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  • III — Méthodes D’inventaire et de Caractérisation de la Diversité Génétique en Milieu Naturel / Methods for Inventory and Characterization of Genetic Diversity in Natural Environment
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Setting conservation priorities: the case study of Carabus solieri (Col. Carabidae)

Choix des priorités de conservation: le cas de Carabus solieri (Col. Carabidae)

Genetics Selection Evolution volume 33, Article number: S141 (2001) Cite this article

Abstract

C. solieri is an endangered species of Carabidae which is mostly associated with humid forests of the Alps, in Prance and in Liguria (Italy). We reanalysed morphological data published by Bonadona and compared the results to the molecular data set presented here. We used partial sequences of the mitochondrial cytochrome b gene and seven microsatellite loci to evaluate genetic diversity among and between populations and to propose a phylogeographic scenario. We recognised two basic entities, considered as subspecies, which probably colonised the present distribution range from two main refugia (in France and in Italy). There is no strict agreement between morphological and molecular data and we propose that hybridisation and introgres-sion between the two subspecies have led to the observed patterns of distribution of the characters. Our results show that sampled populations differ significantly in microsatellite allele frequencies even though some populations are < 15 km apart. Gene flow estimates between the 19 sampled populations indicated very restricted exchange. This is in agreement with the low vagility observed for most species of Carabus. Consequently, the Solier’s Carab is genetically structured on an extremely fine scale, and local population within a definite forest should be considered as management units. In the light of our data on C. solieri we discuss the usefulness, when hybridisation occurs, of the two main criteria usually quoted for identifying candidate populations for conservation management (uniqueness and diversity) and give some conservation recommendations for C. solieri.

Résumé

C. solieri est une espèce de Carabidae en danger d’extinction. Cette espèce est principalement associée aux forêts humides des Alpes frangaises et liguriennes (Italië). Nous réanalysons les données morphologiques publiées par Bonadona et comparons les résultats a ceux obtenus a partir des données géné-tiques présentées ici. Nous utilisons des séquences partielles du gêne du cytochrome b et sept loei microsatellites pour mesurer la diversité génétique au sein et entre les 19 populations échantillonnées et pour proposer un scénario phylogéographique. Nous reconnaissons deux entités de base, considérées comme sous-espèces, qui ont proba-blement colonisé l’actuelle aire de distribution a partir de deux refuges glaciaires (en France et en Italië). Il n’existe pas de congruence stricte entre les données morphologiques et moléculaires, et nous proposons l’hybridation et l’introgression entre les sous-espèces comme facteurs expliquant le patron de distribution des caractères observé. Nos résultats montrent que les populations étudiées différent significative-ment par leurs fréquences alléliques, même pour des populations séparées par moins de 15 kilomètres. Les estimations de flux génique entre les populations indiquent un faible niveau d’échange. Ceci est en accord avec la faible vagilité observée chez la plupart des espèces de Carabus. En conséquence le Carabe de Solier est génétique-ment structuré a une tres fine échelle, en conséquence toute population associée a un bloc forestier peut être considérée comme une unité de gestion. Nos résultats sur C. solieri, et en particulier la mise en évidence de l’introgression mitochondriale, nous amènent a discuter les deux principales methodes (originalité et diversité) utilisées couramment pour identifier les populations susceptibles d’être protégées. Enfin nous donnons quelques considérations générales sur les mesures de protection pouvant être prises.

References

  1. Allemand R., Malausa J.C., Compatibilité génétique et distances phylétiques entre les espèces du genre Chrysocarabus Thomson (Col., Carabidae), Ann. Soc. Entomologique de Prance 20 (1984) 247–263.

    Google Scholar 

  2. Allendorf F.W., Genetic drift and the loss of alleles versus heterozygosity, Zoo Biology 5 (1986) 181–190.

    Google Scholar 

  3. Allendorf F.W., Leary R.F., Heterozygosity and fitness in natural populations of animals, in: Soulé M.E. (Ed.), Conservation biology. The Science of scarcity and diversity, Sinauer Associates, Sunderland, 1986, pp. 57–75.

