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RESEARCH ARTICLE
Contents Vol 38(3)

Novel molecular resources for single-specimen barcoding of enigmatic crustacean y-larvae

Niklas Dreyer https://orcid.org/0000-0002-1391-1642 A B C D J , Jørgen Olesen https://orcid.org/0000-0001-9582-7083 A * , Mark J. Grygier E , Danny Eibye-Jacobsen https://orcid.org/0000-0002-7079-2627 A , Alexandra S. Savchenko https://orcid.org/0000-0001-6167-5405 F , Yoshihisa Fujita https://orcid.org/0000-0003-1906-746X G , Gregory A. Kolbasov https://orcid.org/0000-0002-3762-1834 H , Ryuji J. Machida https://orcid.org/0000-0003-1687-4709 B , Benny K. K. Chan https://orcid.org/0000-0001-9479-024X B * and Ferran Palero https://orcid.org/0000-0002-0343-8329 I *
+ Author Affiliations
- Author Affiliations

A Natural History Museum of Denmark, University of Copenhagen, Denmark.

B Biodiversity Research Center, Academia Sinica, Taipei, Taiwan.

C Department of Life Science, National Taiwan Normal University, Taipei, Taiwan.

D Biodiversity Program, Taiwan International Graduate Program, Academia Sinica, Taipei, Taiwan.

E National Museum of Marine Biology & Aquarium, Checheng, Pingtung, Taiwan.

F Invertebrate Zoology Department, Biological Faculty, Moscow State University, Moscow, Russian Federation.

G General Education Center, Okinawa Prefectural University of Arts, Naha, Okinawa, Japan.

H White Sea Biological Station, Biological Faculty of Moscow State University, Moscow, Russian Federation.

I Institut Cavanilles de Biodiversitat i Biologia Evolutiva (ICBIBE), University of Valencia, Paterna, Spain.

J Present address: Department of Organismic and Evolutionary Biology, Museum of Comparative Zoology, Harvard University, Cambridge, MA, USA.

* Correspondence to: jolesen@snm.ku.dk

Handling Editor: Shane Ahyong

Invertebrate Systematics 38, IS23018 https://doi.org/10.1071/IS23018
Submitted: 25 April 2023  Accepted: 8 January 2024  Published: 8 March 2024

© 2024 The Author(s) (or their employer(s)). Published by CSIRO Publishing.

Abstract

Despite discovery more than 100 years ago and documented global occurrence from shallow waters to the deep sea, the life cycle of the enigmatic crustacean y-larvae isincompletely understood and adult forms remain unknown. To date, only 2 of the 17 formally described species, all based on larval stages, have been investigated using an integrative taxonomic approach. This approach provided descriptions of the morphology of the naupliar and cyprid stages, and made use of exuvial voucher material and DNA barcodes. To improve our knowledge about the evolutionary history and ecological importance of y-larvae, we developed a novel protocol that maximises the amount of morpho-ecological and molecular data that can be harvested from single larval specimens. This includes single-specimen DNA barcoding and daily imaging of y-nauplii reared in culture dishes, mounting of the last naupliar exuviae on a slide as a reference voucher, live imaging of the y-cyprid instar that follows, and fixation, DNA extraction, amplification and sequencing of the y-cyprid specimen. Through development and testing of a suite of new primers for both nuclear and mitochondrial protein-coding and ribosomal genes, we showcase how new sequence data can be used to estimate the phylogeny of Facetotecta. We expect that our novel procedure will help to unravel the complex systematics of y-larvae and show how these fascinating larval forms have evolved. Moreover, we posit that our protocols should work on larval specimens from a diverse array of moulting marine invertebrate taxa.

Keywords: barcoding, biodiversity, Facetotecta, larval barcoding, molecular resources, new primers, systematics, y-larvae.

