Advertisement

Genome size and lifestyle in gnesiotrochan rotifers

  • Patrick D. Brown
  • Elizabeth J. WalshEmail author
ROTIFERA XV
  • 40 Downloads

Abstract

Gnesiotrochan rotifers display a variety of life styles ranging from taxa with free-swimming larval and sessile adult stages to those with motile adult stages and colonial habits. Several explanations for the C-value enigma posit that genome size is correlated with lifestyle. To investigate this, 13 gnesiotrochan species representing nine genera were measured by flow cytometry. Genome sizes (1C) within Gnesiotrocha ranged from 0.05 pg (Hexarthra mira and Hexarthra fennica) to 0.25 pg (Sinantherina ariprepes). Genome sizes varied within genera and species; e.g., the H. fennica (El Huérfano, Mexico) genome was estimated to be 15% larger than that of H. mira and H. fennica (Keystone Wetland, TX, USA). Gnesiotrochan genome sizes are similar to those reported within Ploima, which range from 0.06 pg (Brachionus rotundiformis, B. dimidiatus) to 0.46 pg (B. asplanchnoidis). Within Gnesiotrocha, genome size was found to be significantly smaller in sessile versus motile species as well as in solitary versus colonial species. To account for phylogenetic background, linear mixed models with hierarchical taxonomic ranks showed that there is a taxonomic component underlying genome size. This study provides the first estimates of genome size within the superorder, providing a baseline for genomic and evolutionary studies within the group.

Keywords

C-value Coloniality Flow cytometry Free-swimming Sessile 

Notes

Acknowledgements

Funding was provided by NSF DEB-1257068 (EJW), National Institute of Health (NIH-NIMHD-RCMI 5G12MD007592), and UTEP’s Dodson research Grant (PDB). Samples were collected under permits TPWD 2016-03, CPDCNBSP-2016-32, and EMNRDSPD 2017. Support from CONABIO “Inventario Multitaxonómico del ANP Médanos de Samalayuca” PJ018, facilitated collections from El Huérfano, Chihuahua, MX (EJW, JRA; SEMARNAT SGPA/DGVS/04784/17). Travis LaDuc facilitated collection at Miller Ranch. Kevin Bixby provided access to La Mancha Wetland. Australian sediment samples were kindly provided by John Gilbert and Russell Shiel. Nic Lannutti, Rick Hochberg, Kevin Floyd, Sergio Samaniego, Enrique Garcia, Judith Ríos-Arana (JRA), and Robert L. Wallace provided plankton and/or vegetation samples. We thank Armando Varela for his help with flow cytometry (BBRC CSI Core Facility, funded by NIH-NIMHD-RCMI 5G12MD007592), Kyung-An Han for providing Drosophila and her students for help with rearing them, and Claus-Peter Stelzer for his advice on flow cytometry methods for rotifers. Robert L. Wallace, the guest editors of the rotifer symposium volume, and two anonymous reviewers made helpful suggestions that greatly improved this manuscript.

