Abstract
The obligately parthenogenetic marbled crayfish, Procambarus virginalis, is the first formally described asexual species of the Crustacea Decapoda. It is a triploid descendant of the sexually reproducing slough crayfish, Procambarus fallax. Here we describe the morphology of cultured and wild marbled crayfish of wide size ranges in detail and photodocument all taxonomically relevant characters. Some morphological traits and coloration showed considerable variation within populations despite the monoclonal nature of marbled crayfish. There were also significant differences between wild and laboratory populations with respect to body proportions, coloration and spination. Comparison with Procambarus fallax revealed no qualitative morphological characters that unambiguously identify the marbled crayfish. Analysis of the mitochondrial cytochrome c oxidase subunit I gene (COI) and nuclear microsatellites of marbled crayfish and Procambarus fallax from different sources indicated that the tri-allelic microsatellite PclG-02 is better suitable than COI to identify the marbled crayfish. A respective identification key is provided. The COI and microsatellites of Procambarus fallax from different areas of Florida and southern Georgia suggest that the parents of the first marbled crayfish may have come from northern Union County, northern Florida.
References
Abdul-Muneer, P.M. (2014) Application of microsatellite markers in conservation genetics and fisheries management: Recent advances in population structure analysis and conservation strategies. Genetics Research International, 2014, 691759.
https://doi.org/10.1155/2014/691759Aljanabi, S.M. & Martinez, I. (1997) Universal and rapid salt-extraction of high quality genomic DNA for PCR-based techniques. Nucleic Acids Research, 25, 4692–4693.
https://doi.org/10.1093/nar/25.22.4692Beard, L.S. (2012) Responses to Predator Recognition Odors in Marmorkrebs. Master’s thesis. Department of Biology, The University of Texas-Pan American, Edinburg.
Belfiore, N.M. & May, B. (2000) Variable microsatellite loci in red swamp crayfish, Procambarus clarkii, and their characterization in other crayfish taxa. Molecular Ecology, 9, 2230–2234.
https://doi.org/10.1046/j.1365-294X.2000.105339.xBohman, P., Edsman, L., Martin, P. & Scholtz, G. (2013) The first Marmorkrebs (Decapoda: Astacida: Cambaridae) in Scandinavia. BioInvasions Records, 2, 227–232.
https://doi.org/10.3391/bir.2013.2.3.09Chucholl, C. (2016) Marbled crayfish gaining ground in Europe: The role of the pet trade as invasion pathway. In: Kawai, T., Faulkes, Z. & Scholtz, G. (Eds.), Freshwater Crayfish: Global Overview. CRC Press, Boca Raton, pp. 83–114.
Chucholl, C. & Pfeiffer, M. (2010) First evidence for an established Marmorkrebs (Decapoda, Astacida, Cambaridae) population in Southwestern Germany, in syntopic occurrence with Orconectes limosus (Rafinesque, 1817). Aquatic Invasions, 5, 405–412.
https://doi.org/10.3391/ai.2010.5.4.10Chucholl, C., Morawetz, K. & Groß, H. (2012) The clones are coming – strong increase in Marmorkrebs [Procambarus fallax (Hagen, 1870) f. virginalis] records from Europe. Aquatic Invasions, 7, 511–519.
https://doi.org/10.3391/ai.2012.7.4.008Dümpelmann, C. & Bonacker, F. (2012) Erstnachweis des Marmorkrebses Procambarus fallax f. virginalis (Decapoda: Cambaridae) in Hessen. Forum Flusskrebse, 18, 3–12.
Faulkes, Z. (2016) Marble crayfish as a new model organism and a new threat to native crayfish conservation. In: Kawai, T., Faulkes, Z. & Scholtz, G. (Eds.), Freshwater Crayfish: Global Overview. CRC Press, Boca Raton, pp. 31–53.
Filipová, L., Grandjean, F., Chucholl, C., Soes, D.M. & Petrusek, A. (2011) Identification of exotic North American crayfish in Europe by DNA barcoding. Knowledge and Management of Aquatic Ecosystems, 401, 11.
https://doi.org/10.1051/kmae/2011025Folmer, 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. Molecular Marine Biology and Biotechnology, 3, 294–299.
Günter, C. (2014) Populationsuntersuchung des gebietsfremden Marmorkrebses Procambarus fallax forma virginalis im Moosweiher in Freiburg im Breisgau. Bachelorarbeit. Abteilung für Ökologie und Evolutionsbiologie, Universität Freiburg, Freiburg, 42 pp.
Gutekunst, J., Andriantsoa, R., Falckenhayn, C., Hanna, K., Stein, W., Rasamy, J.R. & Lyko, F. (2018) Clonal genome evolution and rapid invasive spread of the marbled crayfish. Nature Ecology & Evolution, 2, 567–573.
https://doi.org/10.1038/s41559-018-0467-9Harvell, C.D. (1990) The ecology and evolution of inducible defenses. The Quarterly Review of Biology, 65, 323–340.
https://doi.org/10.1086/416841Hebert, P.D.N., Cywinska, A., Bali, S.L. & deWaard, J.R. (2003) Biological identifications through DNA barcodes. Proceedings of the Royal Society of London B, 270, 313–321.
https://doi.org/10.1098/rspb.2002.2218Hobbs, H.H. Jr. (1942) The crayfishes of Florida. University of Florida Publications, Biological Science Series, 3 (2), 1–179.
