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Application of Molecular Genetics to Earthworm Ecology: Current Research and Promising Future Directions

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Biology of Earthworms

Part of the book series: Soil Biology ((SOILBIOL,volume 24))

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Abstract

In earthworm ecology, the use of molecular tools has been restricted to certain fields such as ecotoxicology. In this chapter, we highlight two key issues of earthworm ecology that would greatly benefit from molecular information: dispersal behaviour and reproductive strategies. Elucidating patterns of dispersal is fundamental in guiding our understanding of earthworms’ distribution in both time and space. Field methods traditionally employed for measuring dispersal are difficult to use in species hidden in the soil, such as earthworms. Alternatively, genetic tools allow assessing dispersal from the detailed analysis of the genetic structure within and among populations. Besides, a good understanding of the mating strategy is essential to interpret population genetic patterns, particularly in species that present a great diversity of reproductive modes such as earthworms. After a short presentation of available genetic markers for earthworm genetics and a summary of the recent advances in molecular taxonomy of earthworms, current research in earthworm dispersal and mating behaviour are presented and the interest of using molecular markers for genetic inference is discussed.

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References

  • Angeloni L, Bradbury JW, Burton RS (2003) Multiple mating, paternity, and body size in a simultaneous hermaphrodite, Amplysia californica. Behav Ecol 14:554–560

    Article  Google Scholar 

  • Anthes N, Putz A, Michiels NK (2006) Sex role preferences, gender conflict and sperm trading in simultaneous hermaphrodites: a new framework. Anim Behav 72:1–12

    Article  Google Scholar 

  • Avise JC (1994) Molecular markers, natural history and evolution. Chapman and Hall, New York

    Google Scholar 

  • Avise JC (2000) Phylogeography: the history and formation of species. Harvard University Press, Cambridge, MA

    Google Scholar 

  • Avise JC (2004) Molecular markers, natural history and evolution, 2nd edn. Sinauer Associates, Sunderland, MA

    Google Scholar 

  • Avise JC, Jones AG, Walker D, DeWoody JA (2002) Genetic mating systems and reproductive natural histories of fishes: lessons for ecology and evolution. Annu Rev Genet 36:19–45

    Article  CAS  PubMed  Google Scholar 

  • Berry O, Tocher MD, Sarre SD (2004) Can assignment tests measure dispersal? Mol Ecol 13:551–561

    Article  PubMed  Google Scholar 

  • Beukeboom LW, Sharbel TF, Michiels NK (1998) Reproductive modes, ploidy distribution, and supernumerary chromosome frequencies of the flatworm Polycelis nigra (Platyhelminthes: Tricladida). Hydrobiologia 383:277–285

    Article  Google Scholar 

  • Birkhead TR, Möller AP (1998) Sperm competition and sexual selection. Academic, San Diego, CA

    Google Scholar 

  • Blouin MS (2003) DNA-based methods for pedigree reconstruction and kinship analysis in natural populations. Trends Ecol Evol 18:503–511

    Article  Google Scholar 

  • Bohonak AJ (1999) Dispersal, gene flow, and population structure. Q Rev Biol 74:23–45

    Article  Google Scholar 

  • Bretman A, Wedell N, Tregenza T (2004) Molecular evidence of post-copulatory inbreeding avoidance in the field cricket Gryllus bimaculatus. Proc R Soc Lond B Biol Sci 271:159–164

    Article  CAS  Google Scholar 

  • Broquet T, Petit EJ (2009) Molecular estimation of dispersal for ecology and population genetics. Annu Rev Ecol Evol Syst 40:193–216

    Article  Google Scholar 

  • Butt KR, Nuutinen V (1998) Reproduction of the earthworm Lumbricus terrestris Linne after the first mating. Can J Zool 76:104–109

    Article  Google Scholar 

  • Cameron EK, Bayne EM, Coltman DW (2008) Genetic structure of invasive earthworms Dendrobaena octaedra in the boreal forest of Alberta: insights into introduction mechanisms. Mol Ecol 17:1189–1197

    Article  CAS  PubMed  Google Scholar 

  • Cannavacciuolo M, Bellido A, Cluzeau D, Gascuel C, Trehen P (1998) A geostatistical approach to the study of earthworm distribution in grassland. Appl Soil Ecol 9:345–349

    Article  Google Scholar 

  • Chang CH, Chen JH (2005) Taxonomic status and intraspecific phylogeography of two sibling species of Metaphire (Oligochaeta: Megascolecidae) in Taiwan. Pedobiologia 49:591–600

