Morphological differences between genetic lineages of the peregrine earthworm Aporrectodea caliginosa (Savigny, 1826)
Abstract
Aporrectodea caliginosa is a universally distributed and highly abundant peregrine earthworm that is the object of many ecological and ecotoxicological studies. Molecular phylogenetic analysis suggested that A. caliginosa consists of three highly diverged genetic lineages. In this study, we investigated morphological diversity within a sample of these three lineages from Belarus. We detected a variety of forms with different degrees of pigmentation and a shift in the clitellum position. The three genetic lineages of A. caliginosa demonstrated different propensity to particular morphological variants, including size, colour, and the clitellum position, yet no character could be used to distinguish among the lineages with sufficient accuracy. Thus, our results suggest that identification of the genetic lineage should be recommended for ecological studies involving A. caliginosa to account for possible differences between them.
References
Bart, S., Amossé, J., Lowe, C. N., Mougin, C., Péry, A. R. R. & Pelosi, C. (2018): Aporrectodea caliginosa, a relevant earthworm species for a posteriori pesticide risk assessment: current knowledge and recommendations for culture and experimental design. – Environmental Science and Pollution Research 25(34): 33867–33881. https://doi.org/10.1007/s11356-018-2579-9
Bely, A. E. & Wray, G. A. (2004): Molecular phylogeny of naidid worms (Annelida: Clitellata) based on cytochrome oxidase I. – Molecular Phylogenetics and Evolution 30(1): 50–63. https://doi.org/10.1016/S1055-7903(03)00180-5
Boag, B., Palmer, L. F., Neilson, R., Legg, R. & Chambers, S. J. (1997): Distribution, prevalence and intensity of earthworm populations in arable land and grassland in Scotland. – Annals of Applied Biology 130(1): 153–165. https://doi.org/10.1111/j.1744-7348.1997.tb05791.x
Csuzdi, C. & Zicsi, A. (2003): Earthworms of Hungary (Annelida: Oligochaeta, Lumbricidae). – Hungarian Natural History Museum, Budapest, 278 pp.
Decaëns, T., Porco, D., Rougerie, R., Brown, G. G. & James, S. W. (2013): Potential of DNA barcoding for earthworm research in taxonomy and ecology. – Applied Soil Ecology 65: 35–42. https://doi.org/10.1016/j.apsoil.2013.01.001
Fernández, R., Almodóvar, A., Novo, M., Simancas, B. & Díaz Cosín, D. J. (2012): Adding complexity to the complex: New insights into the phylogeny, diversification and origin of parthenogenesis in the Aporrectodea caliginosa species complex (Oligochaeta, Lumbricidae). – Molecular Phylogenetics and Evolution 64(2): 368–379. https://doi.org/10.1016/j.ympev.2012.04.011
Folmer, O., Hoeh, W. R., Black, M. B. & Vrijenhoek, R. C. (1994): Conserved primers for PCR amplification of mitochondrial DNA from different invertebrate phyla. – Molecular Marine Biology and Biotechnology 3: 294–299.
García, J. A. & Fragoso, C. (2003): Influence of different food substrates on growth and reproduction of two tropical earthworm species (Pontoscolex corethrurus and Amynthas corticis). – Pedobiologia 47(5–6): 754–763. https://doi.org/10.1078/0031-4056-00255
Hendrix, P. F., Callaham, M. A., Drake, J. M., Huang, C.-Y., James, S. W., Snyder, B. A. & Zhang, W. (2008): Pandora’s box contained bait: the global problem of introduced earthworms. – Annual Review of Ecology, Evolution, and Systematics 39(1): 593–613. https://doi.org/10.1146/annurev.ecolsys.39.110707.173426
Ivask, M., Kuu, A. & Sizov, E. (2007): Abundance of earthworm species in Estonian arable soils. – European Journal of Soil Biology 43: S39–S42. https://doi.org/10.1016/j.ejsobi.2007.08.006
King, R. A., Tibble, A. L. & Symondson, W. O. C. (2008): Opening a can of worms: Unprecedented sympatric cryptic diversity within British lumbricid earthworms. – Molecular Ecology 17(21): 4684–4698. https://doi.org/10.1111/j.1365-294X.2008.03931.x
Kumar, S., Stecher, G., Li, M., Knyaz, C. & Tamura, K. (2018): MEGA X: molecular evolutionary genetics analysis across computing platforms. – Molecular Biology and Evolution 35(6): 1547–1549. https://doi.org/10.1093/molbev/msy096
Latif, R., Malek, M., Aminjan, A. R., Pasantes, J. J., Briones, M. J. I. & Csuzdi, C. (2020): Integrative taxonomy of some Iranian peregrine earthworm species using morphology and barcoding (Annelida: Megadrili). – Zootaxa 4877(1): zootaxa-4877. https://doi.org/10.11646/zootaxa.4877.1.7
Maksimova, S. L. & Gurina, N. V. (2014): Earthworm (Lumbricidae) of the fauna of Belarus: reference guide. – Belarusskaya navuka, Minsk, 56 pp.
