Intra- and interpopulation genetic differentiation and gene flow in a group of isolated populations of Bradybaena fruticum (O. F. Muller, 1774) in South Poland
2004; Wiley; Volume: 42; Issue: 1 Linguagem: Inglês
10.1046/j.1439-0469.2003.00244.x
ISSN1439-0469
AutoresAndrzej Falniowski, Magdalena Szarowska, E. Witkowska-Pelc,
Tópico(s)Genetic Mapping and Diversity in Plants and Animals
ResumoJournal of Zoological Systematics and Evolutionary ResearchVolume 42, Issue 1 p. 70-80 Intra- and interpopulation genetic differentiation and gene flow in a group of isolated populations of Bradybaena fruticum (O. F. Müller, 1774) in South Poland Genetische Differenzierung und Genfluß innerhalb und zwischen einer Gruppe von isolierten Populationen von Bradybaena fruticum (O. F. Müller, 1774) in Polen A. Falniowski, A. Falniowski Department of Malacology, *Department of Animal Physiology, Institute of Zoology, Jagiellonian University, Kraków, PolandSearch for more papers by this authorM. Szarowska, M. Szarowska Department of Malacology, *Department of Animal Physiology, Institute of Zoology, Jagiellonian University, Kraków, PolandSearch for more papers by this authorE. Witkowska-Pelc*, E. Witkowska-Pelc* Department of Malacology, *Department of Animal Physiology, Institute of Zoology, Jagiellonian University, Kraków, PolandSearch for more papers by this author A. Falniowski, A. Falniowski Department of Malacology, *Department of Animal Physiology, Institute of Zoology, Jagiellonian University, Kraków, PolandSearch for more papers by this authorM. Szarowska, M. Szarowska Department of Malacology, *Department of Animal Physiology, Institute of Zoology, Jagiellonian University, Kraków, PolandSearch for more papers by this authorE. Witkowska-Pelc*, E. Witkowska-Pelc* Department of Malacology, *Department of Animal Physiology, Institute of Zoology, Jagiellonian University, Kraków, PolandSearch for more papers by this author First published: 24 September 2008 https://doi.org/10.1046/j.1439-0469.2003.00244.xCitations: 8 Authors’ address: Andrzej Falniowski (for correspondence), Magdalena Szarowska and Ewa Witkowska-Pelc, Institute of Zoology, Jagiellonian University, ul. R. Ingardena 6, 30-060 Kraków, Poland. E-mail: [email protected] Read the full textAboutPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onEmailFacebookTwitterLinkedInRedditWechat Abstracten Intra- and interpopulation variation was studied, by means of cellulose acetate allozyme electrophoresis, on 16 populations of helicoid snail Bradybaena fruticum (O. F. Müller, 1774) in South Poland. Four enzyme systems, coded by seven loci, were analysed. Calculated with Fisher's technique and Ohta's D-statistics, four cases of linkage disequilibrium were detected, reflecting population subdivision. The mean number of alleles per locus equalled 2.16 and the mean expected heterozygosity was 0.287. Exact multipopulation and multilocus tests for Hardy–Weinberg equilibrium indicated a statistically significant homozygote excess in all the loci and all populations but three. Each population, however, was at Hardy–Weinberg equilibrium for most loci, though the values of f (FIS) were usually high. Homozygote excess was ascribed partly to inbreeding and partly to Wahlund's effect (spatial subdivision of population; at least two cohorts of adult, reproducing snails), disrupting selection in this polymorphic species not excluded. F-statistics showed relatively low values of θ (FST ; mean for all loci = 0.224) and those of Nm usually below 1 (mean 0.866). Pairwise values of either θ or Cavalli-Sforza and Edwards arc distance were statistically significantly associated with geographic distances. Contrary to this, no geographic pattern of interpopulation differences was detected by correspondence analysis on allele frequencies, non-linear