Abstract
After one year of surveying semiaquatic earthworms (Oligochaeta, Sparganophilidae), we describe Sparganophilus jenkinsi sp. nov., S. carveri sp. nov., S. oconeeae sp. nov., S. williamsae sp. nov., S. muskogee sp. nov., S. youngae sp. nov., and S. borgesae sp. nov. based on extensive differences in morphological characters and molecular data. Three additional species are described morphologically but not formally named due to limited material. The species of Sparganophilus described here can be organized into three species groups: (1) S. jenkinsi, S. oconeeae, S. muskogee, S. carveri, S. williamsae, S. youngae, S. borgesae, and Sparganophilus sp02 have continuous tubercula pubertatis in the region of xvii–xxii, and tubular nephridial bladder; (2) Sparganophilus sp09 have three discrete pairs of tubercula pubertatis and sack-like nephridial bladder; and (3) Sparganophilus sp10 have the tubercula pubertatis posteriorly displaced and reduced to two segments, and have a nephridial “caecum.” These new species contribute to our knowledge of the endemism and biodiversity of earthworms in the Appalachian Piedmont.
References
- Anderson, F.E., Williams, B.W., Horn, K.M., Erséus, C., Halanych, K.M., Santos, S.R. & James, S.W. (2017) Phylogenomic analyses of Crassiclitellata support major Northern and Southern Hemisphere clades and a Pangaean origin for earthworms. BMC Evolutionary Biology, 17, 1–18. https://doi.org/10.1186/s12862-017-0973-4
- Benham, W.B. (1892) A new English genus of aquatic Oligochaeta (Sparganophilus) belonging to the family Rhinodrilidae. Quarterly Journal of Microscopical Science, 34, 155–179. https://doi.org/10.1242/jcs.s2-34.134.155
- Birky, C.W. (2013) Species detection and identification in sexual organisms using population genetic theory and DNA sequences. PLoS ONE, 8, e52544. https://doi.org/10.1371/journal.pone.0052544
- Birky, C.W., Adams, J., Gemmel, M. & Perry, J. (2010) Using population genetic theory and DNA sequences for species detection and identification in asexual organisms. PLoS ONE, 5, e10609. https://doi.org/10.1371/journal.pone.0010609
- Bouché, M.B. & Qiu, J.-P. (1998) Un nouveau Sparganophilus (Annelida: Oligocaeta) d’Europe, avec considérations paléogéographiques sur les Lumbricina. Documents Pédozoologiques et Intégrologiques, 4, 178–180.
- Carrera-Martínez, R., Jones, D., Schoville, S.D., Snyder, B.A. & Callaham Jr., M.A. (2021) Two new species of Bimastos (Oligochaeta, Lumbricidae) from the Southern Appalachian Mountains, North America. Zootaxa, 5052 (3), 395–405. https://doi.org/10.11646/zootaxa.5052.3.5
- Carstens, B.C., Pelletier, T.A., Reid, N.M. & Satler, J.D. (2013) How to fail at species delimitation. Molecular Ecology, 22, 4369–4383. https://doi.org/10.1111/mec.12413
- Chang, C.-H. & James, S. (2011) A critique of earthworm molecular phylogenetics. Pedobiologia, 54, S3–S9. https://doi.org/10.1016/j.pedobi.2011.07.015
- Chang, C.-H., Bartz, M.L.C., Brown, G., Callaham, M.A., Cameron, E.K., Dávalos, A., Dobson, A., Görres, J.H., Herrick, B.M., Ikeda, H., James, S.W., Johnston, M.R., McCay, T.S., McHugh, D., Minamiya, Y., Nouri-Aiin, M., Novo, M., Ortiz-Pachar, J., Pinder, R.A., Ransom, T., Richardson, J.B., Snyder, B.A. & Szlavecz, K. (2021) The second wave of earthworm invasions in North America: biology, environmental impacts, management and control of invasive jumping worms. Biological Invasions, 23, 3291–3322. https://doi.org/10.1007/s10530-021-02598-1
- Cernosvitov, L. (1945) Oligochæta from Windermere and the Lake District. Proceedings of the Zoological Society of London, 114 (4), 523–548. https://doi.org/10.1111/j.1096-3642.1945.tb00241.x
- 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 and Biotechnology, 3, 294–299.
