Exploring evolutionary trends within the Pennellidae (Copepoda: Siphonostomatoida) using molecular data.
Journal
Systematic parasitology
ISSN: 1573-5192
Titre abrégé: Syst Parasitol
Pays: Netherlands
ID NLM: 8111384
Informations de publication
Date de publication:
08 2022
08 2022
Historique:
received:
23
12
2021
accepted:
11
04
2022
pubmed:
19
5
2022
medline:
29
6
2022
entrez:
18
5
2022
Statut:
ppublish
Résumé
The family Pennellidae comprises ecto- and mesoparasitic copepods on marine fishes. Although a preliminary scheme of phylogenetic relationships of pennellids based on morphological characters exists, it is difficult to objectively define character states because of their highly modified bodies and reduced appendages. This molecule-based study analysed phylogenetic relationships among seven genera and 12 species of pennellids, using 18S and 28S ribosomal DNA sequences in order to infer evolutionary trends within the family. Our molecular analysis recovered three clades (Clade-I, Peniculus; Clade-II, Haemobaphes-Lernaeocera-Phrixocephalus-Exopenna-Lernaeenicus radiatus; and Clade-III, Pennella-Lernaeenicus spp.). This result was congruent with some of the morphology-based phylogenetic relationships previously proposed but did not support a sister group comprising Exopenna, Phrixocephalus and Pennella. The second and third offshoots after the divergence of Clade-I species are characterized by reduced body tagmosis and changes in lifestyle from ectoparasites to mesoparasites. In some gill parasites of Clade-II, their sigmoid-shaped bodies and coiled egg strings have likely evolved in adaptation to the limited available space within the gill cavities of the hosts. Phrixocephalus is an eye parasite in Clade-II, which also has coiled egg strings, may have descended from an ancestral gill parasite. All species of Clade-III are characterized by the possession of a head region with processes deeply embedded into the host tissues and functioning as an anchor.
Identifiants
pubmed: 35583766
doi: 10.1007/s11230-022-10040-w
pii: 10.1007/s11230-022-10040-w
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
477-489Informations de copyright
© 2022. The Author(s), under exclusive licence to Springer Nature B.V.
Références
Aneesh, P.T., Helna, A. K., & Bijukumar, A. (2020). New species of Acanthochondria Oakley, 1930 and Chondracanthus Delaroche, 1811 (Copepoda: Cyclopoida: Chondracanthidae) parasitizing marine fishes from Indian waters. Nauplius, 28, 1–21. https://doi.org/10.1590/2358-2936e2020014
Aneesh, P. T., Helna, A. K., Bijukumar, A., & Maran, B. A. V. (2018). Redescription of Lernaeenicus stromatei Gnanamuthu, 1953 (Copepoda: Siphonostomatoida: Pennellidae) infesting the Black Pomfret Parastromateus niger (Bloch) from Indian waters. Zootaxa, 4482, 375–382. https://doi.org/10.11646/zootaxa.4482.2.9
Aneesh, P. T., Helna, A. K., Bijukumar, A., & Maran, B. A. V. (2021). A new species of parasitic copepod of the genus Lernaeenicus Lesueur, 1824 (Siphonostomatoida: Pennellidae) from the torpedo scad Megalaspis cordyla (Linnaeus) off Kerala coast of Arabian Sea, India. Marine Biology Research, 17, 1–11. https://doi.org/10.1080/17451000.2021.1887498
doi: 10.1080/17451000.2021.1887498
Blanco-Bercial, L., Bradford-Grieve, J., & Bucklin, A. (2011). Molecular phylogeny of the Calanoida (Crustacea: Copepoda). Molecular Phylogenetics and Evolution, 59, 103–113.
doi: 10.1016/j.ympev.2011.01.008
Boxshall, G. A. (1986). A new genus and two new species of Pennellidae (Copepoda: Siphonostomatoida) and an analysis of evolution within the family. Systematic Parasitology, 8, 215–225. https://doi.org/10.1007/BF00009890
doi: 10.1007/BF00009890
Boxshall, G. A., & Halsey, S. H. (2004). An introduction to copepod diversity. The Ray Society.
