360
Views
14
CrossRef citations to date
0
Altmetric
Articles

Genome-informed integrative taxonomic description of three cryptic species in the earthworm genus Carpetania (Oligochaeta, Hormogastridae)

, , , &

References

  • Anderson, C., Cunha, L., Sechi, P., Kille, P., & Spurgeon, D. (2017). Genetic variation in populations of the earthworm, Lumbricus rubellus, across contaminated mine sites. BioMedCentral Genetics, 18, 97. doi:10.1186/s12863-017-0557-8
  • Álvarez J. (1977). El género Hormogaster en España. Publicaciones del Centro Pirenaico de Biología Experimental, 9, 27–35.
  • Bickford, D., Lohman, D. J., Sodhi, N. S., Ng, P. K. L., Meier, R., Winker, K., … Das, I. (2007). Cryptic species as a window on diversity and conservation. Trends in Ecology & Evolution, 22, 148–155. doi:10.1016/j.tree.2006.11.004
  • Brown, S. D. J., Collins, R. A., Boyer, S., Lefort, M.-C., Malumbres-Olarte, J., Vink, C. J., & Cruickshank, R. H. (2012). Spider: An R package for the analysis of species identity and evolution, with particular reference to DNA barcoding. Molecular Ecology Resources, 12, 562–565. doi:10.1111/j.1755-0998.2011.03108.x
  • Brunet, B. M. T., Blackburn, G. S., Muirhead, K., Lumley, L. M., Boyle, B., Lévesque, R. C., … Sperling, F. A. H. (2017). Two’s company, three’s a crowd: new insights on spruce budworm species boundaries using genotyping-by-sequencing in an integrative species assessment (Lepidoptera: Tortricidae). Systematic Entomology, 42, 317–328. doi:10.1111/syen.12211
  • Buckley, T. R., James, S., Allwood, J., Bartlam, S., Howitt, R., & Prada, D. (2011). Phylogenetic analysis of New Zealand earthworms (Oligochaeta: Megascolecidae) reveals ancient clades and cryptic taxonomic diversity. Molecular Phylogenetics and Evolution, 58, 85–96. doi:10.1016/j.ympev.2010.09.024
  • Chang, C.-H., Lin, S.-M., & Chen, J.-H. (2008). Molecular systematics and phylogeography of the gigantic earthworms of the Metaphire formosae species group (Clitellata, Megascolecidae). Molecular Phylogenetics and Evolution, 49, 958–968. doi:10.1016/j.ympev.2008.08.025
  • Chenuil, A., Cahill, A. E., Délémontey, N., Du Luc, E. D. S., & Fanton, H. (2019). Problems and Questions Posed by Cryptic Species. A Framework to Guide Future Studies. In From Assessing to Conserving Biodiversity (pp. 77–106). Cham: Springer.
  • Cullingham, C. I., Cooke, J. E. K., Dang, S., & Coltman, D. W. (2013). A species-diagnostic SNP panel for discriminating lodgepole pine, jack pine, and their interspecific hybrids. Tree Genetics & Genomes, 9, 1119–1127. doi:10.1007/s11295-013-0608-x
  • 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. doi:10.1016/j.apsoil.2013.01.001
  • Dixon, P. (2003). VEGAN, a package of R functions for community ecology. Journal of Vegetation Science, 14, 927–930. doi:10.1111/j.1654-1103.2003.tb02228.x
  • Duforet-Frebourg, N., Bazin, E., & Blum, M. G. B. (2014). Genome scans for detecting footprints of local adaptation using a Bayesian factor model. Molecular Biology and Evolution, 31, 2483–2495. doi:10.1093/molbev/msu182
  • Dupont, L., Porco, D., Symondson, W. O. C., & Roy, V. (2016). Hybridization relics complicate barcode-based identification of species in earthworms. Molecular Ecology Resources, 16, 883–894. doi:10.1111/1755-0998.12517
  • Earl, D. A., & vonHoldt, B. M. (2012). STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources, 4, 359–361. doi:10.1007/s12686-011-9548-7
  • Elshire, R. J., Glaubitz, J. C., Sun, Q., Poland, J. A., Kawamoto, K., Buckler, E. S., & Mitchell, S. E. (2011). A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. Plos One, 6, e19379. doi:10.1371/journal.pone.0019379
  • Evanno, G., Regnaut, S., & Goudet, J. (2005). Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology, 14, 2611–2620. doi:10.1111/j.1365-294X.2005.02553.x
  • 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, 368–379. doi:10.1016/j.ympev.2012.04.011
  • Fišer, C., Robinson, C. T., & Malard, F. (2018). Cryptic species as a window into the paradigm shift of the species concept. Molecular Ecology, 27, 613–635. doi:10.1111/mec.14486