    Article  Google Scholar 

  • Chang CH, Lin YH, Chen IH, Chuang SC, Chen JH (2007) Taxonomic re-evaluation of the Taiwanese montane earthworm Amynthas wulinensis Tsai, Shen & Tsai, 2001 (Oligochaeta: Megascolecidae): polytypic species or species complex? Org Divers Evol 7:231–240

    Article  Google Scholar 

  • Chang CH, Rougerie R, Chen J-H (2009) Identifying earthworms through DNA barcodes: pitfalls and promise. Pedobiologia 52:171–180

    Article  CAS  Google Scholar 

  • Charlesworth D (2003) Effects of inbreeding on the genetic diversity of populations. Philos Trans R Soc Lond B Biol Sci 358:1051–1070

    Article  CAS  PubMed  Google Scholar 

  • Charlesworth D, Charlesworth B (1987) Inbreeding depression and its evolutionary consequences. Annu Rev Ecol Syst 18:237–268

    Article  Google Scholar 

  • Charlesworth B, Charlesworth D (1999) The genetic basis of inbreeding depression. Genet Res 74:329–340

    Article  CAS  PubMed  Google Scholar 

  • Charlesworth B, Morgan MT, Charlesworth D (1993) The effect of deleterious mutations on neutral molecular variation. Genetics 134:1289–1303

    CAS  PubMed  Google Scholar 

  • Charnov EL (1979) Simultaneous hermaphroditism and sexual selection. Proc Natl Acad Sci USA 76:2480–2484

    Article  CAS  PubMed  Google Scholar 

  • Ciofi C, Funk SM, Coote T et al (1998) Genotyping with microsatellite loci. In: Karp A, Isaac PG, Ingram DS (eds) Molecular tools for screening biodiversity: plants and animals. Chapman and Hall, London, pp 195–201

    Google Scholar 

  • Clobert J, Anker Ims R, Rousset F (2004) Causes, mechanisms and consequences of dispersal. In: Hanski I, Gaggiotti O (eds) Ecology, genetics and evolution of metapopulations. Elsevier, San Diego, CA

    Google Scholar 

  • Cullingham CI, Pond BA, Kyle CJ et al (2008) Combining direct and indirect genetic methods to estimate dispersal for informing wildlife disease management decisions. Mol Ecol 17:4874–4886

    Article  CAS  PubMed  Google Scholar 

  • DeYoung RW, Honeycutt RL (2005) The molecular toolbox: genetic techniques in wildlife ecology and management. J Wildl Manage 69:1362–1384

    Article  Google Scholar 

  • Dominguez J, Velando A, Aira M, Monroy F (2003) Uniparental reproduction of Eisenia fetida and E-andrei (Oligochaeta: Lumbricidae): evidence of self-insemination. Pedobiologia 47:530–534

    Google Scholar 

  • Dupont L (2009) Perspectives on the application of molecular genetics to earthworm ecology. Pedobiologia 52:191–205

    Article  CAS  Google Scholar 

  • Dyer AR, Fowler JCS, Baker GH (1998) Detecting genetic variation in exotic earthworms, Aporrectodea spp. (Lumbricidae), in australian soils using RAPD markers. Soil Biol Biochem 30:159–165

    Article  CAS  Google Scholar 

  • Eberhard WG (1996) Female control: sexual selection by cryptic female choice. Princeton University Press, Princeton

    Google Scholar 

  • Edwards CA, Bohlen PJ (1996) Biology and ecology of earthworms. Chapman and Hall, London

    Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620

    Article  CAS  PubMed  Google Scholar 

  • Field SG, Lange M, Schulenburg H, Velavan TP, Michiels NK (2007) Genetic diversity and parasite defense in a fragmented urban metapopulation of earthworms. Anim Conserv 10:162–175

    Article  Google Scholar 

  • Freeland JR (2005) Molecular ecology. Wiley, Chichester

    Google Scholar 

  • Futuyma DJ (1998) Evolutionary biology. Sinauer Associates, Sunderland, MA

    Google Scholar 

  • Grigoropoulou N, Butt KR (2010) Field investigations of Lumbricus terrestris spatial distribution and dispersal through monitoring of manipulated, enclosed plots. Soil Biol Biochem 42:40–47

    Article  CAS  Google Scholar 

  • Guillot G, Mortier F, Estoup A (2005) Geneland: a program for landscape genetics. Mol Ecol Notes 5:712–715

    Article  CAS  Google Scholar 

  • Hajibabaei M, Singer GAC, Hebert PDN, Hickey DA (2007) DNA barcoding: how its complements taxonomy, molecular phylogenetics and population genetics. Trends Genet 23:167–172