Hobbs, H.H. Jr. (1972) Crayfishes (Astacidae) of North and Middle America. Biota of Freshwater Ecosystems. Identification Manual 9. Environmental Protection Agency, Washington, D.C., 173 pp., 115 figs.
Hobbs, H.H. Jr. (1981) The crayfishes of Georgia. Smithsonian Contributions to Zoology, 318, 1–549.
https://doi.org/10.5479/si.00810282.318Hobbs, H.H. Jr. (1989) An illustrated checklist of the American crayfishes (Decapoda: Astacidae, Cambaridae, and Parastacidae). Smithsonian Contributions to Zoology, 480, 1–236.
https://doi.org/10.5479/si.00810282.480Kato, M., Hiruta, C. & Tochinai, S. (2016) Behavior of chromosomes during parthenogenetic oogenesis in Marmorkrebs Procambarus fallax f. virginalis. Zoological Science, 33, 426–430.
https://doi.org/10.2108/zs160018Kawai, T., Scholtz, G., Morioka, S., Ramanamandimby, F., Lukhaup, C. & Hanamura, Y. (2009) Parthenogenetic alien crayfish (Decapoda: Cambaridae) spreading in Madagascar. Journal of Crustacean Biology, 29, 562–567.
https://doi.org/10.1651/08-3125.1Lipták, B., Mrugała, A., Pekárik, L., Mutkovič, A., Grul'a, D., Petrusek, A. & Kouba, A. (2016) Expansion of the marbled crayfish in Slovakia: Beginning of an invasion in the Danube catchment? Journal of Limnology, 75, 305–312.
https://doi.org/10.4081/jlimnol.2016.1313Lőkkös, A., Müller, T., Kovács, K., Várkonyi, L., Specziár, A. & Martin, P. (2016) The alien, parthenogenetic marbled crayfish (Decapoda: Cambaridae) is entering Kis-Balaton (Hungary), one of Europe’s most important wetland biotopes. Knowledge and Management of Aquatic Ecosystems, 417, 16.
https://doi.org/10.1051/kmae/2016003Lukhaup, C. (2003) Süßwasserkrebse aus aller Welt. Dähne Verlag, Ettlingen, 300 pp.
Lyko, F. (2017) The marbled crayfish (Decapoda: Cambaridae) represents an independent new species. Zootaxa, 4363 (4), 544–552.
https://doi.org/10.11646/zootaxa.4363.4.6Martin, P., Kohlmann, K. & Scholtz, G. (2007) The parthenogenetic Marmorkrebs (marbled crayfish) produces genetically uniform offspring. Naturwissenschaften, 94, 843–846.
https://doi.org/10.1007/s00114-007-0260-0Martin, P., Dorn, N.J., Kawai, T., van der Heiden, C. & Scholtz, G. (2010a) The enigmatic Marmorkrebs (marbled crayfish) is the parthenogenetic form of Procambarus fallax (Hagen, 1870). Contributions to Zoology, 79, 107–118.
Martin, P., Shen, H., Füllner, G. & Scholtz, G. (2010b) The first record of the parthenogenetic Marmorkrebs (Decapoda, Astacida, Cambaridae) in the wild in Saxony (Germany) raises the question of its actual threat to European freshwater ecosystems. Aquatic Invasions, 5, 397–403.
https://doi.org/10.3391/ai.2010.5.4.09Martin, P., Thonagel, S. & Scholtz, G. (2016) The parthenogenetic Marmorkrebs (Malacostraca: Decapoda: Cambaridae) is a triploid organism. Journal of Zoological Systematics and Evolution Research, 54, 13–21.
https://doi.org/10.1111/jzs.12114Neiman, M., Paczesniak, D., Soper, D.M., Baldwin, A.T. & Hehman, G. (2011) Wide variation in ploidy level and genome size in a New Zealand freshwater snail with coexisting sexual and asexual lineages. Evolution, 65, 3202–3216.
https://doi.org/10.1111/j.1558-5646.2011.01360.xNovitsky, R.A. & Son, M.O. (2016) The first records of Marmorkrebs [Procambarus fallax (Hagen, 1870) f. virginalis] (Crustacea, Decapoda, Cambaridae) in Ukraine. Ecologica Montenegrina, 5, 44–46.
