Allozyme diversity in slugs of the carinarion complex (mollusca, pulmonata)

Allozyme diversity in slugs of the carinarion complex (mollusca, pulmonata)

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ABSTRACT Previous allozyme analyses of the hermaphroditic terrestrial slugs _Arion fasciatus, A. circumscriptus_ and _A. silvaticus_ (subgenus _Carinarion_) have suggested that in North America these species are each single monomorphic strains. However, new data on 18 putative enzyme loci show that in western Europe the three taxa, respectively, consist of at least three, two and 12 homozygous multilocus genotypes (strains), which regularly co-occur. The current opinion that American and European _Carinarion_ populations are similarly structured, and that colonization events did not affect the population genetics of North American _Carinarion_, should therefore be readdressed. The present data also provide the first indication of heterozygosity and possible outcrossing in _Carinarion_. Nevertheless, uniparental reproduction is confirmed as the main breeding system in West European _Carinarion_, although the high incidence of multistrain populations in _A. silvaticus_ and _A. fasciatus_ appears at variance with the current model of population genetic structuring in selfing terrestrial pulmonates. Finally, the systematic status of the three _Carinarion_ spp. is tentatively questioned. SIMILAR CONTENT BEING VIEWED BY OTHERS INVESTIGATION OF GENETIC DIVERSITY AND POLYANDRY OF _LEPTINOTARSA DECEMLINEATA_ USING X-LINKED MICROSATELLITE MARKERS Article Open access 11 December 2023 RETICULATE EVOLUTION IN THE _PTERIS FAURIEI_ GROUP (PTERIDACEAE) Article Open access 01 June 2022 EVOLUTIONARY HISTORY AND COLONIZATION PATTERNS OF THE WING DIMORPHIC GRASSHOPPER _DICHROPLUS VITTATUS_ IN TWO ARGENTINEAN BIOMES Article Open access 21 February 2022 ARTICLE PDF REFERENCES * Armbruster, G, and Schlegel, M. 1994. The land-snail species of _Cochlicopa_ (Gastropoda: Pulmonata: Cochli-copidae): presentation of taxon-specific allozyme patterns, and evidence for a high level of self-fertilization. _J Zool Syst Evol Res_, 32, 282–296. Article  Google Scholar  * Backeljau, T. 1987. Electrophoretic distinction between _Arion hortensis_, _A. distinctus_ and _A. owenii_ (Mollusca: Pulmonata). _Zool Anz_, 219, 33–39. Google Scholar  * Backeljau, T, and De Bruyn, L. 1991. Preliminary report on the genetic variability of _Arion intermedius_ in Europe (Pulmonata). _J Med Appl Malacol_, 3, 19–29. Google Scholar  * Backeljau, T, and De Winter, A J. 1987. An electrophoretic characterisation of three paratypes of _Arion fagophilus_ De Winter, 1986, with notes on the subgeneric division of the genus _Arion_ Férussac, 1819 (Mollusca, Pulmonata). _Z Zool Syst Evolut-forsch_, 25, 169–180. Article  Google Scholar  * Backeljau, T, Ahmadyar, S Z, Selens, M, Van Rompaey, J, and Verheyen, W. 1987. Comparative electrophoretic analyses of three European _Carinarion_ species (Mollusca, Pulmonata, Arionidae). _Zool Scr_, 16, 209–222. Article  Google Scholar  * Backeljau, T, De Brito, C P, Tristā Da Cunha, R M, Frias Martins, A M, and De Bruyn, L. 1992. Colour polymorphism and genetic strains in _Arion intermedius_ from Flores, Azores (Mollusca: Pulmonata). _Biol J Linn Soc_, 46, 131–143. Article  Google Scholar  * Baur, B, and Klemm, M. 1989. Absence of isozyme variation in geographically isolated populations of the land snail _Chondrina clienta_. _Heredity_, 63, 239–244. Article  Google Scholar  * Chichester, L F, and Getz, L L. 1969. The zoogeography and ecology of arionid and limacid slugs introduced into northeastern North America. _Malacologia_, 7, 313–346. Google Scholar  * Coyne, J A, Eanes, W F, Ramshaw, J A M, and Koehn, R K. 1979. Electrophoretic heterogeneity of α-glycerophosphate dehydrogenase among many species of _Drosophila_. _Syst Zool_, 28, 164–175. Article  CAS  Google Scholar  * Dolan, S, and Fleming, C C. 1988. Isoenzymes in the identification and systematics of terrestrial slugs of the _Arion hortensis_ complex. _Biochem Syst Ecol_, 16, 195–198. Article  CAS  Google Scholar  * Foltz, D W, Ochman, H, Jones, J S, Evangelisti, S M, and Selander, R K. 1982. Genetic population structure and breeding systems in arionid slugs (Mollusca: Pulmonata). _Biol J Linn. Soc._, 17, 225–241. Article  Google Scholar  * Foltz, D W, Ochman, H, and Selander, R K. 1984. Genetic diversity and breeding systems in terrestrial slugs of the families Limacidae and Arionidae. _Malacologia_, 25, 593–605. Google Scholar  * Harris, H, and Hopkinson, D A. 1976. _Handbook of Enzyme Electrophoresis in Human Genetics_. Elsevier/North Holland Publishing Company, Amsterdam. Google Scholar  * Hoffmann, R J. 1983. The mating system of the terrestrial slug _Deroceras laeve_. _Evolution_, 37, 423–425. Article  PubMed  Google Scholar  * Jarne, P, and