Skip to main content
SpringerLink
Log in

Genetic diversity of an invasive earthworm, Lumbricus terrestris, at a long-term trading crossroad, the Champlain Valley of Vermont, USA

  • Original Paper
  • Published:
Biological Invasions Aims and scope Submit manuscript

Abstract

The invasive European earthworm, Lumbricus terrestris, is now widely distributed in North America. This success may result from high genetic diversity derived from multiple introductions from founder sources across Europe. Using a mitochondrial gene (COI) and microsatellite markers, L. terrestris from seven sites in the Champlain Valley of Vermont USA were scored for genetic diversity and population structure. This region has been a trading crossroads for centuries, thus likely to have received earthworms from multiple origins. COI sequences matched those reported for L. terrestris from Scotland, France, Austria, Denmark, Sweden, and Norway, and 2–5 haplotypes were found at each site. Genetic diversity (microsatellites) was great for each site, but not notably greater than for earthworm populations in general, possibly because there may be allele size homoplasy, or some restriction in the number of alleles possible at any locus. The earthworms were genetically differentiated among the Vermont study sites, even those 0.6–13 km distant. These results support the view that L. terrestris is a successful invasive earthworm because multiple introductions provided ample genetic variation for natural selection and local differentiation among locations in North America. Last, a large number of microsatellite markers is provided, including suggested PCR programs, for free use by future researchers.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Albers J (2000) Hands on the land. MIT Press, Cambridge

    Google Scholar 

  • Allendorf FW, Lundquist LA (2003) Introduction: population ecology, evolution and control of invasive species. Conserv Biol 17:24–30

    Article  Google Scholar 

  • Boore JL, Brown WM (1995) Complete sequence of the mitochondrial DNA of the annelid worm Lumbricus terrestris. Genetics 141:305–319

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Butt KR, Frederickson J, Morris RM (1992) The intensive production of Lumbricus terrestris L. for soil amelioration. Soil Biol Biochem 24:1321–1325

    Article  Google Scholar 

  • Butt KR, Lowe CN, Beasley T, Hanson I, Keynes R (2008) Darwin’s earthworms revisited. Eur J Soil Biol 44:255–259

    Article  Google Scholar 

  • Cunha L, Thornber A, Kille P, Morgan AJ, Novo M (2017) A large set of microsatellites for the highly invasive earthworm Amynthas corticus predicted from low coverage genomes. Appl Soil Ecol 119:152–155

    Article  Google Scholar 

  • Darwin CR (1881) The formation of vegetable mould through the action of worms with observations on their habitats. Murray, London

    Book  Google Scholar 

  • Dupont L, Lazrek F, Porco D, King RA, Rougerie R, Symondson WOC, Livet A, Richard B, Decaën T, Butt KR, Mathieu J (2011) New insight into the genetic structure of the Allolobophora chorotica aggregate in Europe using microsatellite and mitochondrial data. Pedobiologia 54:217–234

    Article  Google Scholar 

  • Dupont L, Grésille Y, Richard B, Decaëns T, Nathier J (2015) Dispersal constraints and fine-scale spatial genetic structure in two earthworm species. Biol J Linn Soc 114:335–347

    Article  Google Scholar 

  • Dupont L, Pauwels M, Dume C, Deschins V, Audusseau H, Gigon A, Dubs F, Vandenbulke F (2019) Genetic variation of the epigenic eartheorm Lumbricus castaneus populations in urban soils of the Paris region (France) revealed using eight newly developed microsatellite markers. Appl Soil Biol 135:35–37

    Google Scholar 

  • Dybdahl MF, Drown DM (2011) The absence of genotypic diversity in a successful parthenogenetic invader. Biol Invasions 13:1663–1672

    Article  Google Scholar 

  • Eisen GA (1872) Om nagra arkiska Oligochaetre. Öfv. Vet.-Akad. Förhandl Stockholm 29:119–124

    Google Scholar 

  • Elton CS (1958) The ecology of invasions by animals and plants. Chapman and Hall, London