Marchán, D. F., Cosín, D. J. D. & Novo, M. (2018): Why are we blind to cryptic species? Lessons from the eyeless. – European Journal of Soil Biology 86: 49–51. https://doi.org/10.1016/j.ejsobi.2018.03.004
Marchán, D. F., Fernández, R., Domínguez, J., Díaz Cosín, D. J. & Novo, M. (2020): Genome-informed integrative taxonomic description of three cryptic species in the earthworm genus Carpetania (Oligochaeta, Hormogastridae). – Systematics and Biodiversity 18(3): 203–215. https://doi.org/10.1080/14772000.2020.1730474
Mezhzherin, S. V., Garbar, A. V., Vlasenko, R. P., Onishchuk, I. P., Kotsyuba, I. Y. & Zhalai, E. I. (2018): The evolutionary paradox of parthenogenetic earthworms. – Naukova Dumka, Kiev, 231 pp. [In Russian]
Novo, M., Almodóvar, A. & Díaz-Cosín, D. J. (2009): High genetic divergence of hormogastrid earthworms (Annelida, Oligochaeta) in the central Iberian Peninsula: evolutionary and demographic implications. – Zoologica Scripta 38(5): 537–552. https://doi.org/10.1111/j.1463-6409.2009.00389.x
Pérez-Losada, M., Ricoy, M., Marshall, J. C. & Domínguez, J. (2009): Phylogenetic assessment of the earthworm Aporrectodea caliginosa species complex (Oligochaeta: Lumbricidae) based on mitochondrial and nuclear DNA sequences. – Molecular Phylogenetics and Evolution 52(2): 293–302. https://doi.org/10.1016/j.ympev.2009.04.003
Piearce, T. (2002): Yellow earthworms: distinctive pigmentation associated with arsenic- and copper-tolerance in Lumbricus rubellus. – Soil Biology and Biochemistry 34(12): 1833–1838. https://doi.org/10.1016/S0038-0717(02)00176-1
Porco, D., Decaëns, T., Deharveng, L., James, S. W., Skarzyński, D., Erséus, C., Butt, K. R., Richard, B. & Hebert, P. D. N. (2013): Biological invasions in soil: DNA barcoding as a monitoring tool in a multiple taxa survey targeting European earthworms and springtails in North America. – Biological Invasions 15(4): 899–910. https://doi.org/10.1007/s10530-012-0338-2
Shekhovtsov, S. V., Golovanova, E. V. & Peltek, S. E. (2016): Different dispersal histories of lineages of the earthworm Aporrectodea caliginosa (Lumbricidae, Annelida) in the Palearctic. – Biological Invasions 18: 751–761. https://doi.org/10.1007/s10530-015-1045-6
Shekhovtsov, S. V., Berman, D. I., Bulakhova, N. A., Makarova, O. L. & Peltek, S. E. (2018a): Phylogeography of earthworms from high latitudes of Eurasia. – Acta Zoologica Academiae Scientiarum Hungaricae 64(4): 369–382. https://doi.org/10.17109/AZH.64.4.369.2018
Shekhovtsov, S. V., Sundukov, Y. N., Blakemore, R. J., Gongalsky, K. B. & Peltek, S. E. (2018b): Identifying earthworms (Oligochaeta, Megadrili) of the southern Kuril islands using DNA barcodes. – Animal Biodiversity and Conservation 41(1): 9–17. https://doi.org/10.32800/abc.2018.41.0009
Shekhovtsov, S. V., Ershov, N. I., Vasiliev, G. V. & Peltek, S. E. (2019): Transcriptomic analysis confirms differences among nuclear genomes of cryptic earthworm lineages living in sympatry. – BMC Evolutionary Biology 19: 50. https://doi.org/10.1186/s12862-019-1370-y
Sims, R. W. & Gerard, B. M. (1985): Earthworms: keys and notes for the identification and study of the species. Vol. 31. – Brill Archive, 157 pp.
Tiunov, A. V., Hale, C. M., Holdsworth, A. R. & Vsevolodova-Perel, T. S. (2006): Invasion patterns of Lumbricidae into the previously earthworm-free areas of northeastern Europe and the western Great Lakes region of North America. Pp. 23–34. In: Hendrix, P. F. (ed.): Biological invasions below ground: earthworms as invasive species. – Springer Netherlands, Dordrecht. https://doi.org/10.1007/978-1-4020-5429-7_4
Vsevolodova-Perel, T. S. (1997): The earthworms of the fauna of Russia. – Nauka, Moscow, 103 pp. [in Russian]
Copyright (c) 2021 Sergei V Shekhovtsov, Sergei Ermolov, Tatiana Poluboyarova, Maria Kim-Kashmenskaya, Yevgeni Derzhinsky, Sergey Peltek
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
Manuscripts must be solely the work of the author(s) stated, must not have been previously published elsewhere, and must not be under consideration by another journal. This journal provides immediate open access to its content on the principle that making research freely available to the public supports a greater global exchange of knowledge. The authors retain copyright and publishing rights without restrictions of papers published in Acta Zoologica Academiae Scientiarum Hungaricae.
