Cookies Policy

This site uses cookies. By continuing to browse the site you are agreeing to our use of cookies.

I accept this policy

Find out more here

Post-larval developmental dynamics of the Spinicaudatan (Branchiopoda: Diplostraca) carapace

No metrics data to plot.
The attempt to load metrics for this article has failed.
The attempt to plot a graph for these metrics has failed.
The full text of this article is not currently available.

Brill’s MyBook program is exclusively available on BrillOnline Books and Journals. Students and scholars affiliated with an institution that has purchased a Brill E-Book on the BrillOnline platform automatically have access to the MyBook option for the title(s) acquired by the Library. Brill MyBook is a print-on-demand paperback copy which is sold at a favorably uniform low price.

This Article is currently unavailable for purchase.
Add to Favorites
You must be logged in to use this functionality

Cover image Placeholder

The evolution of reproductive systems is of critical importance to evolution and yet has been difficult to examine using paleontological information. Recent studies on freshwater “clam shrimp” in both extant and fossil populations have demonstrated that sex can be inferred by quantifying morphological differences of the carapaces. However, the extent of morphological continuity between juveniles and mature phenotypes remains unclear, which, if extensive, would confound the determination of sex ratios from fossil specimens. Herein, we report studies of clam shrimp ontogeny using quantitative morphometric techniques to assess carapace shape change through juvenile and early adult development. Intra- and inter-species ontogenetic variance was captured in three species from two families (Limnadiidae, Cyzicidae), three genera (Paralimnadia, Eulimnadia and Cyzicus), and three breeding systems (dioecy, androdioecy and hermaphroditism) using geometric morphometric analyses to identify and characterize discrete phenotypic stages during ontogeny. With this approach, we successfully discriminated juvenile, male and female/hermaphrodite phenotypes. Additionally, we generated models that described the ontogenetic trajectory of carapace shape as species developed into sexually mature phenotypes. These findings verify the ability of these morphometric techniques to distinguish sex ratios using only carapace shape and, thus, validate the use of fossil spinicaudatans for studies of reproductive system evolution in deep time.

Affiliations: 1: Integrated Bioscience Program, Department of Biology, University of Akron, Akron, OH 44325-3908, USA


Full text loading...


Data & Media loading...

