Dispersal constraints and fine-scale spatial genetic structure in two earthworm species

Biological Journal of the Linnean Society

Volumn 114, Issue 2, 2015, Pages 335-347

  Dupont, Lise ^a   Grésille, Ysoline ^a   Richard, Benoît ^b,c   Decaëns, Thibaud ^b,d   Mathieu, Jérôme ^e  

^a UNIVERSITÉ PARIS EST CRÉTEIL   (France)

^b UNIVERSITÉ DE ROUEN   (France)

^c Laboratoire BioSol   (France)

^d CENTRE D ECOLOGIE FONCTIONNELLE ET EVOLUTIVE   (France)

^e UPMC University Paris 06   (France)

Author keywords

Gene dispersal; Genetic clustering; Genetic diversity; Isolation by distance; Soil biodiversity; Soil properties

Indexed keywords

AUTOCORRELATION; BAYESIAN ANALYSIS; DISPERSAL; EARTHWORM; GENETIC ISOLATION; GENETIC STRUCTURE; POLYMORPHISM;

ALLOLOBOPHORA CHLOROTICA; APORRECTODEA ICTERICA;

EID: 84921457776     PISSN: 00244066     EISSN: 10958312     Source Type: Journal    
DOI: 10.1111/bij.12436     Document Type: Article

References (62)

