Skip to main content
SpringerLink
Log in

Molecular phylogeny of the genus Clibanarius (Decapoda: Anomura: Diogenidae) based on mitochondrial and nuclear DNA sequences

  • Biology
  • Published:
Journal of Oceanology and Limnology Aims and scope Submit manuscript

Abstract

Clibanarius, a genus of hermit crabs, is one of the most diverse genera within Diogenidae. However, studies on the phylogeny within Clibanarius is very limited. We reconstruct the molecular phylogeny of the genus Clibanarius based on two mitochondrial (16S rRNA and COI) and two nuclear protein-coding (NaK and PEPCK) genes using a multigene phylogenetic approach. Eleven selected Clibanarius species from the Indo-West Pacific are analyzed and the Bayesian and maximum likelihood analyses produced identical results in topology. Results suggest that C. rutilus and C. infraspinatus are more closely related to each other than to C. snelliusi, and C. striolatus shows a close relationship to C. longitarsus. The close association of C. merguiensis with C. englaucus and C. humilis is strongly supported by the divergence of C. virescens from them. Our phylogenetic results contradict the morphological classification scheme proposed for Clibanarius and indicate that the relative length of dactyls and propodi is not phylogenetically significant in Clibanarius. In addition, we speculate that the morphological characteristic of the median cleft of the telson might be phylogenetically important for Clibanarius.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Ahyong S T, Schnabel K E, Maas E W. 2009. Anomuran phylogeny: new insights from molecular data. In: Martin J W, Crandall K A, Felder D L eds. Decapod Crustacean Phylogenetics. CRC Press, Boca Raton, FL, USA. p.399–414.

    Chapter  Google Scholar 

  • Asakura A. 2005. Preliminary report of a review of the genus Clibanarius dana, 1852 (Decapoda: Anomura: Diogenidae) from Japan and the adjacent waters. Umiushitsushin, 47: 5–8.

    Google Scholar 

  • Ball E E Jr, Haig J. 1972. Hermit crabs from eastern New Guinea. Pacific Science, 26(1): 87–107.

    Google Scholar 

  • Bracken-Grissom H D, Cannon M E, Cabezas P, Feldmann R M, Schweitzer C E, Ahyong S T, Felder D L, Lemaitre R, Crandall K A. 2013. A comprehensive and integrative reconstruction of evolutionary history for Anomura (Crustacea: Decapoda). BMC Evolutionary Biology, 13: 128.

    Article  Google Scholar 

  • Brandley M C, Schmitz A, Reeder T W. 2005. Partitioned Bayesian analyses, partition choice, and the phylogenetic relationships of scincid lizards. Systematic Biology, 54(3): 373–390.

    Article  Google Scholar 

  • Brandt J F. 1851. Krebse. In: von MiddendorfA T ed. Reise in den Äussersten Norden und Osten Sibiriens Während der Jahre 1843 und 1844 Mit Allerhöchster Genehmigung auf Veranstaltung der Kaiserlichen Akademie der Wissenschaften Zu St. Petersburg Ausgeführt und in Verbinding mit Vielen Gelehrten Herausgegeben. Vol. 2, Part 1. St. Petersburg. p.145–147.

  • Brown J M, Lemmon L R. 2007. The importance of data partitioning and the utility of Bayes factors in Bayesian phylogenetics. Systematic Biology, 56(4): 643–655.

    Article  Google Scholar 

  • Buitendijk A M. 1937. Biological results of the snellius expedition. IV. the paguridea of the snellius expedition. Temminckia, 2: 251–280.

    Google Scholar 

  • Castoe T A, Doan T M, Parkinson C L. 2004. Data partitions and complex models in Bayesian analysis: the phylogeny of Gymnophthalmid. Systematic Biology, 53(3): 448–469.

    Article  Google Scholar 

  • Chen C L, Goy J W, Bracken-Grissom H D, Felder D L, Tsang L M, Chan T Y. 2016. Phylogeny of Stenopodidea (Crustacea: Decapoda) shrimps inferred from nuclear and mitochondrial genes reveals non-monophyly of the families Spongicolidae and Stenopididae and most of their composite genera. Invertebrate Systematics, 30(5): 479–490.