- Fragoso, C. & Rojas, P. (2019) More new Diplotrema earthworm species from southern Mexico (Annelida, Crassiclitellata, Acanthodrilidae, Acanthodrilinae). Zootaxa, 4688 (4), 483–502. https://doi.org/10.11646/zootaxa.4688.4.2
- Hague, F.S. (1923) Studies on Sparganophilus eiseni Smith. Transactions of the American Microscopical Society, 42, 1–42. https://doi.org/10.2307/3221811
- 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, 593–613. https://doi.org/10.1146/annurev.ecolsys.39.110707.173426
- Ikeda, H., Callaham, M.A., Shefferson, R.P., Wenk, E.S. & Fragoso, C. (2020) A comparison of latitudinal species diversity patterns between riverine and terrestrial earthworms from the North American temperate zone. Journal of Biogeography, 47, 1373–1382. https://doi.org/10.1111/jbi.13826
- Ikeda, H., Fukumori, K., Shoda-Kagaya, E., Takahashi, M., Ito, M.T., Sakai, Y. & Matsumoto, K. (2018) Evolution of a key trait greatly affects underground community assembly process through habitat adaptation in earthworms. Ecology and Evolution, 8, 1726–1735. https://doi.org/10.1002/ece3.3777
- James, S.W. & Davidson, S.K. (2012) Molecular phylogeny of earthworms (Annelida: Crassiclitellata) based on 28S, 18S and 16S gene sequences. Invertebrate Systematics, 26, 213–229. https://doi.org/10.1071/IS11012
- Jamieson, B.G.M. (1971) Family Glossoscolecidae. In: Brinkhurst, R.D. & Jamieson, B.G.M. (Eds.), Aquatic Oligochaeta of the World. Oliver and Boyd, Edimburg, pp. 723–837.
- Jamieson, B.G.M., Tillier, S., Tillier, A., Justine, J.L., Ling, E., James, S., McDonald, K. & Hugall, A.F. (2002) Phylogeny of the Megascolecidae and Crassiclitellata (Annelida, Oligochaeta): combined versus partitioned analysis using nuclear (28S) and mitochondrial (12S, 16S) rDNA. Zoosystema, 24, 707–734.
- Kalyaanamoorthy, S., Minh, B.Q., Wong, T.K.F., von Haeseler, A. & Jermiin, L.S. (2017) ModelFinder: Fast model selection for accurate phylogenetic estimates. Nature Methods, 14, 587–589. https://doi.org/10.1038/nmeth.4285
- Kapli, P., Lutteropp, S., Zhang, J., Kobert, K., Pavlidis, P., Stamatakis, A. & Flouri, T. (2017) Multi-rate Poisson tree processes for single- locus species delimitation under maximum likelihood and Markov chain Monte Carlo. Bioinformatics, 33, 1630–1638. https://doi.org/10.1093/bioinformatics/btx025
- Kozlov, A.M., Darriba, D., Flouri, T., Morel, B. & Stamatakis, A. (2019) RAxML-NG: A fast, scalable and user-friendly tool for maximum likelihood phylogenetic inference. Bioinformatic,s 35, 4453–4455. https://doi.org/10.1093/bioinformatics/btz305
- 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, 1547–1549. https://doi.org/10.1093/molbev/msy096
- Lemoine, F., Domelevo Entfellner, J.-B., Wilkinson, E., Correia, D., Dávila Felipe, M., De Oliveira, T. & Gascuel, O. (2018) Renewing Felsenstein’s phylogenetic bootstrap in the era of big data. Nature, 556, 452–456. https://doi.org/10.1038/s41586-018-0043-0
- Michaelsen, W. (1918) Die Lumbriciden, mit besonderer Berücksichtigung der bisher als Familie Glossoscolecidae zusammengefaßten Unterfamilien. Zoologische Jahrbücher, Abteilung für Systematik, Jena, 41, 1–398.