References

  1. Alfsnes, K., H. P. Leinaas & D. O. Hessen, 2017. Genome size in arthropods; different roles of phylogeny, habitat and life history in insects and crustaceans. Ecology and Evolution 7: 5939–5947.CrossRefGoogle Scholar
  2. Bennett, M. D., I. J. Leitch, H. J. Price & J. S. Johnston, 2003. Comparisons with Caenorhabditis (approximately 100 Mb) and Drosophila (approximately 175 Mb) using flow cytometry show genome size in Arabidopsis to be approximately 157 Mb and thus approximately 25% larger than the Arabidopsis genome initiative estimate of approximately 125 Mb. Annals of Botany 91: 547–557.CrossRefGoogle Scholar
  3. Bevington, D. J., C. White & R. L. Wallace, 1995. Predatory behavior of Cupelopagis vorax (Rotifera; Collothecea; Atrochidae) on protozoan prey. Hydrobiologia 313(314): 213–217.CrossRefGoogle Scholar
  4. Bosco, G., P. Campbell, J. T. Leiva-Neto & T. A. Markow, 2007. Analysis of Drosophila species genome size and satellite DNA content reveals significant differences among strains as well as between species. Genetics 177: 1277–1290.CrossRefGoogle Scholar
  5. Canapa, A., M. Barucca, M. A. Biscotti, M. Forconi & E. Olmo, 2015. Transposons, genome size, and evolutionary insights in animals. Cytogenetic and genome research 147: 217–239.CrossRefGoogle Scholar
  6. Elliott, T. A. & T. R. Gregory, 2015. What’s in a genome? The C-value enigma and the evolution of eukaryotic genome content. Philosophical Transactions of the Royal Society B 370: 20140331.CrossRefGoogle Scholar
  7. Epp, R. W. & W. M. Lewis, 1984. Cost and speed of locomotion for rotifers. Oecologia 16: 289–292.CrossRefGoogle Scholar
  8. Flot, J. F., B. Hespeels, X. Li, B. Noel, I. Archipova, E. G. J. Danchin, A. Ejnol, B. Henrissat, R. Koszul, et al., 2013. Genomic evidence for ameiotic evolution in the bdelloid rotifer Adineta vaga. Nature 500: 453–457.CrossRefGoogle Scholar
  9. Gilbert, J. J., 2018. Attachment behavior in the rotifer Brachionus rubens: induction by Asplanchna and effect on sexual reproduction. Hydrobiologia.  https://doi.org/10.1007/s10750-018-3805-7.CrossRefGoogle Scholar
  10. Gregory, T. R., 2001a. Coincidence, coevolution, or causation? DNA content, cell size, and the C-value enigma. Biological Reviews of the Cambridge Philosophical Society 76: 65–101.CrossRefGoogle Scholar
  11. Gregory, T. R., 2001b. The bigger the C-value, the larger the cell: genome size and red blood cell size in vertebrates. Blood Cells, Molecules and Disease 27: 830–843.CrossRefGoogle Scholar
  12. Gregory, T. R., 2005. Genome size evolution in animals. The evolution of the genome. Elsevier, San Diego, CA: 3–87.CrossRefGoogle Scholar
  13. Gregory, T. R., 2009. Animal Genome Size Database. [available on internet at http://www.genomesize.com].
  14. Gregory, T. R. & P. D. Hebert, 2003. Genome size variation in lepidopteran insects. Canadian Journal of Zoology 81: 1399–1405.CrossRefGoogle Scholar
  15. Hardie, D. C. & P. D. N. Hebert, 2003. The nucleotypic effects of cellular DNA content in cartilaginous and ray-finned fishes. Genome 46: 683–706.CrossRefGoogle Scholar
  16. Hughes, A. L. & M. K. Hughes, 1995. Small genomes for better flyers. Nature 377: 391.CrossRefGoogle Scholar
  17. Hur, J. H., K. Van Doninck, M. L. Mandigo & M. Meselson, 2009. Degenerate tetraploidy was established before bdelloid rotifer families diverged. Molecular Biology and Evolution 26: 375–383.CrossRefGoogle Scholar
  18. Kapusta, A., A. Suh & C. Feschotte, 2017. Dynamics of genome size evolution in birds and mammals. Proceedings of the National Academy of Sciences of the United States of America 114: 1460–1469.CrossRefGoogle Scholar
  19. Kidwell, M. G., 2002. Transposable elements and the evolution of genome size in eukaryotes. Genetica 115: 49–63.CrossRefGoogle Scholar
