Biodiversity and phylogeny of Ammotheidae (Arthropoda: Pycnogonida)

  • Romain Sabroux UMR 7205, Institut de Systématique, Evolution et Biodiversité, Département Systématique et Evolution, Sorbonne Universités, Muséum national d’Histoire naturelle, 55 rue Buffon, CP 51, 75005 Paris
  • Laure Corbari UMR 7205, Institut de Systématique, Evolution et Biodiversité, Département Systématique et Evolution, Sorbonne Universités, Muséum national d’Histoire naturelle, 55 rue Buffon, CP 51, 75005 Paris
  • Franz Krapp Zoologisches Forschungsmuseum Alexander Koenig, Adenauerallee 160, 53113 Bonn
  • Céline Bonillo UMS CNRS 2700, Muséum national d’Histoire naturelle, CP 26, 57 rue Cuvier, 75231 Paris Cedex 05
  • Stéphanie le Prieur UMS CNRS 2700, Muséum national d’Histoire naturelle, CP 26, 57 rue Cuvier, 75231 Paris Cedex 05
  • Alexandre Hassanin UMR 7205, Institut de Systématique, Evolution et Biodiversité, Département Systématique et Evolution, Sorbonne Universités, Muséum national d’Histoire naturelle, 55 rue Buffon, CP 51, 75005 Paris
Keywords: Pantopoda, taxonomy, DNA phylogeny, barcode of life, strand-bias

Abstract

The family Ammotheidae is the most diversified group of the class Pycnogonida, with 297 species described in 20 genera. Its monophyly and intergeneric relationships have been highly debated in previous studies. Here, we investigated the phylogeny of Ammotheidae using specimens from poorly studied areas. We sequenced the mitochondrial gene encoding the first subunit of cytochrome c oxidase (CO1) from 104 specimens. The complete nuclear 18S rRNA gene was sequenced from a selection of 80 taxa to provide further phylogenetic signal. The base composition in CO1 shows a higher heterogeneity in Ammotheidae than in other families, which may explain their apparent polyphyly in the CO1 tree. Although deeper nodes of the tree receive no statistical support, Ammotheidae was found to be monophyletic and divided into two clades, here defined as distinct subfamilies: Achelinae comprises the genera Achelia Hodge, 1864, Ammothella Verrill, 1900, Nymphopsis Haswell, 1884 and Tanystylum Miers, 1879; and Ammotheinae includes the genera Ammothea Leach, 1814, Acheliana Arnaud, 1971, Cilunculus Loman, 1908, Sericosura Fry & Hedgpeth, 1969 and also Teratonotum gen. nov., including so far only the type species Ammothella stauromata Child, 1982. The species Cilunculus gracilis Nakamura & Child, 1991 is reassigned to Ammothella, forming the binomen Ammothella gracilis (Nakamura & Child, 1991) comb. nov. Additional taxonomic re-arrangements are suggested for the genera Achelia, Acheliana, Ammothella and Cilunculus.

References

Arabi J., Cruaud C., Couloux A. & Hassanin A. 2010. Studying sources of incongruence in arthropod molecular phylogenies: sea spiders (Pycnogonida) as a case study. Comptes Rendus Biologies 333 (5): 438–453. http://dx.doi.org/10.1016/j.crvi.2010.01.018

Arabi J., Judson M.L., Deharveng L., Lourenço W.R., Cruaud C. & Hassanin A. 2012. Nucleotide composition of CO1 sequences in Chelicerata (Arthropoda): detecting new mitogenomic rearrangements. Journal of Molecular Evolution 74 (1–2): 81–95. http://dx.doi.org/10.1007/s00239-012-9490-7

Arango C.P. 2003a. Sea spiders (Pycnogonida, Arthropoda) from the Great Barrier Reef, Australia: new species, new records and ecological annotations. Journal of Natural History 37: 2723–2772. http://dx.doi.org/10.1080/00222930210158771

Arango C.P. 2003b. Molecular approach to the phylogenetics of sea spiders (Arthropoda: Pycnogonida) using partial sequences of nuclear ribosomal DNA. Molecular Phylogenetics and Evolution 28 (3): 588–600. http://dx.doi.org/10.1016/S1055-7903(03)00069-1

Arango C.P. & Wheeler W.C. 2007. Phylogeny of the sea spiders (Arthropoda, Pycnogonida) based on direct optimization of six loci and morphology. Cladistics 23 (3): 255–293. http://dx.doi.org/10.1111/j.1096-0031.2007.00143.x

Arango C.P., Soler-Membrives A. & Miller K.J. 2011. Genetic differentiation in the circum-Antarctic sea spider Nymphon australe (Pycnogonida: Nymphonidae). Deep Sea Research II 58 (1): 212–219. http://dx.doi.org/10.1016/j.dsr2.2010.05.019

Arnaud F. 1971a. Acheliana tropicalis n. gen., n. sp., pycnogonide des récifs coralliens du sud-ouest de Madagascar. Beaufortia 18 (241): 199–204.

