Description of a new genus and two new species of Darwinulidae (Crustacea, Ostracoda), from Christmas Island (Indian Ocean) with some considerations on the morphological evolution of ancient asexuals

Authors

  • Giampaolo Rossetti University of Parma, Department of Environmental Sciences, Viale G.P. Usberti 33A, I-43100 Parma, Italy
  • Ricardo L. Pinto University of Brasília, Institute of Geosciences, Laboratory of Micropaleontology, ICC, Campus Universitário Darcy Ribeiro Asa Norte, 70910-900 Brasilia, DF, Brazil
  • Koen Martens Royal Belgian Institute of Natural Sciences, Freshwater Biology, Vautierstraat 29, B-1000 Brussels, Belgium

DOI:

https://doi.org/10.26496/bjz.2011.146

Keywords:

ostracods, ancient asexuals, morphology, taxonomy, evolution, Isabenula humphreysi gen. nov. sp. nov.,, Vestalenula sp. E

Abstract

Darwinulidae is believed to be one of the few metazoan taxa in which fully asexual reproduction might have persisted for millions of years. Although rare males in a single darwinulid species have recently been found, they may be non-functional atavisms. The representatives of this family are characterized by a slow evolutionary rate, resulting in a conservative morphology in the different lineages over long time frames and across wide geographic ranges. Differences between species and genera, although often based on small details of valve morphology and chaetotaxy, are nevertheless well-recognizable. Five Recent genera (Darwinula, Alicenula, Vestalenula, Penthesilenula and Microdarwinula) and about 35 living species, including also those left in open nomenclature, are included in this family. Previous phylogenetic analyses using both morphological characters and molecular data confirmed that the five genera are good phyletic units. Here, we report on the results of a study on darwinulid ostracods from Christmas Island (Indian Ocean). The taxonomic investigation led to the description of a new genus and two new species, namely Isabenula humphreysi gen. nov. sp. nov. and Vestalenula sp. E, this latter being left in open nomenclature, because only one individual was available. A new phylogeny of the family, using 30 morphological characters of 23 described species, is here presented. A key to the genera of Recent Darwinulidae, based on the morphology of valves and soft parts in adult females, is also provided. The discovery of Isabenula gen. nov., which shares intermediate morphological features with the genera Vestalenula and Penthesilenula, opens new opportunities to critically reconsider previous hypotheses on tempo and mode of evolution in the family Darwinulidae and on the phylogenetic relationships between its representatives.

References

Artheau M (2007). Geographical review of the ostracod genus Vestalenula (Darwinulidae) and a new subterranean species from southern France. Invertebrate Systematics, 21: 471-486.

Berthold P (2001). Bird Migration: A General Survey. 2nd ed., Oxford University Press, Oxford.

Brady GS & Robertson D (1870). The Ostracoda and Foraminifera of Tidal Rivers. Annals and Magazine of Natural History, ser. 4, 6: 1-33.

Browne RA (1992). Population genetics and ecology of Artemia: insights into parthenogenetic reproduction. Trends in Ecology & Evolution, 7: 232-237.

Butlin RK, Schön I & Martens K (1998). Asexual reproduction in nonmarine ostracods. Heredity, 81: 473-480.

Calendini F & Martin J-F (2005). PaupUP v1.0.3.1 A free graphical frontend for Paup* Dos software.

Choe K (1988). On ostracod biofacies and five new genera in Korean Seas. In: Hanai T, Ikeya N & Ishizaki K (eds), Evolutionary biology of Ostracoda: Its fundamentals and applications, Elsevier, Amsterdam and Kodansha, Tokyo: 121-133.

Danielopol DL (1968). Microdarwinula n.g. et quelques remarques sur la répartition de la famille Darwinulidae Br. et Norm. (Crustacea, Ostracoda). Annales de Limnologie - International Journal of Limnology, 4: 153-174.

Danielopol DL (1970). Une nouvelle espèce du genre Darwinula des eaux souterraines de Roumanie et quelques remarques sur la morphologie des Darwinulidae (Ostracoda-Podocopida). Travaux de l’Institut de Spéléologie Emile Racovitza, 9 : 135-149.

