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Postembryonic development of Nymphon australe Hodgson, 1902 (Pycnogonida, Nymphonidae) from Antarctica

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Abstract

Developmental modes in pycnogonids are variable, even between congeneric species. Most of our previous knowledge of pycnogonid life history stages is based on morphological descriptions of the larval and those postlarval instars still retained on male ovigers, whereas the free-living instars are largely unknown. In this paper, a combination of morphological and molecular tools is used in order to link those postlarval instars retained on male ovigers to free-living specimens representing putatively later stages in the postembryonic development of a sea spider species. Male specimens of Nymphon australe carrying postembryonic instars were collected from localities off the South Shetland Islands, the Weddell Sea, the Drake Passage, the Bransfield Strait, and the Ross Sea. Three subsequent free-living instars were collected from Drake Passage. Nymphon australe hatch as a postlarval instar with two-articled palps and limb buds of the two first-walking legs. Postlarval instars 1 and 2 (both carried on the ovigers of males), postlarval instars 3 and 4, and a juvenile (all three free living) are all described and illustrated. A molecular phylogenetic based on the cox1 gene links all free-living stages to N. australe populations from the Antarctic Peninsula. The postlarval development of N. australe is discussed here and compared with those known from other pycnogonid species with similar development pathways.

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References

  • Alexeeva N, Bogomolova E, Tamberg Y, Shunatova N (2017) Oligomeric larvae of the pycnogonids revisited. J Morphol. https://doi.org/10.1002/jmor.20713

    Article  PubMed  Google Scholar 

  • Alexeeva N, Tamberg Y, Shunatova N (2018) Postembryonic development of pycnogonids: a deeper look inside. Arthropod Struct Dev 47:299–317

    Article  Google Scholar 

  • Arabi J, Cruaud C, Couloux A, Hassanin A (2010) Studying sources of incongruence in arthropod molecular phylogenies: sea spiders (Pycnogonida) as a case study. C R Biol 333:438–453

    Article  CAS  Google Scholar 

  • Arango CP (2002) Morphological phylogenetics of the sea spiders (Arthropoda: Pycnogonida). Org Divers Evol 2:107–125

    Article  Google Scholar 

  • Arango CP, Wheeler WC (2007) Phylogeny of the sea spiders (Arthropoda, Pycnogonida) based on direct optimization of six loci and morphology. Cladistics 23:1–39

    Article  Google Scholar 

  • Arango CP, Soler-Membrives A, Miller KJ (2011) Genetic differentiation in the circum-Antarctic sea spider Nymphon australe (Pycnogonida; Nymphonidae). Deep Sea Res II 58:212–219

    Article  CAS  Google Scholar 

  • Arnaud F, Bamber R (1987) The biology of Pycnogonida. Adv Mar Biol 24:1–96

    Google Scholar 

  • Bain BA (1992) Pycnogonid higher classification and a revision of the genus Austropallene (Family Callipallenidae). Ph.D. Diss., City University of New York, New York

  • Bain BA (2003a) Larval types and a summary of postembryonic development within the pycnogonids. Invertebr Reprod Dev 43:193–222

    Article  Google Scholar 

  • Bain BA (2003b) Postembryonic development in the pycnogonid Austropallene cornigera (Family Callipallenidae). Invertebr Reprod Dev 43:181–192

    Article  Google Scholar 

  • Bamber RN (2007) A holistic re-interpretation of the phylogeny of the Pycnogonida Latreille, 1810 (Arthropoda). Zootaxa 1668:295–312

    Article  Google Scholar 

  • Bamber RN, El Nagar A (eds) (2018) PycnoBase: world pycnogonida database. https://www.marinespecies.org/pycnobase/. Accessed 7 Sept 2018

  • Behrens W (1984) Larvenentwicklung und Metamorphose von Pycnogonum litorale (Chelicerata, Pantopoda). Zoomorphology 104:266–279

    Article  Google Scholar 

  • Bogomolova EV (2007) Larvae of three sea spider species of the Genus Nymphon (Arthropoda: Pycnogonida) from the White Sea. Russ J Mar Biol 33:145–160

    Article  Google Scholar 

  • Bogomolova EV (2010) Nymphon macronyx (Arthropoda, Pycnogonida), another pycnogonid species with lecytotrophic protonymphon development. Zool Zh 89:528–544

    Google Scholar 

  • Bogomolova EV, Malakhov VV (2003) Larvae of sea spiders (Arthropoda, Pycnogonida) of the White Sea. Entomol Rev 82:213–227

    Google Scholar 

  • Bogomolova EV, Malakhov VV (2004) Fine morphology of sea spider larvae (Arthropoda, Pycnogonida) of the White Sea. Zool Bespozvon 1:3–28

    Google Scholar 

  • Bogomolova EV, Malakhov VV (2006) Lecithotrophic protonymphon is a special type of postembryonic development of sea spiders (Arthropoda, Pycnogonida). Dokl Biol Sci 409:328–331