Arnaud F. 1971b. Pycnogonides des récifs coralliens de Madagascar. 2. Redescription de Pycnogonum madagascariensis Bouvier, 1911. Téthys 1: 161–64.

Arnaud F. 1972. Pycnogonides des récifs coralliens de Madagascar. 3. Famille des Callipallenidae. Téthys 3: 157–64.

Arnaud F. 1973. Pycnogonides des récifs coralliens de Madagascar. 4. Colossendeidae, Phoxichilidiidae et Endeidae. Téthys 4 (4): 953–960.

Arnaud F. & Bamber R.N. 1987. The biology of Pycnogonida. Advances in Marine Biology 24: 1–96. http://dx.doi.org/10.1016/S0065-2881(08)60073-5

Bachraty C., Legendre P. & Desbruyères D. 2009. Biogeographic relationships among deep-sea hydrothermal vent faunas at global scale. Deep Sea Research I 56 (8): 1371–1378. http://dx.doi.org/10.1016/j.dsr.2009.01.009

Bamber R.N. 2004. Pycnogonids (Arthropoda: Pycnogonida) from French cruises to Melanesia. Zootaxa 551: 1–27.

Bamber R.N. 2007a. Pycnogonida of New Caledonia. In: Payri C.E. & Richer de Forges B. (eds) Compendium of Marine Species of New Caledonia: 255–257. Documents Scientifiques et Techniques, deuxième édition, IRD Nouméa 117.

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

Bamber R.N., El Nagar A. & Arango C. (eds) 2015. Pycnobase: World Pycnogonida Database. Available from http://www.marinespecies.org/pycnobase%20on%20 [accessed 2 Nov. 2015].

Benson D. A., Clark K., Karsch-Mizrachi I., Lipman D.J., Ostell J. & Sayers E.W. 2015. GenBank. Nucleic Acids Research 43 (D1): D30–D35. http://dx.doi.org/10.1093/nar/gku1216

Bouchet P., Héros V., Lozouet P. & Maestrati P. 2008. A quarter-century of deep-sea malacological exploration in the South and West Pacific: Where do we stand? How far to go? In: Héros V., Cowie R.H. &

Bouchet P. (eds) Tropical Deep-Sea Benthos 25: 9–40. Mémoires du Muséum national d’Histoire naturelle 196.

Bouvier E.-L. 1910. Les Pycnogonides à cinq paires de pattes recueillis par la mission antarctique Jean Charcot à bord du Pourquoi Pas? Comptes Rendus des Séances Hebdomadaires de l'Académie des Sciences, Paris 142: 15–22.

Bouvier E.-L. 1923. Pycnogonides. Faune de France 7: 1–69.

Charbonnier S., Vannier J. & Riou B. 2007. New sea spiders from the Jurassic La Voulte-sur-Rhône Lagerstätte. Proceedings of the Royal Society of London B 274 (1625): 2555–2561. http://dx.doi.org/10.1098/rspb.2007.0848

Child C.A. 1982. Pycnogonida from the Western Pacific Islands, I. The Marshall Islands. Proceedings of the Biological Society of Washington 95 (2): 270–281.

Child C.A. 1987. Chapter 16. Pycnogonida of Enewetak Atoll. In: Devaney D.M., Reese E.S., Burch B.L. & Helfrich P. (eds) The Natural History of Enewetak Atoll 2: 179–180. Hawaii, United States Department of Energy, Office of Energy Research, Office of Health and Environmental Research, Ecological Research Division.

Child C.A. 1988. Pycnogonida of the Western Pacific Islands, III: Recent Smithsonian-Philippine expeditions. Smithsonian Contributions to Zoology 468 (1–4): 1–32. http://dx.doi.org/10.5479/si.00810282.468

Child C.A. 1990. Pycnogonida of the Western Pacific Islands, VIII: Recent collections from islands of the Great Barrier Reef, Australia. Proceedings of the Biological Society of Washington 103 (2): 311–335.

Child C.A. 1994. Antarctic and Subantarctic Pycnogonida. 1. The Family Ammotheidae. Washington, DC. Biology of the Antarctic Seas 23: 1–48. http://dx.doi.org/10.1029/AR063p0001

Child C.A. 1996. Pycnogonida of the Western Pacific Islands, XIII: Collections from Indonesia, Melanesia, and Micronesia. Oceanographic Literature Review 4 (44): 366.