1. Arnaud JF, Madec L, Guiller A, Bellido A. 2001. Spatial analysis of allozyme and microsatellite DNA polymorphisms in the land snail Helix aspersa (Gastropoda: Helicidae). Molecular Ecology 10: 1563-1576.
2. Belkhir K, Borsa P, Goudet J, Chikhi L, Bonhomme F. 2004. GENETIX 4.05, logiciel sous Windows pour la génétique des populations. Montpellier: Laboratoire Génome, Population, Interactions, CNRS UMR 5000, Université Montpellier II.
3. Benjamini Y, Hochberg Y. 1995. Controlling the false discovery rate - a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society Series B-Methodological 57: 289-300.
4. Bjorklund M, Bergek S, Ranta E, Kaitala V. 2010. The effect of local population dynamics on patterns of isolation by distance. Ecological Informatics 5: 167-172.
5. Bouché MB. 1977. Stratégies lombriciennes. In: Lohm U, Persson T, eds. Soil organisms as components of ecosystems. Stockholm: Ecological Bulletin, 122-132.
6. Cameron EK, Bayne EM, Coltman DW. 2008. Genetic structure of invasive earthworms Dendrobaena octaedra in the boreal forest of Alberta: insights into introduction mechanisms. Molecular Ecology 17: 1189-1197.
7. Capowiez Y, Rault M, Costagliola G, Mazzia C. 2005. Lethal and sublethal effects of imidacloprid on two earthworm species (Aporrectodea nocturna and Allolobophora icterica). Biology and Fertility of Soils 41: 135-143.
8. Caro G, Decaëns T, Lecarpentier C, Mathieu J. 2013. Are dispersal behaviours of earthworms related to their functional group? Soil Biology & Biochemistry 58: 181-187.
9. Carriconde F, Gryta H, Jargeat P, Mouhamadou B, Gardes M. 2008. High sexual reproduction and limited contemporary dispersal in the ectomycorrhizal fungus Tricholoma scalpturatum: new insights from population genetics and spatial autocorrelation analysis. Molecular Ecology 17: 4433-4445.
10. Casellato S. 1987. On polyploidy in oligochaetes with particular reference to Lumbricids. In: Bonvicini Pagliai AM, Omodeo P, eds. On Earthworms. Modena: Selected Symposia and Monographs U.Z.I, 75-87.
11. Clobert J. 2001. Dispersal. New York: Oxford University Press.
12. Costa D, Timmermans MJTN, Sousa JP, Ribeiro R, Roelofs D, Van Straalen NM. 2013. Genetic structure of soil invertebrate populations: collembolans, earthworms and isopods. Applied Soil Ecology 68: 61-66.
13. Dupont L, Lazrek F, Porco D, King RA, Rougerie R, Symondson WOC, Livet A, Richard B, Decaens T, Butt KR, Mathieu J. 2011. New insight into the genetic structure of the Allolobophora chlorotica aggregate in Europe using microsatellite and mitochondrial data. Pedobiologia 54: 217-224.
14. Edwards CA. 2004. The importance of earthworms as key representatives of the soil fauna. In: Edwards CA, ed. Earthworm ecology. Boca Raton, FL: CRC Press, 3-11.
15. Eijsackers H. 2011. Earthworms as colonizers of natural and cultivated soil environments. Applied Soil Ecology 50: 1-13.
16. El Mousadik A, Petit RJ. 1996. High level of genetic differentiation for allelic richness among populations of the argan tree [Argania spinosa (L.) Skeels] endemic to Morocco. Theoretical and Applied Genetics 92: 832-839.
17. Enckell PH, Niklasson M, Stille B, Douwes P. 1986. Insulation and isolation: factors influencing the genetic variation in Lumbricus rubellus Hoffm. (Lumbricidae) in the Faroe Islands. Hereditas 104: 263-271.
18. Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R. 1994. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology & Biotechnology 3: 294-299.
19. Frantz AC, Cellina S, Krier A, Schley L, Burke T. 2009. Using spatial Bayesian methods to determine the genetic structure of a continuously distributed population: clusters or isolation by distance? Journal of Applied Ecology 46: 493-505.
20. Goudet J. 2000. FSTAT, a program to estimate and test gene diversities and fixation indices. Version 2.9.1 ed: Available at: http://www.unil.ch/izea/softwares/fstat.html
21. Goudet J, Raymond M, deMeeus T, Rousset F. 1996. Testing differentiation in diploid populations. Genetics 144: 1933-1940.
22. Guillot G, Mortier F, Estoup A. 2005. Geneland : a program for landscape genetics. Molecular Ecology Notes 5: 712-715.
23. Hall TA. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41: 95-98.
24. Hardy OJ, Vekemans X. 1999. Isolation by distance in a continuous population: reconciliation between spatial autocorrelation analysis and population genetics models. Heredity 83: 145-154.
25. Hardy OJ, Vekemans X. 2002. SPAGEDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Molecular Ecology Notes 2: 618-620.
26. Holt RD. 2003. On the evolutionary ecology of species' ranges. Evolutionary Ecology Research 5: 159-178.
27. Joschko M, Gebbers R, Barkusky D, Timmer J. 2010. The apparent electrical conductivity as a surrogate variable for predicting earthworm abundances in tilled soils. Journal of Plant Nutrition and Soil Science 173: 584-590.
28. Kautenburger R. 2006. Genetic structure among earthworms (Lumbricus terrestris L.) from different sampling sites in western Germany based on random amplified polymorphic DNA. Pedobiologia 50: 257-266.
29. Kimura M. 1956. A model of genetic system which leads to closer linkage by natural selection. Evolution 10: 278-287.
30. King RA, Tibble AL, Symondson OC. 2008. Opening a can of worms: unprecedented sympatric cryptic diversity within British lumbricid earthworms. Molecular Ecology 17: 4694-4698.
31. Lardo E, Coll P, Le Cadre E, Palese AM, Villenave C, Xiloyannis C, Celano G. 2012. Electromagnetic induction (EMI) measurements as a proxy of earthworm presence in Southern French vineyards. Applied Soil Ecology 61: 76-84.