multidimensional scaling, UPGMA clustering or neighbour-joining trees constructed on θ and Cavalli-Sforza and Edwards arc distance. Accordingly, some most distant populations were more similar to one another than the close ones. Zusammenfassungde Für 16 südpolnische Populationen der helicoiden Schnecke Bradybaena fruticum (O. F. Müller, 1774) wurde die genetische Variation mit Hilfe der Cellulosacetat-Allozym-Elektrophorese untersucht. Dabei wurden vier Enzymsysteme, die von sieben Loci codiert werden, analysiert. Bei Berechnungen nach der Methode von Fisher und nach Ohtas D-Statistik konnten vier Fälle von Austauschungleichgewicht gefunden werden, was die Unterteilung der Populationen widerspiegelt. Die durchschnittliche Zahl an Allelen pro Locus war 2,16 und die mittlere erwartete Heterozygotie 0,287. Exakte Multipopulations- und Multilocus-Tests auf Übereinstimmung mit der Hardy-Weinberg-Verteilung ergaben für alle Loci und für alle Populationen, außer in drei Fällen, einen signifikanten Überschuß an Heterozygoten. Jede Population für sich zeigte aber für die meisten Loci Übereinstimmung mit dem Hardy-Weinberg-Gleichgewicht, obgleich die f-Werte (FIS) meist hoch waren. Homozygoten-Überschüsse können teilweise durch Inzucht, teilweise durch den Wahlund-Effekt (räumlich-zeitliche Unterteilung der Populationen; zumindest zwei Kohorten von reproduzierenden Adulten) erklärt werden; auch disruptive Selektion kann nicht ausgeschlossen werden. Die F-statistischen Werte (θ) erwiesen sich als relativ klein (FST ; Mittel über alle Loci = 0,224) und auch die Nm-Werte lagen meist unter 1 (Mittel 0,866). Die paarweisen Werte von θ und die Distanzwerte nach Cavalli-Sforza und Edwards ließen eine signifikannte Assoziation mit den geographischen Distanzen erkennen. Im Gegensatz dazu konnte kein geographisches Muster der Populations-Differenzierung durch eine Korrespondenz-Analyse der Allelfrequenzen, durch nonlineares multidimensionales Scaling und durch UPGM- oder Neigbor-Joining-Bäume, von θ oder von den Cavalli-Sforza und Edwards arc Distanzen abgeleitet, aufgedeckt werden. Nach all diesen Analysen sind voneinander weit entfernte Populationen untereinander ähnlicher als nahe beisammen liegende. References Amos, W., 1999: Two problems with the measurement of genetic diversity and genetic distance. In: L. F. Landweber; A. P. Dobson (eds), Genetics and the Extinction of Species. Princeton, NJ: Princeton University Press, pp. 75–100. Google Scholar Andreassen, H. P.; Hall, S.; Ims, R. A., 1996: Optimal width of movement corridors for root voles: not too narrow and not too wide. J. Appl. Ecol. 33, 63–70. 10.2307/2405016 Web of Science®Google Scholar Arter, H. E., 1990: Spatial relationship and gene flow paths between populations of the land snail Arianta arbustorum (Pulmonata: Helicidae). Evolution 44, 966–980. 10.1111/j.1558-5646.1990.tb03818.x PubMedWeb of Science®Google Scholar Asami, T.; Fukuda, H.; Tomiyama, K., 1993: The inheritance of shell banding in the land snail Bradybaena pellucida. Venus 52, 155–159. Google Scholar Avise, J. C., 2000: Phylogeography. The History and Formation of Species. Cambridge, MA: Harvard University Press. 10.2307/j.ctv1nzfgj7 Google Scholar Bába, K., 1985: Investigation of the growth rate of two terrestrial snails: Bradybaena fruticum (O. F. Müller) and Euomphalia strigella (Draparnaud), Pulmonata. Soosiana 13, 79–88. Google Scholar Black, W. C.; Krafsur, E. S., 1985: A Fortran program for the calculation of two linkage disequilibrium coefficients. Theor. Appl. Genet. 70, 491–496. 10.1007/BF00305981 PubMedWeb of Science®Google Scholar Bossart, J. L.; Prowell, D. P., 1998: Genetic estimates of population structure and gene flow: limitations, lessons and new directions. Trends Ecol. Evol. 13, 202–206. 