    Article  Google Scholar 

  • Cheng J, Gao T X, Miao Z Q, Yanagimoto T. 2011. Molecular phylogeny and evolution of Scomber (Teleostei: Scombridae) based on mitochondrial and nuclear DNA sequences. Chinese Journal of Oceanology and Limnology, 29(2): 297–310.

    Article  Google Scholar 

  • Chu K H, Tsang L M, Ma K Y, Chan T Y, Ng P K L. 2009. Decapod phylogeny: what can protein-coding genes tell us? In: Martin J W, Crandall K A, Felder D L eds. Decapod Crustacean Phylogenetics. CRC Press, Boca Raton. p.89–99.

    Chapter  Google Scholar 

  • Crandall K A, Fitzpatrick J F Jr. 1996. Crayfish molecular systematics: using a combination of procedures to estimate phylogeny. Systematic Biology, 45(1): 1–26.

    Article  Google Scholar 

  • Dana J D. 1851. Conspectus crustaceorum quae in orbis terrarium circumnavigatione, Carolo Wilkes e classe reipublicae foed eratae duce, lexit et descripsit. Proceedings of the Academy of Natural Sciences of Philadelphia, 5: 247–254.

    Google Scholar 

  • Dana J D. 1852. Conspectus crustaceorum, etc., conspectus of the crustacea of the exploring expedition under Capt. Wilkes, U.S.N., including the paguridea, continued, the megalopidea, and the macroura. paguridea, continued, and subtribe megalopidea. Proceedings of the Academy of Natural Sciences of Philadelphia, 6: 6–28.

    Google Scholar 

  • Danforth B N, Brady S G, Sipes S D, Pearson A. 2004. Single-copy nuclear genes recover cretaceous-age divergences in bees. Systematic Biology, 53(2): 309–326.

    Article  Google Scholar 

  • Danforth B N, Fang J, Sipes S, Brady S G, Almeida E A B, Litman J R, Cardinal S. 2011. Phylogeny and Molecular Systematics of Bees (Hymenoptera: Apoidea). Cornell University, Ithaca, NY.

    Google Scholar 

  • Darriba D, Taboada G L, Doallo R, Posada D. 2012. jModelTest 2: more models, new heuristics and parallel computing. Nature Methods, 9(8): 772.

    Article  Google Scholar 

  • de Grave S, Pentcheff N D, Ahyong S T, Chan T Y, Crandall K A, Dworschak P C, Felder D L, Feldmann R M, Fransen C H J M, Goulding L Y D, Lemaitre R, Low M E Y, Martin J W, Ng P K L, Schweitzer C E, Tan S H, Tshudy D, Wetzer R. 2009. A classification of living and fossil genera of decapod crustaceans. The Raffles Bulletin of Zoology, 21: 1–109.

    Google Scholar 

  • de Haan W. 1833–1850. Crustacea. In: von Siebold P F ed. Fauna Japonica sive Descriptio Animalium, Quae in Itinere per Japoniam, Jussu et Auspiciis Superiorum, qui Summum in India Batava Imperium Tenent, Suspecto, Annis 1823–1830 Collegit, Notis, Observationibus et Adumbrationibus Illustravit. Lugduni-Batavorum, Leiden. p.1–243.

    Google Scholar 

  • de Man J G. 1888. Report on the Podophthalmous Crustacea of the Mergui Archipelago, collected for the Trustees of the Indian Museum, Calcutta, by Dr. John Anderson, F.R.S., Superintendent of the Museum. —Part IV. Journal of the Linnean Society of London, 22(139): 177–240.

    Article  Google Scholar 

  • Excoffier L, Lischer H E L. 2010. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources, 10(3): 564–567.

    Article  Google Scholar 

  • Fabricius J C. 1787. Mantissa insectorum, sistens eorum species nuper detectas adiectis characteribus genericis, differentiis specificis, emendationibus observationibus. Vol. 1. Hafniae: C.G. Proft. xx, p.1–348.

    Google Scholar 

  • Friedlander T P, Regier J C, Mitter C, Wagner D L. 1996. A nuclear gene for higher level phylogenetics: phosphoenolpyruvate carboxykinase tracks mesozoic-age divergences within Lepidoptera (Insecta). Molecular Biology and Evolution, 13(4): 594–604.