    Article  CAS  PubMed  Google Scholar 

  • Harper GL, Cesarini S, Casey SP et al (2006) Microsatellite markers for the earthworm Lumbricus rubellus. Mol Ecol Notes 6:325–327

    Article  CAS  Google Scholar 

  • Hebert PDN, Stoeckle MY, Zemlak TS, Francis CM (2004) Identification of birds through DNA barcodes. PLoS Biol 2:e312

    Article  PubMed  CAS  Google Scholar 

  • Hendrix PF (2006) Biological invasions belowground – earthworms as invasive species. Biol Invasions 8:1201–1204

    Article  Google Scholar 

  • Holderegger R, Wagner HH (2008) Landscape genetics. Bioscience 58:199–207

    Article  Google Scholar 

  • Huang J, Xu Q, Sun ZJ, Tang GL, Su ZY (2007) Identifying earthworms through DNA barcodes. Pedobiologia 51:301–309

    Article  CAS  Google Scholar 

  • James SW, Hendrix PF (2004) Invasion of exotic earthworms into North America and other regions. In: Edwards CA (ed) Earthworm ecology. CRC Press, Boca Raton FL, pp 75–88

    Google Scholar 

  • Janicke T, Scharer L (2009) Sex allocation predicts mating rate in a simultaneous hermaphrodite. Proc R Soc Lond B Biol Sci 276:4247–4253

    Article  Google Scholar 

  • Jarne P, Auld JR (2006) Animals mix it up too: the distribution of self-fertilization among hermaphroditic animals. Evolution 60:1816–1824

    PubMed  Google Scholar 

  • Jarne P, David P (2008) Quantifying inbreeding in natural populations of hermaphroditic organisms. Heredity 100:431–439

    Article  CAS  PubMed  Google Scholar 

  • Jarne P, Lagoda J-L (1996) Microsatellites, from molecules to populations and back. Trends Ecol Evol 11:424–429

    Article  Google Scholar 

  • Jarne P, Städler T (1995) Population genetic structure and mating system evolution in freshwater pulmonates. Experientia 51:482–497

    Article  CAS  Google Scholar 

  • Jones AG, Ardren WR (2003) Methods of parentage analysis in natural populations. Mol Ecol 12:2511–2523

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Keller LF, Waller DM (2002) Inbreeding effects in wild populations. Trends Ecol Evol 17:230–241

    Article  Google Scholar 

  • King RA, Tibble AL, Symondson OC (2008) Opening a can of worms: unprecedented sympatric cryptic diversity within British lumbricid earthworms. Mol Ecol 17:4694–4698

    Google Scholar 

  • Lavelle P (2000) Ecological challenges for soil science. Soil Sci 165:73–86

    Article  CAS  Google Scholar 

  • Lee CE (2002) Evolutionary genetics of invasive species. Trends Ecol Evol 17:386–391

    Article  Google Scholar 

  • Lentzsch P, Golldack J (2006) Genetic diversity of Aporrectodea caliginosa from agricultural sites in Northeast Brandenburg, Germany. Pedobiologia 50:369–376

    Article  Google Scholar 

  • Manel S, Schwartz MK, Luikart G, Taberlet P (2003) Landscape genetics: combining landscape ecology and population genetics. Trends Ecol Evol 18:189–197

    Article  Google Scholar 

  • Margulies M, Egholm M, Altman WE et al (2005) Genome sequencing in microfabricated high-density picolitre reactors. Nature 437:376–380

    CAS  PubMed  Google Scholar 

  • Mather JG, Christensen O (1988) Surface movements of earthworms in agricultural land. Pedobiologia 32:399–405

    Google Scholar 

  • Mathieu J, Barot S, Blouin M et al (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 Biol Biochem 42:203–209

    Article  CAS  Google Scholar 

  • Meyer WJ, Bouwman H (1997) Anisopary in compost earthworm reproductive strategies (Oligochaeta). Soil Biol Biochem 29:731–735

    Article  CAS  Google Scholar 

  • Michiels NK, Newman LJ (1998) Sex and violence in hermaphrodites. Nature 391:647–647

    Article  CAS  Google Scholar 

  • Michiels NK, Howner A, Vorndran IC (2001) Precopulatory mate assessment in relation to body size in the earthworm Lumbricus terrestris: avoidance of dangerous liaisons? Behav Ecol 12:612–618

    Article  Google Scholar 

  • Minamiya Y, Yokoyama J & Fukuda T (in press) A phylogeographic study of the Japanese earthworm, Metaphire sieboldi (Horst, 1883) (Oligochaeta: Megascolecidae): inferences from mitochondrial DNA sequences. Eur J Soil Biol 45:423–430