Charlesworth, D. 1993. The evolution of the selfing rate in functionally hermaphrodite plants and animals. _Ann Rev Ecol Syst_, 24, 441–466. Article  Google Scholar  * Jarne, P, and Städler, T. 1995. Population genetic structure and mating system evolution in freshwater pulmonates. _Experientia_, 51, 482–497. Article  CAS  Google Scholar  * Kerney, M P, Cameron, R A D, and Jungbluth, J H. 1983. _Die Landschnecken Nord- und Mitteleuropas_. Paul Parey, Hamburg. Google Scholar  * Lohmander, H. 1937. Ueber die nordischen Formen von _Arion circumscriptus_ Johnston. _Acta Soc Fauna Flora Fenn_, 60, 90–112. Google Scholar  * McCracken, G F, and Selander, R K. 1980. Self-fertilization and monogenic strains in natural populations of terrestrial slugs. _Proc Natl Acad Sci USA_, 77, 684–688. Article  CAS  PubMed  PubMed Central  Google Scholar  * Mogie, M. 1986. Automixis: its distribution and status. _Biol J Linn Soc_, 28, 321–329. Article  Google Scholar  * Nei, M. 1972. Genetic distance between populations. _Am Nat_, 106, 283–292. Article  Google Scholar  * Nei, M. 1978. Estimation of average heterozygosity and genetic distance from a small number of individuals. _Genetics_, 89, 583–590. CAS  PubMed  PubMed Central  Google Scholar  * Nicklas, N L, and Hoffmann, R J. 1981. Apomictic parthenogenesis in a hermaphroditic terrestrial slug, _Deroceras laeve_ (Müller). _Biol Bull_, 160, 123–135. Article  Google Scholar  * Ota, T. 1993. _DISPAN: Genetic distance and phylogenetic analysis_, version 1.1. Pennsylvania State University, University Park, PA. Google Scholar  * Selander, R K, and Hudson, R O. 1976. Animal population structure under close inbreeding: the land snail _Rumina_ in southern France. _Am Nat_, 110, 695–718. Article  Google Scholar  * Selander, R K, and Kaufman, D W. 1973. Self-fertilization and genetic population structure in a colonizing land snail. _Proc Natl Acad Sci USA_, 70, 1186–1190. Article  CAS  PubMed  PubMed Central  Google Scholar  * Selander, R K, and Ochman, H. 1983. The genetic structure of populations as illustrated by molluscs. In: Rattazzi, M. C., Scandalios, J. C. Z. and Whitt, G. S. (eds) _Isozymes: Current Topics in Biological and Medical Research, vol 10: Genetics and Evolution_, pp. 93–123. Alan R. Liss, New York. Google Scholar  * Swofford, D L, and Selander, R B. 1981. BIOSYS-1: A FORTRAN program for the comprehensive analysis of electrophoretic data in population genetics and systematics. _J Hered_, 72, 281–283. Article  Google Scholar  * Tompa, A S. 1984. Land snails (Stylommatophora). In: Tompa, A. S., Verdonk, N. H. and Van Den Biggelaar, J. A. M. (eds) _The Mollusca, vol 7, Reproduction_, pp. 47–140. Academic Press, Orlando, FL. Google Scholar  * Waldén, H W. 1955. The land Gastropoda of the vicinity of Stockholm. _Ark Zool_, 7, 391–448. Google Scholar  Download references AUTHOR INFORMATION AUTHORS AND AFFILIATIONS * Malacology Section, Royal Belgian Institute of Natural Sciences, Vautierstraat 29, Brussels, B-1000 Thierry Backeljau * Department of Biology, University of Antwerp (RUCA), Groenenborgerlaan 171, Antwerp, B-2020, Belgium Luc de Bruyn, Hans de Wolf & Kurt Jordaens * Department of Biology, University of Antwerp (UIA), Universiteitsplein 1, Wilrijk, B-2610, Belgium Stefan van Dongen * Department of Biochemistry, University of Antwerp (UIA), Universiteitsplein 1, Wilrijk, B-2610, Belgium Birgitta Winnepenninckx Authors * Thierry Backeljau View author publications You can also search for this author inPubMed Google Scholar * Luc de Bruyn View author publications You can also search for this author inPubMed Google Scholar * Hans de Wolf View author publications You can also search for this author inPubMed Google Scholar * Kurt Jordaens View author publications You can also search for this author inPubMed Google Scholar * Stefan van Dongen View author publications You can also search for this author inPubMed Google Scholar * Birgitta Winnepenninckx View author publications You can also search for this author inPubMed Google Scholar CORRESPONDING AUTHOR Correspondence to Thierry Backeljau. RIGHTS AND PERMISSIONS Reprints and permissions ABOUT THIS ARTICLE CITE THIS ARTICLE Backeljau, T., de Bruyn, L., de Wolf, H. _et al._ Allozyme diversity in slugs of the _Carinarion_ complex (Mollusca, Pulmonata). _Heredity_ 78, 445–451 (1997). https://doi.org/10.1038/hdy.1997.68 Download citation * Received: 03 June 1996 * Issue Date: 01 April 1997 * DOI: https://doi.org/10.1038/hdy.1997.68 SHARE THIS ARTICLE Anyone you share the following link with will be able to read this content: Get shareable link Sorry, a shareable link is not currently available for this article. Copy to clipboard Provided by the Springer Nature SharedIt content-sharing initiative KEYWORDS * allozymes * hermaphroditic slugs * homozygous strains * population genetics * uniparental reproduction