    Article  Google Scholar 

  • Guindon S, Dufayard J F, Lefort V, Anisimova M, Hordijk W, Gascuel O. 2010. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology, 59(3): 307–321.

    Article  Google Scholar 

  • Hilgendorf F. 1869. Crustaceen. In: van der Decken C C ed. Reisen in Ost-afrika in den Jahren 1859–1865. Leipzig, Heidelberg. p.69–116.

  • Hilgendorf F. 1879. Die von Herrn W. peters in moçambique gesammelten crustaceen. Monatsberichte der kö niglichen Preussischen Akademie des Wissenschaften zu Berlin, 1878: 782–851.

    Google Scholar 

  • Hirose M, Osawa M, Hirose E. 2010. DNA barcoding of hermit crabs of genus Clibanarius Dana, 1852 (Anomura: Diogenidae) in the Ryukyu Islands, southwestern Japan. Zootaxa, 2414(1): 59–66.

    Article  Google Scholar 

  • Huelsenbeck J P, Ronquist F. 2001. MrBayes: Bayesian inference of phylogeny. Bioinformatics, 17: 754–755.

    Article  Google Scholar 

  • Knowlton N, Mills D K. 1992. The systematic importance of color and color pattern: evidence for complexes of sibling species of snapping shrimp (Caridea: Alpheidae: Alpheus) from the Caribbean and Pacific coasts of Panama. Proceedings of the San Diego Society of Natural History, 18: 1–5.

    Google Scholar 

  • Krauss F. 1843. Die Sudafrikanischen Crustaceen. Eine Zusammenstellung aller bekannten Malacostraca. Bemerkungen über Deren Lebensweise und Geographische Verbreitung, Nebst Beschreibung und Abbildung Mehrerer Neuen Arten. E. Schweizerbart’sche Verlagsbuchhandlung, Stuttgart. p.68.

    Google Scholar 

  • Leys R, Cooper S J B, Schwarz M P. 2002. Molecular phylogeny and historical biogeography of the large carpenter bees, genus Xylocopa (Hymenoptera: Apidae). Biological Journal ofthe Linnean Society, 77(2): 249–266.

    Article  Google Scholar 

  • Li C P, de Grave S, Chan T Y, Lei H C, Chu K H. 2011. Molecular systematics of caridean shrimps based on five nuclear genes: implications for superfamily classification. Zoologischer Anzeiger — A Journal of Comparative Zoology, 250(4): 270–279.

    Article  Google Scholar 

  • Malay M C D, Rahayu D L, Chan T Y. 2018. Hermit crabs of the genera Calcinus Dana, Clibanarius Dana, and Dardanus Paul’son from the PANGLAO 2004 Expedition, with description of a new species and a checklist of the hermit crabs of the Philippines (Crustacea: Anomura: Paguroidea). The Raffles Bulletin of Zoology, 66: 23–65.

    Google Scholar 

  • Mantelatto F L M, Robles R, Biagi R, Felder D L. 2006. Molecular analysis of the taxonomic and distributional status for the hermit crab genera Loxopagurus Forest, 1964 and Isocheles Stimpson, 1858 (Decapoda, Anomura, Diogenidae). Zoosystema, 28(2): 495–506.

    Google Scholar 

  • McLaughlin P A, Komai T, Lemaitre R, Rahayu D L. 2010. Annotated checklist of anomuran decapod crustaceans of the world (exclusive of the Kiwaoidea and families Chirostylidae and Galatheidae of the Galatheoidea) Part I—Lithodoidea, Lomisoidea and Paguroidea. The Raffles Bulletin of Zoology, 23: 5–107.

    Google Scholar 

  • McLaughlin P A, Murray T. 1990. Clibanarius fonticola, New species (Anomura: Paguridea: Diogenidae), from a freshwater pool on Espiritu Santo, Vanuatu. Journal of Crustacean Biology, 10(4): 695–702.

    Article  Google Scholar 

  • McLaughlin P A, Rahayu D L, Komai T, Chan T Y. 2007. A Catalog of the Hermit Crabs (Paguroidea) of Taiwan. National Taiwan Ocean University, Keelung, China.

