The Cyclophorids fauna of Taiwan
Before the present investigation, there were 9 genera and 29 cyclophorid species (including 3 unidentified species) in Taiwan reported by me (Lee & Wu 2001). In 2003, Cyathopoma iota and C. ogaitoi were reported as new records of Taiwan by me (Lee & Cheng 2003). The above reports were based on morphology and some viewpoints were immature. In the phylogenetic study of Cyclophoridae I chanced to find a new species of Japonia and will be report in Zootaxa magazine (Lee, Lue &
Wu 2008). Base on morphologic and molecular data, the taxonomic status changed and previous miss identified species were corrected in chapter 1. In summary, there are 10 genera and 29 cyclophorid species in Taiwan.
The phylogeny of East Asia Cyclophoridae
I have undertaken the first molecular phylogenetic analysis of the Cyclophoridae.
Sequence of COI and 16S rRNA were examined in 32 species of 10 genera of cyclophorid encompassing the entire currently recognized major subfamily. It allows an independent test of the present classification based on morphologic characters. At the level of genus, my molecular phylogeny closely supports the current taxonomy, but at subfamily level does not although the bootstrap support is low.
In the other hand, Cyathopoma micron were recognized as Cyclotus micron based on its biconcave operculum morphology (Pilsbry & Hirase 1904). Besides, C. iota was considered a closer relative to C. micron than to C. taiwanicum (Pilsbry & Hirase 1904, Higo & Goto 1993, Lee & Chen 2003). My molecular and radula data indicate that C. iota is closer to C. taiwanicum than to C. micron. In summary C. micron, C.
iota, C. ogaitoi, and C. taiwanicum should be placed in Cyathopoma rather than Cyclotus.
Both COI and 16S rRNA gene trees indicate Japonia and Ptychopoma are sister group of Cyclophorus and Cyclotus, respectively. The former two will be used as the out group of Cyclophorus and Cyclotus in their phylogenetic studies.
Taiwan Cyclophorus speciation model vs. C. taivanus ssp. speciation model
Cyclophorus and Cyclotus widely occur in Taiwan and share similar ecological niche.
Both Taiwan Cyclophorus and C. taivanus ssp. span two morphologic units. In Taiwan Cyclophorus, the keel and round shell occurs in northern and southern Taiwan, respectively. In contrast, tall spire and flat spire previous C. taivanus ssp. also occurs in north and south Taiwan, respectively. The two morphologic units in different two species groups both have north form and south form. Is that a coincidence?
Alternatively, are there different selective pressures on cyclophorid snails in north and south Taiwan?
My result from Cyclophorus PLS analysis showed that differences between populations in some shell traits co-varied significantly with long term climatic conditions and altitude. I found climatically warmer and stable temperature tend to have keeled shell. The warm and stable climate tends to have luxuriant vegetation.
The keeled shell would be at an advantage when roam over the ground in the luxuriant vegetation. Previous C. taivanus ssp. also appears a climatic gradient responsible for the distribution pattern of species (Fig. 4.12). Along this cline, C.
adamsi occupies only the sites with the moist winter and arid summer season. This type of climate seems to exclude C. taivanus group (C. t. dilatus, C. t. diminutus, C. t.
peraffinis, and C. t. taivanus). The actual level of water stress at a particular site depends strongly on the local microclimate, which may account for the observed intermingled pattern in the contact zone. Even though, the sampling population size is few and limited, there is probably a cline in umbilicus proportion between populations near contact zone (Fig. 4.14). Likewise, there are more or less clines in the other eight shell traits between populations near contact zone (Fig. 4.15).
The above showed a highly probability of adaptation of different climate. However, the speciation model of Taiwan Cyclophorus is different from C. taivanus ssp. The molecular and morphology data indicate that there are two distinctive forms of Cyclophorus in southwest Taiwan, one with flat shell and sculpture with spiral cords on shell surface, one with tall shell and without spiral cords. The molecular data show strong geographic structure (Fig. 3.8–3.12) and current gene flow between close populations (Fig. 3.7). Taiwan Cyclophorus probably is a case of ring speciation. Both two distinctive southwest Taiwan forms are keeled shell. It may due to the adaptation of long term climatic conditions described in above section.
