Abstract
Asexually reproducing and polyploid animals are unresolved problems of taxonomy and nomenclature. The present paper discusses this issue from a theoretical perspective and outlines how the problem was treated in the past. The autotriploid, obligately parthenogenetic marbled crayfish is used as an example to elaborate the conditions under which autopolyploids and parthenogens should be described as separate uniparental species.
References
Barker, M.S., Arrigo, N., Baniaga, A.E., Li, Z. & Levin, D.A. (2016) On the relative abundance of autopolyploids and allopolyploids. New Phytologist, 210, 391–398.
https://doi.org/10.1111/nph.13698
Barraclough, T.G., Birky, C.W. Jr. & Burt, A. (2003) Diversification in sexual and asexual organisms. Evolution, 57, 2166–2172.
https://doi.org/10.1111/j.0014-3820.2003.tb00394.x
Birky, C.W. Jr. & Barraclough, T.G. (2009) Asexual speciation. In: Schön, I., Martens, K. & van Dijk, P. (Eds.), Lost Sex: The Evolutionary Biology of Parthenogenesis. Springer, Dordrecht, pp. 201–216.
https://doi.org/10.1007/978-90-481-2770-2_10
Budd, A.F. & Mishler, B.D. (1990) Species and evolution in clonal organisms - Summary and discussion. Systematic Botany, 15, 166–171.
https://doi.org/10.2307/2419025
Butlin, R., Schön, I. & Martens, K. (1998) Asexual reproduction in nonmarine ostracods. Heredity, 81, 473–480.
https://doi.org/10.1046/j.1365-2540.1998.00454.x
Cole, C.J., Taylor, H.L., Baumann, D.P. & Baumann, P. (2014) Neaves’ Whiptail Lizard: The first known tetraploid parthenogenetic tetrapod (Reptilia: Squamata: Teiidae). Breviora, 539 (1), 1–20.
https://doi.org/10.3099/MCZ17.1
Coyne, J.A. & Orr, H.A. (2004) Speciation. Sinauer Associates, Sunderland, Massachusetts, xiii + 545 pp.
Delord, J. (2007) The nature of extinction. Studies in History and Philosophy of Biological and Biomedical Sciences, 38, 656–667.
https://doi.org/10.1016/j.shpsc.2007.06.004
De Meeûs, T., Prugnolle, F. & Agnew, P. (2007) Asexual reproduction: Genetics and evolutionary aspects. Cellular and Molecular Life Sciences, 64, 1355–1372.
https://doi.org/10.1007/s00018-007-6515-2
De Quiroz, K. (2007) Species concepts and species delimitation. Systematic Biology, 56, 879–886.
https://doi.org/10.1080/10635150701701083
Doyle, J.J. & Sherman-Broyles, S. (2017) Double trouble: Taxonomy and definitions of polyploidy. New Phytologist, 213, 487–493.
https://doi.org/10.1111/nph.14276
Dufresne, F. (2011) The history of the Daphnia pulex complex: Asexuality, hybridization, and polyploidy. In: Held, C., Koenemann, S. & Schubart, C.D. (Eds.), Phylogeography and Population Genetics in Crustacea. Crustacean Issues 19. CRC Press, Boca Raton, pp. 217–232.
https://doi.org/10.1201/b11113-14
Ercoli, F., Kaldre, K., Paaver, T. & Gross, R. (2019) First record of an established marbled crayfish Procambarus virginalis (Lyko, 2017) population in Estonia. BioInvasions Records, 8, 675–683.
https://doi.org/10.3391/bir.2019.8.3.25
Eriksson, J.S., Blanco-Pastor, J.L., Sousa, F., Bertrand, Y.J.K. & Pfeil, B.E. (2017) A cryptic species produced by autopolyploidy and subsequent introgression involving Medicago prostrata (Fabaceae). Molecular Phylogenetics and Evolution, 107, 367–381.
