Skip to main content
PMC home page
Proceedings of the Royal Society B: Biological Sciences logoLink to Proceedings of the Royal Society B: Biological Sciences
. 2002 Nov 22;269(1507):2373–2379. doi: 10.1098/rspb.2002.2145

Functional and ecological significance of rDNA intergenic spacer variation in a clonal organism under divergent selection for production rate.

Elena Gorokhova 1, Thomas E Dowling 1, Lawrence J Weider 1, Teresa J Crease 1, James J Elser 1
PMCID: PMC1691159  PMID: 12495506

Abstract

It has recently been hypothesized that variation in the intergenic spacer (IGS) of rDNA has considerable developmental, evolutionary and ecological significance through effects on growth rate and body C : N : P stoichiometry resulting from the role of the IGS in production of rRNA. To test these ideas, we assessed changes in size and structure of the repetitive region of the IGS, juvenile growth rate (JGR), RNA and phosphorus (P) contents in clonal lineages of Daphnia pulex derived from a single female and subjected to divergent selection on weight-specific fecundity (WSF). As a result of selection, WSF diverged rapidly, with significant reductions within two generations. Other significant changes accompanying shifts in WSF were that juveniles produced by low-WSF females grew more rapidly and had higher RNA and P contents. An increased predominance of long IGS variants was observed in lineages with elevated JGRs and low WSF. The observed variations in IGS length were related to the number of subrepeat units carrying a promoter sequence in the repetitive region. These results strongly support the hypothesized relationships, indicate a genetic mechanism for the evolution of such associations and demonstrate that Daphnia (and perhaps other parthenogens) possess considerable potential for rapid adaptive change in major life-history traits.

Full Text

The Full Text of this article is available as a PDF (202.0 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Alvares L. E., Brison O., Ruiz I. R. Identification of enhancer-like elements in the ribosomal intergenic spacer of Odontophrynus americanus 2n and 4n (Amphibia, Anura). Genetica. 1998;104(1):41–44. doi: 10.1023/a:1003475928921. [DOI] [PubMed] [Google Scholar]
  2. Cluster P. D., Marinković D., Allard R. W., Ayala F. J. Correlations between development rates, enzyme activities, ribosomal DNA spacer-length phenotypes, and adaptation in Drosophila melanogaster. Proc Natl Acad Sci U S A. 1987 Jan;84(2):610–614. doi: 10.1073/pnas.84.2.610. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Crease T. J. Ribosomal DNA evolution at the population level: nucleotide variation in intergenic spacer arrays of Daphnia pulex. Genetics. 1995 Dec;141(4):1327–1337. doi: 10.1093/genetics/141.4.1327. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Crease T. J. Sequence of the intergenic spacer between the 28S and 18S rRNA-encoding genes of the crustacean, Daphnia pulex. Gene. 1993 Dec 8;134(2):245–249. doi: 10.1016/0378-1119(93)90101-8. [DOI] [PubMed] [Google Scholar]
  5. Delany M. E., Krupkin A. B. Molecular characterization of ribosomal gene variation within and among NORs segregating in specialized populations of chicken. Genome. 1999 Feb;42(1):60–71. doi: 10.1139/g98-110. [DOI] [PubMed] [Google Scholar]
  6. Elser J. J., Fagan W. F., Denno R. F., Dobberfuhl D. R., Folarin A., Huberty A., Interlandi S., Kilham S. S., McCauley E., Schulz K. L. Nutritional constraints in terrestrial and freshwater food webs. Nature. 2000 Nov 30;408(6812):578–580. doi: 10.1038/35046058. [DOI] [PubMed] [Google Scholar]
  7. Fenton B., Malloch G., Germa F. A study of variation in rDNA ITS regions shows that two haplotypes coexist within a single aphid genome. Genome. 1998 Jun;41(3):337–345. [PubMed] [Google Scholar]
  8. Forneck A., Walker M. A., Blaich R. Ecological and genetic aspects of grape phylloxera Daktulosphaira vitifoliae (Hemiptera: Phylloxeridae) performance on rootstock hosts. Bull Entomol Res. 2001 Dec;91(6):445–451. [PubMed] [Google Scholar]
  9. Ganley A. R., Scott B. Extraordinary ribosomal spacer length heterogeneity in a neotyphodium endophyte hybrid: implications for concerted evolution. Genetics. 1998 Dec;150(4):1625–1637. doi: 10.1093/genetics/150.4.1625. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Grimaldi G., Di Nocera P. P. Multiple repeated units in Drosophila melanogaster ribosomal DNA spacer stimulate rRNA precursor transcription. Proc Natl Acad Sci U S A. 1988 Aug;85(15):5502–5506. doi: 10.1073/pnas.85.15.5502. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Lushai G., De Barro P. J., David O., Sherratt T. N., Maclean N. Genetic variation within a parthenogenetic lineage. Insect Mol Biol. 1998 Nov;7(4):337–344. doi: 10.1046/j.1365-2583.1998.740337.x. [DOI] [PubMed] [Google Scholar]
  12. Lushai Gugs, Loxdale Hugh D. The biological improbability of a clone. Genet Res. 2002 Feb;79(1):1–9. doi: 10.1017/s0016672301009582. [DOI] [PubMed] [Google Scholar]
  13. Mandrioli M., Manicardi G. C., Bizzaro D., Bianchi U. NOR heteromorphism within a parthenogenetic lineage of the aphid Megoura viciae. Chromosome Res. 1999;7(2):157–162. doi: 10.1023/a:1009215721904. [DOI] [PubMed] [Google Scholar]
  14. Marrocco R., Castiglione M. R., Ruberti F., Maggini F., Avanzi S. Ribosomal RNA genes of Phaseolus coccineus. IV. Structure and comparative-analysis of the intergenic spacer: possible involvement of some nucleotides in the transcription control of coding sequences. Sequence of the intergenic spacer of ribosomal genes. DNA Seq. 1998 Mar;9(1):45–48. doi: 10.3109/10425179809050024. [DOI] [PubMed] [Google Scholar]
  15. Moss T., Stefanovsky V. Y. Promotion and regulation of ribosomal transcription in eukaryotes by RNA polymerase I. Prog Nucleic Acid Res Mol Biol. 1995;50:25–66. doi: 10.1016/s0079-6603(08)60810-7. [DOI] [PubMed] [Google Scholar]
  16. Reeder R. H. Enhancers and ribosomal gene spacers. Cell. 1984 Sep;38(2):349–351. doi: 10.1016/0092-8674(84)90489-6. [DOI] [PubMed] [Google Scholar]
  17. Reeder R. H. rRNA synthesis in the nucleolus. Trends Genet. 1990 Dec;6(12):390–395. doi: 10.1016/0168-9525(90)90298-k. [DOI] [PubMed] [Google Scholar]
  18. Rose M. R., Charlesworth B. Genetics of life history in Drosophila melanogaster. II. Exploratory selection experiments. Genetics. 1981 Jan;97(1):187–196. doi: 10.1093/genetics/97.1.187. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Straughan D. J., Lehman N. Genetic differentiation among Oregon lake populations of the Daphnia pulex species complex. J Hered. 2000 Jan-Feb;91(1):8–17. doi: 10.1093/jhered/91.1.8. [DOI] [PubMed] [Google Scholar]
  20. White M. M., McLaren I. A. Copepod development rates in relation to genome size and 18S rDNA copy number. Genome. 2000 Oct;43(5):750–755. doi: 10.1139/g00-048. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the Royal Society B: Biological Sciences are provided here courtesy of The Royal Society

RESOURCES