The molecular data of previous C. taivanus ssp. show two highly divergent haplotype
group. It appears that a climatic gradient is responsible for the distribution pattern of species (Fig. 4.12). The actual level of water stress at a particular site depends strongly on the local microclimate, which may account for the observed intermingled pattern in the contact zone. Event the sampling population is few and limited; there is probably a cline in umbilicus proportion between populations near contact zone (Fig.
4.14). Likewise, there are more or less clines in the other eight shell traits between populations near contact zone (Fig. 4.15). Even though premating or postmating reproductive isolation may have evolved as a byproduct of ecological divergence. The ecological divergence appears to be sufficient to prevent immediate contact and therefore acts as an effective barrier to mating. The ecological divergence probably appears rule of speciation in C. taivanus ssp. case. The speciation process is not complete among C. t. dilatus, C. t. diminutus, C. t. peraffinis, and C. t. taivanus, and the adaptation of climatic pressure continuing be a rule of speciation process.
It appears a chance to understand that even how similar two taxonomic groups is, occupied similar niche, undergo the same geological history, with morphological adaptation to the same long term climates, they may have different speciation model.
The speciation cause of live-form is complex; even a tiny difference will lead to distinct speciation result.
References
Abbot, R.T. 1989. Compendium of Landsnails. American Malacologists, Inc.
VIII+240p.
Akcakaya, H.R. & Baur, B. 1996. Effects of population subdivision and catastrophes on the persistence of a land snail metapopulation. Oecologia, 105: 475–483.
Alonso, M.R., López Alcántara, A. & Rivas, P.M.I. 1985. A biogeographic study of Iberus gualterianus (L.) (Pulmonata: Helicidae). Soosiana, 13: 1–10.
Ancey, C.F. 1904. Notes critiques et synonymiques. Journal de Conchyliologie. 52:
288–316.
ArcGIS, 9.2. 2006. GIS and Mapping software designed by ESRI Inc.
Azuma, M. 1982. Colored illustrations of the land snail of Japan (Enlarged revised edition). Hoikusha Publishing Co. Ltd. Oaska, XVI+343 pp. (in Japanese) Barrett, R.D.H. & Hebert, P.D.N. 2005. Identifying spiders through DNA barcoding.
Canadian Journal of Zoology, 83: 481–489.
Benson, W.H. 1856. Characters of 17 new forms of the Cyclostomacea from the British province of Burmah collected by W. Theobald jun., Esq. Annals and Magazine of Natural History London, 2(17): 225-233.
Benson, W.H. 1859. A sectional distribution of the genus Alycaeus Gray, with characters of 6 new species and of other Cyclostomidae, collected at Darjiling by W.T, Blanford, Esq. Annals and Magazine of Natural History London, 3(3):
176-184.
Benson, W.H. 1861, Annals and Magazine of Natural History London, 3(7): 28.
Blanford, W.T. & Blanford, H.F. 1861. Contributions to Indian malacology, No. II.
The Journal of Asiatic Society of Bengal, 30: 347–366.
Chang, K.M. 1984. A catalogue of Taiwan landsnail. Pei-yu, 9: 3–19. (in Chinese) Chen, W.S. & Wang, U. 1996. The geology of Taiwan East Coastal Mountain Range.
Central Geological Survey, MOEA, 101p. (in Chinese)
Chiba, S. 1999. Accelerated evolution of land snails Mandarina in the oceanic Bonin Islands: evidence from mitochondrial DNA sequences. Evolution, 53(2): 460–
471.
Cook, L.M. & Pettitt, C.W.A. 1979. Shell form in Discula polymorpha. Journal of Molluscan Studies, 45: 45–51.
Davison, A. 2002. Land snails as a model to understand the role of history and selection in the origins of biodiversity. Population Ecology, 44, 129–136.
Excoffier, L. Laval, G. & Schneider, S. 2005. Arlequin ver. 3.0: An integrated software
package for population genetics data analysis. Evolutionary Bioinformatics Online, 1: 47–50.
Farris, J.S., Kallersjo, M. Kluge, A.G. & Bult, C. 1995. Constructing a significance test for incongruence. Systematic Biology, 44: 570–572.