    Google Scholar 

  • Monroy F, Aira M, Velando A, Dominguez J (2003) Have spermatophores in Eisenia fetida (Oligochaeta, Lumbricidae) any reproductive role? Pedobiologia 47:526–529

    Google Scholar 

  • Monroy F, Aira M, Velando A, Dominguez J (2005) Size-assortative mating in earthworm Eisenia fetida (Oligochaeta, Lumbricidae). J Ethol 23:69–70

    Article  Google Scholar 

  • Moritz C, Cicero C (2004) DNA Barcoding: promise and pitfalls. PLoS Biol 2:e279–354

    Article  CAS  Google Scholar 

  • Nakagawa S, Bannister TD, Jensen FR, McLean DA, Waas JR (2002) Relatedness does not affect the mating effort of Eisenia fetida Sav. (Oligochaeta) despite evidence for outbreeding depression. Biol Fertil Soils 35:390–392

    Article  Google Scholar 

  • Nathan R (2001) The challenges of studying dispersal. Trends Ecol Evol 16:481–483

    Article  CAS  Google Scholar 

  • Novo M, Velavan TP, Almodóvar A et al (2008) Microsatellite markers for the drought-resistant earthworm Hormogaster elisae. Mol Ecol Notes 8:901–903

    CAS  Google Scholar 

  • 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. Zool Scr 38:537–552

    Article  Google Scholar 

  • Nutt KJ (2008) A comparison of techniques for assessing dispersal behaviour in gundis: revealing dispersal patterns in the absence of observed dispersal behaviour. Mol Ecol 17:3541–3556

    PubMed  Google Scholar 

  • Parker GA (1970) Sperm competition and its evolutionary consequences in the insects. Biol Rev 45:525–567

    Article  Google Scholar 

  • Parker GA (1979) Sexual selection and sexual conflict. In: Blum MS, Blum SA (eds) Sexual selection and reproductive competition in insects. Academic, New York, pp 123–166

    Google Scholar 

  • Parkinson D, McLean MA, Scheu S (2004) Impact of earthworms on other biota in forest soils, with some emphasis on cool temperate montane forests. In: Edwards CA (ed) Earthworm ecology. CRC Press, Boca Raton FL, pp 241–259

    Google Scholar 

  • Perez-Losada M, Ricoy M, Marshall JC, Dominguez J (2009) Phylogenetic assessment of the earthworm Aporrectodea caliginosa species complex (Oligochaeta: Lumbricidae) based on mitochondrial and nuclear DNA sequences. Mol Phylogenet Evol 52:293–302

    Article  CAS  PubMed  Google Scholar 

  • Pop AA, Wink M, Pop VV (2003) Use of 18S, 16S rDNA and cytochrome c oxidase sequences in earthworm taxonomy (Oligochaeta, Lumbricidae). Pedobiologia 47:428–433

    CAS  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    CAS  PubMed  Google Scholar 

  • Pusey A, Wolf M (1996) Inbreeding avoidance in animals. Trends Ecol Evol 11:201–206

    Article  Google Scholar 

  • Rossi J-P (2003) Clusters in earthworm spatial distribution. Pedobiologia 47:490–496

    Google Scholar 

  • Rossi J-P, Lavelle P, Albrecht A (1997) Relationships between spatial pattern of the endogeic earthworm Polypheretima elongata and soil heterogeneity. Soil Biol Biochem 29:485–488

    Article  CAS  Google Scholar 

  • Sakai AK, Allendorf FW, Holt JS et al (2001) The population biology of invasive species. Annu Rev Ecol Syst 32:305–332

    Article  Google Scholar 

  • Scharer L (2009) Tests of sex allocation theory in simultaneously hermaphroditic animals. Evolution 63:1377–1405

    Article  PubMed  Google Scholar 

  • Sharma PC, Grover A, Kahl G (2007) Mining microsatellites in eukaryotic genomes. Trends Biotechnol 25:490–498

    Article  CAS  PubMed  Google Scholar 

  • Shields WM (1993) The natural and unnatural history of inbreeding and outbreeding. In: Thornhill NW (ed) The natural history of inbreeding and outbreeding. The University of Chicago Press, Chicago IL, pp 143–172

    Google Scholar 

  • Slatkin M (1993) Isolation by distance in equilibrium and non-equilibrium populations. Evolution 47:264–279

    Article  Google Scholar 

  • Storfer A, Murphy MA, Evans JS et al (2007) Putting the ‘landscape’ in landscape genetics. Heredity 98:128–142