  20. Kim, H. S., B. Y. Lee, J. Han, C. B. Jeong, D. S. Hwang, M. C. Lee, H. M. Kang, D. H. Kim, H. J. Kim, S. Papakostas & S. A. Declerck, 2018. The genome of the freshwater monogonont rotifer Brachionus calyciflorus. Molecular ecology resources 18: 646–655.CrossRefGoogle Scholar
  21. Kiørboe, T., 2011. How zooplankton feed: mechanisms, traits and trade-offs. Biological Reviews of the Cambridge Philosophical Society 86: 311–339.CrossRefGoogle Scholar
  22. Koste, W., 1973. Das Rädertier-Porträt. Ein merkwürdiges festsitzendes Rädertier: Cupelopagis vorax. Mikrokosmos 62: 101–106. In German.Google Scholar
  23. Lynch, M., 2007. The origins of genome architecture. Sinauer Associates Inc, Sunderland.Google Scholar
  24. Lynch, M. & J. S. Conery, 2003. The origins of genome complexity. Science 302: 1401–1404.CrossRefGoogle Scholar
  25. Mark Welch, D. M. & M. Meselson, 1998a. Measurements of the genome size of the monogonont rotifer Brachionus plicatilis and the bdelloid rotifers Philodina roseola and Habrotrocha constricta. Hydrobiologia 387(388): 395–402.CrossRefGoogle Scholar
  26. Mark Welch, J. L. & M. Meselson, 1998b. Karyotypes of bdelloid rotifers from three families. Hydrobiologia 387: 403–407CrossRefGoogle Scholar
  27. Mark Welch, D. B. & M. Meselson, 2001. Rates of nucleotide substitution in sexual and anciently asexual rotifers. Proceedings of the National Academy of Sciences of the United States of America 98: 6720–6724.CrossRefGoogle Scholar
  28. Mark Welch, D. B. & M. Meselson, 2003. Oocyte nuclear DNA content and GC proportion in rotifers of the anciently asexual Class Bdelloidea. Biological Journal of the Linnean Society 79: 85–91.CrossRefGoogle Scholar
  29. Mark Welch, D. B., J. L. Mark Welch & M. Meselson, 2008. Evidence for degenerate tetraploidy in bdelloid rotifers. Proceedings of the National Academy of Sciences of the United States of America 105: 5145–5149.CrossRefGoogle Scholar
  30. May, L., 1989. Epizoic and parasitic rotifers. Hydrobiologia 186/187: 59–67.CrossRefGoogle Scholar
  31. Meksuwan, P., P. Pholpunthin & H. Segers, 2013. The Collothecidae (Rotifera, Collothecacea) of Thailand, with the description of a new species and an illustrated key to the Southeast Asian fauna. ZooKeys 315: 1–16.CrossRefGoogle Scholar
  32. Meksuwan, P., P. Pholpunthin & H. H. Segers, 2015. Molecular phylogeny confirms Conochilidae as ingroup of Flosculariidae (Rotifera, Gnesiotrocha). Zoologica Scripta 44: 562–573.CrossRefGoogle Scholar
  33. Mills, S., J. A. Alcantara-Rodriguez, J. Ciros-Pérez, A. Gómez, A. Hagiwara, K. Hinson Galindo, C. D. Jersabek, R. Malekzadeh-Viayeh, F. Leasi, J.-S. Lee, D. B. Mark Welch, S. Papakostas, S. Riss, H. Segers, M. Serra, R. Shiel, R. Smolak, T. W. Snell, C. P. Stelzer, C. Q. Tang, R. L. Wallace, D. Fontaneto & E. J. Walsh, 2017. Fifteen species in one: deciphering the Brachionus plicatilis species complex (Rotifera, Monogononta) through DNA taxonomy. Hydrobiologia 796: 39–58.CrossRefGoogle Scholar
  34. Nishibuchi, G. & J. Déjardin, 2017. The molecular basis of the organization of repetitive DNA-containing constitutive heterochromatin in mammals. Chromosome Research 25: 77–87.CrossRefGoogle Scholar
  35. Nowell, R. W., P. Almeida, C. G. Wilson, T. P. Smith, D. Fontaneto, A. Crisp, G. Micklem, A. Tunnacliffe, C. Boschetti & T. G. Barraclough, 2018. Comparative genomics of bdelloid rotifers: insights from desiccating and nondesiccating species. PLoS biology 16: e2004830.CrossRefGoogle Scholar
  36. Organ, C. L. & A. M. Shedlock, 2009. Palaeogenomics of pterosaurs and the evolution of small genome size in flying vertebrates. Biology Letters 5: 47–50.CrossRefGoogle Scholar
  37. Pagani, M., C. Ricci & C. A. Redi, 1993. Oogenesis in Macrotrachela quadricornifera (Rotifera, Bdelloidea)—I. Germarium eutely, karyotype and DNA content. Hydrobiologia 255: 225–230.CrossRefGoogle Scholar
  38. R Core Team, 2018. R: a language and environment for statistical computing. R Core Team. R Foundation for Statistical Computing, Vienna.Google Scholar