1. Adams D. C. , Rohlf F. J. , Slice D. E. . 2004. "Geometric morphometrics: ten years of progress following the ‘revolution.’" Italian Journal of Zoology Vol 71: 5- 16.
2. Astrop T. I. , Park L. E. , Brown B. , Weeks S. C. . 2012. "Sexual discrimination at work: Spinicaudatan ‘Clam Shrimp’ (Crustacea: Branchiopoda) as a model organism for the study of sexual system evolution". Palaeontologia Electronica 15.2.20A.
3. Benítez H. A. 2013. "Sexual dimorphism using geometric morphometric approach". In, Moriyama H. (ed.), Sexual Dimorphism. InTech, DOI: .
4. Bishop J. 1968. "Resistance of Limnadia stanleyanaKing (Branchiopoda, Conchostraca) to desiccation". Crustaceana Vol 14: 35- 38.
5. Brantner J. S. , Ott D. W. , Duff R. J. , Orridge J. I. , Waldman J. R. , Weeks S. C. . 2013a. "Evidence of selfing hermaphroditism in the clam shrimp Cyzicus gynecia(Branchiopoda: Spinicaudata)". Journal of Crustacean Biology Vol 33: 184- 190.
6. Brantner J. S. , Ott D. W. , Duff R. J. , Sanoamuang L. O. , Simhachalam G. P. , Babu K. K. S. , Weeks S. C. . 2013b. "Androdioecy and hermaphroditism in five species of clam shrimps (Crustacea: Branchiopoda: Spinicaudata) from India and Thailand". Invertebrate Biology Vol 132: 27- 37.
7. Cannon H. G. 1924. "On the development of an estherid crustacean". Philosophical Transactions of the Royal Society of London Series B Vol 212: 395- 430.
8. Chasnov J. R. 2010. "The evolution from females to hermaphrodites results in a sexual conflict over mating in androdioecious nematode worms and clam shrimp". Journal of Evolutionary Biology Vol 23: 539- 556.
9. Cobbett A. , Wilkinson M. , Wills M. A. . 2007. "Fossils impact as hard as living taxa in parsimony analyses of morphology". Systematic Biology Vol 56: 753- 766.
10. Darwin C. 1871. The Descent of Man, and Selection in Relation to Sex. John Murray, London.
11. Dobrynina T. 2011. "Resting eggs of conchostracans and their adaptive possibilities". Inland Water Biology Vol 4: 111- 118.
12. Dumont H. , Negrea S. . 2002. Introduction to the Class Branchiopoda. Backhuys, Leiden.
13. Fischer G. W. 1834. "Notice sur une nouvelle espece de Branchipus de Latreille". Bull. Soc. Imper. Sci. Nat. de Moscou. Bulletin de la Société Impériale des Naturalistes de Moscou Vol 7: 452- 461.
14. Frank P. 1988. "Conchostraca". Palaeogeography, Palaeoclimatology, Palaeoecology Vol 62: 399- 403.
15. Gallego O. F. , Monferran M. D. , Astrop T. I. , Zacarias I. A. . 2013. "Reassignment of Lioestheria codoensis cardoso(Spinicaudata, Anthronestheriidae) from the lower cretaceous of Brazil: systematics and paleoecology". Revista Brasileira de Paleontologia Vol 16: 47- 60.
16. Hammer Ø. , Harper D. A. T. . 2006. Paleontological Data Analysis. Blackwell, Oxford.
17. Hössler J. , Maier G. , Tessenow U. . 1995. "Some notes on the ecology of a German Branchipus schaefferipopulation (Crustacea: Anostraca)". Hydrobiologia Vol 298: 105- 112.
18. Jones P. 2000. "Carboniferous and Permian Leaioidea (Branchiopoda: Conchostraca) from Australia: taxonomic revision and biostratigraphic implications". Records Australian Museum Vol 52: 223.
19. King R. L. 1855. "On Australian entomostracans". Papers and Proceedings on the Royal Society of Van Diemen’s Land Vol 2: 253- 262.
20. Kobayashi T. 1973. "On the classification of the fossil Conchostraca and the discovery of Estheriids in the Cretaceous of Borneo". Geology and Paleontology of Southeast Asia Vol 13: 47- 72.
21. Legg D. A. , Sutton M. D. , Edgecombe G. D. . 2013. "Arthropod fossil data increase congruence of morphological and molecular phylogenies". Nature Communications Vol 4: 2485.
22. Lohmann G. 1983. "Eigenshape analysis of microfossils: a general morphometric procedure for describing changes in shape". Journal of the International Association for Mathematical Geology Vol 15: 659- 672.