https://doi.org/10.1016/j.ympev.2016.11.020
Frost, D.R. & Kluge, A.G. (1994) A consideration of epistemology in systematic biology, with special reference to species. Cladistics, 10, 259–294.
https://doi.org/10.1006/clad.1994.1018
Frost, D.R. & Wright, J.W. (1988) The taxonomy of uniparental species, with special reference to parthenogenetic Cnemidophorus (Squamata: Teiidae). Systematic Zoology, 37, 200–209.
https://doi.org/10.2307/2992277
Fussey, G.D. (1984) The distribution of the two forms of the woodlouse Trichoniscus pusillus Brandt (Isopoda: Oniscoidea) in the British Isles: A reassessment of geographic parthenogenesis. Biological Journal of the Linnean Society, 22, 309–321.
https://doi.org/10.1111/j.1095-8312.1984.tb01681.x
Gatzmann, F., Falckenhayn, C., Gutekunst, J., Hanna, K., Raddatz, G., Coutinho Carneiro, V. & Lyko, F. (2018) The methylome of the marbled crayfish links gene body methylation to stable expression of poorly accessible genes. Epigenetics Chromatin, 11 (57), 1–12.
https://doi.org/10.1186/s13072-018-0229-6
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 and Evolution, 2, 567–573.
https://doi.org/10.1038/s41559-018-0467-9
Hobbs, 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.00810282.480
Hossain, M.S., Kouba, A. & Buric, M. (2019) Morphometry, size at maturity, and fecundity of marbled crayfish (Procambarus virginalis). Zoologischer Anzeiger, 281, 68–75.
https://doi.org/10.1016/j.jcz.2019.06.005
International Commission on Zoological Nomenclature (1999) International Code of Zoological Nomenclature, 4th edition. The International Trust for Zoological Nomenclature, London.
Kluge, A.G. (1990) Species as historical individuals. Biology and Philosophy, 5, 417–431.
https://doi.org/10.1007/BF02207380
Lewis, H. (1967) The taxonomic significance of autopolyploidy. Taxon, 16, 267–271.
https://doi.org/10.2307/1216373
Lyko, F. (2017) The marbled crayfish (Decapoda: Cambaridae) represents an independent new species. Zootaxa, 4363 (4), 544–552.
https://doi.org/10.11646/zootaxa.4363.4.6
Mark Welch, D.B., Ricci, C. & Meselson, M. (2009) Bdelloid rotifers: Progress in understanding the success of an evolutionary scandal. In: Schön, I., Martens, K. & van Dijk, P. (Eds.), Lost Sex: The Evolutionary Biology of Parthenogenesis. Springer, Dordrecht, pp. 259–280.
https://doi.org/10.1007/978-90-481-2770-2_13
Martin, P., Kohlmann, K. & Scholtz, G. (2007) The parthenogenetic Marmorkrebs (marbled crayfish) produces genetically uniform offspring. Naturwissenschaften, 94, 843–846.
https://doi.org/10.1007/s00114-007-0260-0
Martin, P., Dorn, N.J., Kawai, T., van der Heiden, C. & Scholtz, G. (2010) The enigmatic Marmorkrebs (marbled crayfish) is the parthenogenetic form of Procambarus fallax (Hagen, 1870). Contributions to Zoology, 79, 107–118.
https://doi.org/10.1163/18759866-07903003
Martin, 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.12114
Mayr, E. (1963) Animal Species and Evolution. Harvard University Press, Cambridge, xiv + 797 pp.
https://doi.org/10.4159/harvard.9780674865327
Mayr, E. (1996) What is a species, and what is not? Philosophy of Science, 63, 262–277.
https://doi.org/10.1086/289912
Mishler, B.D. & Budd, A.F. (1990) Species and evolution in clonal organisms—Introduction. Systematic Botany, 15, 79–85.
https://doi.org/10.2307/2419018
Neiman, 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.x
Ros, V.I., Breeuwer, J.A. & Menken, S.B. (2008) Origins of asexuality in Bryobia mites (Acari: Tetranychidae). BMC Evolutionary Biology, 19 (153), 1–16.
