Skip to main content
Log in

Intra-specific variability in the thirteen known populations of the fairy shrimp Chirocephalus ruffoi (Crustacea: Anostraca): resting egg morphometrics and mitochondrial DNA reveal decoupled patterns of deep divergence

  • Primary Research Paper
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

Chirocephalus ruffoi is a fairy shrimp endemic to the Italian peninsula, where it is known only from thirteen high mountain locations. Twelve of these are in the Northern Apennines while the thirteenth is about 700 km away in the Calabrian Apennines (Southern Italy). We quantified degree of genetic divergence within the species by sequencing a fragment of the mitochondrial DNA encoding for Cytochrome Oxidase I. We then combined genetic data with the re-analysis of two different datasets on the morphometrics of the resting eggs (cysts) produced by the species as an adaptation to survive seasonal droughts. Genetic data revealed profound divergence; we identified four clusters of haplotypes within the species phylogeography, three in the Northern Apennines and one in the Calabrian Apennines with most of the genetic variation (≈70%) being apportioned among haplogroups. We found high variability in cyst morphometrics, especially in cyst size and height of the spines ornamenting the surface. Genetic and morphometric data are decoupled suggesting that cyst morphology is either under selection or a plastic trait. We, therefore, caution against using cyst morphology for taxonomic purposes in anostracans.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Alekseev, V. & W. Lampert, 2004. Maternal effects of photoperiod and food level on life history characteristics of the cladoceran Daphnia pulicaria Forbes. Hydrobiologia 526: 225–230.

    Article  Google Scholar 

  • Ali, J. A., A. S. Sarma & H. Dumont, 1999. Cyst production in the fairy shrimp Streptocephalus proboscideus (Anostraca) in relation to algal and loricated rotifer diet. Crustaceana 72: 517–530.

    Article  Google Scholar 

  • Beladjal, L. & J. Mertens, 2003. Interstitial remains for fauna reconstruction of desert pools using fairy shrimps as example (Anostraca). Journal of Crustacean Biology 23: 60–68.

    Article  Google Scholar 

  • Beladjal, L. & J. Mertens, 2009. Diaspora dispersal of Anostraca by flying insects. Journal of Crustacean Biology 29: 666–668.

    Article  Google Scholar 

  • Beladjal, L., J. Weekers & P. H. H. Mertens, 2007. Life cycle and genetic differences of two Branchipus schaefferi populations from Morocco (Anostraca: Crustacea). Animal Biology 57: 409–421.

    Article  Google Scholar 

  • Belk, D., 1977. Evolution of egg size strategies in fairy shrimps. Southwestern Naturalist 22: 99–105.

    Article  Google Scholar 

  • Belk, D., G. Anderson & S.-Y. Hsu, 1990. Additional observations on variations in egg size among populations of Streptocephalus seali (Anostraca). Journal of Crustacean Biology 10: 128–133.

    Article  Google Scholar 

  • Belmonte, G., 1992. Diapause egg production in Acartia (Paracartia) latisetosa (Crustacea, Copepoda, Calanoida). Bollettino di Zoologia 59: 363–366.

    Article  Google Scholar 

  • Belmonte, G. & M. Puce, 1994. Morphological aspects of subitaneous and restin eggs from Acartia josephinae (Calanoida). Hydrobiologia 292(293): 131–135.

    Article  Google Scholar 

  • Belmonte, G., A. Miglietta, F. Rubino & F. Boero, 1997. Morphological convergence of resting stages of planktonic organisms: a review. Hydrobiologia 355: 159–165.

    Article  Google Scholar 

  • Brendonck, L. & A. Coomans, 1994a. Egg morphology in African Streptocephalidae (Crustacea: Branchiopoda: Anostraca). Part 1: south of Zambezi and Kunene rivers. Archiv für Hydrobiologie 99: 313–334.

    Google Scholar 

  • Brendonck, L. & A. Coomans, 1994b. Egg morphology in African Streptocephalidae (Crustacea: Branchiopoda: Anostraca). Part 2: North of Zambezi and Kunene rivers and Madagascar. Archiv für Hydrobiologie 99: 335–356.

    Google Scholar 

  • Brendonck, L., M. Hamer & A. Thiéry, 1992. Occurrence of tetrahedral eggs in the Streptocephalidae (Branchiopoda, Anostraca), with descriptions of a new subgenus Parastreptocephalus, and a new species Streptocephalus (Parastreptocephalus) zuluensis. Journal of Crustacean Biology 12: 282–297.

    Article  Google Scholar 

  • Brendonck, L., L. De Meester & B. J. Riddoch, 2000. Regional structuring of genetic variation in short-lived rock pool populations of Branchipodopsis wolfi (Crustacea: Anost-raca). Oecologia 123: 206–215.