Pârvulescu, L., Togor, A., Lele, S.-F., Scheu, S., Șinca, D. & Panteleit, J. (2017) First established population of marbled crayfish Procambarus fallax (Hagen, 1870) f. virginalis (Decapoda, Cambaridae) in Romania. BioInvasions Records, 6, 357–362.
https://doi.org/10.3391/bir.2017.6.4.09Piferrer, F., Beaumont, A., Falguière, J.-C., Flajšhans, M., Haffray, P. & Colombo, L. (2009) Polyploid fish and shellfish: Production, biology and applications to aquaculture for performance improvement and genetic containment. Aquaculture, 293, 125–156.
https://doi.org/10.1016/j.aquaculture.2009.04.036Price, S.A., Friedman, S.T. & Wainwright, P.C. (2015) How predation shaped fish: The impact of fin spines on body form evolution across teleosts. Proceedings of the Royal Society of London B, 282, 20151428.
https://doi.org/10.1098/rspb.2015.1428Reinders, M. (2012) Untersuchungen zur klonalen Reproduktion beim Marmorkrebs, Procambarus spec. Masterarbeit. Lehrstuhl für Evolutionsökologie und Biodiversität der Tiere, Ruhr-Universität Bochum, Bochum, 169 pp.
Scholtz, G. (2016) Happy birthday! The first decade of Marmorkrebs research—results and perspectives. In: Kawai, T., Faulkes, Z. & Scholtz, G. (Eds.), Freshwater Crayfish: Global Overview. CRC Press, Boca Raton, pp. 3–12.
Scholtz, G., Braband, A., Tolley, L., Reimann, A., Mittmann, B., Lukhaup, C., Steuerwald, F. & Vogt, G. (2003) Parthenogenesis in an outsider crayfish. Nature, 421, 806.
https://doi.org/10.1038/421806aSellars, M.J., Degnan, B.M. & Preston, N.P. (2006) Production of triploid Kuruma shrimp, Marsupenaeus (Penaeus) japonicus (Bate) nauplii through inhibition of polar body I, or polar body I and II extrusion using 6-dimethylaminopurine. Aquaculture, 256, 337–345.
https://doi.org/10.1016/j.aquaculture.2006.02.052Sellars, M.J., Li, F., Preston, N.P. & Xiang, J. (2010) Penaeid shrimp polyploidy: Global status and future direction. Aquaculture, 310, 1–7.
https://doi.org/10.1016/j.aquaculture.2010.10.002Usio, N., Azuma, N., Sasaki, S., Oka, T. & Inoue, M. (2017) New record of Marmorkrebs from western Japan and its potential threats to freshwater ecosystems. Cancer, 26, 5–11. [in Japanese with English abstract]
Van der Heiden, C.A. & Dorn, N.J. (2017) Benefits of adjacent habitat patches to the distribution of a crayfish population in a hydro-dynamic wetland landscape. Aquatic Ecology, 51, 219–233.
https://doi.org/10.1007/s10452-016-9612-1Vogt, G. (2008) The marbled crayfish: A new model organism for research on development, epigenetics and evolutionary biology. Journal of Zoology, 276, 1–13.
https://doi.org/10.1111/j.1469-7998.2008.00473.xVogt, G. (2015) Stochastic developmental variation, an epigenetic source of phenotypic diversity with far-reaching biological consequences. Journal of Biosciences, 40, 159–204.
https://doi.org/10.1007/s12038-015-9506-8Vogt, G. (2017) Facilitation of environmental adaptation and evolution by epigenetic phenotype variation: Insights from clonal, invasive, polyploid, and domesticated animals. Environmental Epigenetics, 3, dvx002.
https://doi.org/10.1093/eep/dvx002Vogt, G. (2018a) Annotated bibliography of the parthenogenetic marbled crayfish, Procambarus virginalis, a new research model, potent invader and popular pet. Zootaxa, 4418 (4), 301–352.
https://doi.org/10.11646/zootaxa.4418.4.1Vogt, G. (2018b) Investigating the genetic and epigenetic basis of big biological questions with the parthenogenetic marbled crayfish: A review and perspective. Journal of Biosciences, 43, 189–223.
https://doi.org/10.1007/s12038-018-9741-x
Vogt, G., Tolley, L. & Scholtz, G. (2004) Life stages and reproductive components of the Marmorkrebs (marbled crayfish), the first parthenogenetic decapod crustacean. Journal of Morphology, 261, 286–311.
https://doi.org/10.1002/jmor.10250
Vogt, G., Huber, M., Thiemann, M., van den Boogaart, G., Schmitz, O.J. & Schubart, C.D. (2008) Production of different phenotypes from the same genotype in the same environment by developmental variation. Journal of Experimental Biology, 211, 510–523.
https://doi.org/10.1242/jeb.008755Vogt, G., Falckenhayn, C., Schrimpf, A., Schmid, K., Hanna, K., Panteleit, J., Helm, M., Schulz, R. & Lyko, F. (2015) The marbled crayfish as a paradigm for saltational speciation by autopolyploidy and parthenogenesis in animals. Biology Open, 4, 1583–1594.
https://doi.org/10.1242/bio.014241Vogt, G., Dorn, N.J., Pfeiffer, M., Lukhaup, C., Williams, B.W., Schulz, R. & Schrimpf, A. (2018) The dimension of biological change caused by autotriploidy: A multidisciplinary case study with the marbled crayfish. [submitted]
Vojkovská, R., Horká, I., Tricarico, E. & Ďuriš, Z. (2014) New record of the parthenogenetic marbled crayfish Procambarus fallax f. virginalis from Italy. Crustaceana, 87, 1386–1392.
https://doi.org/10.1163/15685403-00003365