    Article  Google Scholar 

  • Brenneis G, Arango CP (2019) First description of epimorphic development in Antarctic Pallenopsidae (Arthropoda, Pycnogonida) with insights into the evolution of the four-articled sea spider cheliphore. Zool Lett 5:4. https://doi.org/10.1186/s40851-018-0118-7

    Article  Google Scholar 

  • Brenneis G, Arango CP, Scholtz G (2011a) Morphogenesis of Pseudopallene sp. (Pycnogonida, Callipallene) II: postembryonic development. Dev Genes Evol 221:329–350. https://doi.org/10.1007/s00427-011-0381-5

    Article  PubMed  Google Scholar 

  • Brenneis G, Arango CP, Scholtz G (2011b) Morphogenesis of Pseudopallene sp (Pycnogonida, Callipallene) I: embryonic development. Dev Genes Evol 221:309–328. https://doi.org/10.1007/s00427-011-0382-4

    Article  PubMed  Google Scholar 

  • Brenneis G, Bogomolova EV, Arango CP, Krapp F (2017) From egg to no-body: an overview and revision of developmental pathways in the ancient arthropod linage Pycnogonida. Front Zool 14:6. https://doi.org/10.1186/s12983-017-0192-2

    Article  PubMed  PubMed Central  Google Scholar 

  • Burris ZP (2011) Larval morphologies and potential developmental modes of eight sea spider species (Arthropoda: Pycnogonida) from the southern Oregon coast. J Mar Biol Assoc 91:845–855. https://doi.org/10.1017/S0025315410001554

    Article  Google Scholar 

  • Cano-Sánchez E, López-González PJ (2009) Novel mode of postembryonic development in Ammothea genus (Pycnogonida: Ammotheidae) from Antarctic waters. Sci Mar 73:541–550

    Article  Google Scholar 

  • Cano-Sánchez E, López-González PJ (2010) Postembryonic development of Nymphon unguiculatum Hodgson 1915 (Pycnogonida, Nymphonidae) from the South Shetland Islands (Antarctica). Polar Biol 33:1205–1214. https://doi.org/10.1007/s00300-010-0810-3

    Article  Google Scholar 

  • Cano-Sánchez E, López-González PJ (2013) New data concerning postembryonic development in Antarctic Ammothea species (Pycnogonida: Ammotheidae). Polar Biol 36:1175–1193. https://doi.org/10.1007/s00300-013-1338-0

    Article  Google Scholar 

  • Child CA (1995) Antarctic and subantarctic Pycnogonida III. The Family Nymphonidae. In: Cairns SD (ed) Biology of the Antarctic seas XXIII. Antarct Res Ser 69:1–68

  • Clement M, Snell Q, Walke P, Posada D, Crandall K (2002) TCS: estimating gene genealogies. In: Proceedings 16th International Parallel and Distributed Processing Symposium, vol 2, p 184

  • Dogiel V (1913) Embryologische studien an pantopoden. Z Wiss Zool 107:575–741

    Google Scholar 

  • Dohrn A (1881) Die Pantopoden des Golfes von Neapel und der angrenzenden Meeres-Abschnitte. Fauna und Flora des Golfes von Neapel. Verlag von Wilhem Engelmann, Leipzig

    Google Scholar 

  • Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucl Acids Res. 32:1792–1797. https://doi.org/10.1093/nar/gkh340

    Article  CAS  PubMed  Google Scholar 

  • 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. Mol Mar Biol Biotech 3:294–299

    CAS  Google Scholar 

  • Fornshell JA (2015) Larval stages of two deep sea pycnogonids. Invertebr Zool 12:197–205. https://doi.org/10.15298/invertzool.12.2.05

    Article  Google Scholar 

  • Fornshell JA (2017) Larval stages Nymphon charcoti Bouvier 1911. Arthropods 6:1–7

    Google Scholar 

  • Fornshell JA (2019) Early post hatching stages of Nymphon australe Hodgson. Arthropods 8:45–52

    Google Scholar 

  • Gillespie JM, Bain BA (2006) Postembryonic development of Tanystylum bealensis (Pycnogonida, Ammotheidae) from Barkley Sound, British Columbia, Canada. J Morphol 267:308–317

    Article  CAS  Google Scholar 

  • Hedgpeth JW (1947) On the evolutionary significance of the Pycnogonida. Smithson Misc Coll 106:1–54

    Google Scholar 

  • Hoang DT, Chernomor O, von Haeseler A, Minh BQ, Vinh LS (2018) UFBoot2: improving the ultrafast bootstrap approximation. Mol Biol Evol 35:518–522. https://doi.org/10.1093/molbev/msx281

    Article  CAS  PubMed  Google Scholar 

  • Hoek PPC (1881) Report on the Pycnogonida, dredged by HMS challenger during the years 1973–1976. Chall Rep Zool 3:1–167

    Google Scholar 

  • Hooper J (1980) Some aspects of the reproductive biology of Parapallene avida Stock (Pycnogonida: Callipallenidae) from Northern New South Wales. Aust Zool 30:473–783