    Article  Google Scholar 

  • Bruner, E., D. Constantini & G. Mura, 2012. Fractal analysis of the egg shell ornamentation in anostracans cysts: a quantitative approach to the morphological variations in Chirocephalus ruffoi. Hydrobiologia. doi:10.1007/s10750-012-1343-2.

    Google Scholar 

  • Clement, M., D. Posada & K. A. Crandall, 2000. TCS: a computer program to estimate gene genealogies. Molecular Ecology 9: 1657–1659.

    Article  PubMed  CAS  Google Scholar 

  • Cottarelli, V. & G. Mura, 1983. Anostraci, Notostraci, Concostraci. Guide per il riconoscimento delle specie delle acque interne italiane. Quaderni C.N.R 18: 1–71.

    Google Scholar 

  • Daniels, S. R., M. Hamer & D. C. Rogers, 2004. Molecular evidence suggests an ancient radiation for the fairy shrimp genus Streptocephalus (Branchiopoda: Anostraca). Biological Journal of the Linnean Society 82: 313–327.

    Article  Google Scholar 

  • De Gelas, K. & L. De Meester, 2005. Phylogeography of Daphnia magna in Europe. Molecular Ecology 14: 753–764.

    Article  PubMed  Google Scholar 

  • De Meester, L., A. A., B. Okamura & K. Schwenk, 2002. The Monopolization Hypothesis and the dispersal-gene flow paradox in aquatic organisms. Acta Oecologica 23: 121–135.

    Article  Google Scholar 

  • De Roeck, R., A. Waterkeyn & L. Brendonck, 2010. Life-history traits of Streptocephalus purcelli Sars, 1898 (Branchiopoda, Anostraca) from temporary waters with different phenology. Water SA 36: 323–328.

    Google Scholar 

  • Dumont, H. J., S. Nandini & S. Sarma, 2002. Cyst ornamentation in aquatic invertebrates: a defense against egg-predation. Hydrobiologia 486: 161–167.

    Article  Google Scholar 

  • Excoffier, L., 2004. Patterns of DNA sequence diversity and genetic structure after a range expansion: lessons from the infinite-island model. Molecular Ecology 13: 853–864.

    Article  PubMed  CAS  Google Scholar 

  • Excoffier, L. & H. E. L. Lischer, 2010. ARLEQUIN suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10: 564–567.

    Article  PubMed  Google Scholar 

  • Excoffier, L., P. E. Smouse & J. M. Quattro, 1992. Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131: 479–491.

    PubMed  CAS  Google Scholar 

  • Frisch, D., E. Moreno-Ostos & A. Green, 2006. Species richness and distribution of copepods and cladocerans and their relation to hydroperiod and other environmental variables in Doñana, South-West Spain. Hydrobiologia 556: 327–340.

    Article  Google Scholar 

  • Fu, Y.-X., 1997. Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147: 915–925.

    PubMed  CAS  Google Scholar 

  • Gaudy, R., 1971. Etude expérimentale de la ponte chez trois espèces de copepodes pélagiques (Centropages typicus, Acartia clausi et Temora stylifera). Marine Biology 9: 65–70.

    Article  Google Scholar 

  • Gilchrist, B., 1978. Scanning electron microscope studies of the egg shell in some Anostraca (Crustacea, Branchiopoda). Cell and Tissue Research 193: 337–351.

    Article  PubMed  CAS  Google Scholar 

  • Ketmaier, V., P. Zarattini, E. De Matthaeis, M. Cobolli & G. Mura, 2003. Intra- and inter-specific relationships in the six Italian species of the fairy shrimp genus Chirocephalus: combining allozymes and mtDNA data. Journal of Zoological Systematics and Evolutionary Research 41: 276–285.

    Article  Google Scholar 

  • Ketmaier, V., R. Mandatori, E. De Matthaeis & G. Mura, 2005. Molecular systematics and phylogeography in the fairy shrimp Tanymastix stagnalis based on mitochondrial DNA. Journal of Zoology 206: 401–410.

    Article  Google Scholar 

  • Ketmaier, V., D. Pirollo, E. De Matthaeis, R. Tiedemann & G. Mura, 2008. Large scale mitochondrial phylogeography in the halophilic fairy schrimp Phallocryptus spinosa (Milne-Edwards 1840) (Branchiopoda: Anostraca). Aquatic Sciences 70: 65–76.