Fu, Y.-X. & Li, W.-H. 1993. Statistical tests of neutrality of mutations. Genetics, 133:
693-709.
Goodfriend, G.A. 1986. Variation in land-snail shell from and size and its causes: a review. Systematic Zoology, 35: 204–223.
Goto, Y. & Poppe, G.T. 1996. A list of living Mollusca Part II, Vol 1. Ancona, 520p.
Gould, A.A. 1859. Descriptions of shells collected in the North Pacific Exploring Expedition under Captains Ringgold and Rodgers. Proceeding of Boston Society of Natural History, 6: 422–426; 7: 40–45, 138–142.
Gould, S.J. 1969. An evolutionary microcosm: Pleistocene and recent history of the land snail P. (Poecilozonites) in Bermuda. Bulletin of the Museum of Comparative Zoology at Harvard University, 138: 407–532.
Gould, S.J. 1971. Precise but fortuitous convergence in Pleistocene land snails from Bermuda. Journal of Paleontology, 45: 409–418.
Guindon, S. & Gascuel, O. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology, 52(5): 696–
704.
Habe, T. 1942. Classification of Japanese Assimineidae. Venus, 12(1–2): 33–56.
Hall, T.A. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acid Research Symposium Series, 41: 95–98.
Harrison, S.P., Yu, G., Takahara, H. & Prentice, I.C. 2001. Palaeovegetation Diversity of temperate plants in east Asia. Nature, 129–130.
Healy, J.M. 1996. Molluscan sperm ultrastructure: correlation with taxonomic units within the Gastropoda, Cephalopoda and Bivalvia. In: Taylor, J.D. (Ed.), Origin and Evolutionary Radiation of the Mollusca. Oxford University Press, New York, pp. 99–113.
Hebert, P.D.N., Penton, E.H., Burns, J.M., Janzen, D.H. & Hallwachs, W. 2004a. Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator. Proceedings of the National Academy of Science, 101: 14812–14817.
Ho, C.S. 1982. Tectonic evolution of Taiwan : Explanatory text of the tectonic map of Taiwan. The Ministry of Economic Affairs, ROC. 126p.
Hogg, I.D., & Hebert, P.D.N. 2004. Biological identification of springtails (Collembola: Hexapoda) from the Canadian Arctic, using mitochondrial DNA barcodes. Canadian Journal of Zoology, 82: 749–754.
Hsieh, B.C. 2003. Landsnails of Taiwan. Council of Agriculture Executive Yuan, 242p.
(in Chinese)
Hsieh, B.C. 2004. Incredible snails, Yuan-Liou Publishing Co.,Ltd, 208p. (in Chinese) Hsieh, B.C., Hwang, C.C. & Wu, S.P. 2006. Landsnails of Taiwan. Forestry Bureau
Council of Agriculture Executive Yuan, Taipei, 277p. (in Chinese)
Hull, D.L. 1997. The ideal species concept – and why we can’t get it. In: Species: the Units of Biodiversity (eds Claridge M.F., Dawah H.A., Wilson M.R.), pp. 357–
380. Chapmann & Hall, London.
Hyman, L.H. 1967. The invertebrates Vol. VII, Mollusca I. McGraw-Hill Book Company, New York. VII+792.
Irwin, D.E. 2000. Song variation in an avian ring species. Evolution, 54: 998–1010.
Irwin, D.E., Bensch, S. & Price, T.D. 2001. Speciation in a ring. Nature, 409: 333–
337.
Irwin, D.E. Irwin, J.H. & Price, T.D. 2001. Ring species as bridges between microevolution and speciation. Genetica, 112–113: 223–243.
Jackman, T.R. & Wake, D.B. 1994. Evolutionary and historical analysis of protein variation in the blotched forms of salamanders of the Ensatina complex (Amphibia: Plethodontidae). Evolution, 48: 876–897.
Jiang, L., Wu, W.L. & Lin, Y.S. 1997. Efficient methods for isolating mitochondrial DNA from fresh or fixed molluscan specimens. Zoological Studies, 36: 74–78.