Boxshall, G. A., & Justine, J. L. (2005). A new genus of parasitic copepod (Siphonostomatoida: Caligidae) from a Razorback Scabbardfish, Assurger anzac Alexander (Trichiuridae) off New Caledonia. Folia Parasitologica, 52, 349–358.
doi: 10.14411/fp.2005.048
Brooker, A. J., Shinn, A. P., & Bron, J. E. (2007). A review of the biology of the parasitic copepod Lernaeocera branchialis (L.,1767) (Copepoda: Pennellidae). Advances in Parasitology, 65, 297–341. https://doi.org/10.1016/S0065-308X(07)65005-2
doi: 10.1016/S0065-308X(07)65005-2
pubmed: 18063099
Freeman, M. A., Anshary, H., & Ogawa, K. (2013). Multiple gene analyses of caligid copepods indicate that the reduction of a thoracic appendage in Pseudocaligus represents convergent evolution. Parasites & Vectors, 6, 336. https://doi.org/10.1186/1756-3305-6-336
doi: 10.1186/1756-3305-6-336
Hata, H., Sogabe, A., Tada, S., Nishimoto, R., Nakano, R., Kohya, N., Takeshima, H., & Kawanishi, R. (2017). Molecular phylogeny of obligate fish parasites of the family Cymothoidae (Isopoda, Crustacea): evolution of the attachment mode to host fish and the habitat shift from saline water to freshwater. Marine Biology, 164, 105. https://doi.org/10.1007/s00227-017-3138-5
doi: 10.1007/s00227-017-3138-5
Hirabayashi, T., Ohtsuka, S., Urata, M., Tomikawa, K., & Tanaka, H. (2016). Molecular evidence on evolutionary switching from particle-feeding to sophisticated carnivory in the calanoid copepod family Heterorhabdidae: drastic and rapid changes in functions of homologues. Journal of Natural History, 50, 1759–1772.
doi: 10.1080/00222933.2016.1155779
Hirose, E., & Uyeno, D. (2016). Regional differentiation of the cuticular surface structure in the mesoparasitic copepod Cardiodectes shini (Siphonostomatoida: Pennellidae) on a pygmy goby. Invertebrate Survival Journal, 13, 134–139.
Ho, J. S., & Kim, I. H. (1996). Copepods parasitic on fishes of western North Pacific. Publications of the Seto Marine Biological Laboratory, 37, 275–303.
doi: 10.5134/176263
Hogans, W. E. (2017). Review of Pennella Oken, 1816 (Copepoda: Pennellidae) with a description of Pennella benzi sp. nov., a parasite of escolar, Lepidocybium flavobrunneum (Pisces) in the northwest Atlantic Ocean. Zootaxa, 4244, 1–38. https://doi.org/10.11646/zootaxa.4244.1.1
Hogans, W. E. (2018). Functional morphology and structural variability in Lernaeenicus (Copepoda: Pennellidae) parasitic on teleost fishes from the northwest Atlantic Ocean. Comparative Parasitology, 85, 13–26. https://doi.org/10.1654/1525-2647-85.1.13
doi: 10.1654/1525-2647-85.1.13
Huys, R., Hughes, J. L., Dalton, S. C., Olson, P. D., Spinks, J. N., & Johnston, A. D. (2007). Extraordinary host switching in siphonostomatoid copepods and the demise of the Monstrilloida: Integrating molecular data, ontogeny and antennulary morphology. Molecular Phylogenetics and Evolution, 43, 368–378. https://doi.org/10.1016/j.ympev.2007.02.004
doi: 10.1016/j.ympev.2007.02.004
pubmed: 17383905
Huys, R., Hughes, J. L., Olson, P. D., & Nagasawa, K. (2006). Small subunit rDNA and Bayesian inference reveal Pectenophilus ornatus (Copepoda incertae sedis) as highly transformed Mytilicolidae, and support assignment of Chondracanthidae and Xarifiidae to Lichomolgoidea (Cyclopoida). Biological Journal of the Linnean Society, 87, 403–425. https://doi.org/10.1111/j.1095-8312.2005.00579.x
doi: 10.1111/j.1095-8312.2005.00579.x
Kabata, Z. (1979). Parasitic Copepoda of British Fishes. The Ray Society.