https://doi.org/10.1186/1471-2148-8-153
Ryskov, A.P., Osipov, F.A., Omelchenko, A.V., Semyenova, S.K., Girnyk, A.E., Korchagin, V.I., Vergun, A.A. & Murphy, R.W. (2017) The origin of multiple clones in the parthenogenetic lizard species Darevskia rostombekowi. PLoS ONE, 12 (9), e0185161.
https://doi.org/10.1371/journal.pone.0185161
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/10.1038/421806a
Schmid, M., Evans, B.J. & Bogart, J.P. (2015) Polyploidy in Amphibia. Cytogenetics and Genome Research, 145, 315–330.
https://doi.org/10.1159/000431388
Schön, I., Rossetti, G. & Martens, K. (2009) Darwinulid ostracods: Ancient asexual scandals or scandalous gossip? In: Schön, I., Martens, K. & van Dijk, P. (Eds.), Lost Sex: The Evolutionary Biology of Parthenogenesis. Springer, Dordrecht, pp. 217–240.
https://doi.org/10.1007/978-90-481-2770-2_11
Schön, I., Pinto, R.L., Halse, S., Smith, A.J., Martens, K. & Birky, C.W. Jr. (2012) Cryptic species in putative ancient asexual darwinulids (Crustacea, Ostracoda). PLoS ONE, 7 (7), e39844.
https://doi.org/10.1371/journal.pone.0039844
Soltis, D.E., Soltis, P.S., Schemske, D.W., Hancock, J.F., Thompson, J.N., Husband, B.C. & Judd, W.S. (2007) Autopolyploidy in angiosperms: Have we grossly underestimated the number of species? Taxon, 56, 13–30.
https://doi.org/10.2307/25065732
Stenberg, P., Lundmark, M., Knutelski, S. & Saura, A. (2003) Evolution of clonality and polyploidy in a weevil system. Molecular Biology and Evolution, 20, 1626–1632.
https://doi.org/10.1093/molbev/msg180
Suomalainen, E., Saura, A. & Lokki, J. (1987) Cytology and Evolution in Parthenogenesis. CRC Press, Boca Raton, 232 pp.
Vogt, G. (2019a) Biology, ecology, evolution, systematics and utilization of the parthenogenetic marbled crayfish, Procambarus virginalis. In: Ribeiro, F.B. (Ed.), Crayfish: Evolution, Habitat and Conservation Strategies. Nova Science Publishers, Hauppauke, NY, in press.
Vogt, G. (2019b) Estimating the young evolutionary age of marbled crayfish from museum samples. Journal of Natural History, submitted.
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.008755
Vogt, 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.014241
Vogt, G., Lukhaup, C., Pfeiffer, M., Dorn, N.J., Williams, B.W., Schulz, R. & Schrimpf, A. (2018) Morphological characterization and genotyping of the marbled crayfish and new evidence on its origin. Zootaxa, 4524 (3), 329–350.
https://doi.org/10.11646/zootaxa.4524.3.3
Vogt, G., Dorn, N.J., Pfeiffer, M., Lukhaup, C., Williams, B.W., Schulz, R. & Schrimpf, A. (2019) The dimension of biological change caused by autotriploidy: A meta-analysis with triploid crayfish Procambarus virginalis and its diploid parent Procambarus fallax. Zoologischer Anzeiger, 281, 53–67.
https://doi.org/10.1016/j.jcz.2019.06.006
Wheeler, Q.D. & Meier, R. (Eds.) (2000) Species Concepts and Phylogenetic Theory: A Debate. Columbia University Press, New York, 256 pp.
Wood, T.E., Takebayashi, N., Barker, M.S., Mayrose, I., Greenspoon, P.B. & Rieseberg, L.H. (2009) The frequency of polyploid speciation in vascular plants. Proceedings of the National Academy of Sciences USA, 106, 13875–13879.
https://doi.org/10.1073/pnas.0811575106