    Google Scholar 

  4. Amato G., Gatesy J., Brazaitis P., PCR assays of variable nucleotide sites for identification of conservation units: an example from Caiman, in: De-Salle R., Schierwater B. (Eds.), Molecular approaches to ecology and evolution, Birkhaüser Verlag, Basel, 1998, pp. 177–190.

    Google Scholar 

  5. Arnold M.L., Bulger M.R., Burke J.M., Hempel A.L., Willimas J.H., Natural hybridization: How low can you go and still be important?, Ecology 80 (1999) 371–381.

    Google Scholar 

  6. Arnold M.L., Emms S.K., Paradigm lost. Natural hybridization and evolutionary innovations, in: Howard D.J., Berlocher S.H. (Eds.), Endless Forms, Oxford University Press, Oxford, 1998, pp. 379–389.

    Google Scholar 

  7. Aubert J., Barascud B., Descimon H., Michel F., Ecology and genetics of interspecific hybridization in the swallowtails, Papilio hospiton Géné and P. machaon L., in Corsica (Lepidoptera: Papilionidae), Biological Journal of the Linnean Society 60 (1997) 467–492.

    Google Scholar 

  8. Avise J.C., Molecular markers, natural history, and evolution, Chapman and Hall, New York, 1994.

    Book  Google Scholar 

  9. Bar low G.W., The relevance of behavior and natural history to evolutionarily significant units, in: Nielsen J.L. (Ed.), Evolution and the aquatic ecosystem: Defïning units in population conservation, American Fisheries Society Symposium 17, Bethesda, 1995, pp. 169–175.

    Google Scholar 

  10. Barrowclough G.F., Flesness N.R., Species, subpecies, and races: the problem of units of management in conservation, in: Kleinman G.G., Allen L., Harris H. (Eds.), Wild Animal in Captivity, University of Chicago Press, Chicago, 1996, pp. 247–254.

    Google Scholar 

  11. Barton N.H., Hewitt G.M., Analysis of hybrid zones, Ann. Rev. Ecol. Syst. (1985) 113–148.

    Google Scholar 

  12. Barton N.H., Hewitt G.M., A chromosomal cline in the grasshopper Podisma terrestris, Evolution 35 (1981) 1008–1018.

    CAS  Google Scholar 

  13. Bonadona P., Caractères distinctifs des races frangaises de C. solieri Dejean, Entomops 7 (1967) 202–223.

    Google Scholar 

  14. Bonadona P., Nouvelle contribution a la connaissance des races frangaises de Chrysocarabus solieri (Col. Carabidae), Annales de la Société Entomologique de France (N.S) 9 (1973) 759–812.

    Google Scholar 

  15. Brower A.V.Z., Rapid morphological radiation and convergence among races of the butterfly Heliconius erato inferred from patterns of mitochondrial DNA evolution, Proc. Nat. Acad. Sci. USA 76 (1994) 1967–1971.

    Google Scholar 

  16. Bullini L., Origin and evolution of animal hybrid species, Trends Ecol. Evolut. 9 (1994) 422–426.

    Article  CAS  Google Scholar 

  17. Casale A., Cavazzuti P.F., Sul Carabus (Chrysocarabus) solieri Dejean in Italia (Col. Carabidae): Sistematics, corologia, ecologia, Boll. Ist. Entomologia della Universita di Bologna 32 (1975) 231–255.

    Google Scholar 

  18. Cavalli-Sforza L.L., Edwards A.W.F., Phylogenetics analysis: Models and estimation procedures, Am. J. Hum. Genet. 19 (1967) 233–257.

    CAS  Google Scholar 

  19. Clarke G.M., O’Dwyer C., Genetic variability and population structure of the endangered golden sun moth, Synemon plana, Biol. Conservation 92 (2000) 371–381.