Katoh, K., & Standley, D. M. (2013). MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution, 30, 772–780. https://doi.org/10.1093/molbev/mst010
doi: 10.1093/molbev/mst010
pubmed: 23329690
pmcid: 3603318
Kruger, W., Avenant-Oldewage, A., & Oldewage, W.H. (1998). A diagnostic species compendium of the genus Mugilicola Tripathi, 1960 (Copepoda). South African Journal of Wildlife Research, 28, 33–46.
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
doi: 10.1093/molbev/msy096
pubmed: 29722887
pmcid: 5967553
Leis, J.M. (1978). Systematics and zoogeography of the porcupine fishes (Diodon, Diodontidae, Tetraodontiformes), with comments on egg and larval development. Fishery Bulletin, 76, 535–567.
Lovy, J., & Friend, S. E. (2020). Black sea bass are a host in the developmental cycle of Lernaeenicus radiatus (Copepoda: Pennellidae): insights into parasite morphology, gill pathology and genetics. Parasitology, 147, 478–490. https://doi.org/10.1017/S0031182019001781
doi: 10.1017/S0031182019001781
pubmed: 31852554
Nakabo, T. (2013). Fishes of Japan with Pictorial Keys to the Species. The Third Edition. Tokai University Press.
Nitta, M., Hotta, T., & Nagasawa, K. (2017). New record of Lernaeenicus ramosus (Copepoda: Pennellidae) parasitic on Epinephelus akaara (Perciformes: Serranidae) from the Amakusa-nada Sea, western Japan. Biogeography, 19, 80–84.
Nylander, J. A. A. (2004). MrModeltest. Program distributed by the author. Evolutionary Biology Centre, Uppsala University.
Ohtsuka, S., Lindsay, D. J., & Izawa, K. (2018a). A new genus and species of the family Pennellidae (Copepoda, Siphonostomatoida) infecting the Pacific viperfish Chauliodus macouni. Parasite, 25, 6.
doi: 10.1051/parasite/2018003
Ohtsuka, S., Nishikawa, J., & Boxshall, G. A. (2018b). A new species of Peniculus (Copepoda: Siphonostomatoida) parasitizing mesopelagic myctophid fish: first discovery of colonization of the genus in deep water. Parasite, 25, 58.
doi: 10.1051/parasite/2018057
Ohtsuka, S., Piasecki, W., Ismail, N., & Kamarudin, A. S. (2020). A new species of Brachiella (Copepoda, Siphonostomatoida, Lernaeopodidae) from Peninsular Malaysia, with relegation of two genera Charopinopsis and Eobrachiella to junior synonyms of Brachiella. Parasite, 27, 40.
doi: 10.1051/parasite/2020038
R Development Core Team. (2016). R v4.0.3. R Foundation for Statistical Computing, Vienna. http://www.R-project.org .
Rambaut, A. (2012). FigTree v1.4. Institute of Evolutionary Biology, University of Edinburgh, Edinburgh. http://tree.bio.ed.ac.uk/software/figtree/ .