Danielopol DL (1980). An essay to assess the age of the freshwater interstitial ostracods of Europe. Bijdragen tot de Dierkunde, 50: 243-291.

Domes K, Norton RA, Maraun M. & Scheu S (2007). Reevolution of sexuality breaks Dollo’s law. Proceedings of the National Academy of Sciences of the United States of America, 104: 7139-7144.

Fontaneto D, Herniou E, Boschetti C, Caprioli M, Melone G, Ricci C & Barraclough TG 2007). Independently evolving species in asexual bdelloid rotifers. PLoS Biology, 5: e87.

Frisch D, Green AJ & Figuerola J (2007). High dispersal capacity of a broad spectrum of aquatic invertebrates via waterbirds. Aquatic Sciences, 69: 568-574.

Goldberg EE & Igic B (2008). On Phylogenetic Tests of Irreversible Evolution. Evolution 62: 2727-2741.

Geiger W, Otero M & Rossi V (1998). Clonal ecological diversity. In: Martens K (ed.), Sex and Parthenogenesis - Evolutionary ecology of reproductive modes in non-marine ostracods, Backhuys, Leiden: 243-256.

Gorelick R (2003). Transposable elements suppress recombination in all meiotic eukaryotes, including automictic ancient asexuals: a reply to Schön and Martens. Journal of Natural History, 37: 903-909.

Grimes KG (2001). Karst features of Christmas Island (Indian Ocean). Helictite, 37: 41-58.

Gross M (2008). A limnic ostracod fauna from the surroundings of the Central Paratethys (Late Middle Miocene/Early Late Miocene; Styrian Basin; Austria). Palaeogeography, Palaeoclimatology, Palaeoecology, 264: 263-276.

Halkett F, Simon JC & Balloux F (2005). Tackling the population genetics of clonal and partially clonal organisms. Trends in Ecology & Evolution, 20: 194-201.

Heethoff M, Norton RA, Scheu S & Mauraun M (2009). Parthenogenesis in oribatid mites (Acari, Oribatida): evolution without sex. In Schön I, Martens K, Van Dijk P. (Eds), Lost Sex, The evolutionary biology of parthenogenesis. Springer, 241-258.

Higuti J, Machado Velho LF, Lansac-Tôha FA & Martens K (2007). Pleuston communities are buffered from regional flood pulses: the example of ostracods in the Paraná River floodplain, Brazil. Freshwater Biology, 52: 1930-1943.

Horne DJ & Smith RJ (2004). First British record of Potamocypris humilis (Sars, 1924), a freshwater ostracod with a disjunct distribution in Europe and southern Africa. Bollettino della Società Paleontologica Italiana, 43: 297-306.

Horne DJ, Schön I, Smith RJ & Martens K (2005). What are ostracoda? A cladistic analysis of the extant superfamilies of the subclasses Myodocopa and Podocopa (Crustacea: Ostracoda) In: Koene-mann S & Jenner RA (Eds), Crustacea and arthropod relationships. Crustacean issiues. Vol. 16. Taylor & Francis.

Humphreys WF & Eberhard S (2001). Subterranean fauna of Christmas Island, Indian Ocean. Helictite, 37: 59-74.

Judson OP & Normark B (1996). Ancient asexual scandals. Trends in Ecology & Evolution, 11: 41-45.

Klie W (1932). Die Ostracoden der Deutschen Limnologischen Sunda-Expedition. Archiv für Hydrobiologie, Supplement, 11: 447-502.

Lunt P (2003). Biogeography of some Eocene larger Foraminifera, and their application in distinguishing geological plates. Palaeontologia Electronica, 6: 22. (Internet address: http://palaeo-electronica.org/2003_2/geo/geo.pdf/).

Martens K & Rossetti G (2002). On the Darwinu-lidae (Crustacea: Ostracoda) from Oceania. Invertebrate Systematics, 16: 195-208.

Martens K & Schön I (2008). Ancient asexuals: darwinulids not exposed! Nature, 453: 587.

Martens K, Rossetti G & Fuhrmann R (1997). Pleistocene and Recent species of the family Darwinulidae Brady & Norman, 1889 (Crustacea, Ostracoda) in Europe. Hydrobiologia, 357: 99-116.

