Moniliformis cryptosaudi n. sp. (Acanthocephala: Moniliformidae) from the Long-eared Hedgehog Hemiechinus auritus (Gmelin) (Erinaceidae) in Iraq; A Case of Incipient Cryptic Speciation Related to M. saudi in Saudi Arabia

Abstract

Moniliformis cryptosaudi n. sp. (Moniliformidae) is an acanthocephalan described from the long-eared hedgehog Hemiechinus auritus (Gmelin) (Erinaceidae) in Iraq as an incipient cryptic species of Moniliformis saudi Amin, Heckmann, Mohammed, Evans, 2016 described from the desert hedgehog Paraechinus aethiopicus (Ehrenberg) (Erinaceidae) in Saudi Arabia. Microscopical studies demonstrate that the two species are morphologically indistinguishable with practically identical measurements and counts but differed significantly in their energy dispersive X-ray analysis (EDXA) of metal composition of hooks. Hooks of specimens of the new species appeared to be of collagen material with very low levels of phosphorus and calcium unlike those of M. saudi and Moniliformis kalahariensis Meyer, 1931 that had high levels of calcium and phosphorus. Using 18S rDNA and cox1 genes, M. Saudi and M. kalahariensis were shown to be molecularly distinct but the molecular profiles of M. saudi and M. cryptosaudi were more similar. The molecular profile of M. kalahariensis collected from the South African hedgehog Atelerix frontalis Smith (Erinaceidae) in South Africa is reported for the first time and is studied only for comparative purposes. Moniliformis saudi and M. kalahariensis had comparable EDXA metal analysis that was distinct from that of M. cryptosaudi.

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

Figs. 1−6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11

References

  1. 1.

    Amin OM, Heckmann RA, Halajian A, El-NaggarA., Takavol S. (2014) Description of Moniliformis kalahariensis (Acanthocephala: Moniliformidae) from the South African hedgehog Atelerix frontalis (Erinaceidae) in South Africa. Comparative Parasitology 81:33–43

  2. 2.

    Amin OM, Evans RP, Boungou M, Heckmann RA (2016a) Morphological and molecular description of Tenuisentis niloticus (Meyer, 1932) (Acanthocephala: Tenuisentidae) from Heterotis niloticus (Cuvier) (Actinopterygii: Arapaimidae), in Burkina Faso, with emendation of the family diagnosis and notes on new features, cryptic genetic diversity and histopathology. Systematic Parasitology 93:173–191

  3. 3.

    Amin O.M., Heckmann R.A., Mohamed O., Evans R.P. 2016b. Morphological and molecular descriptions of Moniliformis saudi sp. n. (Acanthocephla: Moniliformidae) from the desert hedgehog Paraechinus aethiopicus (Ehrenberg) in Saudi Arabia, with a key to species and notes on histopathology. Folia Parasitologica, 63,014.

  4. 4.

    Brown W.M., George M. Jr., Wilson A.C. 1979. Rapid evolution of animal mitochondrial DNA. Proceedings of the National Academy of Science, USA, 76, 1967–1971.

  5. 5.

    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

  6. 6.

    Goulding TC, Cohen CS (2014) Phylogeography of a marine acanthocephalan: lack of cryptic diversity in a cosmopolitan parasite of mole crabs. Journal of Biogeography 41:965–976

  7. 7.

    Ha N.V., Amin O.M., Ngo H.D., Heckmann R.A. 2018. Descriptions of the acanthocephalans Cathayacanthus spinitruncatus (Rhadinorhynchidae) males and Pararhadinorhynchus magnus n. sp. (Diplosentidae) from marine fish of Vietnam, with notes on Heterosentis holospinus (Arhythmacanthidae). Parasite, in press

  8. 8.

    Hulmes D.J. 1992. The collagen superfamily—diverse structures and assemblies. Essays in Biochemistry, 27, 49–67. PMID 1425603.

  9. 9.

    Hulmes DJ (2002) Building collagen molecules, fibrils, and suprafibrillar structures. Journal of Structural Biology 137:2–10

  10. 10.

    Hulmes DJ, Miller A (1979) Quasi-hexagonal molecular packing in collagen fibrils. Nature 282:878–880

  11. 11.

    Lee RE (1992) Scanning Electron Microscopy and X-Ray Microanalysis. Prentice Hall, Englewood Cliffs, New Jersey, pp 1–464

  12. 12.

    Martınez-Aquino A, Reyna-Fabián ME, Rosas-Valdez R, Razo-Mendivil U, Pérez-Ponce de León G, Garcıa-Varela M (2009) Detecting a complex of cryptic species within Neoechinorhynchus golvani (Acanthocephala: Neoechinorhynchidae) inferred from ITSs and LSU rDNA gene sequences. Journal of Parasitology 95:1040–1047

  13. 13.

    Nadler SA, Pérez-Ponce de León G (2011) Integrating molecular and morphological approaches for characterizing parasite cryptic species: implications for parasitology. Parasitology 138:1688–1709

  14. 14.

    Near TJ, Garey JR, Nadler SA (1998) Phylogenetic relationships of the Acanthocephala inferred from 18S ribosomal DNA sequences. Molecular Phylogenetics and Evolution 10:287–98

  15. 15.

    Pérez-Ponce de León G, Nadler SA (2010) What we don’t recognize can hurt us: a plea for awareness about cryptic species. Journal of Parasitology 96:453–464

  16. 16.

    Pinacho-Pinacho CD, García-Varela M, Sereno-Uribe AL, Pérez-Ponce de León G (2018) A hyper-diverse genus of acanthocephalans revealed by tree-based and non-tree-based species delimitation methods: Ten cryptic species of Neoechinorhynchus in Middle American freshwater fishes. Molecular Phylogenetics and Evolution 127:30–45

  17. 17.

    Steinauer ML, Nickol BB, Orti G (2007) Cryptic speciation and patterns of phenotypic variation of a highly variable acanthocephalan parasite. Molecular ecology 16:4097–4109

  18. 18.

    Zittel M, Grabner D, Wlecklik A, Sures B, Leese F, Taraschewski H, Weigand AM (2018) Cryptic species and their utilization of indigenous and non-indigenous intermediate hosts in the acanthocephalan Polymorphus minutus sensu lato (Polymorphidae). Parasitology 19:1–9

Download references

Acknowledgements

This project was supported by the Department of Biology, Brigham Young University (BYU), Provo, Utah and by an Institutional Grant from the Parasitology Center, Inc. (PCI), Scottsdale, Arizona. We thank Sarah Vorkink Child, Bean Museum (BYU) for expert help in the preparation and organization of plates.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Omar M. Amin.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Amin, O.M., Heckmann, R.A., Sharifdini, M. et al. Moniliformis cryptosaudi n. sp. (Acanthocephala: Moniliformidae) from the Long-eared Hedgehog Hemiechinus auritus (Gmelin) (Erinaceidae) in Iraq; A Case of Incipient Cryptic Speciation Related to M. saudi in Saudi Arabia. Acta Parasit. 64, 195–204 (2019). https://doi.org/10.2478/s11686-018-00021-9

Download citation

Keywords

  • Acanthocephala
  • Moniliformis cryptosaudi
  • M. saudi
  • M. kalahariensis
  • Molecular profiles
  • Metal analysis of hooks