A new genus and species of uncertain phylogenetic position within the family Hydrobiidae (Caenogastropoda: Truncatelloidea) discovered in Tunisian springs

  • Noureddine KHALLOUFI University of Carthage - Environmental Biomonitoring Laboratory (Group of Hydrobiology), Faculty of Sciences of Bizerte - Zarzouna 7021
  • Mustapha BÉJAOUI University of Carthage - Environmental Biomonitoring Laboratory (Group of Hydrobiology), Faculty of Sciences of Bizerte - Zarzouna 7021
  • Diana DELICADO Justus Liebig University Giessen, Department of Animal Ecology & Systematics, Heinrich-Buff-Ring 26-32 IFZD, 35392 Giessen
DOI: https://doi.org/10.5852/ejt.2017.328
Keywords: freshwater snails, Western Palaearctic, North Africa, anatomy, Belgrandiella

Abstract

The species richness of the aquatic (non-marine) gastropod family Hydrobiidae Stimpson, 1865 reaches its peak in the European region partly because other areas, such as North Africa, remain to be extensively surveyed. Most of the hydrobiid species described in North Africa have been ascribed to the subfamilies Pseudamnicolinae, Hydrobiinae and the genus Mercuria. Little is known about the presence of other hydrobiid subfamilies. This study examines several specimens of gastropods collected from two springs in Tunisia. Based on a comprehensive literature review and rigorous anatomical and molecular comparisons with known species from North Africa, Europe and Asia Minor of similar morphology, we here describe a new genus, Bullaregia gen. nov., and new species Bullaregia tunisiensis gen. et sp. nov. Although the shell shape of this Tunisian species resembles that of European hydrobiid genera such as Belgrandiella, it differs in other anatomical structures (i.e., penis with a glandular strap-like lobe, and two seminal receptacles, SR1 pedunculate, SR2 sessile and less developed). Using maximum likelihood and Bayesian approaches, phylogenetic relationships inferred from mtCOI sequences point to an independent evolutionary lineage for this new taxon outside Belgrandiella and other known hydrobiid subfamilies.

References

Akaike H. 1974. A new look at the statistical model identification. IEEE Transactions on Automatic Control 19: 716–723. https://doi.org/10.1109/TAC.1974.1100705

Bodon M., Ghamizi M. & Giusti F. 1999. The Moroccan stygobiont genus Heideella (Gastropoda: Prosobranchia: Hydrobiidae). Basteria 63: 89–105.

Boeters H.D. 1976. Hydrobiidae Tunesiens. Archiv für Molluskenkunde 107 (1–3): 89–105.

Boeters H.D. 1988. Westeuropäische Moitessieriidae und Hydrobiidae in Spanien und Portugal (Gastropoda: Prosobranchia). Archiv für Molluskenkunde 118: 181–261.

Bourguignat J.R. 1860. Malacologie terrestre et fluviatile de la Bretagne. J.B. Baillière, Paris.

Bourguignat J.R. 1864. Malacologie de l’Algérie. Histoire naturelle des animaux Mollusques terrestres et fluviatiles. Challamed Bastid, Paris.

Bourguignat J.R. 1877 Descriptions de deux nouveaux genres algériens, suivies d‘une classification des familles et des genres de mollusques terrestres et fluviatiles du système européen. Extrait de la Société des Sciences physiques et naturelles de Toulouse, Imprimerie Louis et Jean-Matthieu, Douladoure.

Brown D.S. 1994. Freshwater snails of Africa and their medical importance. Second revised edition, Taylor & Francis, London.

Charni M., Harrath A., Sluys R., Tekaya S. & Zghal F. 2004. The freshwater planarian Dugesia sicula Lepori, 1948 (Platyhelminthes, Tricladida) in Tunisia: ecology, karyology and morphology. Hydrobiologia 517: 161–170. https://doi.org/10.1023/B:HYDR.0000027344.07747.f7

Debeaux O. 1863. Notice sur quelques Mollusques nouveaux, ou peu connus, de la grande Kabylie. Journal de Conchyliologie 11: 10–21.