Martens K, Rossetti G & Baltanas A (1998). Reproductive modes and taxonomy. In: Martens K (ed.), Sex and Parthenogenesis - Evolutionary ecology of reproductive modes in non-marine ostracods, Backhuys, Leiden: 197-214.

Martens K., Rossetti G & Horne DJ (2003). How ancient are ancient asexuals? Proceedings of the Royal Society of London B: Biological Sciences, 270: 723-729.

Martens K, Rossetti G, Butlin RK & Schön I (2005). Molecular and morphological phylogeny of the ancient asexual Darwinulidae (Crustacea, Ostracoda). Hydrobiologia, 538: 153-165.

Martens K, Schön I, Meisch C & Horne DJ (2008). Global diversity of ostracods (Ostracoda, Crustacea) in freshwater. Hydrobiologia, 595: 185-193.

Martens K & Schön I (2008). Ancient asexuals: darwinulids not exposed! Nature, 453 : 587.

Maynard Smith J (1978). The evolution of sex. Cambridge University Press, Cambridge.

Meisch C, Mary-Sasal N, Colin J-P & Wouters K (2007). Freshwater Ostracoda (Crustacea) collected from the islands of Futuna and Wallis, Pacific Ocean, with a checklist of the non-marine Ostracoda of the Pacific Islands. Bulletin de la Société des naturalistes luxembourgeois, 108: 89-103.

Namiotko T, Wouters K, Danielopol DL & Humphreys WF (2004). On the origin and the evolution of a new anchialine stygobitic Microceratina species (Crustacea, Ostracoda) from Christmas Island (Indian Ocean). Journal of Micropalaeontology, 23: 49-59.

Namiotko T, Marmonier P, Danielopol DL, Horne DJ & Artheau M (2005). New records of rare males of Cryptocandona vavrai Kaufmann, 1900 (Crustacea, Ostracoda), with further additions to the description of the species. Annales de Limnologie - International Journal of Limnology, 41: 203-219.

Pinto RL, Rocha CEF & Martens K (2003). On two new species of the genus Vestalenula Rossetti & Martens, 1998 (Crustacea, Ostracoda, Darwinulidae) from semiterrestrial habitats in São Paulo State (Brazil). Zoological Journal of the Linnean Society, 139: 305-313.

Pinto RL, Rocha CEF & Martens K (2004). On the genus Penthesilenula Rossetti & Martens, 1998 (Crustacea, Ostracoda, Darwinulidae) from (semi-) terrestrial habitats in São Paulo State (Brazil), with a description of a new species. Journal of Natural History, 38: 2657-2589.

Pinto RL, Rocha CEF & Martens K (2005). On the evolution of the genus Microdarwinula Danielopol, 1968 (Ostracoda, Darwinulidae) with a description of a new species from semi-terrestrial habitats in São Paulo State (Brazil). Crustaceana, 78: 975-986.

Pinto RL, Rocha CEF & Martens K (2007). Early release of eggs and embryos in a brooding ancient asexual ostracod: brood selection or a gambling strategy to increase fecundity? Hydrobiologia, 585: 249-253.

Proctor VW, Malone CR & DeVlaming VL (1967). Dispersal of aquatic organisms: viability of disseminules recovered from the intestinal tract of captive killdeer. Ecology, 48: 672-676.

Reeves JM, De Deckker P & Halse SA (2007). Groundwater Ostracods from the arid Pilbara region of northwestern Australia: distribution and water chemistry. Hydrobiologia, 585: 99-118.

Rossetti G & Martens K (1996). Redescription and morphological variability of Darwinula stevensoni (Brady & Robertson, 1870) (Crustacea, Ostracoda). Bulletin van het Koninklijk Belgisch Instituut voor Natuurwetenschappen, Biologie, 66: 73-92.

Rossetti G & Martens K (1998). Taxonomic revi-sion of the Recent and Holocene representatives of the family Darwinulidae (Crustacea, Ostracoda), with a description of three new genera. Bulletin van het Koninklijk Belgisch Instituut voor Natuurwetenschappen, Biologie, 68: 55-110.