    Google Scholar 

  • Meyer C P. 2003. Molecular systematics of cowries (Gastropoda: Cypraeidae) and diversification patterns in the tropics. Biological Journal ofthe Linnean Society, 79(3): 401–459.

    Article  Google Scholar 

  • Milne Edwards P M. 1848. Note sur quelques nouvelles espèces du genre Pagure. In: Annales des Sciences Naturelles- Zoologie et Biologie Animale. Paris. p.59–64.

  • Minegishi Y, Aoyama J, Inoue J G, Miya M, Nishida M, Tsukamoto K. 2005. Molecular phylogeny and evolution of the freshwater eels genus Anguilla based on the whole mitochondrial genome sequences. Molecular Phylogenetics and Evolution, 34(1): 134–146.

    Article  Google Scholar 

  • Moritz C, Dowling T E, Brown W M. 1987. Evolution of animal mitochondrial DNA: relevance for population biology and systematics. Annual Review of Ecology and Systematics, 18: 269–292.

    Article  Google Scholar 

  • Moriyama E N, Powell J R. 1997. Synonymous substitution rates in Drosophila: mitochondrial versus nuclear genes. Journal of Molecular Evolution, 45(4): 378–391.

    Article  Google Scholar 

  • Negri M, Lemaitre R, Mantelatto F L. 2014. Molecular and morphological resurrection of Clibanarius symmetricus (Randall, 1840), a cryptic species hiding under the name for the “Thinstripe” hermit crab C. vittatus (Bosc, 1802) (Decapoda: Anomura: Diogenidae). Journal of Crustacean Biology, 34(6): 848–861.

    Article  Google Scholar 

  • Ortmann A E. 1892. Die decapoden-krebse des strassburger museums, mit besonderer berücksichtigung der von herrn dr. döederlein bei Japan und bei den Liu-Kiu-Inseln gesammelten und zur zeit im strassburger museum auf bewahrten formen. IV Theil. Die abtheilungen galatheidea und paguridea. Zoologische Jahrbücher, 6: 241–325.

    Article  Google Scholar 

  • Osawa M, Chan T Y. 2009. Additional records of hermit crabs (Crustacea: Decapoda: Anomura: Paguroidea) from Taiwan. Proceedings of the Biological Society of Washington, 122(3): 317–332.

    Article  Google Scholar 

  • Palero F, Crandall K A. 2009. Phylogenetic inference using molecular data. In: Martin J W, Crandall K A, Felder D L eds. Decapod Crustacean Phylogenetics. CRC Press, Boca Raton. p.67–88.

    Chapter  Google Scholar 

  • Rahayu D L. 1999. Descriptions of two new species of hermit crabs, Clibanarius rubroviria and C. rutilus (Crustacea: Decapoda: Anomura: Diogenidae) from Indonesia. The Raffles Bulletin of Zoology, 47(2): 299–307.

    Google Scholar 

  • Roterman C N, Lee W K, Liu X M, Lin R C, Li X Z, Won Y J. 2018. A new yeti crab phylogeny: vent origins with indications of regional extinction in the East Pacific. PLoS One, 13(3): e0194696.

    Article  Google Scholar 

  • Sha Z L, Xiao L C, Wang Y L. 2015. Study on the Taxonomy of the Family Diogenidae (Crustacea: Decapoda: Anomura: Paguroidea) from China Seas. Science Press, Beijing, China. p.1–252. (in Chinese)

    Google Scholar 

  • Swofford D L. 2002. PAUP*: Phylogenetic Analysis Using Parsimony (and Other Methods). Sinauer Associates, Sunderland, MA.

    Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. 2013. MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution, 30(12): 2 725–2 729.

    Article  Google Scholar 

  • Tirelli T, Pessani D, Silvestro D, Tudge C. 2008. Reproductive biology of Mediterranean hermit crabs: fine structure of spermatophores and spermatozoa of Diogenes pugilator (Decapoda: Anomura) and its bearing on a sperm phylogeny of Diogenidae. Journal of Crustacean Biology, 28(3): 534–542.

    Article  Google Scholar 

  • Tirelli T, Silvestro D, Pessani D, Tudge C C. 2010. Description of the male reproductive system of Paguristes eremita (Anomura, Diogenidae) and its placement in a phylogeny of diogenid species based on spermatozoal and spermatophore ultrastructure. Zoologischer Anzeiger — A Journal of Comparative Zoology, 248(4): 299–312.