- Misirlioğlu, M., Reynolds, J.W., Stojanović, M., Trakić, T., Sekulić, J., James, S.W., Csuzdi, C., Decaëns, T., Lapied, E., Phillips, H.R.P., Cameron, E.K. & Brown, G.G. (2023) Earthworms (Clitellata, Megadrili) of the world: an updated checklist of valid species and families, with notes on their distribution. Zootaxa, 5255 (1), 417–438. https://doi.org/10.11646/zootaxa.5255.1.33
- Nguyen, L.-T., Schmidt, H.A., von Haeseler, A. & Minh, B.Q. (2015) IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies. Molecular Biology and Evolution, 32, 268–274. https://doi.org/10.1093/molbev/msu300
- 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, 293–302. https://doi.org/10.1016/j.ympev.2009.04.003
- Puillandre, N., Brouillet, S. & Achaz, G. (2021) ASAP: assemble species by automatic partitioning. Molecular Ecology Resources, 21, 609–620. https://doi.org/10.1111/1755-0998.13281
- R Core Team (2023) R: A language and environment for statistical computing. R Foundation for Statistical Computing. Vienna. Available from: https://www.r-project.org/ (accessed 23 December 2024)
- Reeves, W.K., Reynolds, J.W. & Wetzel, M.J. (2024) Sparganophilus (Annelida, Oligochaeta, Sparganophilidae) in North America. Megadrilogica, 28 (5), 53–80.
- Reynolds, J.W. (1975) Sparganophilus pearsei n. sp. (Oligochaeta: Sparganophilidae) a neartic earthworm from western North Carolina. Megadrilogica, 2 (2), 9–11.
- Reynolds, J.W. (1977) The earthworms of Tennessee (Oligochaeta). II. Sparganophilidae, with the description of a new species. Megadrilogica, 3 (3), 61–64.
- Reynolds, J.W. (1980) The earthworm family Sparganophilidae (Annelida, Oligochaeta) in North America. Megadrilogica, 3 (12), 189–204.
- Reynolds, J.W. (2008) Sparganophilidae (Annelida, Oligochaeta) distribution in North America and elsewhere, revisited. Megadrilogica, 12 (9), 125–143.
- Reynolds, J.W. & Wetzel, M.J. (2012) Terrestrial Oligochaeta (Annelida: Clitellata) in North America, including Mexico, Puerto Rico, Hawaii, and Bermuda. III. Megadrilogica, 15 (8), 191–214.
- Rota, E., Martinsson, S., Bartoli, M., Beylich, A., Graefe, U., Laini, A., Wetzel, M.J. & Erséus, C. (2016) Mitochondrial evidence supports a Nearctic origin for the spreading limicolous earthworm Sparganophilus tamesis Benham, 1892 (Clitellata, Sparganophilidae). Contributions to Zoology, 85, 113–119. https://doi.org/10.1163/18759866-08501005
- Smith, F. (1895) A preliminary account of two new Oligochaeta from Illinois. Bulletin of the Illinois State Museum of Natural History, 4, 138–148. https://doi.org/10.21900/j.inhs.v4.428
- Sievers F., & Higgins D.G. (2018) Clustal Omega for making accurate alignments of many protein sequences. Protein Science, 27, 135–145. https://doi.org/10.1002/pro.3290
- Spöri, Y., Stoch, F., Dellicour, S., Birky, C.W. & Flot, J.-F. (2021) KoT: an automatic implementation of the K/θ method for species delimitation. bioRxiv, 2021.08.17.454531. [published online] https://doi.org/10.1101/2021.08.17.454531
- Wei, T. & Simko, V. (2021) R package “corrplot”: Visualization of a Correlation Matrix (Version 0.92). Available from: https://github.com/taiyun/corrplot (accessed 23 December 2024)
- Whiting, M.F. (2002) Mecoptera is paraphyletic: Multiple genes and phylogeny of Mecoptera and Siphonaptera. Zoologica Scripta, 31, 93–104. https://doi.org/10.1046/j.0300-3256.2001.00095.x
- Yu, G., Smith, D.K., Zhu, H., Guan, Y. & Lam, T.T. (2017) ggtree: an R package for visualization and annotation of phylogenetic trees with their covariates and other associated data G. McInerny (Ed). Methods in Ecology and Evolution, 8, 28–36. https://doi.org/10.1111/2041-210X.12628
- Zicsi, A. & Vaucher, C. (1987) A propos de la présence de Sparganophilus tamesis Benham dans le lac Léman à Geneve (Oligochaeta: Sparganophilidae). Revue suisse de Zoologie, 94 (4), 861–864. https://doi.org/10.5962/bhl.part.79555