    Google Scholar 

  20. Cracraft J., Speciation and ontology: The empirical consequences of alternative species concepts for understanding patterns and processes of differentiation, in: Otte D., Endier J.A. (Eds.), Speciation and its consequences, Sinauer Associates, Sunderland, 1989, pp. 28–57.

    Google Scholar 

  21. Cracraft J., Species concepts in systematics and conservation biology - an ornithology viewpoint, in: Claridge M.F., Dawah H.A., Wilson M.R. (Eds.), Species: The units of biodiversity, Chapman and Hall, New York, 1997, pp. 325–340.

    Google Scholar 

  22. De Jong H., In search of historical biogeographic patterns in the western Mediterranean terrestrial fauna, Biol. J. Linnean Soc. 65 (1998) 99–164.

    Google Scholar 

  23. DeMarais B.D., Dowling T.E., Douglas M.E., Minckley W.L., Marsh P.C., Origin of Gila seminuda (Teleostei: Cyprinidae) through introgressive hybridization: Implications for evolution and conservation, Proc. Nat. Acad. Sci. USA 89 (1992) 2747–2751.

    CAS  PubMed  Google Scholar 

  24. den Boer P.J., On the dispersal power of carabid beetles and its possible significance, Landbouwhogeschool Miscellenous Papers 8 (1971) 119–137.

    Google Scholar 

  25. Deuve T., Une classification du genre Carabus, Bibliotheque Entomologique, Venette 5 (1994) 1–296.

    Google Scholar 

  26. Dizon A.E., Lockyer C, Perrin W.F., Demaster D.P., Sisson J., Rethinking the stock concept: A phylogenetic approach, Conserv. Biol. 6 (1992) 24–36.

    Google Scholar 

  27. Dowling T.E., Secor C.L., The role of hybridization and introgression in the diversification of animals, Annu. Rev. Ecol. Syst. 28 (1997) 593–619.

    Article  Google Scholar 

  28. Dujardin F., Bellon J., Mise au point concernant la nomenclature de certains taxa de D. solieri Dejean, Entomops 22 (1971) 195–198.

    Google Scholar 

  29. El Mousadik A., Petit R.J., High level of genetic differentiation for allelic richness among populations of the argan tree [Argania spinosa (L.), Skeels] endemic to Morocco, Theor. Applied Genetics 92 (1996) 832–839.

    Google Scholar 

  30. Estoup A., Solignac M., Harry M., Cornuet J.M., Characterization of (GT)n and (CT)n microsatellites in two insect species: Apis mellifera and Bombus terrestris, Nucleic Acids Res. 21 (1993) 1427–1431.

    CAS  PubMed  Google Scholar 

  31. Felsenstein J., PHYLIP (Phylogenetic Inference Package), version 3.5c, ed., Departement of Genetics, University of Washington, Seattle, 1993.

    Google Scholar 

  32. Fuerst P.A., Maruyama T., Considerations on the conservation of alleles and of genie heterozygosity in small managed populations, Zoo Biology 5 (1986) 171–179.

    Google Scholar 

  33. Gaggiotti O.E., Lange O., Rassmann K., Gliddons C., A comparison of two indirect methods for a estimating average levels of gene flow using microsatellite data, Mol. Ecol. 8 (1999) 1513–1520.

    CAS  Google Scholar 

  34. Goldstein P.Z., DeSalle R., Amato G., Vogler A.P., Conservation genetics at the species boundary, Conserv. Biol. 14 (2000) 120–131.

    Article  Google Scholar 

  35. Grant B.R., Grant P.R., High survival of Darwin’s finch hybrids: Effect of beak morphology and diets, Ecology 77 (1996) 500–509.