    Book  Google Scholar 

  • Enckell PH, Bengston S-A, Duwes P, Niklasson M, Stille B, Wiman B (1986) The dispersal pattern of an anthropochorous species: genetic variation in populations of Lumbricus terrestris L. (Lumbricidae) in the Faroe Islands. Hereditas 104:253–261

    Article  Google Scholar 

  • Estoup A, Jarne P, Cornuet J-M (2002) Homoplasy and mutation model at microsatellite loci and their consequences for population genetics analysis. Mol Ecol 11:1591–1604

    Article  CAS  PubMed  Google Scholar 

  • Folmer O, Black M, Hoch W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299

    CAS  PubMed  Google Scholar 

  • François O (2016) Running structure-like population genetic analysis with R. R Tutorials in Population Genetics, U Grenoble-Alpes, pp 1–9

    Google Scholar 

  • Gailing O, Hickey R, Lilleskov E, Szlavecz K, Richter K (2012) Genetic comparisons between North American and European populations of Lumbricus terrestris L. Biochem Syst Ecol 45:23–30. https://doi.org/10.1016/j.bse.2012,07.018

    Article  CAS  Google Scholar 

  • Gates GE (1976) More on earthworm distribution in North America. Proc Biol Soc Wash 89:467–476

    Google Scholar 

  • Görres JH, Melnichuk RDS (2012) Asian invasive earthworms of the genus Amynthas Kinberg in Vermont. Northeast Nat 19:313–322

    Article  Google Scholar 

  • Görres JH, Connolly ST, Chang C-H, Carpenter NR, Keller EL, Nouri-Aiin M, Schall JJ (2018) Winter hatching in New England populations of invasive pheretimoid earthworms Amynthas agrestis and Amynthas tokioensis: a limit on population growth, or aid in peripheral expansion? Biol Invasions 20:1651–1655

    Article  Google Scholar 

  • Gunn A (1992) The use of mustard to estimate earthworm populations. Pedobiologia 36:65–67

    Google Scholar 

  • Hale CM (2008) Evidence for human-mediated dispersal of exotic earthworms: support for exploring strategies to limit further spread. Mol Ecol 17:1165–1169

    Article  PubMed  Google Scholar 

  • Hale CM, Frelich LE, Reich PB (2005) Exotic European earthworm invasion dynamics in northern hardwood forests of Minnesota, USA. Ecol Appl 15:848–860

    Article  Google Scholar 

  • Hamilton MB, Pincus EL, DiFiore A, Fleisher RC (1999) Universal linker and ligation procedures for construction of genomic SNA libraries enriched for microsatellites. Biotechniques 27:500–507

    Article  CAS  PubMed  Google Scholar 

  • Harper GL, Casey CP, Morgan AJ, Kille P, Bruford MW (2006) Microsatellite markers for the earthworm Lumbricus rubellus. Mol Ecol Notes 6:325–327

    Article  CAS  Google Scholar 

  • Holmstrup M, Westh P (1994) Dehydration of earthworm cocoons exposed to cold: a novel cold hardiness mechanism. J Comp Phys B 164:312–315

    Article  Google Scholar 

  • James SW, Porco D, Decaens T, Richard B, Rougerie R, Erseus C (2010) DNA barcoding reveals cryptic diversity in Lumbricus terrestris L., 1758 (Clitellata): Resurrection of L. herculeus (Savigny, 1826). PLoS ONE 5:15629

    Article  CAS  Google Scholar 

  • Jones G (2001) A history of the vikings. Oxford University Press, Oxford

    Google Scholar 

  • Kautenburger R (2006a) Genetic structure among earthworms (Lumbricus terrestris L.) from different sampling sites in western Germany based on random amplified polymorphic DNA. Pedobiologia 50:257–266. https://doi.org/10.1016/j.pedobi.2006.02.005

    Article  CAS  Google Scholar 

  • Kautenburger R (2006b) Impact of different agricultural practices on the genetic structure of Lumbricus terrestris, Arion lusitanicus, and Microtus arvalis. Anim Biodiv Conserv 29:19–32

    Google Scholar 

  • Kirk H, Dorn S, Mazzi D (2013) Molecular genetics and genomics generate new insights into invertebrate pest invasion. Evol Appl 6:842–856