Child, C. A. 1998. Pycnogonida of the Western Pacific Islands, XIV: A shallow-water collection from Tonga. Species Diversity 3 (2): 289–300.

Dietz L., Arango C.P., Dömel J.S., Halanych K.M., Harder A.M., Held C., Mahon A.R., Mayer C., Melzer R.R., Rouse G.W., Weis A., Wilson N.G. & Leese F. 2015. Regional differentiation and extensive hybridization between mitochondrial clades of the Southern Ocean giant sea spider Colossendeis megalonyx. Royal Society Open Science 2 (7): e140424. http://dx.doi.org/10.1098/rsos.140424

Dohrn A. 1881. Die Pantopoden des Golfes von Neapel und der angrenzenden Meeres-Abschnitte. Monographie der Fauna und Flora des Golfes von Neapel 3: 1–252.

Fry W.G. 1978. A classification within the pycnogonids. Zoological Journal of the Linnean Society 63 (1–2): 35–58. http://dx.doi.org/10.1111/j.1096-3642.1978.tb02089.x

Griffiths H.J., Arango C.P., Munilla T. & McInnes S.J. 2011. Biodiversity and biogeography of Southern Ocean pycnogonids. Ecography 34 (4): 616–627. http://dx.doi.org/10.1111/j.1600-0587.2010.06612.x

Hassanin A. 2006. Phylogeny of Arthropoda inferred from mitochondrial sequences: strategies for limiting the misleading effects of multiple changes in pattern and rates of substitution. Molecular Phylogenetics and Evolution 38 (1): 100–116. http://dx.doi.org/10.1016/j.ympev.2005.09.012

Hassanin A., Léger N. & Deutsch J. 2005. Evidence for multiple reversals of asymmetric mutational constraints during the evolution of the mitochondrial genome of Metazoa, and consequences for phylo-genetic inferences. Systematic Biology 54 (2): 277–298. http://dx.doi.org/10.1080/10635150590947843

Hedgpeth J.W. 1941. A key to the Pycnogonida of the Pacific coast of North America. Transactions of the San Diego Society of Natural History 9 (26): 253–264. Available from http://biodiversitylibrary.org/page/5715977 [accessed 28 Jan. 2017].

Hedgpeth J.W. 1948. The Pycnogonida of the Western North Atlantic and the Caribbean. Proceedings of the United States Museum 97 (3216): 157–342.

Hoek P.P.C. 1881. Nouvelles études sur les pycnogonides. Archives de Zoologie Expérimentale et Générale 9: 445–542.

Krabbe K., Leese F., Mayer C., Tollrian R. & Held C. 2010. Cryptic mitochondrial lineages in the widespread pycnogonid Colossendeis megalonyx Hoek, 1881 from Antarctic and Subantarctic waters. Polar Biology 33 (3): 281–292. http://dx.doi.org/10.1007/s00300-009-0703-5

León T.M. 2001. Synopsis of the pycnogonids from Antarctic and Subantarctic waters. Polar Biology 24: 941–945. http://dx.doi.org/10.1007/s003000100305

Loman J.C. 1908. Die Pantopoden der Siboga-Expedition. Siboga Expedition 40: 1–88.

Mallatt J.M., Garey J.R. & Shultz J.W. 2004. Ecdysozoan phylogeny and Bayesian inference: first use of nearly complete 28S and 18S rRNA gene sequences to classify the arthropods and their kin. Molecular Phylogenetics and Evolution 31(1): 178–191. http://dx.doi.org/10.1016/j.ympev.2003.07.013

Müller H.-G. 1989. Shallow-water Pycnogonida from coral reefs at Moorea, Society Islands, with description of Rhynchothorax tiahurensis n. sp. Bonner Zoologische Beiträge 40 (2): 123–139.

Müller H.-G. 1990a. Shallow-water Pycnogonida from Kenya and Sri Lanka, with descriptions of three new species. Bonner Zoologische Beiträge 41 (1): 63–79.

Müller H.-G. 1990b. On some Indo-West-Pacific Pycnogonida from the Zoologisk Museum, Copenhagen. Zoologische Abhandlungen, Staatliches Museum für Tierkunde Dresden 45 (10): 103–110.

Munilla T. & Soler-Membrives A. 2009. Check-list of the pycnogonids from Antarctic and sub-Antarctic waters: zoogeographic implications. Antarctic Science 21 (2): 99–111. http://dx.doi.org/10.1017/S095410200800151X

Munilla T. & Soler-Membrives A. 2015. Pycnogonida from the Bellingshausen and Amundsen seas: taxonomy and biodiversity. Polar Biology 38 (3): 413–430. http://dx.doi.org/10.1007/s00300-014-1585-8

Nakamura K. & Child A.C. 1988. Pycnogonida of the western Pacific Islands. V. A collection by the Kakuyo Maru from Samoa. Proceedings of the Biological Society of Washington 101 (4): 809–816. https://dx.doi.org/10.5479/si.00810282.512

Nakamura K. & Child C.A. 1991. Pycnogonida from waters adjacent to Japan. Smithsonian Contributions to Zoology 512 (1–4): 1–74.