ABSTRACT Previous allozyme analyses of the hermaphroditic terrestrial slugs _Arion fasciatus, A. circumscriptus_ and _A. silvaticus_ (subgenus _Carinarion_) have suggested that in North


America these species are each single monomorphic strains. However, new data on 18 putative enzyme loci show that in western Europe the three taxa, respectively, consist of at least three,


two and 12 homozygous multilocus genotypes (strains), which regularly co-occur. The current opinion that American and European _Carinarion_ populations are similarly structured, and that


colonization events did not affect the population genetics of North American _Carinarion_, should therefore be readdressed. The present data also provide the first indication of


heterozygosity and possible outcrossing in _Carinarion_. Nevertheless, uniparental reproduction is confirmed as the main breeding system in West European _Carinarion_, although the high


incidence of multistrain populations in _A. silvaticus_ and _A. fasciatus_ appears at variance with the current model of population genetic structuring in selfing terrestrial pulmonates.


Finally, the systematic status of the three _Carinarion_ spp. is tentatively questioned. SIMILAR CONTENT BEING VIEWED BY OTHERS INVESTIGATION OF GENETIC DIVERSITY AND POLYANDRY OF


_LEPTINOTARSA DECEMLINEATA_ USING X-LINKED MICROSATELLITE MARKERS Article Open access 11 December 2023 RETICULATE EVOLUTION IN THE _PTERIS FAURIEI_ GROUP (PTERIDACEAE) Article Open access 01


June 2022 EVOLUTIONARY HISTORY AND COLONIZATION PATTERNS OF THE WING DIMORPHIC GRASSHOPPER _DICHROPLUS VITTATUS_ IN TWO ARGENTINEAN BIOMES Article Open access 21 February 2022 ARTICLE PDF


REFERENCES * Armbruster, G, and Schlegel, M. 1994. The land-snail species of _Cochlicopa_ (Gastropoda: Pulmonata: Cochli-copidae): presentation of taxon-specific allozyme patterns, and


evidence for a high level of self-fertilization. _J Zool Syst Evol Res_, 32, 282–296. Article  Google Scholar  * Backeljau, T. 1987. Electrophoretic distinction between _Arion hortensis_,