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Klein A, Cameron EK, Heimburger B, Eisenhauer N, Scheu S, Schaefer I (2017) Changes in the genetic structure of an invasive earthworm species (Lumbricus terrestris, Lumbricidae) along an urban–rural gradient in North America. Appl Soil Ecol 120:265–272. https://doi.org/10.1016/j.apsoil.2017.08.009

    Article  PubMed Central  PubMed  Google Scholar 

  • Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) ClustalX. Bioinformatics 23:2947–2948

    Article  CAS  PubMed  Google Scholar 

  • McCay TS, Pinder RA, Alvarado E, Hanson WC (2017) Distribution and habitat of the endemic earthwormEisenoides lonnbergi (Michaelsen) in the northeastern United States. Northeast Nat 24:239–248

    Article  Google Scholar 

  • Mergeay J, Verschuren D, De Meester L (2006) Invasion of an sexual American water flea clone throughout Africa and rapid displacement of a native sibling species. Proc R Soc B 2783:2839–2844

    Article  Google Scholar 

  • Meshcheryakova EN, Berman DI (2014) Cold hardiness and geographic distribution of earthworms (Oligochaeta, Lumbricidae, Moniligastridae). Entomol Rev 94:486–497

    Article  Google Scholar 

  • Neal AT, Ross MS, Schall JJ, Vardo-Zalik AM (2016) Genetic differentiation over a small spatial scale of the sand fly Lutzomyia vexator (Diptera: Psychodidae). Parasite Vector 9:550

    Article  CAS  Google Scholar 

  • Nouri-Aiin M, Görres JH (2019) Earthworm cocoons: the cryptic side of invasive earthworm populations. Appl Soil Ecol 141:54–60

    Article  Google Scholar 

  • Novo M, Velavan TP, Almodovar A, Schulenberg H, Diaz-Cosin DJ, Michiels NK (2008) Microsatellite markers for the drought-resistant earthworm Hormogaster elisae. Mol Ecol Resour 8:901–903

    Article  CAS  PubMed  Google Scholar 

  • Novo M, Almodóvar A, Fernández RM, Gutiérrez M, Díaz Cosín DJ (2010) Mate choice of an endogeic earthworm revealed by microsatellite markers. Pedobiologia 53:373–379

    Article  Google Scholar 

  • Nuutinen V, Butt KR (1997) The mating behavior of the earthworm Lumbricus terrestris (Oligochaeta: Lumbricieae). J Zool Lond 242:783–798

    Article  Google Scholar 

  • Nuutinen V, Butt KR (2005) Homing ability widens the sphere of influence of the earthworm Lumbricus terrestris L. Soil Biol Biochem 37:805–807

    Article  CAS  Google Scholar 

  • Paetkau D, Slade R, Burden M, Estoup A (2004) Genetic assignment methods for the direct, real-time estimation of migration rate: a simulation-based exploration of accuracy and power. Mol Ecol 13:55–65

    Article  CAS  PubMed  Google Scholar 

  • Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics 28:2537–2539

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Pompanon F, Bonin A, Bellemain E, Taberlet P (2005) Genotyping errors: causes, consequences and solutions. Nat Rev Genet 6:847–859

    Article  CAS  PubMed  Google Scholar 

  • Pop VV, Pop AA (2006) Lumbricid earthworm invasion in the Carpathian Mountains and some other sites in Romania. Biol Invasions 8:1219–1222

    Article  Google Scholar 

  • Porco D, Decaëns T, Deharveng L, James SW, Skarzynski D, Erséus C, Butt KR, Richard B, Hebert PDN (2013) Biological invasions in soil: DNA barcoding as a monitoring tool in a multiple taxa survey targeting European earthworms and springtails in North America. Biol Invasions 15:899–910

    Article  Google Scholar 

  • Reynolds JW (2008) Terrestrial Oligochaeta (Annelida: Clitellata) in North America, including Mexico, Puerto Rico, Hawaii, and Bermuda. Megadrilogica 12:157–210

    Google Scholar 

  • Richter K (2009) Genetic structure in European populations of the earthworm Lumbricus terrestris. Dissertation, Kassel University, Kassel, Germany