References

Hansen HJ (1899) Die Cladoceren und Cirripedien der Plankton-Expedition. Ergebnisse der in dem Atlantischen Ocean von Mitte Juli bis Angang November 1999 ausgeführten Plankton-Expedition der Humboldt-Stiftung 2(G, d), 1-58 [In German].
| Google Scholar |

Hartop E, Srivathsan A, Ronquist F, Meier R (2022) Towards large-scale integrative taxonomy (LIT): resolving the data conundrum for dark taxa. Systematic Biology 71, 1404-1422.
| Crossref | Google Scholar | PubMed |

Hunter SJ, Gooddall T, Walsh K, Owen R, Day JC (2008) Nondestructive DNA extraction from blackflies (Diptera: Simuliidae): retaining voucher specimens for DNA barcoding projects. Molecular Ecology Resources 8(1), 56-61.
| Crossref | Google Scholar |

Itô T (1985) Contributions to the knowledge of cypris y (Crustacea: Maxillopoda) with reference to a new genus and three new species from Japan. Special Publication of the Mukaishima Marine Biological Station 1985, 113-122.
| Google Scholar |

Itô T (1986) Three types of “nauplius y” (Maxillopoda: Facetotecta) from the North Pacific. Publications of the Seto Marine Biological Laboratory 31, 63-73.
| Crossref | Google Scholar |

Kalyaanamoorthy S, Minh BQ, Wong TKF, Von Haeseler A, Jermiin LS (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nature Methods 14, 587-589.
| Crossref | Google Scholar | PubMed |

Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30, 772-780.
| Crossref | Google Scholar | PubMed |

Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Meintjes P, Drummond A (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28(12), 1647-1649.
| Crossref | Google Scholar |

Kolbasov GA, Petrunina AS, Dreyer N, Prudkovsky AA, Olesen J, Chan BKK, Høeg JT (2021) Naupliar development of Facetotecta (Crustacea: Thecostraca) and the nature of the first nauplius instar in the Crustacea – pro et contra the Hexanauplia concept. Organisms Diversity & Evolution 21, 209-230.
| Crossref | Google Scholar |

Kolbasov GA, Savchenko AS, Dreyer N, Chan BKK, Høeg JT (2022) A synthesis of the external morphology of cypridiform larvae of Facetotecta (Crustacea: Thecostraca) and the limits of the genus Hansenocaris. Ecology and Evolution 12, e9488.
| Crossref | Google Scholar | PubMed |

Leray M, Yang JY, Meyer CP, Mills SC, Agudelo N, Ranwez V, Boehm JT, Machida RJ (2013) A new versatile primer set targeting a short fragment of the mitochondrial COI region for metabarcoding metazoan diversity: application for characterizing coral reef fish gut contents. Frontiers in Zoology 10, 34.
| Crossref | Google Scholar |

Lozano-Fernández J, Giacomelli M, Fleming JF, Chen A, Vinther J, Thomsen PF, Glenner H, Palero F, Legg DA, Iliffe TM, Pisani D, Olesen J (2019) Pancrustacean evolution illuminated by taxon-rich genomic-scale data sets with an expanded remipede sampling. Genome Biology and Evolution 11, 2055-2070.
| Crossref | Google Scholar | PubMed |

Minh BQ, Schmidt HA, Chernomor O, Schrempf D, Woodhams MD, Von Haeseler A, Lanfear R (2020) IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Molecular Biology and Evolution 37, 1530-1534.
| Crossref | Google Scholar | PubMed |

Oakley TH, Wolfe JM, Lindgren AR, Zaharoff AK (2013) Phylotranscriptomics to bring the understudied into the fold: monophyletic Ostracoda, fossil placement, and pancrustacean phylogeny. Molecular Biology and Evolution 30, 215-233.
| Crossref | Google Scholar | PubMed |

Olesen J, Grygier MJ (2022) Two new species of lecithotrophic nauplius y with remarkable labra from Okinawa, Japan, and a family-group name for y-larvae (Crustacea: Thecostraca: Facetotecta: Hansenocarididae fam. nov.). Species Diversity 27(2), 301-317.
| Crossref | Google Scholar |