    Google Scholar 

  • Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler A, Jermiin LS (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods 14:587–589. https://doi.org/10.1038/nmeth.4285

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leigh JW, Bryant D (2015) PopART: full-feature software for haplotype network construction. Methods Ecol Evol 6:1110–1116

    Article  Google Scholar 

  • Mahon AR, Arango CP, Halanych KM (2008) Genetic diversity of Nymphon (Arthropoda: Pycnogonida: Nymphonidae) along the Antarctic Peninsula with a focus on Nymphon australe Hodgson 1902. Mar Biol 155:315–323. https://doi.org/10.1007/s00227-008-1029-5

    Article  Google Scholar 

  • Mercier A, Baillon S, Hamel JF (2015) Life history and feeding biology of the deep-sea pycnogonid Nymphon hirtipes. Deep Sea Res I 106:1–8. https://doi.org/10.1016/j.dsr.2015.08.015

    Article  Google Scholar 

  • Munilla T, Soler-Membrives A (2009) Check-list of the pycnogonids from Antarctic and sub-Antarctic waters: zoogeographic implications. Antarct Sci 21:99–111

    Article  Google Scholar 

  • Nakamura K (1981) Post-embryonic development of a pycnogonid, Propallene longiceps. J Nat Hist 15:49–62

    Article  Google Scholar 

  • Nakamura K, Kano Y, Suzuki N, Namatame T, Kosaku A (2007) 18S rRNA phylogeny of sea spiders with emphasis on the position of Rhynchothoracidae. Mar Biol. https://doi.org/10.1007/s00227-007-0803-0

    Article  Google Scholar 

  • Nguyen LT, Schmidt HA, von Haeseler A, Minh BQ (2015) IQTREE: a fast and effective stochastic algorithm for estimating maximumlikelihood phylogenies. Mol Biol Evol 32:268–274. https://doi.org/10.1093/molbev/msu300

    Article  CAS  Google Scholar 

  • Okuda S (1940) Metamorphosis of a pycnogonid parasitic in a hydromedusa. J Fac Sci Hokkaido Imp Univ Zool 7:73–86

    Google Scholar 

  • Sánchez S (1959) Le développement des pycnogonides et leurs affinites avec les arachnides. Arch Zool Exp Gén 98:1–102

    Google Scholar 

  • Soler-Membrives A, Linse K, Miller KJ, Arango CP (2017) Genetic signature of Last Glacial Maximum regional refugia in a circum-Antarctic sea spider. R Soc open sci 4:170615. https://doi.org/10.1098/rsos.170615

    Article  PubMed  PubMed Central  Google Scholar 

  • Tomaschko KH, Wilhelm E, Bückmann D (1997) Growth and reproduction of Pycnogonum littorale (Pycnogonida) under laboratory conditions. Mar Biol 129:595–600

    Article  Google Scholar 

  • Vilpoux K, Waloszek D (2003) Larval development and morphogenesis of the sea spider Pycnogonum litorale (Ström, 1762) and the tagmosis of the body of Pantopoda. Arthropod Struct Dev 32:349–383

    Article  Google Scholar 

  • Wilhelm E, Bückmann D, Tomaschko KH (1997) Life cycle and population dynamics of Pycnogonum litorale (Pycnogonida) in a natural habitat. Mar Biol 129:601–606

    Article  Google Scholar 

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Acknowledgements

The authors wish to thank the officers and crew and many colleagues for their help on board during the cruise VLT-2004 (Italica, XIX Spedizione), Polarstern ANT-XXIII/8, and Polarstern ANT-XXIX/3. We take this opportunity to extend our thanks to the cruise leader and steering committee of these cruises, especially Riccardo Cattaneo (Università Politecnica delle Marche, Ancona, Italy) and Maria Chiara Chiantore (Università degli Studi di Genova, Genoa, Italy), Julian Gutt (Alfred Wegener Institut, Bremerhaven), and Enrique Isla (Instituto de Ciencias del Mar, CSIC, Barcelona), who kindly facilitated the work on board and provided the opportunity to collaborate in these Antarctic programmes. Support for this work was provided by projects CGL2004-20062-E (VTL-2004) and POL2006-06399/CGL (CLIMANT) funded by the Spanish CICYT and by the Project CTM2012-39350-C02-01 (ECOWED) funded by the Ministerio de Economía y Competitividad (Plan Nacional de I + D + i 2008–2011). Sequencing was supported by US National Science Foundation (NSF) Grant No. IOS-1552610 to PPS. Mr. Tony Krupa is thanked for reviewing the English version.

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Correspondence to Esperanza Cano-Sánchez.

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Cano-Sánchez, E., Sharma, P.P. & López-González, P.J. Postembryonic development of Nymphon australe Hodgson, 1902 (Pycnogonida, Nymphonidae) from Antarctica. Polar Biol 43, 207–223 (2020). https://doi.org/10.1007/s00300-020-02624-3

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