    Google Scholar 

  36. Haig S.M., Molecular contributions to conservation, Ecology 79 (1998) 413–425.

    Google Scholar 

  37. Harry M., Solignac M., Lachaise D., Molecular evidence for multiple homoplasies of complex adaptative syndromes in fig-breeding Lissocephala (Drosophilidae), Mol. Phylogenet. Evol. 9 (1998) 542–551.

    CAS  Google Scholar 

  38. Hewitt G.M., Post-glacial re-colonization of European biota, Biol. J. Linnean Soc. 68 (1999) 86–112.

    Google Scholar 

  39. Hoole J.C., Joyce D.A., Pullin A.S., Estimate of gene flow between populations of the swallowtail butterfly, Papilio in Broadland, UK and implications for conservation, Biological Conservation 89 (1999) 293–299.

    Google Scholar 

  40. Hurlbert S.H., The nonconcept of species diversity: A critique and alternative parameters, Ecology 52 (1971) 577–586.

    PubMed  Google Scholar 

  41. Jermiin L.S., Crozier R.H., The cytochrome b region in the mitochondrial DNA of the ant Tetraponera rufonige, sequence divergence in Hymenoptera may be associated with nucleotide contents, J. Mol. Evol. 38 (1994) 282–294.

    CAS  Google Scholar 

  42. Juan C, Oromi P., Hewitt G.M., Mitochondrial DNA phylogeny and sequential colonization of Canary islands by darkling beetles of the genus Pimelia (Tenebrionidae), Proc. R. Soc. Lond. [Biol.] 261 (1995) 173–180.

    CAS  Google Scholar 

  43. Kimura M., A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences, J. Mol. Evol. 16 (1980) 111–120.

    CAS  PubMed  Google Scholar 

  44. Kumar S., Tamura K., Nei M., MEGA: Molecular evolutionary genetic analysis., 1.01 ed., Pensylvania State University, University Park, 1993.

    Google Scholar 

  45. Lande R., Genetics and demography in biological conservation, Science 41 (1988) 1455–1460.

    Google Scholar 

  46. Largiadèr C.R., Klingenberg C.P., Zimmermann M., Morphometric variation in a hybrid zone of two subspecies of Gerris costae (Heteroptera: Gerridae) in the Maritime Alps, J. Evolutionary Biology 7 (1994) 697–712.

    Google Scholar 

  47. Leberg P.L., Effects of population bottlenecks on genetic diversity as measured by allozyme electrophoresis, Evolution 46 (1992) 477–494.

    PubMed  Google Scholar 

  48. Legge J.T., Roush R., DeSalle R., Vogler A.P., May B., Genetic criteria for establishing evolutionarily significant units in Cryan’s buckmoth, Conservation Biology 7 (1996) 856–865.

    Google Scholar 

  49. Malausa J.C., État actuel des connaissances sur l’hybridation des espèces du genre Chrysocarabus Thomson (Coleoptera, Carabidae), Buil. mensuel de la Société Linnéenne de Lyon 51 (1982) 41–47.

    Google Scholar 

  50. Malausa J.C., Drescher J., Elevage et acclimatation de Carabes; un exemple d’action pour la protection d’un groupe tres collectionné, Cahiers de liaison de TOPIE 21 (1987) 67–79.

    Google Scholar 

  51. Malausa J.C., Raviglione M., Boggio F., Il Carabus olympiae Sella dell’Alta Valle Sessera, ed., Pro Natura Biellese, 1983.

    Google Scholar 

  52. Médail F., Verlaque R., Ecological characteristics and rarity of endemic plants of southeast France and Corsica: Implications for biodiversity conservation, Biol. Conservation 80 (1997) 269–271.

    Google Scholar 

  53. Moritz C., Defining “Evolutionarily Significant Units” for conservation, Trends Ecol. Evolut. 9 (1994) 373–375.

    CAS  Google Scholar 

  54. Mossakowski D., Braun S., Roschen A., Hybridization in natural populations of ground beetles (Coleoptera, Carabidae), Can. J. Zool. 68 (1990) 1783–1789.