_A. distinctus_ and _A. owenii_ (Mollusca: Pulmonata). _Zool Anz_, 219, 33–39. Google Scholar  * Backeljau, T, and De Bruyn, L. 1991. Preliminary report on the genetic variability of _Arion


intermedius_ in Europe (Pulmonata). _J Med Appl Malacol_, 3, 19–29. Google Scholar  * Backeljau, T, and De Winter, A J. 1987. An electrophoretic characterisation of three paratypes of _Arion


fagophilus_ De Winter, 1986, with notes on the subgeneric division of the genus _Arion_ Férussac, 1819 (Mollusca, Pulmonata). _Z Zool Syst Evolut-forsch_, 25, 169–180. Article  Google


Scholar  * Backeljau, T, Ahmadyar, S Z, Selens, M, Van Rompaey, J, and Verheyen, W. 1987. Comparative electrophoretic analyses of three European _Carinarion_ species (Mollusca, Pulmonata,


Arionidae). _Zool Scr_, 16, 209–222. Article  Google Scholar  * Backeljau, T, De Brito, C P, Tristā Da Cunha, R M, Frias Martins, A M, and De Bruyn, L. 1992. Colour polymorphism and genetic


strains in _Arion intermedius_ from Flores, Azores (Mollusca: Pulmonata). _Biol J Linn Soc_, 46, 131–143. Article  Google Scholar  * Baur, B, and Klemm, M. 1989. Absence of isozyme variation


in geographically isolated populations of the land snail _Chondrina clienta_. _Heredity_, 63, 239–244. Article  Google Scholar  * Chichester, L F, and Getz, L L. 1969. The zoogeography and


ecology of arionid and limacid slugs introduced into northeastern North America. _Malacologia_, 7, 313–346. Google Scholar  * Coyne, J A, Eanes, W F, Ramshaw, J A M, and Koehn, R K. 1979.


Electrophoretic heterogeneity of α-glycerophosphate dehydrogenase among many species of _Drosophila_. _Syst Zool_, 28, 164–175. Article  CAS  Google Scholar  * Dolan, S, and Fleming, C C.


1988. Isoenzymes in the identification and systematics of terrestrial slugs of the _Arion hortensis_ complex. _Biochem Syst Ecol_, 16, 195–198. Article  CAS  Google Scholar  * Foltz, D W,


Ochman, H, Jones, J S, Evangelisti, S M, and Selander, R K. 1982. Genetic population structure and breeding systems in arionid slugs (Mollusca: Pulmonata). _Biol J Linn. Soc._, 17, 225–241.


Article  Google Scholar  * Foltz, D W, Ochman, H, and Selander, R K. 1984. Genetic diversity and breeding systems in terrestrial slugs of the families Limacidae and Arionidae. _Malacologia_,


25, 593–605. Google Scholar  * Harris, H, and Hopkinson, D A. 1976. _Handbook of Enzyme Electrophoresis in Human Genetics_. Elsevier/North Holland Publishing Company, Amsterdam. Google


Scholar  * Hoffmann, R J. 1983. The mating system of the terrestrial slug _Deroceras laeve_. _Evolution_, 37, 423–425. Article  PubMed  Google Scholar  * Jarne, P, and Charlesworth, D. 1993.


The evolution of the selfing rate in functionally hermaphrodite plants and animals. _Ann Rev Ecol Syst_, 24, 441–466. Article  Google Scholar  * Jarne, P, and Städler, T. 1995. Population


genetic structure and mating system evolution in freshwater pulmonates. _Experientia_, 51, 482–497. Article  CAS  Google Scholar  * Kerney, M P, Cameron, R A D, and Jungbluth, J H. 1983.


_Die Landschnecken Nord- und Mitteleuropas_. Paul Parey, Hamburg. Google Scholar  * Lohmander, H. 1937. Ueber die nordischen Formen von _Arion circumscriptus_ Johnston. _Acta Soc Fauna Flora


Fenn_, 60, 90–112. Google Scholar  * McCracken, G F, and Selander, R K. 1980. Self-fertilization and monogenic strains in natural populations of terrestrial slugs. _Proc Natl Acad Sci USA_,


77, 684–688. Article  CAS  PubMed  PubMed Central  Google Scholar  * Mogie, M. 1986. Automixis: its distribution and status. _Biol J Linn Soc_, 28, 321–329. Article  Google Scholar  * Nei,


