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Myoanatomy of three aberrant kinorhynch species: similar but different?

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Abstract

Aberrant kinorhynchs show several modifications deviating from the typical kinorhynch body plan, including a modified introvert with very elongated and flexible scalids, a weakly developed neck, and a slender trunk with less distinct segmentation. How these aberrant external features are reflected in the inner anatomy and how their aberrant body plan evolved are not understood. Here, we provide a comprehensive and comparative myoanatomical study of three putatively, distantly related worm-like species: Cateria styx, Franciscideres kalenesos and Zelinkaderes yong. Despite the weak external segmentation of the trunk, the studied species show a distinct segmental arrangement of the musculature. However, this arrangement is shifted posteriorly with respect to the external segmentation, because the extremely thin and flexible cuticle is lacking the apodeme-like cuticular thickenings (pachycycli) where the longitudinal muscles usually attach. The muscular arrangement in the three species is overall similar, yet, C. styx shows most resemblance to the allomalorhagid F. kalenesos, whereas the cyclorhagid Z. yong differs in several ways. This suggests a closer relationship of C. styx to Allomalorhagida. Whereas most kinorhynchs prefer muddy sediments, both the allomalorhagid and cyclorhagid worm-like kinorhynchs are mainly found in sandy environments, suggesting that a flexible, slender body evolved at least twice independently as an adaptation to the interstitial environment.

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Data availability

All data analysed during this study is included in the present contribution and its associated files (online resources 1 and 2).

References

  • Altenburger A (2016) The neuromuscular system of Pycnophyes kielensis (Kinorhyncha: Allomalorhagida) investigated by confocal laser scanning microscopy. Evodevo 7(1):25. https://doi.org/10.1186/s13227-016-0062-6

    Article  PubMed  PubMed Central  Google Scholar 

  • Altenburger A, Rho HS, Chang CY, Sørensen MV (2015) Zelinkaderes yong sp. nov. from Korea—the first recording of Zelinkaderes (Kinorhyncha: Cyclorhagida) in Asia. Zool Stud 54:25. https://doi.org/10.1186/s40555-014-0103-6

    Article  Google Scholar 

  • Bauer-Nebelsick M (1995) Zelinkaderes klepali sp. n., from shallow water sands of the Red Sea. Ann Nat Mus Wien 97B:57–74

    Google Scholar 

  • Cepeda D, Sánchez N, Pardos F (2019) First report of the family Zelinkaderidae (Kinorhyncha: Cyclorhagida) for the Caribbean Sea, with the description of a new species of Triodontoderes Sørensen and Rho, 2009 and an identification key for the family. Zool Anz 282:116–126. https://doi.org/10.1016/j.jcz.2019.05.017

    Article  Google Scholar 

  • Dal Zotto M, Di Domenico M, Garraffoni A, Sørensen MV (2013) Franciscideres gen. nov.—a new, highly aberrant kinorhynch genus from Brazil, with an analysis of its phylogenetic position. Syst Biodivers 11:303–321. https://doi.org/10.1080/14772000.2013.819045

    Article  Google Scholar 

  • Gerlach SA (1956) Über einen aberranten Vertreter der Kinorhynchen aus dem Küstengrundwasser. Kieler Meeresforsch 12:120–124

    Google Scholar 

  • Giere O (2009) Meiobenthology. The microscopic motile fauna of aquatic sediments, 2nd edn. Springer, Berlin, p 527

    Google Scholar 

  • Herranz M, Pardos F, Boyle MJ (2013) Comparative morphology of serotonergic-like immunoreactive elements in the central nervous system of kinorhynchs (Kinorhyncha, Cyclorhagida). J Morphol 274:258–274. https://doi.org/10.1002/jmor.20089

    Article  PubMed  Google Scholar 

  • Herranz M, Boyle MJ, Pardos F, Neves RC (2014) Comparative myoanatomy of Echinoderes (Kinorhyncha): a comprehensive investigation by CLSM and 3D reconstruction. Front Zool 11:1–26. https://doi.org/10.1186/1742-9994-11-31

    Article  Google Scholar 

  • Herranz M, Yangel E, Leander BS (2018) Echinoderes hakaiensis sp. nov.: a new mud dragon (Kinorhyncha, Echinoderidae) from the northeastern Pacific Ocean with the redescription of Echinoderes pennaki Higgins, 1960. Mar Biodiv 48:303–325. https://doi.org/10.1007/s12526-017-0726-z

    Article  Google Scholar 

  • Herranz M, Di Domenico M, Sørensen MV, Leander BS (2019) The enigmatic kinorhynch C. styx Gerlach, 1956—a sticky son of a beach. Zool Anz 282:10–30. https://doi.org/10.1016/j.jcz.2019.05.016

    Article  Google Scholar 

  • Herranz M, Sørensen MV, Park T, Leander BS, Worsaae K (2020) Insights into mud dragon morphology (Kinorhyncha, Allomalorhagida): myoanatomy and neuroanatomy of Dracoderes abei and Pycnophyes ilyocryptus. Org Divers Evol 20:467–493. https://doi.org/10.1007/s13127-020-00451-2