23. MacLeod N. 1999. "Generalizing and extending the eigenshape method of shape space visualization and analysis". Paleobiology Vol 25: 107- 138.
24. Martens K. , Rossetti G. , Baltanas A. . 1998. "Reproductive modes and taxonomy", pp.  197- 214. In, Martens K. (ed.), Sex and Parthenogenesis – Evolutionary Ecology of Reproductive Modes in Non-marine Ostracods. Backhuys, Leiden.
25. Martens K. , Rossetti G. , Horne D. J. . 2003. "How ancient are ancient asexuals?" Proceedings of the Royal Society of London Series B: Biological Sciences Vol 270: 723- 729.
26. Mattox N. T. 1950. "Notes on the life history and description of a new species of conchostracan phyllopod, Caenestheriella gynecia ". Transactions of the American Microscopical Society Vol 69: 50- 53.
27. Monferran M. D. , Gallego O. F. , Astrop T. I. , Cabaleri N. . 2013. "Autecology of Wolfestheria smekali(Spinicaudata) from the Upper Jurassic (Canadon Asfalto Formation), Patagonia, Argentina". Palaeogeography, Palaeoclimatology, Palaeoecology Vol 392: 52- 61.
28. Negrea S. , Botnariuc N. , Dumont H. J. . 1999. "Phylogeny, evolution and classification of the Branchiopoda (Crustacea)". Hydrobiologia Vol 412: 191- 212.
29. Novojilov N. 1961. "Dvustvorchaty elistonogie devona (Devonian bivalve crustaceans)". Akademiâ Nauk SSSR Trudy Paleontogices kogo Instituta Vol 81: 1- 132.
30. Novozhilov N. 1953. "Dvustvorchatye Listonogie Rakoobraznye Devona Kurskoi Oblasti". Doklady Akademii Nauk SSSR Vol 91: 947- 948.
31. O’Dea A. , Jackson J. B. C. , Taylor P. D. , Rodriguez F. . 2008. "Modes of reproduction in recent and fossil cupuladriid bryozoans". Palaeontology Vol 51: 847- 864.
32. Olesen J. 1999. "Larval and post-larval development of the branchiopod clam shrimp Cyclestheria hislopi(Baird, 1859) (Crustacea, Branchiopoda, Conchostraca, Spinicaudata)". Acta Zoologica Vol 80: 163- 184.
33. Olesen J. , Grygier M. . 2003. "Larval development of Japanese ‘conchostracans’: part 1, larval development of Eulimnadia braueriana(Crustacea, Branchiopoda, Spinicaudata, Limnadiidae) compared to that of other limnadiids". Acta Zoologica Vol 84: 41- 61.
34. Olesen J. , Grygier M. . 2004. "Larval development of Japanese ‘conchostracans’: part 2, larval development of Caenestheriella gifuensis(Crustacea, Branchiopoda, Spinicaudata, Cyzicidae), with notes on homologies and evolution of certain naupliar appendages within the Branchiopoda". Arthropod Structure and Development Vol 33: 453- 469.
35. Pabst T. , Richter S. . 2004. "The larval development of an Australian limnadiid clam shrimp (Crustacea, Branchiopoda, Spinicaudata), and a comparison with other Limnadiidae". Zoologischer Anzeiger – A Journal of Comparative Zoology Vol 243: 99- 115.
36. Packard A. S. 1871. "Preliminary notice of North American Phyllopoda". The American Journal of Science and Arts, Series 3 Vol 2: 108- 113.
37. Pannell J. R. 2008. "Consequences of inbreeding depression due to sex-linked loci for the maintenance of males and outcrossing in branchiopod crustaceans". Genetical Research Vol 90: 73- 84.
38. Rohlf F. 2000. tpsUtil – TPS utility program. State University at Stony Brook, Stony Brook, NY.
39. Rohlf F. . 1986. "Relationships among eigenshape analysis, Fourier analysis, and analysis of coordinates". Mathematical Geology Vol 18: 845- 854.
40. Rohlf F. . 1993. "Relative warp analysis and an example of its application to mosquito". Contributions to Morphometrics Vol 8: 131.
41. Sassaman C. 1995. "Sex determination and evolution of unisexuality in the Conchostraca". Hydrobiologia Vol 298: 45- 65.
42. Schwentner M. , Timms B. V. , Bastrop R. , Richter S. . 2009. "Phylogeny of Spinicaudata (Branchiopoda, Crustacea) based on three molecular markers – an Australian origin for Limnadopsis ". Molecular Phylogenetics and Evolution Vol 53: 716- 725.
43. Shen Y. B. 1994. "Jurassic conchostracans from carapace Nunatak, southern Victoria Land, Antarctica". Antarctic Science Vol 6: 105- 113.