    Article  CAS  Google Scholar 

  • Ketmaier, V., F. Marrone, G. Alfonso, K. Paulus, A. Wiemann, R. Tiedemann & G. Mura, 2012. Mitochondrial DNA regionalism and historical demography in the extant populations of Chirocephalus kerkyrensis (Branchiopoda: Anostraca). PLoS ONE 7: e30082.

    Article  PubMed  CAS  Google Scholar 

  • Maniatsi, S., I. Kappas, A. D. Baxevanis, T. Farmaki & T. J. Abatzopoulos, 2009. Sharp phylogeographic breaks and patterns of genealogical concordance in the brine shrimp Artemia franciscana. International Journal of Molecular Science 10: 5455–5470.

    Article  CAS  Google Scholar 

  • Marcus, V. & S. Weeks, 1997. The effect of pond duration on the life history traits of an ephemeral pond crustacean, Eulimnadia texana. Hydrobiologia 359: 213–221.

    Article  Google Scholar 

  • Meintjes, S., M. T. Seaman & D. J. Kok, 1994. Duration of inundation and change in physical and chemical characteristics of small temporary pans in South Africa. Hydrobiologia 281: 79–94.

    Article  CAS  Google Scholar 

  • Munoz, J., A. Gómez, A. J. Green, J. Figuerola, F. Amat & C. Rico, 2008. Phylogeography and local endemism of the native Mediterranean brine shrimp Artemia salina (Branchiopoda: Anostraca). Molecular Ecology 17: 3160–3177.

    Article  PubMed  CAS  Google Scholar 

  • Munoz, J., A. Gómez, A. J. Green, I. Figuerola, F. Amat & C. Rico, 2010. Evolutionary origin and phylogeography of the diploid obligate parthenogen Artemia parthenogenetica (Branchiopoda: Anostraca). PLoS One 5: e11932.

    Article  PubMed  Google Scholar 

  • Mura, G., 1991. Additional remarks on cyst morphometrics in anostracans and its significance. Part I: egg size. Crustaceana 61: 241–252.

    Article  Google Scholar 

  • Mura, G., 1992. Additional remarks on cyst morphometrics in anostracans and its significance. Part II: egg morphology. Crustaceana 63: 225–246.

    Article  Google Scholar 

  • Mura, G., 1999. Current status of Anostraca of Italy. Hydrobiologia 405: 57–65.

    Article  Google Scholar 

  • Mura, G., 2001. Morphological diversity of the resting eggs in the anostracan genus Chirocephalus (Crustacea, Branchiopoda). Hydrobiologia 450: 173–185.

    Article  Google Scholar 

  • Mura, G. & L. Nagorskaya, 1995. Remarks on variability in Thamnocephalus platyurus Packard 1877 (Crustacea, Anostraca) resting eggs: morphometrical diversity and eventually related differences in cyst behaviour. Rivista di Idrobiologia 34: 132–146.

    Google Scholar 

  • Mura, G. & G. Rossetti, 2002. On the rediscovery of Chirocephalus ruffoi Cottarelli & Mura, 1984 in temporary pools of the Secchia and Panaro valleys (Tuscan-Emilian Apennines, Northern Italy) (Branchiopoda, Anostraca). Crustaceana 75: 969–977.

    Article  Google Scholar 

  • Mura, G. & G. Rossetti, 2010. Intraspecific morphological diversity of anostracan resting eggs: Chirocephalus ruffoi Cottarelli & Mura, 1984 as a study case. Journal of Biological Research 14: 137–150.

    Google Scholar 

  • Mura, G. & P. Zarattini, 1999. Influence of parental rearing conditions on cyst production and hatching of Chirocephalus ruffoi, an endemic fairy shrimp from Italy. Crustaceana 72: 449–465.

    Article  Google Scholar 

  • Mura, G., F. Accordi & M. Rampini, 1978. Studies on the resting eggs of some freshwater fairy shrimp of the genus Chirocephalus: biometry and scanning electron microscopic morphology. Crustaceana 35: 190–194.

    Article  Google Scholar 

  • Mura, G., P. Zarattini & S. Petkowski, 2002. Morphological divergencies and similarities among Chirocephalus diaphanus carinatus populations from the Balkan area. Journal of Crustacean Biology 22: 162–172.

    Article  Google Scholar 

  • Nagorskaya, L., J. Brtek & G. Mura, 1998. The Anostraca of the republic of Belarus. Hydrobiologia 367: 21–30.

    Article  Google Scholar 

  • Posada, D., 2008. jModelTest: phylogenetic model averaging. Molecular Biology and Evolution 25: 1253–1256.

    Article  PubMed  CAS  Google Scholar 

  • Puillandre, N., A. Lambert, S. Brouillet & G. Achaz, 2012. ABGD, automatic barcode gap discovery for primary species delimitation. Molecular Ecology 21: 1864–1877.