Rambaut, A., Drummond, A. J., Xie, D., Baele, G., & Suchard, M. A. (2018). Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Systematics and Evolution, 67, 901–904. https://doi.org/10.1093/sysbio/syy032
doi: 10.1093/sysbio/syy032
Rijin, K., Mumthaz, T., Sudha, K., & Gopinathan, A. (2019). Clupeid fish hosts a Peniculus sp. (Pennellidae, Siphonostomatoida, Copepoda)—First report on new host and season dependent prevalence. Acta Oceanologica Sinica, 38, 118–125. https://doi.org/10.1007/s13131-019-1517-0
doi: 10.1007/s13131-019-1517-0
Ronquist, F., Teslenko, M., Mark, P. V. D., Ayres, D. L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M. A., & Huelsenbeck, J. P. (2012). MrBayes 3.2: efficient bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61, 539–542. https://doi.org/10.1093/sysbio/sys029
doi: 10.1093/sysbio/sys029
pubmed: 22357727
pmcid: 3329765
Shih, H. T., Ng, P. K. L., Davie, P. J. F., Schubart, C. D., Türkay, M., Naderloo, R., Jones, D. S., & Liu, M. Y. (2016). Systematics of the family Ocypodidae Rafinesque, 1815 (Crustacea: Brachyura), based on phylogenetic relationships, with a reorganization of subfamily rankings and a review of the taxonomic status of Uca Leach, 1814, sensu lato and its subgenera. Raffles Bulletin of Zoology, 64, 139–175.
Shiino, S. (1956a). Copepods parasitic on Japanese fishes. 11. Genus Phrixocephalus. Report of Faculty of Fisheries, Prefectural University of Mie, 2, 242–267.
Shiino, S. (1956b). Copepods parasitic on Japanese fishes. 7. Peniculus and Peniculisa. Japanese Journal of Zoology, 11, 593–608.
Song, Y., Wang, G.T., Yao, W. J., Gao, Q., & Nie, P. (2008). Phylogeny of freshwater parasitic copepods in the Ergasilidae (Copepoda: Poecilostomatoida) based on 18S and 28S rDNA sequences. Parasitology Research, 102, 299–306. https://doi.org/10.1007/s00436-007-0764-8
doi: 10.1007/s00436-007-0764-8
pubmed: 17940799
Stamatakis, A. (2006). RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics, 22, 2688–2690. https://doi.org/10.1093/bioinformatics/btl446
doi: 10.1093/bioinformatics/btl446
pubmed: 16928733
Stamatakis, A., Hoover, P., & Rougemont, J. (2008). A rapid bootstrap algorithm for the RAxML web servers. Systematic Biology, 57, 758–771. https://doi.org/10.1080/10635150802429642
doi: 10.1080/10635150802429642
pubmed: 18853362
Suzuki, N., Murakami, K., Takeyama, H., & Chow, S. (2006). Molecular attempt to identify prey organisms of lobster phyllosoma larvae. Fisheries Science, 72, 342–349. https://doi.org/10.1111/j.1444-2906.2006.01155.x
doi: 10.1111/j.1444-2906.2006.01155.x
Tokşen, E., Boxshall, G.A., & Altinozek, S. (2012). Sagum posteli Delamare Deboutteville & Nunes-Ruivo, 1954 (Copepoda: Siphonostomatoida: Lernanthropidae) parasitic on Epinephelus aeneus (Geoffroy Saint-Hilaire) in Turkish waters, with a key to the species of Sagum Wilson, 1913. Systematic Parasitology, 82, 71–80. https://doi.org/10.1007/s11230-012-9350-2
doi: 10.1007/s11230-012-9350-2
pubmed: 22488434
Vidjak, O., Zorica, B., & Sinovčič, G. (2008). First record of parasitic copepod Peniculus fistula von Nordmann, 1832 (Siphonostomatoida: Pennellidae) from garfish Belone belone (Linnaeus, 1761) in the Adriatic Sea. Cahiers de Biologie Marine, 49, 209–213.
Walter, T.C., & Boxshall, G. A. (2021). World of Copepods database. Retrieved January 12, 2021, from http://www.marinespecies.org/copepoda . https://doi.org/10.14284/356
Whitfield, P. J., Pilcher, M.W., Grant, H. J., & Riley, J. (1988). Experimental studies on the development of Lernaeocera branchialis (Copepoda: Pennellidae): population processes from egg production to maturation on the flatfish host. Biology of Copepods, 47, 579–586. https://doi.org/10.1007/978-94-009-3103-9_68
doi: 10.1007/978-94-009-3103-9_68