10.1016/S0169-5347(97)01284-6 CASPubMedWeb of Science®Google Scholar Brookes, M. I.; Graneau, Y. A.; King, P.; Rose, O. C.; Thomas, C. D.; Mallet, J. L. B., 1997: Genetic analysis of founder bottlenecks in the rare British butterfly Plebejus argus. Conserv. Biol. 11, 648–661. 10.1046/j.1523-1739.1997.96163.x Web of Science®Google Scholar Chen, X.; Baur, B., 1993: The effect of multiple mating on female reproductive success in the simultaneously hermaphroditic land snail Arianta arbustorum. Can. J. Zool. 71, 2431–2436. 10.1139/z93-339 Web of Science®Google Scholar Cockerham, C. C.; Weir, B. S., 1993: Estimation of gene flow from F-statistics. Evolution 47, 855–863. 10.1111/j.1558-5646.1993.tb01239.x PubMedWeb of Science®Google Scholar Crow, J. F.; Kimura, M., 1970: Introduction to Population Genetics Theory. New York: Harper and Row. Google Scholar Downes, S. J.; Handasyde, K. A.; Elgar, M. A., 1997: The use of corridors by mammals in fragmented Australian eucalypt forests. Conserv. Biol. 11, 718–726. 10.1046/j.1523-1739.1997.96094.x Google Scholar Endler, J., 1977: Geographic Variation, Speciation, and Clines. Princeton, NJ: Princeton University Press. 10.1126/science.179.4070.243 PubMedGoogle Scholar Falniowski, A.; Kozik, A.; Szarowska, M., 1993a: Biometrical and esterases pattern differences between local populations in Bradybaena fruticum (O.F. Müller, 1777) (Gastropoda: Stylommatophora: Helicoidea). Malak. Abh. Mus. Tierkde. Dresden 16, 147–164. Google Scholar Falniowski, A.; Kozik, A.; Szarowska, M.; Rąpała-Kozik, M.; Turyna, I., 1993b: Morphological and allozymic polymorphism and differences among local populations in Bradybaena fruticum (O. F. Müller, 1777) (Gastropoda: Stylommatophora: Helicoidea). Malacologia 35, 371–388. Web of Science®Google Scholar Falniowski, A.; Kozik, A.; Szarowska, M.; Fiałkowski, W.; Mazan, K., 1996: Allozyme and morphology evolution in European Viviparidae (Mollusca: Gastropoda: Architaenioglossa). J. Zool. Syst. Evol. Research 34, 49–62. 10.1111/j.1439-0469.1996.tb00810.x Web of Science®Google Scholar Falniowski, A.; Szarowska, M.; Fiałkowski, W.; Mazan, K., 1998: Unusual geographic pattern of interpopulation variation in a spring snail Bythinella (Gastropoda: Prosobranchia). J. Nat. Hist. 32, 605–616. 10.1080/00222939800770311 Web of Science®Google Scholar Falniowski, A.; Mazan, K.; Szarowska, M., 1999: Homozygote excess and gene flow inBythinella. J. Zool. Syst. Evol. Research 37, 165–175. 10.1111/j.1439-0469.1999.tb00980.x Web of Science®Google Scholar Falniowski, A.; Heller, J.; Mazan-Mamczarz, K.; Szarowska, M., 2002a: Genetic structure of the closely related species of Melanopsis (Gastropoda: Cerithiacea) in Israel. J. Zool. Syst. Evol. Research 40, 92–104. 10.1046/j.1439-0469.2002.00182.x Web of Science®Google Scholar Falniowski, A.; Heller, J.; Szarowska, M.; Mazan-Mamczarz, K., 2002b: Allozymic taxonomy within the genus Melanopsis (Gastropoda: Cerithiacea) in Israel: a case in which slight differences are congruent. Malacologia 44, 307–324. Web of Science®Google Scholar Frömming, E., 1954: Biologie der Mitteleuropäischen Landgastropoden. Berlin: Duncker-Humblot. Google Scholar Garnier-Gere, P.; Dillmann, C., 1992: A computer program for testing pairwise linkage disequilibria in subdivided populations. J. Hered. 83, 239. 10.1093/oxfordjournals.jhered.a111204 PubMedGoogle Scholar Goudet, J., 1995: FSTAT version 1.2: a computer program to calculate F-statistics. J. Hered. 86, 485–486. 10.1093/oxfordjournals.jhered.a111627 Web of Science®Google Scholar Greenwood, J. J. D., 1974: Effective population number in the snail Cepaea nemoralis. Evolution 28, 513–526. 