    Article  PubMed  CAS  Google Scholar 

  • Ray, N., M. Currat & L. Excoffier, 2003. Intra-deme molecular diversity in spatially expanding populations. Molecular Biology and Evolution 20: 76–86.

    Article  PubMed  CAS  Google Scholar 

  • Rebecchi, L., S. Leonardi & M. A. Sabatini, 1990. Presenza di Chirocephalus ruffoi Cottarelli & Mura, 1984 (Crustacea, Anostraca) nell’Appennino tosco-emiliano e descrizione del cariotipo. Rivista di Idrobiologia 29: 587–595.

    Google Scholar 

  • Remigio, E. A., B. V. Timms & P. D. N. Hebert, 2003. Phylogenetic systematics of the Australian fairy shrimp genus Branchinella based on mitochondrial DNA sequences. Journal of Crustacean Biology 23: 436–442.

    Article  Google Scholar 

  • Rogers, D. C., 2002. Female-biased characters for anostracan (Crustacea: Branchiopoda) identification: a key for species of California and Oregon, USA. Hydrobiologia 486: 125–132.

    Article  Google Scholar 

  • Rogers, D. C., 2003. Revision of the thamnocephalid genus Phallocryptus (Crustacea; Branchiopoda; Anostraca). Zootaxa 251: 1–12.

    Google Scholar 

  • Rogers, A. R. & H. Harpending, 1992. Population growth makes wave in the distribution of pairwise genetic differences. Molecular Biology and Evolution 9: 552–569.

    PubMed  CAS  Google Scholar 

  • Ronquist, F., M. Teslenko, P. van der Mark, D. L. Ayres, A. Darling, S. Hohna, B. Larget, L. Liu, M. A. Suchard & J. P. Huelsenbeck, 2012. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61: 539–542.

    Article  PubMed  Google Scholar 

  • Sanoamuang, L., G. Murugan, P. H. H. Weekers & H. J. Dumont, 2000. Streptocephalus sirindhornae, a new species of freshwater fairy shrimp (Anostraca) from Thailand. Journal of Crustacean Biology 20: 559–565.

    Article  Google Scholar 

  • Spencer, M., S. S. Schwartz & L. Blaustein, 2002. Are there fine-scale spatial patterns in community similarity among temporary freshwater pools? Global Ecology & Biogeography 11: 71–78.

    Article  Google Scholar 

  • Swofford, D., 2002. PAUP*: phylogenetic analysis using parsimony* (and other methods), Version 4.10. Sunderland, MA: Sinauer Associates.

  • Tajima, F., 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123: 585–595.

    PubMed  CAS  Google Scholar 

  • Tavernini, S., G. Mura & G. Rossetti, 2005. Factors influencing the seasonal phenology and composition of zooplankton communities in mountain pools. International Review of Hydrobiology 90: 358–375.

    Article  CAS  Google Scholar 

  • Timms, B. & S. Lindsay, 2011. Morphometrics of the resting eggs of the fairy shrimp Branchinella in Australia (Anostraca: Thamnocephalida). Proceedings of the Linnean Society of New South Wales 133: 53–70.

    Google Scholar 

  • Wang, S. & S. Sun, 2007. Comparative observations on the cyst shell of seven Artemia strains from China. Microscopy Research and Technique 70: 663–670.

    Article  PubMed  Google Scholar 

  • Zarattini, P., V. Ketmaier, E. De Matthaeis & G. Mura, 2001. Phenotypic and genotypic variation in the two known populations of Chirocephalus ruffoi Cottarelli & Mura, 1984 (Anostraca), endemic to Italy. Crustaceana 74: 377–388.

    Article  Google Scholar 

  • Zofkova, M. & B. V. Timms, 2009. A conflict of morphological and genetic patterns in the Australian anostracan Branchinella longirostris. Hydrobiologia 635: 67–80.

    Article  Google Scholar 

Download references

Acknowledgments

Financial support to this research came from a grant (Progetti di Ricerca, “Sapienza” Universita’ di Roma, Anno 2011) to VK. An anonymous reviewer provided helpful comments on the paper.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Valerio Ketmaier.

Additional information

Handling editor: Christian Sturmbauer

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zarattini, P., Mura, G. & Ketmaier, V. Intra-specific variability in the thirteen known populations of the fairy shrimp Chirocephalus ruffoi (Crustacea: Anostraca): resting egg morphometrics and mitochondrial DNA reveal decoupled patterns of deep divergence. Hydrobiologia 713, 19–34 (2013). https://doi.org/10.1007/s10750-013-1487-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-013-1487-8

Keywords

Navigation