Delicado D., Pešić V. & Glöer P. 2016. Unraveling a new lineage of Hydrobiidae genera (Caenogastropoda: Truncatelloidea) from the Ponto-Caspian region. European Journal of Taxonomy 208: 1–29. https://doi.org/10.5852/ejt.2016.208

Falniowski A. & Szarowska M. 2011. A new genus and new species of valvatiform hydrobiid (Rissooidea; Caenogastropoda) from Greece. Molluscan Research 31 (3): 189–199.

Falniowski A. & Szarowska M. 2012. Phylogenetic position of Boleana umbilicata (Kuščer, 1932) (Caenogastropoda: Rissooidea). Folia Malacologica 20 (4): 265–270. https://doi.org/10.2478/v10125-012-0022-2

Falniowski A. & Szarowska M. 2013. Phylogenetic relationships of Dalmatinella fluviatilis Radoman, 1973 (Caenogastropoda: Rissooidea). Folia Malacologica 21 (1): 1–7. https://doi.org/10.12657/folmal.021.001

Felsenstein J. 1981. Evolutionary trees from DNA sequences: A maximum likelihood approach. Journal of Molecular Evolution 17: 368–376. https://doi.org/10.1007/BF01734359

Felsenstein J. 1985. Confidence limits on phylogenies: An approach using the bootstrap. Evolution 39: 783. https://doi.org/10.2307/2408678

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.

García N., Cuttelod A. & Abdul Malak D. 2010. The Status and Distribution of Freshwater Biodiversity in Northern Africa. IUCN, Gland, Switzerland, UK; Malaga, Spain.

Ghamizi M., Bodon M., Boulal M. & Guisti F. 1999. Atebbania bernasconii, a new genus and species from subterranean waters of the Tiznit plain, southern Morocco (Gastropoda: Hydrobiidae). Journal of Molluscan Studies 65: 89–98. https://doi.org/10.1093/mollus/65.1.89

Glöer P., Boeters H.D. & Pešić V. 2014. Freshwater molluscs of Kyrgyzstan with description of one new genus and species (Mollusca: Gastropoda). Folia Malacologica 22 (2): 73–81. https://doi.org/10.12657/folmal.022.009

Harrath A., Charni M., Sluys R., Zghal F. & Tekaya S. 2004. Ecology and distribution of the freshwater planarian Schmidtea mediterranea in Tunisia. Italian Journal of Zoology 71: 233–236. https://doi.org/10.1080/11250000409356577

Harrath A., Tekaya S. & Zghal F. 2001. Biodiversity of freshwater planarians (Turbellaria, Tricladida) from Tunisia. Bulletin de la Société zoologique de France 126 (1–2): 228–229.

Hershler R. & Liu H.P. 2009. New species and records of Pyrgulopsis (Gastropoda: Hydrobiidae) from the Snake River basin, southeastern Oregon: further delineation of a highly imperiled fauna. Zootaxa 2006: 1–22.

Hershler R. & Ponder W.F. 1998. A review of the morphological characters of hydrobioid snails. Smithsonian Contributions to Zoology 600: 1–55.

Hershler R., Liu H.P. & Thompson F.G. 2003. Phylogenetic relationships of North American nymphophiline gastropods based on mitochondrial DNA sequences. Zoologica Scripta 32 (4): 357–366. https://doi.org/10.1046/j.1463-6409.2003.00115.x

Hershler R., Thompson F.G. & Liu H.P. 2011. A large range extension and molecular phylogenetic analysis of the monotypic North American aquatic gastropod genus Cincinnatia (Hydrobiidae). Journal of Molluscan Studies 77 (3): 232–240. https://doi.org/10.1093/mollus/eyr008

Huelsenbeck J.P. 2000. MrBayes: Bayesian Inference of Phylogeny. NCBI, New York.

Huelsenbeck J.P. & Ronquist F. 2001. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17: 754–755. https://doi.org/10.1093/bioinformatics/17.8.754

Hurvich C.M. & Tsai C.L. 1989. Regression and time series model selection in small samples. Biometrikam 76: 297–307 https://doi.org/10.1093/biomet/76.2.297

Issel A. 1880. Molluschi terrestri e d’acqua dolce viventi e fossili della Tunisia. Annali del Museo Genova XV, Instituto Sordo-Muti, Genova.