    Article  Google Scholar 

  • Toon A, Finley M, Staples J, Crandall K A. 2009. Decapod phylogenetics and molecular evolution. In: Martin J W, Crandall K A, Felder D L eds. Decapod Crustacean Phylogenetics. CRC Press, Boca Raton. p.15–29.

    Chapter  Google Scholar 

  • Tsang L M, Chan T Y, Ahyong S T, Chu K H. 2011. Hermit to King, or Hermit to all: multiple transitions to Crab-like forms from Hermit crab ancestors. Systematic Biology, 60(5): 616–629.

    Article  Google Scholar 

  • Tsang L M, Ma K Y, Ahyong S T, Chan T Y, Chu K H. 2008. Phylogeny of Decapoda using two nuclear protein-coding genes: origin and evolution of the Reptantia. Molecular Phylogenetics and Evolution, 48(1): 359–368.

    Article  Google Scholar 

  • Tsang L M, Schubart C D, Ahyong S T, Lai J C Y, Au E Y C, Chan T Y, Ng P K L, Chu K H. 2014. evolutionary history of true crabs (Crustacea: Decapoda: Brachyura) and the origin of freshwater crabs. Molecular Biology and Evolution, 31(5): 1 173–1 187.

    Article  Google Scholar 

  • Tudge C C. 1997. Phylogeny of the Anomura (Decapoda, Crustacea): spermatozoa and spermatophore morphological evidence. Contributions to Zoology, 67(2): 125–141.

    Article  Google Scholar 

  • Wiegmann B M, Mitter C, Regier J C, Friedlander T P, Wagner D M, Nielsen E S. 2000. Nuclear genes resolve Mesozoicaged divergences in the insect order Lepidoptera. Molecular Phylogenetics and Evolution, 15(2): 242–259.

    Article  Google Scholar 

  • Williams J D, McDermott J J. 2004. Hermit crab biocoenoses: a worldwide review of the diversity and natural history of hermit crab associates. Journal of Experimental Marine Biology and Ecology, 305(1): 1–128.

    Article  Google Scholar 

  • Yoshikawa A, Nakano T, Satoh T P, Asakura A. 2018. A colour variation of Clibanarius virescens (Krauss, 1843) (Decapoda, Anomura) collected from Amami Oshima Island and Okinawa, Japan. Crustaceana, 91(1): 85–101.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institute of Oceanology, Chinese Academy of Sciences, Qingdao, 266071, China

    Wenjie Li, Jiao Cheng, Min Hui & Zhongli Sha

  2. Center for Ocean Mega-Science, Chinese Academy of Sciences, Qingdao, 266071, China

    Jiao Cheng, Min Hui & Zhongli Sha

  3. Laboratory for Marine Biology and Biotechnology, Qingdao National Laboratory for Marine Science and Technology, Qingdao, 266237, China

    Zhongli Sha

  4. University of Chinese Academy of Sciences, Beijing, 100049, China

    Wenjie Li, Jiao Cheng, Min Hui & Zhongli Sha

Authors
  1. Wenjie Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jiao Cheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Min Hui
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Zhongli Sha
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Zhongli Sha.

Additional information

6 Data Availabilty Statement

The datasets generated and/or analyzed during the current study are available from the corresponding author on reasonable request. Sequence data that support the findings of this study have been deposited in GenBank under the accession numbers MH508045-MH508087 and MK076123-MK076149.

Supported by the National Key R&D Program of China (No. 2018YFD0900804), the Project of the S&T Basic Work from the Ministry of Science and Technology of China (Nos. 2014FY110500, 2013FY110700), and the “Key Research Program of Frontier Sciences” of the Chinese Academy of Sciences (No. QYZDB-SSW-DQC036)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, W., Cheng, J., Hui, M. et al. Molecular phylogeny of the genus Clibanarius (Decapoda: Anomura: Diogenidae) based on mitochondrial and nuclear DNA sequences. J. Ocean. Limnol. 37, 1686–1697 (2019). https://doi.org/10.1007/s00343-019-8329-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00343-019-8329-0

Keyword

Search

Navigation