10.1111/j.1558-5646.1974.tb00785.x CASPubMedWeb of Science®Google Scholar Guo, S. W.; Thompson, E. A., 1992: Performing the exact test of Hardy–Weinberg proportions for multiple alleles. Biometrica 48, 361–372. PubMedGoogle Scholar Hartl, D. L.; Clark, A. G., 1997: Principles of Population Genetics, 3rd edn. Sunderland, MA: Sinauer Associates. Google Scholar Hedrick, P. W., 1996: Bottleneck(s) or metapopulation in cheetahs. Conserv. Biol. 10, 897–899. 10.1046/j.1523-1739.1996.10030897.x Web of Science®Google Scholar Hillis, D. M., 1989: Genetic consequences of partial self-fertilization on populations of Liguus fasciatus (Mollusca: Pulmonata: Bulimulidae). Am. Malac. Bull. 7, 7–12. Web of Science®Google Scholar Honda, C.; Asami, T., 1993: Temporal and spatial variations of genetic structure of populations in the land snail Bradybaena similaris. J. Tach. Coll. Tokyo 26, 103–112. Google Scholar Jarne, P.; Vianey-Liaud, M.; Delay, B., 1993: Selfing and outcrossing in hermaphrodite freshwater gastropods (Basommatophora): where, when and why. Biol. J. Linn. Soc. Lond. 49, 99–125. 10.1111/j.1095-8312.1993.tb00893.x Web of Science®Google Scholar Jones, J. S.; Leith, B. H.; Rawlings, P., 1977: Polymorphism in Cepaea: a problem with too many solutions? Annu. Rev. Ecol. Syst. 8, 109–143. 10.1146/annurev.es.08.110177.000545 Web of Science®Google Scholar Jones, J. S.; Selander, R. K.; Schnell, G. D., 1980: Patterns of morphological and molecular polymorphism in the land snail Cepaea nemoralis. Biol. J. Linn. Soc. 14, 359–387. 10.1111/j.1095-8312.1980.tb00114.x CASWeb of Science®Google Scholar Kerney, M. P.; Cameron, R. A. D.; Jungbluth, J. H., 1983: Die Landschnecken Nord- und Mitteleuropas. Ein Bestimmungsbuch für Biologen und Naturfreunde. Hamburg and Berlin: Verlag Paul Parey. Google Scholar Khokhutkin, I. M., 1979: Inheritance of banding in natural populations of the land snail Bradybaena fruticum (Müll.). Genetika (Moscow) 15, 868–871 (in Russian). Web of Science®Google Scholar Khokhutkin, I. M., 1984: Organization and variation of the polymorphic structure of species of land molluscs. J. Gen. Zool. 45, 615–623. Web of Science®Google Scholar Khokhutkin, I. M.; Lazareva, A. I., 1975: Polymorphism and concealing coloration of land mollusc population. Zhurnal Obshchei Biologii 36, 863–868 (in Russian). Web of Science®Google Scholar Khokhutkin, I. M.; Lazareva, A. I., 1983: Biotopic and geographic changes in the polymorphic structure of Bradybaena fruticum (Müll.) mollusca systematics, ecology and bionomic distribution. Aftorefer. Proceedings of the 7th Pansovietic Society on Malacological Studies, pp. 62–63 (in Russian). Google Scholar Khokhutkin, I. M.; Lazareva, A. I., 1987: Variability structure in land snails: adaptation on populational and superspecific levels. In: Ya. I. Starobogatov; A. N. Golikov; I. M. Likharev (eds), Molluscs, Results and Perspectives of Investigation. Eight Meeting on the Investigations of Molluscs, Abstracts of Communications. Leningrad: USSR Acad. Sci., Zool. Inst., Izd. Nauka, pp. 441–442 (in Russian). Google Scholar Lande, R., 1999: Extinction risks from anthropogenic, ecological, and genetic factors. In: L. F. Landweber; A. P. Dobson (eds), Genetics and the Extinction of Species. Princeton, NJ: Princeton University Press, pp. 1–22. Google Scholar Lazaridou-Dimitriadou, M.; Karakousis, Y.; Staikou, A., 1994: Geographical variation in shell morphology and isoenzymes of Helix aspersa Müller, 1774 (Gastropoda, Pulmonata), the edible land snail, from Greece and Cyprus. Heredity 72, 23–35. 