Kabat A.R. & Hershler R. 1993. The Prosobranch snail family Hydrobiidae (Gastropoda: Rissooidea): Review of classification and supraspecific taxa. Smithsonian Contributions to Zoology 547: 1–94. https://doi.org/10.5479/si.00810282.547

Kristensen T.K. 1985. Guide pratique des Gastéropodes d’eau douce Africains. Espèces présentes en Afrique du Nord-Ouest. Charlottenlund, Denmark Danish Bilharziasis Laboratory 7: 1–21.

Lanfear R., Calcott B., Ho S.Y.W. & Guindon S. 2012. PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution 29 (6): 1695–1701. https://doi.org/10.1093/molbev/mss020

Letourneux A. & Bourguignat J.R. 1887. Prodrome de la malacologie terrestre et flviatile de la Tunisie. Exploration scientifique de la Tunisie, Zoologie, Malacologie. Imprimerie nationale, Paris.

Morelet A. 1857. Appendice à la conchyliologie de l’Algérie; voyage de M. Grasset à EI-Aghouat. Journal de Conchyliologie 6: 369–376.

Pallary P. 1921. Faune malacologique du Grand Atlas. Journal de Conchyliologie 66: 81–217.

Pallary P. 1923. Faune malacologique des eaux douces de la Tunisie. Archives des Instituts Pasteur de l'Afrique du Nord 1: 22–47.

Radoman P. 1983. Hydrobioidea a Superfamily of Prosobranchia (Gastropoda): Systematics. Serbian Academy of Sciences and Arts, Belgrade. European Journal of Taxonomy 328: 1–15

Schreiber K., Hauffe T., Albrecht C. & Wilke T. 2012. The role of barriers and gradients in differentiation processes of pyrgulinid microgastropods of Lake Ohrid. Hydrobiologia 682: 61–73. https://doi.org/10.1007/s10750-011-0864-4

Seurat E.G. 1921. Faune des Eaux continentales de la Berbérie. Travaux du Laboratoire de Zoologie Appliquée, Faculté des Sciences, Université d’Alger, Algeria.

Seurat E.G. 1934 Formations littorales et estuaires de la Syrte mineure (golfe de Gabès). Bulletin de la Station océanographique de Salambo, Tunisia.

Stamatakis A. 2014. RAxML Version 8: A tool for Phylogenetic Analysis and Post-Analysis of Large Phylogenies. Bioinformatics 30 (9): 1312–1313. https://doi.org/10.1093/bioinformatics/btu033

Strong E., Gargominy O., Ponder W.F. & Bouchet P. 2008. Global diversity of gastropods (Gastropoda; Mollusca) in freshwater. Hydrobiologia 595: 149–166. https://doi.org/10.1007/s10750-007-9012-6

Sugiura N. 1978. Further analysis of the data by Akaike’s information criterion and the finite corrections. Communications in Statistics − Theory and Methods A 7: 13–26. https://dx.doi.org/10.1080/03610927808827599

Swofford D.L. 2002. PAUP*. Phylogenetic analysis using parsimony (*and other methods). Sinauer Associates, Sunderland, Massachusetts.

Szarowska M. 2006. Molecular phylogeny, systematics and morphological character evolution in the Balkan Rissooidea (Caenogastropoda). Folia Malacologica 14: 99–168. https://doi.org/10.12657/folmal.014.014

Szarowska M. & Falniowski A. 2011. An unusual, flagellum-bearing hydrobiid snail (Gastropoda: Rissooidea: Hydrobiidae) from Greece, with descriptions of a new genus and a new species. Journal of Natural History 45 (35–36): 2231–2246. https://doi.org/10.1080/00222933.2011.591067

Szarowska M. & Falniowski A. 2014. Horatia Bourguignat, 1887: Is this genus really phylogenetically very close to Radomaniola Szarowska, 2006 (Caenogastropoda: Truncatelloidea)? Folia Malacologica 22: 31–39. https://doi.org/10.12657/folmal.022.003

Szarowska M., Grzmil P., Falniowski A. & Sirbu I. 2007. Grossuana codreanui (Grossu, 1946) and the phylogenetic relationships of the East Balkan genus Grossuana (Radoman, 1973) (Gastropoda: Rissooidea). Hydrobiologia 579: 379–391. https://doi.org/10.1007/s10750-006-0530-4

Tamura K. & Nei M. 1993. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology and Evolution 10: 512–526.