Kay, E.A., Wells, F.E. & Ponder, W.F. 1998. Class Gastropoda. In: Beesley, P.L., Ross, G.J.B., Wells, A. (Eds.), Mollusca: The Southern Synthesis. Fauna of Australia, vol. 5, part B. CSIRO Publishing, Melbourne, pp. 565–604.
Kantor, Y.I. 1996. Phylogeny and relationships of Neogastropoda. In: Taylor, J.D.
(Ed.), Origin and evolutionary radiation of the Mollusca. Oxford University Press, New York, pp. 221–230.
Kilburn, R.N. 1988. Turridae (Mollusca: Gastropoda) of southern Africa and Mozambique. Part 4. subfamilies Drilliinae, Crassispirinae and Strictispirinae.
Annals of the Natal Museum, 29(1): 167–320.
Knijff, P., Denkers, F., van Swelm, N.D. & Kuiper, M. 2001. Genetic affinities within the Herring Gull Larus argentatus assemblage revealed by AFLP genotyping.
Journal of Molecular Evolution, 52: 85–93.
Kishino, H. & Hasegawa, M. 1989. Evaluation of the maximum likelihood estimate of
the evolutionary tree topologies from DNA sequence data, and the branching order in Hominoidea. Journal of Molecular Evolution, 29: 170–179.
Kobelt, W. & Molledorff, O. 1897. Catalog der gegenwärtig lebend bekannten Pneumonopomen. Nachrichtenblatt der Deutschen Malakozoologischen Gesellschaft, 29: 137–152.
Kobelt, W. 1902. Cyclophoridae. Das Tierreich 16. Mollusca. Berlin XXXIX+662p.
Kuroda, T. 1941. A catalogue of molluscan shells from Taiwan (Formosa), with description of new species. Memoirs of the Faculty of Science and Agriculture Taihoku Imperial University, 22 (4): 65–216.
Lai, K.Y. 1990. World of Landsnail. Taiwan Museum, Taipei, IV + 98p. (in Chinese) Lee, Y.C. & Wu, W.L. 2001.The cyclophorids fauna of Taiwan. Bulletin of Malacoloy
R.O.C., 25: 45–78.
Lee, Y.C. & Chen, W.D. 2003. Natural observational illustrations 3－Land snail.
Chin-Chin Publications Ltd. Taipei, 287pp. (in Chinese)
Lee, Y.C., Lue, K.Y. & Wu, W.L. 2008. Molecular evidence for a polyphyletic genus Japonia (Architaenioglossa: Cyclophoridae) and with the description of a new genus and two new species. Zootaxa, 1972: 22-38.
Lee, Y.C., Lue, K.Y. & Wu, W.L. 2008. A molecular phylogenetics investigation of Cyathopoma (Prosobranchia: Cyclophoridae) in East Asia. Zoological Studies, in press.
Lesson, R.P. 1830. Voy. de la Coquillezoologie, 2(1): 346. Taf. 13 Fig. 16.
Lin, M.S. 1990. Climatic Atlas of Taiwan Republic of China. Central Weather Bureau, III+96. (in Chinese)
Lindberg, D.R. & McLean, J.H. 1981. Tropical eastern Pacific limpets of the family Acmaeidae (Mollusca: Archaeogastropoda): generic criteria and descriptions of six new species from the mainland and the Galapagos Islands. Proceeding of the California Academy of Sciences, 42: 323–339.
Lydeard, C., Holznagel, W.E., Ueshima, R. & Kurabayashi, A. 2002. Systematic implications of extreme loss or reduction of mitochondrial LSU rRNA helical-loop structures in gastropods. Malacologia, 44: 349–352.
Lydeard, C., Holznagel, W.E., Glaubrecht, M. & Ponder, W.F. 2002. Molecular phylogeny of a circum-global, diverse gastropod superfamily (Cerithioidea:
Mollusca: Caenogastropoda): pushing the deepest phylogenetic limits of
McKnight, M.L. 1995. Mitochondrial DNA phylogeography of Perognathus amplus and Perognathus longimembris (Rodentia: Heteromydae): a possible mammalian ring species. Evolution, 49: 816–826.
Millard, V. 1996. Classification of Mollusca－A Classification of World Wide Mollusca. Victor Millard South Africa, p76.