32. Leblois R, Estoup A, Rousset F. 2003. Influence of mutational and sampling factors on the estimation of demographic parameters in a 'Continuous' population under isolation by distance. Molecular Biology and Evolution 20: 491-502.
33. Legendre P, Legendre L. 1998. Numerical ecology, 2nd edn. Amsterdam, Boston, London, New York, San Francisco, Singapore, Sydney, Tockyo: Elsevier.
34. Lentzsch P, Golldack J. 2006. Genetic diversity of Aporrectodea caliginosa from agricultural sites in Northeast Brandenburg, Germany. Pedobiologia 50: 369-376.
35. Liiri M, Hasa M, Haimi J, Setala H. 2012. History of land-use intensity can modify the relationship between functional complexity of the soil fauna and soil ecosystem services - a microcosm study. Applied Soil Ecology 55: 53-61.
36. Lowe CN, Butt KR. 2007. Life-cycle traits of the dimorphic earthworm species Allolobophora chlorotica (Savigny, 1826) under controlled laboratory conditions. Biology and Fertility of Soils 43: 495-499.
37. Lowe CN, Butt KR. 2008. Allolobophora chlorotica (Savigny, 1826): evidence for classification as two separate species. Pedobiologia 52: 81-84.
38. Marinissen JCY, Vandenbosch F. 1992. Colonization of new habitats by Earthworms. Oecologia 91: 371-376.
39. Mathieu J, Barot S, Blouin M, Caro G, Decaens T, Dubs F, Dupont L, Jouquet P, Nai P. 2010. Habitat quality, conspecific density, and habitat pre-use affect the dispersal behaviour of two earthworm species, Aporrectodea icterica and Dendrobaena veneta, in a mesocosm experiment. Soil Biology and Biochemistry 42: 203-209.
40. Novo M, Almodovar A, Fernandez R, Gutierrez M, Cosin DJD. 2010a. Mate choice of an endogeic earthworm revealed by microsatellite markers. Pedobiologia 53: 375-379.
41. Novo M, Almodovar A, Fernandez R, Trigo D, Cosin DJD. 2010b. Cryptic speciation of hormogastrid earthworms revealed by mitochondrial and nuclear data. Molecular Phylogenetics and Evolution 56: 507-512.
42. Novo M, Almodóvar A, Díaz-Cosín DJ. 2009. High genetic divergence of hormogastrid earthworms (Annelida, Oligochaeta) in the central Iberian Peninsula: evolutionary and demographic implications. Zoologica Scripta 38: 537-552.
43. Ohta T. 1982. Linkage disequilibrium due to random genetic drift in finite subdivided populations. Proceedings of the National Academy of Sciences of the United States of America 79: 1940-1944.
44. Ohta T, Kimura M. 1969. Linkage disequilibrium due to random genetic drift. Genetical Research 13: 47-55.
45. Papadopoulos NG, Tsokas GN, Dabas M, Yi MJ, Kim JH, Tsourlos P. 2009. Three-dimensional inversion of automatic resistivity profiling data. Archaeological Prospection 16: 267-278.
46. Perry W, Lugo R, Hathaway SA, Vandergast AG. 2010. Genetic Landscapes GIS Toolbox: tools to create genetic divergence and diversity landscapes in ArcGIS [Computer Software]. V.1. 1 ed. Sacramento, CA: U.S. Geological Survey Western Ecological Research Center, June 15, 2010. Using: ArcGIS [software]. Version 9.3.1. Redlands, CA: Environmental Systems Research Institute, Inc., 1982-2009.
47. Prasankok P, Bantaowong U, James SW, Panha S. 2013. Low heterogeneity in populations of the terrestrial earthworm, Metaphire peguana (Rosa, 1890), in Thailand, as revealed by analysis of mitochondrial DNA COI sequences and nuclear allozymes. Biochemical Systematics and Ecology 51: 8-15.
48. Richard B, Legras M, Margerie P, Mathieu J, Barot S, Caro G, Desjardins T, Dubs F, Dupont L, Decaëns T. 2012. Spatial organization of earthworm assemblages in pastures of northwestern France. European Journal of Soil Biology 53: 62-69.
49. Robertson A, Hill WG. 1984. Deviations from Hardy-Weinberg proportions: sampling variances and use in estimation of inbreeding coefficients. Genetics 107: 703-718.
50. Rousset F. 2000. Genetic differentiation between individuals. Journal of Evolutionary Biology 13: 58-62.
51. Rousset F. 2008. GENEPOP ' 007: a complete re-implementation of the GENEPOP software for Windows and Linux. Molecular Ecology 8: 103-106.
52. Sims RW, Gerard BM. 1999. Synopsis of the British Fauna (31)- earthworms. London: The Linnean Society of London and the Estuarine and Brackish-water Sciences Association, 1-169.
53. Sullivan TJ, Dreyer AP, Peterson JW. 2009. Genetic variation in a subterranean arthropod (Folsomia candida) as a method to identify low-permeability barriers in an aquifer. Pedobiologia 53: 99-105.
54. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. 2013. MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30: 2725-2729.
55. Torres-Leguizamon M, Mathieu J, Decaëns T, Dupont L. 2014. Genetic structure of earthworm populations at a regional scale: inferences from mitochondrial and microsatellite molecular markers in Aporrectodea icterica (Savigny 1826). PLoS ONE 9: e101597.
56. Torres-Leguizamon M, Mathieu J, Livet A, Dupont L. 2012. Isolation of polymorphic microsatellite markers in Aporrectodea icterica (Savigny 1826). Soil Biology & Biochemistry 51: 16-19.
57. Valckx J, Cockx L, Wauters J, Van Meirvenne M, Govers G, Hermy M, Muys B. 2009. Within-field spatial distribution of earthworm populations related to species interactions and soil apparent electrical conductivity. Applied Soil Ecology 41: 315-328.
58. Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P. 2004. MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes 4: 535-538.
59. Weir BS, Cockerham CC. 1984. Estimating F-statistics for the analysis of population structure. Evolution 38: 1358-1370.
60. Wilson AG, Arcese P, Chan YL, Patten MA. 2011. Micro-spatial genetic structure in song sparrows (Melospiza melodia). Conservation Genetics 12: 213-222.
61. Wright S. 1943. Isolation by distance. Genetics 28: 114-138.
62. Wright S. 1946. Isolation by distance under diverse systems of mating. Genetics 31: 39-59.