    Google Scholar 

  55. Nei M., Molecular Evolutionary Genetics, ed., Columbia University Press, New York, 1987.

    Google Scholar 

  56. Paetkau D., Using genetics to identify intraspecific conservation units: A critique of current methods, Conserv. Biol. 13 (1999) 1507–1509.

    Google Scholar 

  57. Petit R.J., El Mousadik A., Pons O., Identifying populations for conservation on the basis of genetic markers, Conserv. Biol. 12 (1998) 844–855.

    Google Scholar 

  58. Porter A.H., Wenger R., Geiger H., Scholl A., Shapiro A.M., The Pontia daplidice-edusa hybrid zone in northwestern Italy, Evolution 51 (1997) 1561–1573.

    Google Scholar 

  59. Prunier D., Marcilhac J., Réflexions sur Chrysocarabus solieri Dejean 1.- Étude du secteur situé au Sud du fleuve Var (Coleoptera Carabidae), L’Entomologiste 45 (1989) 15–22.

    Google Scholar 

  60. Prüser F., Mossakowski F., Low substitution rates in mitochondrial DNA in Mediterranean carib beetles, Insect Mol. Biol. 7 (1998) 121–128.

    Google Scholar 

  61. Rasplus J.Y., Meusnier S., Mondor G., Pyri S., Cornuet J.M., Microsatellite analysis of genetic population structure in the endangered Carabid: Carabus solieri (Carabidae), in: Brandmayr P., Casale A., Lövei G., Taglianti V. (Eds.), Natural History and Applied Ecology of Carabid Beetles. Proceedings of the IX European Carabidologists Meeting, Universita di Calabria, Coscenza (2001) (in press).

    Google Scholar 

  62. Raymond M., Rousset F., GENEPOP (version 1.2): Population genetics software for exact tests and ecumenism, J. Hered. 86 (1995) 248–249.

    Google Scholar 

  63. Rhymer J.M., Simberloff D., Extinction by hybridization and introgression, Ann. Rev. Ecol. Syst. 27 (1996) 83–109.

    Article  Google Scholar 

  64. Ryder O., Species conservation and systematics: The dilemma of subspecies, Trends Ecol. Evolut. 1 (1986) 9–10.

    Google Scholar 

  65. Saccheri L., Kuussaari M., Kankare M., Vikman P., Forteliust W., Hanski I., Inbreeding and extinction in a butterfly metapopulation, Nature 392 (1998) 491–494.

    CAS  Google Scholar 

  66. Saitou N., Nei M., The neighbor-joining method: A new method for reconstruct-ing phylogenetic trees, Mol. Biol. Evol. 4 (1987) 406–425.

    CAS  PubMed  Google Scholar 

  67. Sambrook J., Fritsch E.F., Maniatis T., Molecular cloning: A laboratory manual, 2nd edition, ed., Cold Spring Harbor Laboratory Press, New York, 1989.

    Google Scholar 

  68. Scribner K.T., Hybrid zone dynamics are infmenced by genotypic-specific vari-ation in life-history traits: Experimental evidence from hybridizing Gambusia species, Evolution 47 (1993) 632–646.

    Google Scholar 

  69. Sneath P.H.A., Sokal R.R., Numerical Taxonomy, ed., Freeman and Co., San Francisco, 1973.

    Google Scholar 

  70. Sperling F.A.H., Harrison R.G., Mitochondrial DNA variation within and be-tween species of the Papilio machaon group of swallowtail butterflies, Evolution 48 (1994) 408–422.

    Google Scholar 

  71. Stauffer J.R.J., Bowers N.J., McKaye K.R., Kocher T.D., Evolutionarily significant units among cichlid fishes: the role of behavioral studies, in: Nielsen J.L. (Ed.), Evolution and the aquatic ecosystem: Defining units in population conservation, American Fisheries Society Symposium 17, Bethesda, 1995, pp. 227–244.