  • Flanagan, S. P., & Jones, A. G. (2017). Constraints on the FST–Heterozygosity Outlier Approach. Journal of Heredity, 108, 561–573. doi:10.1093/jhered/esx048
  • Ganin, G. N., & Atopkin, D. M. (2018). Molecular differentiation of epigeic and anceic forms of Drawida ghilarovi Gates, 1969 (Moniligastridae, Clitellata) in the Russian Far East: Sequence data of two mitochondrial genes. European Journal of Soil Biology, 86, 1–7. doi:10.1016/j.ejsobi.2018.02.004
  • Garg, K. M., Tizard, R., Ng, N. S. R., Cros, E., Dejtaradol, A., Chattopadhyay, B., … Rheindt, F. E. (2016). Genome-wide data help identify an avian species-level lineage that is morphologically and vocally cryptic. Molecular Phylogenetics and Evolution, 102, 97–103. doi:10.1016/j.ympev.2016.05.028
  • Giska, I., Sechi, P., & Babik, W. (2015). Deeply divergent sympatric mitochondrial lineages of the earthworm Lumbricus rubellus are not reproductively isolated. BioMed Central Evolutionary Biology, 15, 217. doi:10.1186/s12862-015-0488-9
  • Haas, B. J., Papanicolaou, A., Yassour, M., Grabherr, M., Blood, P. D., Bowden, J., … Regev, A. (2013). De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nature Protocols, 8, 1494–1512. doi:10.1038/nprot.2013.084
  • Hand, B. K., Hether, T. D., Kovach, R. P., Muhlfeld, C. C., Amish, S. J., Boyer, M. C., … Luikart, G. (2015). Genomics and introgression: Discovery and mapping of thousands of species-diagnostic SNPs using RAD sequencing. Current Zoology, 61, 146–154. doi:10.1093/czoolo/61.1.146
  • Hebert, P. D. N., Ratnasingham, S., & de Waard, J. R. (2003). Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proceedings of the Royal Society of London. Series B: Biological Sciences, 270, 96–99. doi:10.1098/rsbl.2003.0025
  • Heethoff, M. (2018). Cryptic species – Conceptual or terminological chaos? A response to Struck et al. Trends in Ecology & Evolution, 33, 310. doi:10.1016/j.tree.2018.02.006
  • Huerta-Cepas, J., Forslund, K., Coelho, L. P., Szklarczyk, D., Jensen, L. J., von Mering, C., & Bork, P. (2017). Fast Genome-Wide Functional Annotation through Orthology Assignment by eggNOG-Mapper. Molecular Biology and Evolution, 34, 2115–2122. doi:10.1093/molbev/msx148
  • James, S. W., Porco, D., Decaëns, T., Richard, B., Rougerie, R., & Erséus, C. (2010). DNA barcoding reveals cryptic diversity in Lumbricus terrestris L., 1758 (Clitellata): resurrection of L. herculeus (Savigny, 1826). Public Library of Science One, 5, e15629. doi:10.1371/journal.pone.0015629
  • Jombart, T. (2008). adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics, 24, 1403–1405. doi:10.1093/bioinformatics/btn129
  • Jombart, T., & Ahmed, I. (2011). adegenet 1.3-1: new tools for the analysis of genome-wide SNP data. Bioinformatics. Bioinformatics, 27, 3070–3071. doi:10.1093/bioinformatics/btr521
  • Jörger, K. M., & Schrödl, M. (2013). How to describe a cryptic species? Practical challenges of molecular taxonomy. Frontiers in Zoology, 10, 59. doi:10.1186/1742-9994-10-59
  • King, R. A., Andrew King, R., Tibble, A. L., & Symondson, W. O. C. (2008). Opening a can of worms: unprecedented sympatric cryptic diversity within British lumbricid earthworms. Molecular Ecology, 17, 4684–4698. doi:10.1111/j.1365-294X.2008.03931.x
  • Knowlton, N. (1993). Sibling Species in the Sea. Annual Review of Ecology and Systematics, 24, 189–216. doi:10.1146/annurev.es.24.110193.001201
  • Koene, J. M., Pförtner, T., & Michiels, N. K. (2005). Piercing the partner’s skin influences sperm uptake in the earthworm Lumbricus terrestris. Behavioral Ecology and Sociobiology, 59, 243–249. doi:10.1007/s00265-005-0030-y
  • Korshunova, T., Picton, B., Furfaro, G., Mariottini, P., Pontes, M., Prkić, J., … Martynov, A. (2019). Multilevel fine-scale diversity challenges the ‘cryptic species’ concept. Scientific Reports, 9, 6732. doi:10.1038/s41598-019-42297-5