44. Stigall A. L. , Hartman J. H. . 2008. "A new spinicaudatan genus (Crustacea: ‘Conchostraca’) from the Late Cretaceous of Madagascar". Palaeontology Vol 51: 1053- 1067.
45. Stigall A. L. , Hembree D. I. , Gierlowski-Kordesch E. H. , Weismiller H. C. . 2014. "Evidence for a dioecious mating system in early Jurassic Hardapestheria maxwelligen. et sp. nov. (Crustacea, Branchiopoda, Spinicaudata) from the Kalkrand Formation of Namibia". Palaeontology Vol 57: 127- 140.
46. Suzuki R. , Shimodaira H. . 2006. "Pvclust: an R package for assessing the uncertainty in hierarchical clustering". Bioinformatics Vol 22: 1540- 1542.
47. Tasch P. 1963. "Evolution of the Branchiopoda", pp.  145- 162. In, Whittington H. , Rolfe W. D. I. (eds.), Phylogeny and Evolution of Crustacea. Museum of Comparative Zoology, Harvard, Cambridge, MA.
48. Tasch P. . 1969. "Branchiopoda", pp.  128- 191. In, Moore R. C. (ed.), Treatise on Invertebrate Paleontology, Part R, Arthropoda 4. Geological Society of America and University of Kansas Press, Lawrence, KS.
49. Tasch P. . 1987. Fossil Conchostraca of the Southern Hermisphere and Continental Drift. Paleontology, Biostratigraphy, and Dispersal. Geological Society of America, Boulder, CO.
50. Timms B. V. 2009. "A revision of the Australian endemic clam shrimp genus LimnadopsisSpencer and Hall (Crustacea: Branchiopoda: Spinicaudata: Limnadiidae)". Records of the Australian Museum Vol 61: 49- 72.
51. Timms B. V. , Benvenuto C. , Reed S. K. . 2006a. "When males and hermaphrodites coexist: a review of androdioecy in animals". Integrative and Comparative Biology Vol 46: 449- 464.
52. Timms B. V. , Brantner J. S. , Astrop T. I. , Ott D. W. , Rabet N. . 2014. "The evolution of hermaphroditism from dioecy in crustaceans: selfing hermaphroditism described in a fourth spinicaudatan genus". Evolutionary Biology Vol 41: 251- 261.
53. Timms B. V. , Chapman E. , Rogers D. , Senyo D. , Hoeh W. . 2009a. "Evolutionary transitions among dioecy, androdioecy and hermaphroditism in limnadiid clam shrimp (Branchiopoda: Spinicaudata)". Journal of Evolutionary Biology Vol 22: 1781- 1799.
54. Timms B. V. , Chapman E. , Rogers D. , Senyo D. , Hoeh W. . 2009b. "Evolutionary transitions among dioecy, androdioecy and hermaphroditism in limnadiid clam shrimp (Branchiopoda: Spinicaudata)". Journal of Evolutionary Biology Vol 22: 1781- 1799.
55. Timms B. V. , Crosser B. R. , Bennett R. , Gray M. , Zucker N. . 2000. "Maintenance of androdioecy in the freshwater shrimp, Eulimnadia texana: estimates of inbreeding depression in two populations". Evolution Vol 54: 878- 887.
56. Timms B. V. , Marcus V. , Alvarez S. . 1997. "Notes on the life history of the clam shrimp, Eulimnadia texana ". Hydrobiologia Vol 359: 191- 197.
57. Timms B. V. , Marcus V. , Crosser B. R. . 1999. "Inbreeding depression in a self-compatible, androdioecious crustacean, Eulimnadia texana ". Evolution Vol 53: 472- 483.
58. Timms B. V. , Sanderson T. F. , Zofkova M. , Knott B. . 2008. "Breeding systems in the clam shrimp family Limnadiidae (Branchiopoda, Spinicaudata)". Invertebrate Biology Vol 127: 336- 349.
59. Timms B. V. , Zofkova M. , Knott B. . 2006b. "Limnadiid clam shrimp biogeography in Australia (Crustacea: Branchiopoda: Spinicaudata)". Journal of the Royal Society of Western Australia Vol 89: 155- 161.
60. Wolf E. 1911. "Phyllopoda", pp.  253- 276. In, Michaelsen W. , Hartmeyer R. (eds.), Die Fauna Sudwest-Australiens. Ergebnisse der Hamburger Sudwest-Australischen Forschungsreise 1905. G. Fischer, Jena.
61. Woolfe K. J. 1990. "Trace fossils as paleoenvironmental indicators in the Taylor group (Devonian) of Antarctica". Palaeogeography, Palaeoclimatology, Palaeoecology Vol 80: 301- 310.

Article metrics loading...



Can't access your account?
  • Key

  • Full access
  • Open Access
  • Partial/No accessInformation