10.1038/hdy.1994.3 CASWeb of Science®Google Scholar Leberg, P. L., 1992: Effects of population bottlenecks on genetic diversity as measured by allozyme electrophoresis. Evolution 46, 447–494. Web of Science®Google Scholar Makeeva, V. M., 1987: The role of the anthropogene barriers in the formation of the population structure of Bradybaena fruticum (Müll.) in the Moscow region. In: Ya. I. Starobogatov; A. N. Golikov; I. M. Likharev (eds), Molluscs, Results and Perspectives of Investigation. Eight Meeting on the Investigations of Molluscs, Abstracts of Communications. Leningrad: USSR Acad. Sci., Zool. Inst., Izd. Nauka, pp. 463–464 (in Russian). Google Scholar Makeeva, V. M.; Matiokin, P. V., 1987: The role of the natural selection in the genetic population structure of Bradybaena fruticum (Müll.) in Moscow region. In: Ya. I. Starobogatov; A. N. Golikov; I. M. Likharev (eds), Molluscs, Results and Perspectives of Investigation. Eight Meeting on the Investigations of Molluscs, Abstracts of Communications. Leningrad: USSR Acad. Sci., Zool. Inst., Izd. Nauka, pp. 475–476 (in Russian). Google Scholar Maruyama, T.; Kimura, M., 1980: Genetic variation and effective population size when local extinction and recolonization of subpopulations are frequent. Proc. Natl. Acad. Sci. USA 77, 6710–6714. 10.1073/pnas.77.11.6710 CASPubMedWeb of Science®Google Scholar Murphy, R. W.; Sites, J. W., Jr.; Buth, D. G.; Haufler, H., 1996: Proteins: isozyme electrophoresis. In: D. M. Hillis; C. Moritz; B. K. Mable (eds), Molecular Systematics, 2nd edn. Sunderland, MA: Sinauer Associates, pp. 51–120. Google Scholar Nevo, E.; Beiles, A.; Ben-Shlomo, R., 1984: The evolutionary significance of genetic diversity: ecological, demographic and life history correlates. In: G. S. Mani (ed.), Evolutionary Dynamics of Genetic Eiversity. Berlin: Springer Verlag, pp. 13–213. 10.1007/978-3-642-51588-0_2 Google Scholar Ohta, T., 1982: Linkage disequilibrium due to random genetic drift in finite subdivided populations. Proc. Natl. Acad. Sci. USA 79, 1940–1944. 10.1073/pnas.79.6.1940 CASPubMedWeb of Science®Google Scholar Oxford, G. S., 1973a: the genetics of Cepaea esterases. 1. Cepaea nemoralis. Heredity 30, 127–139. 10.1038/hdy.1973.17 CASPubMedWeb of Science®Google Scholar Oxford, G. S., 1973b: The biochemical properties of esterases in Cepaea (Mollusca: Helicidae). Comp. Bioch. Physiol. 45B, 529–538. 10.1016/0305-0491(73)90191-0 Web of Science®Google Scholar Oxford, G. S., 1973c: Molecular weight relationships of the esterases in Cepaea nemoralis and Cepaea hortensis (Mollusca:Helicidae) and their genetic implications. Bioch. Genet. 8, 365–382. 10.1007/BF00487342 CASPubMedWeb of Science®Google Scholar Raymond, M.; Rousset, F., 1995: genepop (Version 1.2): Population genetics software for exact tests and ecumenicism. J. Hered. 86, 248–249. 10.1093/oxfordjournals.jhered.a111573 Web of Science®Google Scholar Richardson, B. J.; Baverstock, P. R.; Adams, M., 1986: Allozyme Electrophoresis: a Handbook for Animal Systematics and Population Studies. Sydney: Academic Press. Google Scholar Riedel, A., 1988: Gastropoda terrestria. Catalogus faunae Poloniae 36, 1. Polska Akademia Nauk, Instytut Zoologii, Warszawa: Panstwowe Wydawnictwo Naukowe (in Polish). Google Scholar Robertson, A.; Hill, W. G., 1984: Deviations from Hardy–Weinberg proportions: sampling variances used in estimation of inbreeding coefficients. Genetics 107, 703–718. PubMedWeb of Science®Google Scholar Rohlf, F. J., 1998: NTSYSpc, Numerical Taxonomy and Multivariate Analysis System. Version 2.0. Seatuket, NY: Exeter Software. Google Scholar Rousset, F.; Raymond, M., 1995: Testing heterozygote excess and deficiency. Genetics 140, 1413–1419. 10.1093/genetics/140.4.1413 CASPubMedWeb of Science®Google Scholar Selander, R. K.; Ochman, H., 1983: Genetics and evolution. In: M. C. Rattazzi; J. Scandalios; G. Whitt (eds), Isozymes: Current Topics in Biological and Medical Research, Vol. 10. New York: Alan R. Liss, pp. 93–123. Web of Science®Google Scholar Shibata, S.; Asami, T.; Shimamura, R., 1993: Is the shell polymorphism controlled by a supergene in the land snailBradybaena similaris? J. Tach. Coll. Tokyo 26, 95–102. Google Scholar Shileiko, A. A., 1978: Nazemnye molliuski nadsemeistva Helicoidea. Fauna SSSR, Molliuski, T. III, 6, Akad. Nauk SSSR, Zool. Inst., n. s. 117. Leningrad: Izd. Nauka. Google Scholar Slatkin, M., 1993: Isolation by distance in equilibrium and non-equilibrium populations. Evolution 47, 264–279. 