    Article  Google Scholar 

  • Higgins RP (1968) Taxonomy and postembryonic development of the Cryptorhagae, a new suborder for the mesopsammic kinorhynch genus Cateria. Trans Amer Microsc Soc 87:21–39

    Article  Google Scholar 

  • Higgins RP (1986) A new species of Echinoderes (Kinorhyncha: Cyclorhagida) from a coarse-sand California beach. Trans Am Microsc Soc 105:266–273

    Article  Google Scholar 

  • Higgins RP (1990) Zelinkaderidae, a new family of cyclorhagid Kinorhyncha. Smithson Contr Zool 500:1–26

    Google Scholar 

  • Hirose E, Yamasaki H (2015) Fine structure of the integumentary cuticles and alimentary tissues of pycnophyid kinorhynchs Pycnophyes oshoroensis and Kinorhynchus yushini (Kinorhyncha, Homalorhagida). Zool Sci 32:389–395. https://doi.org/10.2108/zs150021

    Article  Google Scholar 

  • Kristensen RM, Higgins RP (1991) Kinorhyncha. In: Harrison FW, Ruppert EE (eds) Microscopic anatomy of invertebrates, The Aschelminthes, vol 4. Wiley, New York, pp 377–404

    Google Scholar 

  • Lopes Mello C, Carvalho AL, Cabral de Faria L, Baldoni L, Di Domenico M (2019) Spatial distribution pattern of the aberrant Franciscideres kalenesos (Kinorhyncha) on sandy beaches of Southern Brazil. Zool Anz 282:44–51. https://doi.org/10.1016/j.jcz.2019.05.008

    Article  Google Scholar 

  • Moritz K, Storch V (1972) Zur Feinstruktur des Integumentes von Trachydemus giganteus (Kinorhyncha). Z Morphol Tiere 71:189–202

    Article  Google Scholar 

  • Müller MCM, Schmidt-Rhaesa A (2003) Reconstruction of the muscle system in Antygomonas sp. (Kinorhyncha, Cyclorhagida) by means of phalloidin labeling and cLSM. J Morphol 256:103–110. https://doi.org/10.1002/jmor.10058

    Article  PubMed  Google Scholar 

  • Nebelsick, (1993) Introvert, mouth cone, and nervous system of Echinoderes capitatus (Kinorhyncha, Cyclorhagida) and implications for the phylogenetic relationships of Kinorhyncha. Zoomorphology 113:211–232. https://doi.org/10.1007/BF00403313

    Article  Google Scholar 

  • Neuhaus B (1994) Ultrastructure of alimentary canal and body cavity, ground pattern, and phylogenetic relationships of the Kinorhyncha. Microfauna Mar 9:61–156

    Google Scholar 

  • Neuhaus B (2013) Kinorhyncha (=Echinodera). In: Schmidt-Rhaesa A (ed) Handbook of Zoology. Gastrotricha, Cycloneuralia and Gnathifera. Volume 1: Nematomorpha, Priapulida, Kinorhyncha, Loricifera. De Gruyter, Berlin/Boston, pp. 181–348

  • Neuhaus B, Kegel A (2015) Redescription of Cateria gerlachi (Kinorhyncha, Cyclorhagida) from Sri Lanka and of C. styx from Brazil, with notes on C. gerlachi from India and C. styx from Chile, and the ground pattern of the genus. Zootaxa 3965:1–77. https://doi.org/10.11646/zootaxa.3965.1.1

    Article  PubMed  Google Scholar 

  • Remane A (1933) Verteilung und Organisation der benthonischen Mikrofauna der Kieler Bucht. Wiss Meeresuntersuch 21:161–221

    Google Scholar 

  • Rothe B, Schmidt-Rhaesa A (2004) Probable development from continuous to segmental longitudinal musculature in Pycnophyes kielensis (Kinorhyncha Homalorhagida). Meiofauna Marina 13:21–28

  • Rucci KA, Neuhaus B, Bulnes VN, Cazzaniga NJ (2020) New record of the soft-bodied genus Franciscideres (Kinorhyncha) from Argentina, with notes on its movement and morphological variation. Zootaxa 4780:107–131. https://doi.org/10.11646/zootaxa.4780.1.5

    Article  Google Scholar 

  • Sánchez N, Herranz M, Benito J, Pardos F (2012) Kinorhyncha from the Iberian Peninsula: new data from the first intensive sampling campaigns. Zootaxa 3402:24–44. https://doi.org/10.11646/zootaxa.3402.1.2

    Article  Google Scholar 

  • Schmidt-Rhaesa A, Rothe B (2006) Postembryonic development of dorsoventral and longitudinal musculature in Pycnophyes kielensis (Kinorhyncha, Homalorhagida). Integr Comp Biol 46:144–150. https://doi.org/10.1093/icb/icj019

    Article  PubMed  Google Scholar 

  • Sørensen MV (2008) A new kinorhynch genus from the Antarctic deep-sea and a new species of Cephalorhyncha from Hawaii (Kinorhyncha: Cyclorhagida: Echinoderidae). Org Div Evol 8:233–246. https://doi.org/10.1016/j.ode.2007.11.003