    Google Scholar 

  72. Storfer A., Quantitative genetics: A promising approach for the assessment of genetic diversity in endangered species, Trends Ecol. Evolut. 11 (1996) 343–348.

    CAS  Google Scholar 

  73. Strimmer K., Von Haeseler A., Puzzle 4.0: Maximum likelihood analysis for nucleotide and amino acid alignments, 4.0 ed., Zoologisches Institut, Universitaet Muenchen, Muenchen, Germany, 1997.

    Google Scholar 

  74. Syzmura J.M., Lunt D.H., Hewitt G.M., The sequence and structure of the meadow grasshopper (Chorthippus parallelus) mitochondrial 12s TRNA, ND2, COI, COII, ATPase8 and tRNA genes, Insect Mol. Biol. 5 (1996) 127–139.

    Google Scholar 

  75. Taberlet P., Fumagali L., Wust-Saucy A.G., Cosson J.F., Comparative phylo-geography and post-glacial colonization routes in Europe, Mol. Ecol. 7 (1998) 453–464.

    CAS  Google Scholar 

  76. Takezaki N., Nei M., Genetic distances and reconstruction of phylogenetic trees from microsatellite DNA, Genetics 144 (1996) 389–399.

    CAS  PubMed  Google Scholar 

  77. Tarrier M., Essai d’une hiërarchie objective et raisonnée de Carabus (Dysmictocarabus) solieri Dejean. Contribution a la connaissance de Carabus (Dysmictocarabus) solieri Dej., VIII, Carabologia 2 (1975) 65–75.

    Google Scholar 

  78. Thompson J.D., Higgins D.G., Gibson T.J., CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice, Nucleic Acids Res. 22 (1994) 4673–4680.

    CAS  PubMed  Google Scholar 

  79. Turin H., Casale A., Kryzhanouskij O.L., Makarov K.V., Penev L.D., Checklist and atlas of the genus Carabus Linnaeus in Europe (Coleoptera, Carabidae), ed., Backhuys, Universal Book Service, Leiden, 1993.

    Google Scholar 

  80. Vogel J.C., Rumsey F.J., Schneller J.J., Barrett J.A., Gibby M., Where are the glacial refugia in Europe? Evidence from pterydophytes, Biol. J. Linnean Soc. 66 (1999) 23–37.

    Google Scholar 

  81. Vogler A.P., Extinction and the evolutionary process in endangered species: What to conserve?, in: DeSalle R., Schierwater B. (Eds.), Molecular approaches to ecology and evolution, Birkhaüser Verlag, Basel, 1998, pp. 191–210.

    Google Scholar 

  82. Vogler A.P., DeSalle R., Diagnosing units of conservation management, Conserv. Biol. (1994) 354–363.

    Google Scholar 

  83. Waples R.S., Pacific salmon, Onchorhynchus spp., and the defmition of species under the Endangered Species Act, Marine Fisheries Reviews 53 (1991) 11–22.

    Google Scholar 

  84. Weir B.S., Cockerham C.C., Estimating F-statistic for the analysis of population structure, Evolution 38 (1984) 1358–1370.

    CAS  Google Scholar 

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  1. Institut national de la Recherche agronomique, Centre de gestion et de biologie des populations, Campus International de Baillarguet, CS 30 016, 34988, Montferrier-sur-Lez Cedex, France

    Jean-Yves Rasplus, Stéphane Garnier, Serge Meusnier, Silvain Piry, Guénaëlle Mondor, Philippe Audiot & Jean-Marie Cornuet

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  1. Jean-Yves Rasplus
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Rasplus, JY., Garnier, S., Meusnier, S. et al. Setting conservation priorities: the case study of Carabus solieri (Col. Carabidae). Genet Sel Evol 33 (Suppl 1), S141 (2001). https://doi.org/10.1186/BF03500878

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Genetics Selection Evolution

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