M. 1972. Genetic distance between populations. _Am Nat_, 106, 283–292. Article  Google Scholar  * Nei, M. 1978. Estimation of average heterozygosity and genetic distance from a small number


of individuals. _Genetics_, 89, 583–590. CAS  PubMed  PubMed Central  Google Scholar  * Nicklas, N L, and Hoffmann, R J. 1981. Apomictic parthenogenesis in a hermaphroditic terrestrial slug,


_Deroceras laeve_ (Müller). _Biol Bull_, 160, 123–135. Article  Google Scholar  * Ota, T. 1993. _DISPAN: Genetic distance and phylogenetic analysis_, version 1.1. Pennsylvania State


University, University Park, PA. Google Scholar  * Selander, R K, and Hudson, R O. 1976. Animal population structure under close inbreeding: the land snail _Rumina_ in southern France. _Am


Nat_, 110, 695–718. Article  Google Scholar  * Selander, R K, and Kaufman, D W. 1973. Self-fertilization and genetic population structure in a colonizing land snail. _Proc Natl Acad Sci


USA_, 70, 1186–1190. Article  CAS  PubMed  PubMed Central  Google Scholar  * Selander, R K, and Ochman, H. 1983. The genetic structure of populations as illustrated by molluscs. In:


Rattazzi, M. C., Scandalios, J. C. Z. and Whitt, G. S. (eds) _Isozymes: Current Topics in Biological and Medical Research, vol 10: Genetics and Evolution_, pp. 93–123. Alan R. Liss, New


York. Google Scholar  * Swofford, D L, and Selander, R B. 1981. BIOSYS-1: A FORTRAN program for the comprehensive analysis of electrophoretic data in population genetics and systematics. _J


Hered_, 72, 281–283. Article  Google Scholar  * Tompa, A S. 1984. Land snails (Stylommatophora). In: Tompa, A. S., Verdonk, N. H. and Van Den Biggelaar, J. A. M. (eds) _The Mollusca, vol 7,


Reproduction_, pp. 47–140. Academic Press, Orlando, FL. Google Scholar  * Waldén, H W. 1955. The land Gastropoda of the vicinity of Stockholm. _Ark Zool_, 7, 391–448. Google Scholar 


Download references AUTHOR INFORMATION AUTHORS AND AFFILIATIONS * Malacology Section, Royal Belgian Institute of Natural Sciences, Vautierstraat 29, Brussels, B-1000 Thierry Backeljau *


Department of Biology, University of Antwerp (RUCA), Groenenborgerlaan 171, Antwerp, B-2020, Belgium Luc de Bruyn, Hans de Wolf & Kurt Jordaens * Department of Biology, University of


Antwerp (UIA), Universiteitsplein 1, Wilrijk, B-2610, Belgium Stefan van Dongen * Department of Biochemistry, University of Antwerp (UIA), Universiteitsplein 1, Wilrijk, B-2610, Belgium


Birgitta Winnepenninckx Authors * Thierry Backeljau View author publications You can also search for this author inPubMed Google Scholar * Luc de Bruyn View author publications You can also


search for this author inPubMed Google Scholar * Hans de Wolf View author publications You can also search for this author inPubMed Google Scholar * Kurt Jordaens View author publications


You can also search for this author inPubMed Google Scholar * Stefan van Dongen View author publications You can also search for this author inPubMed Google Scholar * Birgitta Winnepenninckx


View author publications You can also search for this author inPubMed Google Scholar CORRESPONDING AUTHOR Correspondence to Thierry Backeljau. RIGHTS AND PERMISSIONS Reprints and


permissions ABOUT THIS ARTICLE CITE THIS ARTICLE Backeljau, T., de Bruyn, L., de Wolf, H. _et al._ Allozyme diversity in slugs of the _Carinarion_ complex (Mollusca, Pulmonata). _Heredity_


78, 445–451 (1997). https://doi.org/10.1038/hdy.1997.68 Download citation * Received: 03 June 1996 * Issue Date: 01 April 1997 * DOI: https://doi.org/10.1038/hdy.1997.68 SHARE THIS ARTICLE


Anyone you share the following link with will be able to read this content: Get shareable link Sorry, a shareable link is not currently available for this article. Copy to clipboard Provided


by the Springer Nature SharedIt content-sharing initiative KEYWORDS * allozymes * hermaphroditic slugs * homozygous strains * population genetics * uniparental reproduction