Tavaré S. 1986. Some probabilistic and statistical problems in the analysis of DNA sequences. In: Miura R.M. (ed.) Some mathematical questions in biology - DNA sequence analysis: 57–86. Lectures on Mathematics in the Life Sciences, Vol. 17. American Mathematical Society, Providence, RI.

Toumi H., Béjaoui M. & Boumaiza M. 2013. Contribution to the ecological study of epigean Cladocera and Copepoda (Cyclopoida) from groundwater in Northern Tunisia. Nature & Technology Journal. C-Environmental Sciences 8: 12–18.

Van Damme D. 1984. The freshwater Mollusca of Northern Africa. Distribution, biogeography and palaeoecology. Developments in Hydrobiology 25: 1–164.

Van Damme D., Ghamizi M., Soliman G., McIvor A. & Seddon M.B. 2010. The status and distribution of freshwater molluscs. In: García N., Cuttelod A. & Abdul Malak D. (eds) The status and distribution of freshwater biodiversity in Northern Africa: 30–50. IUCN, Gland, Switzerland; Cambridge, UK; Malaga, Spain.

Wilke T. & Davis G.M. 2000. Infraspecific mitochondrial sequence diversity in Hydrobia ulvae and Hydrobia ventrosa (Hydrobiidae: Rissooidea: Gastropoda): Do their different life histories affect biogeographic patterns and gene flow? Biological Journal of the Linnean Society 70: 89–105. https://doi.org/10.1111/j.1095-8312.2000.tb00202.x

Wilke T., Davis G.M., Falniowski A., Giusti F., Bodon M. & Szarowska M. 2001. Molecular systematics of Hydrobiidae (Mollusca: Gastropoda: Rissooidea): testing monophyly and phylogenetic relationships. Proceedings of the Academy of Natural Sciences of Philadelphia 151: 1–21. https://doi.org/10.1635/0097-3157(2001)151[0001:MSOHMG]2.0.CO;2

Wilke T., Davis G.M., Qiu D.C. & Spear R.C. 2006. Extreme mitochondrial sequence diversity in the intermediate schistosomiasis host Oncomelania hupensis robertsoni: another case of ancestral polymorphism? Malacologia 48: 143–157.

Wilke T., Haase M., Hershler R., Liu H.P., Misof B. & Ponder W. 2013. Pushing short DNA fragments to the limit: Phylogenetic relationships of ‘hydrobioid’ gastropods (Caenogastropoda: Rissooidea). Molecular Phylogenetics and Evolution 66: 715–736. https://doi.org/10.1016/j.ympev.2012.10.025

Zhang Z., Schwartz S., Wagner L. & Miller W. 2000. A greedy algorithm for aligning DNA sequences. Journal of Computational Biology 7 (1–2): 203–214. https://doi.org/10.1089/10665270050081478

Published
2017-06-09
How to Cite
KHALLOUFI, N., BÉJAOUI, M., & DELICADO, D. (2017). A new genus and species of uncertain phylogenetic position within the family Hydrobiidae (Caenogastropoda: Truncatelloidea) discovered in Tunisian springs. European Journal of Taxonomy, (328). https://doi.org/10.5852/ejt.2017.328
Issue
No. 328 (2017): A new genus and species of uncertain phylogenetic position within the family Hydrobiidae (Caenogastropoda: Truncatelloidea) discovered in Tunisian springs
Section
Zoology
Copyright (c) 2017 Noureddine KHALLOUFI, Mustapha BÉJAOUI, Diana DELICADO

Creative Commons Copyright Notices

Authors who publish with this journal agree to the following terms:

  1. Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution License (CC BY 4.0) that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
  2. Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.
  3. Authors are NOT PERMITTED to post their submitted work online (e.g., in institutional repositories or on personal websites) prior to publication, as it may lead to nomenclatural issues.