Minato, H. 1980. Occurrence of Cyathopoma (Cyclophoridae) in Kyushu, Japan.
Venus, 39(1): 15–16.
Minato, H. 1988. A new cyclophorid species, Nakadaella ogaitoi from Awaji Island, Japan. Venus, 47(3): 155–157.
Moellndorff, O. 1875. Chinesische Landschnecken. Jahrbücher der Deutschen Malakozoologischen Gesellschaft, 2: 118–135.
Moellndorff, O. 1885. Materialien zur Fauna von China. Die Auriculaceen.
Jahrbücher der Deutschen Malakozoologischen Gesellschaft. 12: 362.
Moellendorff, O. 1890. Die Landschnecken Fauna der Insel Cebu. Bericht über die Senckenbergische Naturforschende Gesellschaft, 1890: 190-292.
Müller, O.F. 1774. Vermium terrestrium et fluviatilium seu animalium Infusorum, Helminthicorum et Testaceorum, non marienorum, succincta historia, 2 Bd. Hist.
Verm. 2: 82.
Montfort, P.D. 1810. de. Conchyliologie systematique et classification méthodique des coquilles, etc., 2 Bd., Couch. Syst. 2: 290.
Paquin, P. & Hedin, M. 2004. The power and perils of molecular taxonomy: a case study of eyeless and endangered Circurina (Araneae: Dictynidae) from Texas caves. Molecular Ecology, 13: 3239–3255.
Pfeiffer, L. 1847. Übersicht aller bekannten Arten von Cyclostomaceen. Zeitschrift für Malakozoologie, 4: 47, 101–112.
Pfenninger, M. & Magnin, F. 2001. Phenotypic evolution and hidden speciation in Candidula unifasciata ssp. (Helicellinae, Gastropoda) inferred by 16S variation and quantitative shell traits. Molecular Ecology, 10: 2541–2554.
Pfenninger, M., Eppenstein & Magnin, F. 2003. Evidence for ecological speciation in the sister species Candidula unifasciata (Poiret, 1801) and C. rugosiuscula (Michaud, 1831) (Helicellinae, Gastropoda). Biological Journal of the Linnean Society, 79: 611–328.
Pilsbry, H. 1900. Notices of some new Japanese mollusks. The Nautilus, 14: 11–12.
Pilsbry, H.A. & Hirase, Y. 1904. Descriptions of new land snails of the Japanese Empire. Academy of Natural Sciences of Philadelphia, 56: 616–632.
Pilsbry, H.A. & Hirase, Y. 1905. New land molluskd of the Jananese Empire.
Academy of Natural Sciences of Philadelphia, 57: 705–719.
Pilsbry, H.A. & Hirase, Y. 1906. Catalogue of the land and freshwater Mollusca of
Taiwan (Formosa), with description of new species. Academy of Natural Sciences of Philadelphia, 57: 720–752.
Pinceel, J., Jordaens, K., Van Houtte, N., De Winter, A. J. & Backeljau, T. 2004.
Molecular and morphological data reveal cryptic taxonomic diversity in the terrestrial slug complex Arion subfuscus/fuscus (Mollusca, Pulmonata, Arionidae) in continental north-west Europe. Biological Journal of the Linnean Society, 83: 23–38.
Ponder, W.F. & Lingberg, D.R. 1996. Gastropod phylogeny – Challenges for the 90s.
In: Taylor, J.D. (Ed.), Origin and Evolutionary Radiation of the Mollusca.
Oxford University Press, New York, pp. 135–154.
Ponder, W.F. & Lindberg, D.R. 1997. Towards a phylogeny of gastropod molluscs: an analysis using morphological characters. Zoological Journal of the Linnean Society, 119: 88–265.
Posada, D. & Crandall, K.A. 1998. Modeltest: testing the model of DNA substitution.
Bioinformatics, 14 (9): 817–818.
Primer 5. 2000. Statistical software for Ecological Research designed by PRIMER-E Ltd.
Remigio, E.A. & Hebert, P.D.N. 2003. Testing the utility of partial COI sequences for phylogenetic estimates of gastropod relationships. Molecular Phylogenetics and Evolution, 29: 641–647.
