf mammoths, and is similar in size to the smallest dwarf Palaeoloxodon species from Sicily and Malta, making it the smallest mammoth species known to have existed. These findings indicate that extreme insular dwarfism has evolved to a similar degree independently in two elephant lineages.

    References

    • 1
      Van Valen L. M.. 1973Pattern and the balance of nature. Evol. Theory 1, 31–49. Google Scholar
    • 2
      Palombo M. R.. 2001Endemic elephants of the Mediterranean Islands: knowledge, problems and perspectives. 1st Int. Congress of the World of Elephants (eds , Cavarretta G., Gioia P., Mussi M.& Palombo M. R.), pp. 486–491. Rome, Italy: Consiglio Nazionale delle Ricerche. Google Scholar
    • 3
      Poulakakis N., Parmakelis A., Lymberakis P., Mylonas M., Zouros E., Reese D. S., Glaberman S.& Caccone A.. 2006Ancient DNA forces reconsideration of evolutionary history of Mediterranean pygmy elephantids. Biol. Lett. 2, 451–454.doi:10.1098/rsbl.2006.0467 (doi:10.1098/rsbl.2006.0467). LinkGoogle Scholar
    • 4
      Bate D. M. A.. 1907On elephant remains from Crete, with description of Elephas creticus, sp. n.Proc. Zool. Soc. Lond. 1907, 238–250. Google Scholar
    • 5
      Binladen J., Gilbert M. T. P.& Willerslev E.. 2007800 000 year old mammoth DNA, modern elephant DNA or PCR artefact.? Biol. Lett. 3, 55–56.doi:10.1098/rsbl.2006.0537 (doi:10.1098/rsbl.2006.0537). LinkGoogle Scholar
    • 6
      Orlando L., Pagés M., Calvignac S., Hughes S.& Hänni C.. 2007Does the 43 bp sequence from an 800 000 year old Cretan dwarf elephantid really rewrite the textbook on mammoths.? Biol. Lett. 3, 57–59.doi:10.1098/rsbl.2006.0536 (doi:10.1098/rsbl.2006.0536). LinkGoogle Scholar
    • 7
      Poulakakis N., Parmakelis A., Lymberakis P., Mylonas M., Zouros E., Reese D. S., Glaberman S.& Caccone A.. 2007It remains a mammoth DNA fragment. A reply to Binladen et al. (2006) and Orlando et al. (2006). Biol. Lett. 3, 60–63.doi:10.1098/rsbl.2006.0555 (doi:10.1098/rsbl.2006.0555). LinkGoogle Scholar
    • 8
      Mol D., de Vos J., van den Bergh G. D.& Sondaar P. Y.. 1996The taxonomy and ancestry of the fossil elpehants of Crete: faunal turnover and a comparison with Proboscidean faunas of Indonesian islands. The Pleistocene and Holocene fauna of Crete and its first settlers (ed. & Reese D. S.), pp. 81–98. Philadelphia, PA: Prehistory Press. Google Scholar
    • 9
      Poulakakis N., Mylonas M., Lymberakis P.& Fassoulas C.. 2002Origin and taxonomy of the fossil elephants of the island of Crete (Greece): problems and perspectives. Palaeogeogr. Palaeoclimatol. Palaeoecol. 186, 163–183.doi:10.1016/S0031-0182(02)00451-0 (doi:10.1016/S0031-0182(02)00451-0). CrossrefGoogle Scholar
    • 10
      Reese D. S., Belluomini G.& Ikeya M.. 1996Absolute dates for the Pleistocene fauna of Crete. Pleistocene and Holocene fauna of Crete and its first settlers (ed. & Reese D. S.), pp. 47–52. Madison, WI: Prehistory Press. Google Scholar
    • 11
      Blackwell B., Rutter N. W.& Debénath A.. 1990Amino acid racemization in mammalian bones and teeth from La Chaise-de-Vouthon (Charente), France. Geoarchaeol. Int. J. 5, 121–147.doi:10.1002/gea.3340050203 (doi:10.1002/gea.3340050203). CrossrefGoogle Scholar
    • 12
      Lister A. M.. 2004Ecological interactions of elephantids in Pleistocene Eurasia: Palaeoloxodon and Mammuthus. Human palaeoecology in the levantine corridor (eds , Goren-Inbar N.& Spelth J. D.), pp. 53–60. Oxford, UK: Oxbow. Google Scholar
    • 13
      Lister A. M.. 1989Rapid dwarfing of Red Deer on Jersey in the last interglacial. Nature 342, 539–542.doi:10.1038/342539a0 (doi:10.1038/342539a0). Crossref, PubMedGoogle Scholar