    Article  Google Scholar 

  • Sørensen MV, Landers SC (2017) Description of a new species, Paracentrophyes sanchezae n. sp. (Kinorhyncha: Allomalorhagida) from the Gulf of Mexico, with differential notes on one additional, yet undescribed species of the genus. Zootaxa 4242:61–76. https://doi.org/10.11646/zootaxa.4242.1.3

    Article  PubMed  Google Scholar 

  • Sørensen MV, Pardos F (2020) Kinorhyncha. In: Schmidt-Rhaesa A (ed) Guide to the identification of Marine Meiofauna. Verlag Dr Friedrich Pfeil, Munich, pp 391–414

    Google Scholar 

  • Sørensen MV, Rho HS (2009) Triodontoderes anulap gen. et sp. nov.—a new cyclorhagid kinorhynch genus and species from Micronesia. J Mar Biol Assoc UK 89:1269–1279. https://doi.org/10.1017/S0025315409000526

    Article  Google Scholar 

  • Sørensen MV, Heiner I, Ziemer O, Neuhaus B (2007) Tubulideres seminoli gen. et sp. nov. and Zelinkaderes brightae sp. nov. (Kinorhyncha, Cyclorhagida) from Florida. Helgoland Mar Res 61:247–265

  • Sørensen MV, Herranz M, Rho HS, Min W, Yamasaki H, Sánchez N, Pardos F (2012) On the genus Dracoderes Higgins & Shirayama, 1990 (Kinorhyncha: Cyclorhagida) with a redescription of its type species, D. abei, and a description of a new species from Spain. Mar Biol Res 8:210–232. https://doi.org/10.1080/17451000.2011.615328

    Article  Google Scholar 

  • Sørensen MV, Dal Zotto M, Rho HS, Herranz M, Sánchez N, Pardos F, Yamasaki H (2015) Phylogeny of Kinorhyncha based on morphology and two molecular loci. PLoS ONE 10(7):e0133440. https://doi.org/10.1371/journal.pone.0133440

    Article  CAS  PubMed  Google Scholar 

  • Swedmark B (1964) The interstitial fauna of marine sand. Biol Rev 39:1–42

    Article  Google Scholar 

  • Yamasaki H (2019) Gracilideres mawatarii, a new genus and species of Franciscideridae (Allomalorhagida: Kinorhyncha)—a kinorhynch with thin body cuticle, adapted to the interstitial environment. Zool Anz 282:176–188. https://doi.org/10.1016/j.jcz.2019.05.010

    Article  Google Scholar 

  • Yamasaki H, Hiruta SF, Kajihara H (2013) Molecular phylogeny of kinorhynchs. Mol Phylogenet Evolut 67:303–310. https://doi.org/10.1016/j.ympev.2013.02.016

    Article  Google Scholar 

  • Yildiz NÖ, Sørensen MV, Karaytuğ S (2016) A new species of Cephalorhyncha Adrianov, 1999 (Kinorhyncha: Cyclorhagida) from the Aegean Coast of Turkey. Helgol Mar Res 70:24. https://doi.org/10.1186/s10152-016-0476-5

    Article  Google Scholar 

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Acknowledgments

We are grateful to the Bioimaging facility of University of British Columbia, to the Unidade Integrada de Imagens and Laboratorio de Invertebrados from Instituto de Biodiversidade e Sustentabilidade, Federal University of Rio de Janeiro UFRJ (NUPEM/UFRJ—Macaé) for offering laboratory space; and to Center for Marine Studies, Federal University of Paraná (CEM/UFPR) for offering lab space and student support with field collections in Pontal du Sul in 2015 and 2019.

Funding

This project received funding from the European Union’s Horizon 2020 research and innovation programme, under the Marie Sklodowska-Curie grant agreement No 797140 to MH. Sampling in South Korea was funded by the Carlsberg Foundation to MVS (CF17-0054). CLSM facilities were supported by the Villum foundation (Grant # 102544) and the Carlsberg Foundation to KW (CF15-0946). CLSM imaging at the University of British Columbia was funded by the Hakai Institute (Tula foundation) and the National Science and Engineering Research Council of Canada (NSERC 2019–03986) to BSL.

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MH, MVS, KW conceived the study. MH, MVS, KW, TP, and MDD collected specimens from South Korea and Brazil. MH prepared and performed the experiments and imaging at the University of Copenhagen and University of British Columbia. MH prepared all figures and 3D reconstructions. MH, MVS, and KW drafted the manuscript. All authors have proofed and approved the final version of this manuscript.

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Correspondence to Maria Herranz.

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Supplementary file1 Online resource 1. Movie showing F. kalenesos movement. (MP4 51615 KB)

Supplementary file2 Online resource 2. Movie showing C. styx movement. (MP4 21715 KB)

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Herranz, M., Worsaae, K., Park, T. et al. Myoanatomy of three aberrant kinorhynch species: similar but different?. Zoomorphology 140, 193–215 (2021). https://doi.org/10.1007/s00435-021-00519-3

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