Rossetti G & Martens K (1999). Contribution to taxonomy and distribution of the genus Vestalenula Rossetti & Martens, 1998 (Crustacea, Ostracoda, Darwinulidae), with the description of two new species. Bulletin van het Koninklijk Belgisch Instituut voor Natuurwetenschappen, Biologie, 68: 57-66.

Rossetti G, Eagar S & Martens K (1998). On two new species of the genus Darwinula (Crustacea, Ostracoda) from New Zealand. Italian Journal of Zoology, 65: 325-332.

Schön I & Martens K (1998). Opinion: DNA-repair in ancient asexuals: a new solution to an old problem? Journal of Natural History, 32: 943-948.

Schön I & Martens K (2003). No slave to sex. Proceedings of the Royal Society of London B: Biological Sciences, 270: 827-833.

Schön I, Butlin RK, Griffiths HI & Martens K (1998). Slow molecular evolution in an ancient asexual ostracod. Proceedings of the Royal Society of London B: Biological Sciences, 265: 235-242.

Schön I, Martens K, Van Doninck K & Butlin RK (2003). Evolution in the slow lane: molecular rates of evolution in sexual and asexual ostracods (Crustacea: Ostracoda). Biological Journal of the Linnean Society, 79: 93-100.

Schön I, Lamatsch D & Martens K (2008). Lessons to learn from Ancient Asexuals. In: Egel R, Lankenau DH (Eds) Recombination and meiosis. Models, means and evolution. Springer Berlin Heidelberg, 341-376.

Schön I, Rossetti G & Martens K (2009). Darwinulid ostracods: ancient asexual scandal or scandalous gossip? In: Schön I, Martens K & Van Dijk P (eds), Lost Sex. The Evolutionary Biology of Parthenogenesis, Springer, Dordrecht: 217-240.

Schwander T, Henry L & Crespy BJ (2011). Molecular Evidence for Ancient Asexuality in Timema Stick Insects. Current Biology 21, 1129-1134.

Smith RJ & Kamiya T (2008). The ontogeny of two species of Darwinuloidea (Ostracoda, Crustacea). Zoologischer Anzeiger, 247: 275-302.

Smith RJ, Kamiya T & Horne DJ (2006). Living males of the ‘ancient asexual’ Darwinulidae (Ostracoda: Crustacea). Proceedings of the Royal Society of London B: Biological Sciences, 273: 1569-1578.

Swofford D L (2002). ‘PAUP*: Phylogenetic Analysis Using Parsimony (*and Other Methods) Version 4.0b10. Sinauer Associates, Sunderland.

Turner CH (1895). Fresh-water Ostracoda of the United States. Minnesota Geological and Natural History Survey, Zoological Series, 2: 277-337.

Van Doninck K, De Bruyn L, Schön I & Martens K (2002). A general purpose genotype in an ancient asexual. Oecologia, 132: 205-212.

Van Doninck K, Schön I, Maes F, De Bruyn L & Martens K (2003). Ecological strategies in the ancient asexual animal group Darwinulidae (Crustacea, Ostracoda). Freshwater Biology, 48: 1285-1294.

Van Doninck K, Schön I, Martens K & Backeljau T (2004). Clonal diversity in the ancient asexual ostracod Darwinula stevensoni assessed by RAPD-PCR. Heredity, 93: 154-160.

Whittaker RJ (1998). Island Biogeography: Ecology, Evolution, and Conservation. Oxford University Press, Oxford.

Yin Y, Geiger W & Martens K (1999). Effects of genotype and environment on phenotypic variability in Limnocythere inopinata (Crustacea: Ostracoda). Hydrobiologia, 400: 85-114.

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Published

2024-03-15

How to Cite

Rossetti, G., Pinto, R. L., & Martens, K. (2024). Description of a new genus and two new species of Darwinulidae (Crustacea, Ostracoda), from Christmas Island (Indian Ocean) with some considerations on the morphological evolution of ancient asexuals. Belgian Journal of Zoology, 141(2), 55–74. https://doi.org/10.26496/bjz.2011.146

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