    • 14
      Osborn H. F.. 1942The Proboscidea (Vol. II). New York, NY: The American Museum Press. Google Scholar
    • 15
      Maglio V. J.. 1973Origin and evolution of the Elephantidae. Trans. Am. Phil. Soc. 63, 1–149.doi:10.2307/1006229 (doi:10.2307/1006229). CrossrefGoogle Scholar
    • 16
      Albayrak E.& Lister A. M.In press. Dental remains of fossil elephants from Turkey. Quat. Int. (doi:10.1016/j.quaint.2011.05.042). Google Scholar
    • 17
      Lister A. M.& van Essen H.. 2003Mammuthus rumanus (Ştefănescu), the earliest mammoth in Europe. Advances in vertebrate paleontology ‘Hen to Panta’ (eds , Petculescu A.& Ştiucă E.), pp. 47–52. Bucharest, Romania: Romanian Academy ‘Emil Racoviţă’ Institute of Speleology. Google Scholar
    • 18
      Markov G. N.& Spassov N.. 2003Primitive mammoths from Northeast Bulgaria in the context of the earliest mamoth migrations in Europe. Advances in vertebrate paleontology ‘Hen to Panta’ (eds , Petculescu A.& Ştiucă E.), pp. 53–58. Bucharest, Romania: Romanian Academy ‘Emil Racoviţă'Institute of Speleology. Google Scholar
    • 19
      Baygusheva V.& Titov V.. 2012The evolution of Eastern European meridionaloid elephants’ dental characteristics. Quat. Int. 255, 206–216.doi:10.1016/j.quaint.2011.07.045 (doi:10.1016/j.quaint.2011.07.045). CrossrefGoogle Scholar
    • 20
      Palombo M. R.& Ferretti M. P.. 2005Elephant fossil record from Italy: knowledge, problems, and perspectives. Quat. Int. 126–128, 107–136.doi:10.1016/j.quaint.2004.04.018 (doi:10.1016/j.quaint.2004.04.018). CrossrefGoogle Scholar
    • 21
      Ferretti M. P.. 2008The dwarf elephant Palaeoloxodon mnaidriensis from Puntali Cave, Carini (Sicily, late Middle Pleistocene): anatomy, systematics and phylogenetic relationships. Quat. Int. 182, 90–108.doi:10.1016/j.quaint.2007.11.003 (doi:10.1016/j.quaint.2007.11.003). CrossrefGoogle Scholar
    • 22
      Theodorou G. E., Symeonidis N.& Stathopoulou E.. 2007Elephas tiliensis n. sp. from Tilos island (Dodecanese, Greece). Hel. J. Geosci. 42, 19–32. Google Scholar
    • 23
      Vartanyan S. L., Garutt V. E.& Sher A. V.. 1993Holocene dwarf mammoths from Wrangel Island in the Siberian Arctic. Nature 362, 337–340.doi:10.1038/362337a0 (doi:10.1038/362337a0). Crossref, PubMedGoogle Scholar
    • 24
      Veltre D. W., Yesner D. R., Crossen K. J., Graham R. W.& Coltrain J. B.. 2008Patterns of faunal extinction and paleoclimatic change from mid-Holocene mammoth and polar bear remains, Pribilof Islands, Alaska. Quat. Res. 70, 40–50.doi:10.1016/j.yqres.2008.03.006 (doi:10.1016/j.yqres.2008.03.006). CrossrefGoogle Scholar
    • 25
      Agenbroad L. D.. 2003New absolute dates and comparisons for California's Mammuthus exilis. Deinsea 9, 1–16. Google Scholar
    • 26
      Higham T., et al.2011The earliest evidence for anatomically modern humans in northwestern Europe. Nature 479, 521–524.doi:10.1038/nature10484 (doi:10.1038/nature10484). Crossref, PubMedGoogle Scholar
    • 27
      Maglio V. J.. 1972Evolution of mastication in the Elephantidae. Evolution 26, 638–658.doi:10.2307/2407059 (doi:10.2307/2407059). Crossref, PubMedGoogle Scholar
    • 28
      Lister A. L.& Joysey K. A.. 1992Scaling effects in elephant dental evolution—the example of Eurasian Mammuthus. Structure, function and evolution of teeth (eds , Smith P.& Tchernov E.), pp. 185–213. Tel Aviv, Israel: Freund Publishing House Ltd. Google Scholar
    • 29
      Aguirre E.. 1969Evolutionary history of the elephant. Science 164, 1366–1376.doi:10.1126/science.164.3886.1366 (doi:10.1126/science.164.3886.1366). Crossref, PubMedGoogle Scholar
    • 30