  • Lajus, D., Sukhikh, N., & Alekseev, V. (2015). Cryptic or pseudocryptic: can morphological methods inform copepod taxonomy? An analysis of publications and a case study of theEurytemora affinisspecies complex. Ecology and Evolution, 5, 2374–2385. doi:10.1002/ece3.1521
  • León, G. P.-P D., de León, G. P.-P., & Nadler, S. A. (2010). What We Don’t Recognize Can Hurt Us: A Plea for Awareness About Cryptic Species. Journal of Parasitology, 96, 453–464. doi:10.1645/GE-2260.1
  • Lewis, P. O. (2001). A likelihood approach to estimating phylogeny from discrete morphological character data. Systematic Biology, 50, 913–925. doi:10.1080/106351501753462876
  • Marchán, D. F., Fernández, R., de Sosa, I., Díaz Cosín, D. J., & Novo, M. (2017). Pinpointing cryptic borders: Fine-scale phylogeography and genetic landscape analysis of the Hormogaster elisae complex (Oligochaeta, Hormogastridae). Molecular Phylogenetics and Evolution, 112, 185–193. doi:10.1016/j.ympev.2017.05.005
  • Marchán, D. F., Fernández, R., de Sosa, I., Sánchez, N., Díaz Cosín, D. J., & Novo, M. (2018). Integrative systematic revision of a Mediterranean earthworm family: Hormogastridae (Annelida, Oligochaeta). Invertebrate Systematics, 32, 652. doi:10.1071/IS17048
  • Marchán, D. F., Novo, M., Fernández, R., de Sosa, I., Trigo, D., & Díaz Cosín, D. J. (2016). Evaluating evolutionary pressures and phylogenetic signal in earthworms: a case study - the number of typhlosole lamellae in Hormogastridae (Annelida, Oligochaeta). Zoological Journal of the Linnean Society, 178, 4–14. doi:10.1111/zoj.12410
  • Marchán, D. F., Novo, M., Sánchez, N., Domínguez, J., Díaz Cosín, D. J., & Fernández, R. (2020). Local adaptation fuels cryptic speciation in terrestrial annelids. Molecular phylogenetics and evolution, 146, 106767. doi:10.1016/j.ympev.2020.106767
  • Marchán, D. F., Sánchez, N., Novo, M., Fernández, R., Pardos, F., & Díaz Cosín, D. J. (2016). Cryptic characters for cryptic taxa: On the taxonomic utility of the genital chaetae in earthworms (Oligochaeta, Hormogastridae). Zoologischer Anzeiger - A Journal of Comparative Zoology, 264, 17–28. doi:10.1016/j.jcz.2016.06.008
  • 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, 537–552. doi:10.1111/j.1463-6409.2009.00389.x
  • Novo, M., Almodóvar, A., Fernández, R. M., Gutiérrez, M., & Díaz Cosín, D. J. (2010). Mate choice of an endogeic earthworm revealed by microsatellite markers. Pedobiologia, 53, 375–379. doi:10.1016/j.pedobi.2010.07.002
  • Novo, M., Almodóvar, A., Fernández, R., Trigo, D., & Díaz Cosín, D. J. (2010). Cryptic speciation of hormogastrid earthworms revealed by mitochondrial and nuclear data. Molecular Phylogenetics and Evolution, 56, 507–512. doi:10.1016/j.ympev.2010.04.010
  • Novo, M., Almodóvar, A., Fernández, R., Trigo, D., Díaz Cosín, D. J., & Giribet, G. (2012). Appearances can be deceptive: different diversification patterns within a group of Mediterranean earthworms (Oligochaeta, Hormogastridae). Molecular Ecology, 21, 3776–3793. doi:10.1111/j.1365-294X.2012.05648.x
  • Nygren, A. (2014). Cryptic polychaete diversity: a review. Zoologica Scripta, 43, 172–183. doi:10.1111/zsc.12044
  • Pfenninger, M., & Schwenk, K. (2007). Cryptic animal species are homogeneously distributed among taxa and biogeographical regions. BioMedCentral Evolutionary Biology, 7, 121doi:10.1186/1471-2148-7-121
  • Pons, J., Barraclough, T. G., Gomez-Zurita, J., Cardoso, A., Duran, D. P., Hazell, S., … Vogler, A. P. (2006). Sequence-based species delimitation for the DNA taxonomy of undescribed insects. Systematic Biology, 55, 595–609. doi:10.1080/10635150600852011
  • Porco, D., Chang, C.-H., Dupont, L., James, S., Richard, B., & Decaëns, T. (2018). A reference library of DNA barcodes for the earthworms from Upper Normandy: Biodiversity assessment, new records, potential cases of cryptic diversity and ongoing speciation. Applied Soil Ecology, 124, 362–371. doi:10.1016/j.apsoil.2017.11.001
  • Porto, P. G. (2014). La selección sexual post-cópula en la lombriz roja (Eisenia andrei Bouché, 1972). (Doctoral dissertation), Universidade de Vigo.