Ronquist, F. & Huelsenbeck, J.P. 2003. MrBayes 3: Baysian phylogenetic inference under mixed models. Bioinformatics, 19: 1572–1574.
Rosenberg, G., Tillier, S., Tillier, A., Kuncio, G.S., Hanlon, R.T., Masselot, M. &
Williams, C.J. 1997. Ribosomal RNA phylogeny of selected major clades in the mollusca. Journal of Molluscan Studies, 63: 301–309.
Smith, M.A., Woodley, N.E., Janzen, D.H., Hallwachs, W. & Hebert, P.D.N. 2006.
DNA barcodes reveal cryptic host-specificity within the presumed polyphagous members of a genus of parasitoid flies (Diptera: Tachinidae). Proceedings of the National Academy of Science, 103: 3657–3662.
Solem, A. & Climo, F.M. 1985. Structure and habitat correlations of sympatric New Zealand land snail species. Malacologia, 26: 1–30.
Sowerby G.B. 1843. Descriptions of new species of shells belonging to the genus Cyclostoma. Proceedings of the Zoological Society, London, S: 59–66.
DNA polymorphism. Genetics 123:585–595.
Tamura, K., Dudley, J., Nei, M. & Kumar, S. 2007. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Molecular Biology and Evolution, 24: 1596–1599.
Teshima, H., Davison, A., Kuwahara, Y., Yokoyama, J., Chiba, S., Fukuda, T., Ogimura, H. & Kawata, M. 2003. The evolution of extreme shell shape variation in the land snail Ainohelix editha: a phylogeny and hybrid zone analysis.
Molecular Ecology, 12: 1869–1878.
Thollesson, M. 1999. Phylogenetic analysis of Euthyneura (Gastropoda) by means of the 16S rRNA gene: use of a ‘fast’ gene for ‘higher-level’ phylogenies.
Proceedings of the Royal Society of London Series B, 266: 75–83.
Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F. & Higgins, D.G., 1997.
The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research, 25: 4876–
4882.
Tillier, S., Masselot, M., Philippe, H. & Tillier, A. 1992. Phylogenie moleculaire des Gastropoda (Mollusca) fondee sur le sequencage partiel de l’ARN ribosome 28S.
Comptes Rendus de l’Academie Des Sciences Paris, 314: 79–85.
Trochel, F.H. 1856-1863. Das Gebiβ der Schnecken zur Begründung einer natürlichen Classification, Vol. 1. Nicolaische Verlagsbuchhandlung, Berlin. 252pp., 20pls.
Vaught, R.C. 1989. A Classification of the Living Mollusca. American Malacologists, Inc. Xll+189p.
Wake, D.B., Yanev, K.P. & Brown, C.W. 1986. Geographic Variation in Allozymes in a "Ring Species," the Plethodontid Salamander Ensatina eschscholtzii of Western North America. Evolution, 40: 866–868.
Williams, S.T., Reid, D.G. & Littlewood, D.T. 2003. A molecular phylogeny of the Littorininae (Gastropoda: Littorinidae): unequal evolutionary rates, morphological parallelism, and biogeography of the Southern Ocean. Molecular Phylogenetics and Evolution, 28(1): 60–86.
XLSTAT. 2007. Statistical software for MS Excel designed by Addinsoft.
Yen, T.C. 1939. Die chinesischen Land- und Süßwasser-Gastropoden des Natur-Museums Senckenberg. Abhandlungen der Senckenbergischen Naturforschenden Gesellschaft, 444: 1-234.
Acknowledgments
This study was support by a grant from the “Digital Archives of Malacofauna from Taiwan” project of Research Center for Biodiversity, Academia Sinica. Thanks are due to Dr. Hai-Tau Sht, Dr. Wei Liang of Hainan Normal University, Ming-Hui Lin and Mr. Zan-Chen Hwang for their help to collect some materials from China. The author also wishes to appreciate Mr. Chen-Lung Tung and Ms. Chih-Hui Wang for their help to collect some species from Taiwan and Mr. Ming-Hui Lin for providing living Leptopoma tigris. I also thank Mr. Tai-Lang Lin of Institute of Cellular and Organismic Biology for SEM study and all members of Malacology Laboratory for molecular study.