      Sokal R. R.& Rohlf F. J.. 1995Biometry, 3rd edn.New York, NY: W. H. Freeman and Company. Google Scholar
    • 31
      Bate D. M. A.. 1905Four and a half months in Crete in search of Pleistocene mammalian remains. Geol. Mag. 2, 195–203.doi:10.1017/S0016756800132078 (doi:10.1017/S0016756800132078). CrossrefGoogle Scholar
    • 32
      van der Geer A., Lyras G.& de Vos J.. 2010Evolution of island mammals. Oxford, UK: Wiley-Blackwell. CrossrefGoogle Scholar
    • 33
      Accordi B.& Palombo M. R.. 1971Morfologia endocranica degli elefanti nani pleistocenici di Spinagallo (Siracusa) e comparazione con l'endocranio di Elephas antiquus. Atti della Accad. Naz. Lincei Cl. Sci. Fis. Mat. Nat. 51, 111–124. Google Scholar
    • 34
      Palombo M. R.. 2001Paedomorphic features and allometric growth in the skull of Elephas falconeri from Spinagallo (Middle Pleistocene, Sicily). 1st Int. Congress of the World of Elephants (eds , Cavarretta G., Gioia P., Mussi M.& Palombo M. R.), pp. 492–496. Rome, Italy: Consiglio Nazionale delle Ricerche. Google Scholar
    • 35
      Palombo M. R., Ferretti M. P., Pillola G. L.& Chiappini L.. 2012A reappraisal of the dwarfed mammoth Mammuthus lamarmorai (Major, 1883) from Gonnesa (south-western Sardinia, Italy). Quat. Int. 257, 158–170.doi:10.1016/j.quaint.2011.05.037 (doi:10.1016/j.quaint.2011.05.037). CrossrefGoogle Scholar
    • 36
      Roth V. L.. 1982Dwarf mammoths from the Santa Barbara, California Channel Islands: size, shape, development and evolution. PhD thesis, Yale University, New Haven, CT. Google Scholar
    • 37
      Gould S. J.. 1975On the scaling of tooth size in mammals. Am. Zool. 15, 353–362. CrossrefGoogle Scholar
    • 38
      Raia P.& Meiri S.. 2006The island rule in large mammals: paleontology meets ecology. Evolution 60, 1731–1742. Crossref, PubMedGoogle Scholar
    • 39
      Roth V. L.. 1984How elephants grow: heterochrony and the calibration of developmental stages in some living and fossil species. J. Vert. Paleontol. 4, 126–145.doi:10.1080/02724634.1984.10011993 (doi:10.1080/02724634.1984.10011993). CrossrefGoogle Scholar
    • 40
      Christiansen P.. 2004Body size in proboscideans, with notes on elephant metabolism. Zool. J. Linn. Soc. 140, 523–549.doi:10.1111/j.1096-3642.2004.00113.x (doi:10.1111/j.1096-3642.2004.00113.x). CrossrefGoogle Scholar
    • 41
      Lister A. M.& Stuart A. J.. 2010The West Runton mammoth (Mammuthus trogontherii) and its evolutionary significance. Quat. Int. 228, 180–209.doi:10.1016/j.quaint.2010.07.032 (doi:10.1016/j.quaint.2010.07.032). CrossrefGoogle Scholar
    • 42
      Haynes G.. 1991Mammoths, mastodonts and elephants: biology, behaviour and the fossil record. Cambridge, UK: Cambridge University Press. Google Scholar
    • 43
      Roth V. L.. 1992Quantitative variation in elephant dentitions: implications for the delimitation of fossil species. Paleobiology 18, 184–202. CrossrefGoogle Scholar
    • 44
      Welter-Schultes F. W.. 2000The paleogeography of late Neogene central Crete inferred from the sedimentary record combined with Albinaria land snail biogeography. Palaeogeogr. Palaeoclimatol. Palaeoecol. 157, 27–44.doi:10.1016/S0031-0182(99)00176-5 (doi:10.1016/S0031-0182(99)00176-5). CrossrefGoogle Scholar
    • 45
      Bonfiglio L., Mangano G., Marra A. C., Masini F., Pavia M.& Petruso D.. 2002Pleistocene Calabrian and Sicilian bioprovinces. Geobios 35((Suppl. 1)), 29–39.doi:10.1016/S0016-6995(02)00046-3 (doi:10.1016/S0016-6995(02)00046-3). CrossrefGoogle Scholar
    • 46
      Bada J. L., Belluomini G., Bonfiglio L., Branca M., Burgio E.& Delitala L.. 1991Isoleucine epimerization ages of Quaternary mammals from Sicily. Il Quat. 4, 49–54. Google Scholar