    Article  CAS  PubMed  Google Scholar 

  • Sturzenbaum SR, Andre J, Kille P, Morgan AJ (2009) Earthworm genomes, genes and proteins: the (re)discovery of Darwin's worms. Proc R Soc Lond B Biol Sci 276:789–797

    Article  CAS  Google Scholar 

  • Sunnucks P (2000) Efficient genetic markers for population biology. Trends Ecol Evol 15: 199–203

    Article  PubMed  Google Scholar 

  • Tato A, Velando A, Dominguez J (2006) Influence of size and partner preference on the female function of the earthworm Eisenia andrei (Oligochaeta, Lumbricidae). Eur J Soil Biol 42:S331–S333

    Article  Google Scholar 

  • Terhivuo J, Saura A (2006) Dispersal and clonal diversity of North-European parthenogenetic earthworms. Biol Invasions 8:1205–1218

    Article  Google Scholar 

  • Terhivuo J, Saura A (2008) Clone distribution of the earthworm Eiseniella tetraedra (Sav.) (Oligochaeta: Lumbricidae) across an altitudinal gradient on subarctic mountains of NW Europe. Pedobiologia 51:375–384

    Article  Google Scholar 

  • Tregenza T, Wedell N (2000) Genetic compatibility, mate choice and patterns of parentage: invited review. Mol Ecol 9:1013–1027

    Article  CAS  PubMed  Google Scholar 

  • van Velzen E, Scharer L, Pen I (2009) The effect of cryptic female choice on sex allocation in simultaneous hermaphrodites. Proc R Soc Lond B Biol Sci 276:3123–3131

    Article  Google Scholar 

  • Velando A, Dominguez J, Ferreiro A (2006) Inbreeding and outbreeding reduces cocoon production in the earthworm Eisenia andrei. Eur J Soil Res 42:S354–S357

    Article  Google Scholar 

  • Velando A, Eiroa J, Dominguez J (2008) Brainless but not clueless: earthworms boost their ejaculates when they detect fecund non-virgin partners. Proc R Soc Lond B Biol Sci 275: 1067–1072

    Article  Google Scholar 

  • Velavan TP, Schulenburg H, Michiels N (2007) Development and characterization of novel microsatellite markers for the common earthworm (Lumbricus terrestris L). Mol Ecol Notes 7:1060–1062

    Article  CAS  Google Scholar 

  • Velavan TP, Weller S, Schulenburg H, Michiels NK (2009) High genetic diversity and heterogeneous parasite load in the earthworm Lumbricus terrestris on a German meadow. Soil Biol Biochem 41:1591–1595

    Article  CAS  Google Scholar 

  • Viktorov AG (1997) Diversity of polyploid races in the family Lumbricidae. Soil Biol Biochem 29:217–221

    Article  Google Scholar 

  • Vorpahl P, Moenickes S, Richter O (2009) Modelling of spatio-temporal population dynamics of earthworms under wetland conditions - An integrated approach. Econ Model 220:3647–3657

    Article  Google Scholar 

  • Waser NM (1993) Population structure, optimal outbreeding, and assortative mating in Angiosperms. In: Thornhill NW (ed) The natural history of inbreeding and outbreeding. The University of Chicago Press, Chicago, IL

    Google Scholar 

  • Wheeler DA, Srinivasan M, Egholm M et al (2008) The complete genome of an individual by massively parallel DNA sequencing. Nature 452:872–U875

    Article  CAS  PubMed  Google Scholar 

  • Wilmer JW, Elkin C, Wilcox C et al (2008) The influence of multiple dispersal mechanisms and landscape structure on population clustering and connectivity in fragmented artesian spring snail populations. Mol Ecol 17:3733–3751

    Article  Google Scholar 

  • Wilson GA, Rannala B (2003) Bayesian inference of recent migration rates using multilocus genotypes. Genetics 163:1177–1191

    PubMed  Google Scholar 

  • Wright S (1951) The genetical structure of populations. Ann Eugen 15:323–354

    Google Scholar 

  • Zhang AB, He LJ, Crozier RH, Muster C, Zhu C-D (2010) Estimating sample sizes for DNA barcoding. Mol Phylogenet Evol 54:1035–1039

    Article  CAS  PubMed  Google Scholar 

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Lazrek, F., Velavan, T.P., Mathieu, J., Dupont, L. (2011). Application of Molecular Genetics to Earthworm Ecology: Current Research and Promising Future Directions. In: Karaca, A. (eds) Biology of Earthworms. Soil Biology, vol 24. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-14636-7_17

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