  • Pritchard, J. K., Stephens, M., & Donnelly, P. (2000). Inference of population structure using multilocus genotype data. Genetics, 155, 945–959.
  • Puillandre, N., Lambert, A., Brouillet, S., & Achaz, G. (2012). ABGD, Automatic Barcode Gap Discovery for primary species delimitation. Molecular Ecology, 21, 1864–1877. doi:10.1111/j.1365-294X.2011.05239.x
  • Queiroz, K. D., & De Queiroz, K. (2007). Species Concepts and Species Delimitation. Systematic Biology, 56, 879–886. doi:10.1080/10635150701701083
  • Rancilhac, L., Goudarzi, F., Gehara, M., Hemami, M.-R., Elmer, K. R., Vences, M., & Steinfarz, S. (2019). Phylogeny and species delimitation of near Eastern Neurergus newts (Salamandridae) based on genome-wide RADseq data analysis. Molecular Phylogenetics and Evolution, 133, 189–197. doi:10.1016/j.ympev.2019.01.003
  • Rochette, N. C., Rivera-Colón, A. G., & Catchen, J. M. (n.d). Stacks 2: Analytical Methods for Paired-end Sequencing Improve RADseq-based Population Genomics. doi:10.1101/615385
  • Rougerie, R., Decaëns, T., Deharveng, L., Porco, D., James, S. W., Chang, C.-H., … Hebert, P. D. N. (2009). DNA barcodes for soil animal taxonomy. Pesquisa Agropecuária Brasileira, 44, 789–802. doi:10.1590/S0100-204X2009000800002
  • Shekhovtsov, S. V., Golovanova, E. V., & Peltek, S. E. (2013). Cryptic diversity within the Nordenskiold’s earthworm, Eisenia nordenskioldi subsp. nordenskioldi (Lumbricidae, Annelida). European Journal of Soil Biology, 58, 13–18. doi:10.1016/j.ejsobi.2013.05.004
  • Stamatakis, A. (2014). RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics, 30, 1312–1313. doi:10.1093/bioinformatics/btu033
  • Struck, T. H., Feder, J. L., Bendiksby, M., Birkeland, S., Cerca, J., Gusarov, V. I., … Stedje, B. (2018). Cryptic species–more than terminological chaos: a reply to Heethoff. Trends in Ecology & Evolution, 33, 310–312.
  • Taheri, S., James, S., Roy, V., Decaëns, T., Williams, B. W., Anderson, F., … Dupont, L. (2018). Complex taxonomy of the “brush tail” peregrine earthworm Pontoscolex corethrurus. Molecular Phylogenetics and Evolution, 124, 60–70.
  • Trontelj, P., & Fišer, C. (2009). Perspectives: Cryptic species diversity should not be trivialised. Systematics and Biodiversity, 7, 1–3. doi:10.1017/S1477200008002909
  • Wang, Y., Zhou, Q.-S., Qiao, H.-J., Zhang, A.-B., Yu, F., Wang, X.-B., … Zhang, Y.-Z. (2016). Formal nomenclature and description of cryptic species of the Encyrtus sasakii complex (Hymenoptera: Encyrtidae). Scientific Reports, 6, 34372. doi:10.1038/srep34372
  • Yang, Z. (2015). The BPP program for species tree estimation and species delimitation. Current Zoology, 61, 854–865. doi:10.1093/czoolo/61.5.854
  • Yang, Z., & Rannala, B. (2010). Bayesian species delimitation using multilocus sequence data. Proceedings of the National Academy of Sciences, 107, 9264–9269. doi:10.1073/pnas.0913022107
  • Zhang, J., Kapli, P., Pavlidis, P., & Stamatakis, A. (2013). A general species delimitation method with applications to phylogenetic placements. Bioinformatics, 29, 2869–2876. doi:10.1093/bioinformatics/btt499

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.