  • Roman J, Darling JA (2007) Paradox lost: genetic diversity and the success of aquatic invasions. Trends Ecol Evol 22:454–464

    Article  PubMed  Google Scholar 

  • Rousset F (2008) Genepop’007: a complete reimplementation of the Genepop software for Windows and Linux. Mol Ecol Resour 8:103–106

    Article  PubMed  Google Scholar 

  • Sakai AK, Allendorf FW, Holt JS, Lodge DM, Molofsky J, With KA, Baughman S, Cabin RJ, Cohen JE, Ellstrand NC, McCauley DE, O’Neil P, Parker IM, Thompson JN, Welle SG (2001) The population biology of invasive species. Ann Rev Ecol Syst 32:305–332

    Article  Google Scholar 

  • Somers CM, Neudorf K, Jones KL, Lance SL (2011) Novel microsatellite loci for the compost earthworm Eisenia fedida: a genetic comparison of three North American vermiculture stocks. Pedobiologia 54:111–117

    Article  CAS  Google Scholar 

  • Souleman D, Grumiaux F, Frérot H, Vandenbulcke F, Pauwels M (2016) Isolation and characterization of eight polymorphic microsatellites markers for the earthworm Lumbricus terrestris. Eur J Soil Biol 74:76–80

    Article  CAS  Google Scholar 

  • Strunk H, Hochkirch A, Veith M, Hankeln T, Emmerling C (2012) Isolation and characterization of eleven polymorphic microsatellite markers for the earthworm Aporrectodea longa. Eur J Soil Biol 48:56–58

    Article  CAS  Google Scholar 

  • Tiunov AV, Hale CM, Holdsworth AR, Vsevolodova-Perel TS (2006) Invasion patterns of Lumbricidae into the previously earthworm-free areas of northeastern Europe and the western Great Lakes region of North America. Biol Invasions 8:1223–1234

    Article  Google Scholar 

  • Tomlin AD (1983) The earthworm bait market in North America. In: Satchell JE (ed) Earthworm ecology. Springer, Dordrecht

    Google Scholar 

  • Torres-Leguizamon M, Mathieu J, Decaens T, Dupont L (2014) Genetic structure of earthworm populations at a regional scale: inferences from mitochondrial and microsatellite markers in Aporrectoda icterica. PLOS ONE 9:e1015971-11

    Article  Google Scholar 

  • Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538

    Article  CAS  Google Scholar 

  • Velavan TP, Schulenburg H, Michiels NK (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 

  • Wallace AR (1876) The geographical distribution of animals; with a study of the relations of living and extinct faunas as elucidating the past changes of the earth’s surface, 2 vols. Macmillan, New York

    Book  Google Scholar 

  • Wallace AR (1911) Island life, 3rd edn. Macmillian, London

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Dana Bishop, Woodlands Manager, Shelburne Farms, and Rick Paradis, University of Vermont Natural Areas Director, for aid in use of property under their stewardship. The research was funded by a USDA-Hatch grant from the University of Vermont Agricultural Research Station.

Author information

Authors and Affiliations

  1. School of Biological Sciences, Washington State University, Pullman, WA, 99163, USA

    Erin L. Keller

  2. Department of Plant Biology, University of Vermont, Burlington, VT, 05405, USA

    Samantha T. Connolly

  3. Department of Plant and Soil Science, University of Vermont, Burlington, VT, 05405, USA

    Josef H. Görres

  4. Department of Biology, University of Vermont, Burlington, VT, 05405, USA

    Jos. J. Schall

Authors
  1. Erin L. Keller
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Samantha T. Connolly
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Josef H. Görres
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jos. J. Schall
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jos. J. Schall.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Keller, E.L., Connolly, S.T., Görres, J.H. et al. Genetic diversity of an invasive earthworm, Lumbricus terrestris, at a long-term trading crossroad, the Champlain Valley of Vermont, USA. Biol Invasions 22, 1723–1735 (2020). https://doi.org/10.1007/s10530-020-02215-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-020-02215-7

Keywords

Search

Navigation