Nakamura K., Kano Y., Suzuki N., Namatame T. & Kosaku A. 2007. 18S rRNA phylogeny of sea spiders with emphasis on the position of Rhynchothoracidae. Marine Biology 153 (2): 213–223. http://dx.doi.org/10.1007/s00227-007-0803-0

Posada D. 2008. jModelTest: phylogenetic model averaging. Molecular Biology and Evolution 25 (7): 1253–1256. http://dx.doi.org/10.1093/molbev/msn083

Rambaut A. 2002. Sequence Alignment Editor, version 2.0 alpha 11. Available from http://www.evolve.zoo.ox.ac.uk/ [accessed 28 Jan. 2017].

Ratnasingham S. & Hebert P.D. 2007. BOLD: The Barcode of Life Data System. Molecular Ecology Notes 7 (3): 355–364. http://dx.doi.org/10.1111/j.1471-8286.2007.01678.x

Regier J.C., Shultz J.W., Zwick A., Hussey A., Ball B., Wetze R., Martin J.W. & Cunningham C.W. 2010. Arthropod relationships revealed by phylogenomic analysis of nuclear protein-coding sequences. Nature 463 (7284): 1079–1083. http://dx.doi.org/10.1038/nature08742

Rehm P., Meusemann K., Borner J., Misof B. & Burmester T. 2014. Phylogenetic position of Myriapoda revealed by 454 transcriptome sequencing. Molecular Phylogenetics and Evolution 77: 25–33. http://dx.doi.org/10.1016/j.ympev.2014.04.007

Richer de Forges B., Chan T.-Y., Corbari L., Lemaitre E., Macpherson E., Ahyong S.T. & Ng P.K.L. 2013. The MUSORSTOM-TDSB deep sea benthos exploration programme (1976–2012): An overview of crustacean discoveries and new perspectives on deep-sea zoology and biogeography. In: Ahyong A., Chan T.-Y., Corbari L. & Ng P.K.L. (eds) Tropical Deep-Sea Benthos vol. 27: 13–66. Muséum national d’Histoire naturelle, Paris.

Roeding F., Borner J., Kube M., Klages S., Reinhardt R. & Burmester T. 2009. A 454 sequencing approach for large scale phylogenomic analysis of the common emperor scorpion (Pandinus imperator). Molecular Phylogenetics and Evolution 53 (3): 826–834. http://dx.doi.org/10.1016/j.ympev.2009.08.014

Ronquist F.R. & Huelsenbeck J.P. 2003. MRBAYES: Bayesian phylogenetic inference under mixed models. Bioinformatics 19 (12): 1572–1574. http://dx.doi.org/10.1093/bioinformatics/btg180

Schiaparelli S., Oliverio M., Taviani M., Griffiths H., Lörz A.N. & Albertelli G. 2008. Circumpolar distribution of the pycnogonid-ectoparasitic gastropod Dickdellia labioflecta (Dell, 1990) (Mollusca: Zerotulidae). Antarctic Science 20 (5): 497–498. http://dx.doi.org/10.1017/S0954102008001302

Spalding M.D., Fox H.E., Allen G.R., Davidson N., Ferdaña Z.A., Finlayson M., Halpern B.S., Jorge M.A., Lombana A., Lourie S.A., Martin K.D., McManus E., Molnar J., Recchia C.A. & Robertson J. 2007. Marine ecoregions of the world: a bioregionalization of coastal and shelf areas. BioScience 57 (7): 573–583. http://dx.doi.org/10.1641/B570707

Stephensen K.H. 1933. Havedderkopper (Pycnogonida) og rankefødder (Cirripedia). Danmarks Fauna 38: 1–158.

Stock J.H. 1974. Medio- and infralittoral Pycnogonida collected during the IIOE near the landbase on Nossi-Be, Madagascar. Bulletin Zöologisch Museum 4 (3): 11–18.

Stock J.H. 1994. Indo-west Pacific Pycnogonida collected by some major oceanographic expeditions. Beaufortia 44 (3): 17–77.

Published
2017-02-24
How to Cite
Sabroux, R., Corbari, L., Krapp, F., Bonillo, C., le Prieur, S., & Hassanin, A. (2017). Biodiversity and phylogeny of Ammotheidae (Arthropoda: Pycnogonida). European Journal of Taxonomy, (286). https://doi.org/10.5852/ejt.2017.286