10.2307/2410134 PubMedWeb of Science®Google Scholar Staikou, A.; Lazaridou-Dimitriadou, M.; Pana, E., 1990: The life cycle, population dynamics, growth and secondary production of the snail Bradybaena fruticum (Müller, 1774) (Gastropoda Pulmonata) in northern Greece. J. Moll. Stud. 56, 137–146. 10.1093/mollus/56.2.137 Web of Science®Google Scholar Swofford, D. L.; Selander, R. B., 1981: BIOSYS-1: a FORTRAN program for the comprehensive analysis for electrophoretic data in population genetics and systematics. J. Hered. 72, 281–283. 10.1093/oxfordjournals.jhered.a109497 Web of Science®Google Scholar Szarowska, M.; Falniowski, A.; Mazan, K.; Fiałkowski, W., 1998: Adaptive significance of glucose phosphate isomerase (GPI) allozymes in the spring snail Bythinella? J. Moll. Stud. 64, 257–261. 10.1093/mollus/64.2.257 Web of Science®Google Scholar Szarowska, M.; Falniowski, A.; Mazan-Mamczarz, K., 2003: Genetic structure of isolated selfers: Chondrina clienta (Westerlund, 1888) (Gastropoda: Stylommatophora) in Kraków-Częstochowa Upland. Malak. Abh. Staat. Mus. Tierkd. Dresden Vol. 21 , 79–89. Google Scholar Templeton, A. R., 1998: Nested clade analyses of phylogeographic data: testing hypotheses about gene flow and population history. Mol. Ecol. 7, 381–397. 10.1046/j.1365-294x.1998.00308.x CASPubMedWeb of Science®Google Scholar Thomaz, D.; Guillar, A.; Clarke, B., 1996: Extreme divergence of mitochondrial DNA within species of pulmonate land snails. Proc. Roy. Soc. Lond. B 263, 363–368. 10.1098/rspb.1996.0056 CASPubMedWeb of Science®Google Scholar Weir, B. S., 1990: Genetic Data Analysis. Sunderland, MA: Sinauer Associates. Google Scholar Weir, B. S., 1996: Intraspecific differentiation. In: D. M. Hillis; C. Moritz; B. K. Mable (eds), Molecular Systematics, 2nd edn. Sunderland, MA: Sinauer Associates, pp. 385–405. Web of Science®Google Scholar Weir, B. S.; Cockerham, C. C., 1984: Estimating F-statistics for the analysis of population structure. Evolution 38, 1358–1370. 10.1111/j.1558-5646.1984.tb05657.x CASPubMedWeb of Science®Google Scholar Whitlock, M. C.; McCauley, D. E., 1999: Indirect measures of gene flow and migration: FST? 1/(4Nm + 1). Heredity 82, 117–125. 10.1046/j.1365-2540.1999.00496.x PubMedWeb of Science®Google Scholar Williamson, P; Cameron, R. A. D.; Carter, M. A., 1977: Population dynamics of the land snail Cepaea nemoralis (L.): a six year study. J. Anim. Ecol. 46, 181–194. 10.2307/3955 Web of Science®Google Scholar Wright, S., 1940: Breeding structure of populations in relation to speciation. Am. Nat. 74, 232–248. 10.1086/280891 Web of Science®Google Scholar Wright, S., 1969: Genetics and the Evolution of Populations. Vol. 2: The Theory of Gene Frequencies. Chicago, IL: University of Chicago Press. Google Scholar Wright, S., 1978: Evolution and the Genetics of Populations. Vol. 4: Variability Within and Among Natural Populations. Chicago, IL: University of Chicago Press. Google Scholar Zeifert, D. V., 1987: The population dynamics of the land snail Bradybaena fruticum (Müller) in different habitats. In: Ya. I. Starobogatov; A. N. Golikov; I. M. Likharev (eds), Molluscs, Results and Perspectives of Investigation. Eight Meeting on the Investigations of Molluscs, Abstracts of Communications. Leningrad: USSR Acad. Sci., Zool. Inst., Izd. Nauka, pp. 442–445 (in Russian). Google Scholar Zeifert, D. V.; Shutov, S. V., 1979: Role of certain terrestrial molluscs in the transformation of leaf litter. Ekologiya 5, 58–61. Google Scholar Citing Literature Volume42, Issue1February 2004Pages 70-80 ReferencesRelatedInformation
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