Olesen J, Grygier MJ (in press) Taxonomic diversity of marine planktonic “y-larvae” (Crustacea: Facetotecta) from a coral reef hotspot locality (Japan, Okinawa), with a key to y-nauplii. European Journal of Taxonomy
| Google Scholar |

Olesen J, Dreyer N, Palero F, Eibye-Jacobsen D, Fujita Y, Chan BKK, Grygier MJ (2022) Integrative taxonomy of crustacean y-larvae (Thecostraca: Facetotecta) using laboratory-rearing and molecular analyses of single specimens, with the description of a new vermiform species. Zoological Journal of the Linnean Society 196, 549-592.
| Crossref | Google Scholar |

Olesen J, Grygier MJ, Herranz M (2024) Autofluorescence imaging of exuviae as a tool for studying slide preparations of micro-arthropods, exemplified by a museum collection of the enigmatic crustacean “y-larvae” (Pancrustacea: Facetotecta). Zoomorphology 0, 0 [Published 16 February 2024].
| Crossref | Google Scholar |

Pérez-Losada M, Crandall KA, Kolbasov GA, Høeg JT (2002) Reanalysis of the relationships among the Cirripedia and the Ascothoracida and the phylogenetic position of the Facetotecta (Maxillopoda: Thecostraca) using 18S rDNA sequences. Journal of Crustacean Biology 22, 661-669.
| Crossref | Google Scholar |

Pérez-Losada M, Høeg JT, Crandall KA (2009) Remarkable convergent evolution in specialized parasitic Thecostraca (Crustacea). BMC Biology 7, 15.
| Crossref | Google Scholar | PubMed |

Petrunina AS, Neretina TV, Mugue NS, Kolbasov GA (2014) Tantulocarida versus Thecostraca: inside or outside? First attempts to resolve phylogenetic position of Tantulocarida using gene sequences. Journal of Zoological Systematics and Evolutionary Research 52, 100-108.
| Crossref | Google Scholar |

Regier JC, Shultz JW, Zwick A, Hussey A, Ball B, Wetzer R, Martin JW, Cunningham CW (2010) Arthropod relationships revealed by phylogenomic analysis of nuclear protein-coding sequences. Nature 463, 1079-1083.
| Crossref | Google Scholar | PubMed |

Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539-542.
| Crossref | Google Scholar | PubMed |

Schizas NV, Street GT, Coull BC, Chandler GT, Quattro JM (1997) An efficient DNA extraction method for small metazoans. Molecular Marine Biology and Biotechnology 6(4), 381-383.
| Google Scholar | PubMed |

Schram TA (1972) Further records of nauplius y type IV Hansen from Scandinavian waters. Sarsia 50, 1-24.
| Crossref | Google Scholar |

Schwentner M, Combosch DJ, Pakes Nelson J, Giribet G (2017) A phylogenomic solution to the origin of insects by resolving crustacean-hexapod relationships. Current Biology 27(12), 1818-1824.
| Crossref | Google Scholar | PubMed |

Tsang LM, Chan BKK, Shih FL, Chu KH, Allen Chen C (2009) Host-associated speciation in the coral barnacle Wanella milleporae (Cirripedia: Pyrgomatidae) inhabiting the Millepora coral. Molecular Ecology 18(7), 1463-1475.
| Crossref | Google Scholar | PubMed |

von Reumont BM, Jenner RA, Wills MA, Dell’Ampio E, Pass G, Ebersberger I, Meyer B, Koenemann S, Iliffe TM, Stamatakis A, Niehuis O, Meusemann K, Misof B (2012) Pancrustacean phylogeny in the light of new phylogenomic data: support for Remipedia as the possible sister group of Hexapoda. Molecular Biology and Evolution 29(3), 1031-1045.
| Crossref | Google Scholar | PubMed |

Watanabe HK, Senokuchi R, Shimanaga M, Yamamoto H (2016) Comparison of the efficiency of three methods of DNA extraction for deep-sea benthic copepods. JAMSTEC Report of Research and Development 23, 52-59.
| Crossref | Google Scholar |