  39. Riss, S., W. Arthofer, F. M. Steiner, B. C. Schlick-Steiner, M. Pichler, P. Stadler & C. P. Stelzer, 2017. Do genome size differences within Brachionus asplanchnoidis (Rotifera, Monogononta) cause reproductive barriers among geographic populations? Hydrobiologia 796: 59–75.CrossRefGoogle Scholar
  40. Schröder, T. & E. J. Walsh, 2007. Cryptic speciation in the cosmopolitan Epiphanes senta complex (Monogononta, Rotifera) with the description of new species. Hydrobiologia 593: 129–140.CrossRefGoogle Scholar
  41. Segers, H., 2007. Annotated checklist of the rotifers (Phylum Rotifera), with notes on nomenclature, taxonomy and distribution. Zootaxa 1564: 1–104.Google Scholar
  42. Segers, H. & R. J. Shiel, 2008. Diversity of cryptic Metazoa in Australian freshwaters: a new genus and two new species of sessile rotifer (Rotifera, Monogononta, Gnesiotrocha, Flosculariidae). Zootaxa 1750: 19–31.Google Scholar
  43. Smith, E. M. & T. R. Gregory, 2009. Patterns of genome size diversity in the ray-finned fishes. Hydrobiologia 625: 1–25.CrossRefGoogle Scholar
  44. Stelzer, C. P., 2011. A first assessment of genome size diversity in monogonont rotifers. Hydrobiologia 662: 77–82.CrossRefGoogle Scholar
  45. Stelzer, C. P., S. Riss & P. Stadler, 2011. Genome size evolution at the speciation level: the cryptic species complex Brachionus plicatilis (Rotifera). BMC Evolutionary Biology 11: 90–100.CrossRefGoogle Scholar
  46. Stemberger, R. S., 1981. A general approach to the culture of planktonic rotifers. Canadian Journal of Fisheries and Aquatic Sciences 38: 721–724.CrossRefGoogle Scholar
  47. Tavares, S., A. P. Ramos, A. S. Pires, H. G. Azinheira, P. Caldeirinha, T. Link, R. Abranches, M. D. C. Silva, R. T. Voegele, J. Loureiro & P. Talhinhas, 2014. Genome size analyses of Pucciniales reveal the largest fungal genomes. Frontiers in Plant Science 5: 1–11.CrossRefGoogle Scholar
  48. Vadstein, O., L. M. Olsen, & T. Andersen, 2012. Prey-predator dynamics in rotifers: density-dependent consequences of spatial heterogeneity due to surface attachment. Ecology 93: 1795–1801.CrossRefGoogle Scholar
  49. Vasisht, H. S. & B. L. Dawar, 1969. Anatomy and histology of the rotifer Cupelopagis vorax Leidy. Research Bulletin (N.S.) Panjab University 20: 207–221.Google Scholar
  50. Vindeløv, L. L., I. J. Christensen & N. I. Nissen, 1983. A detergent-trypsin method for the preparation of nuclei for flow cytometric DNA analysis. Cytometry: The Journal of the International Society for Analytical Cytology 3: 323–327.CrossRefGoogle Scholar
  51. Wallace, R. L., 1987. Coloniality in the phylum Rotifera. Hydrobiologia 147: 141–155.CrossRefGoogle Scholar
  52. Wallace, R. L., 2002. Rotifers: exquisite metazoans. Integrative and Comparative Biology 42: 660–667.CrossRefGoogle Scholar
  53. Wallace, R. L. & P. L. Starkweather, 1985. Clearance rates of sessile rotifers: in vitro determinations. Hydrobiologia 121: 139–144.CrossRefGoogle Scholar
  54. Walsh, E. J. & L. Zhang, 1992. Polyploidy in a natural population of the rotifer Euchlanis dilatata. Journal of Evolutionary Biology 5: 345–353.CrossRefGoogle Scholar
  55. Wright, N. A., T. R. Gregory & C. C. Witt, 2014. Metabolic “engines” of flight drive genome size reduction in birds. Proceedings of the Royal Society B 281: 20132780.CrossRefGoogle Scholar
  56. Young, A. N., R. Hochberg, E. J. Walsh & R. L. Wallace, 2018. Modeling the life history of sessile rotifers: larval substratum selection through reproduction. Hydrobiologia.  https://doi.org/10.1007/s10750-018-3802-x.CrossRefGoogle Scholar
  57. Zhang, Q. & S. V. Edwards, 2012. The evolution of intron size in amniotes: a role for powered flight? Genome Biology and Evolution 4: 1033–1043.CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Department of Biological SciencesUniversity of Texas at El PasoEl PasoUSA

Personalised recommendations