Summary
Repetitive DNA families in sexual species are subject to a variety of turnover mechanisms capable of homogenising newly arising mutations. Very high levels of homogeneity in DNA families in some species ofDrosophila indicate that the rate of turnover is fast relative to that of mutation. To gauge the generality of such phenomena, we cloned and sequenced individual members of homologous repetitive DNA families from two subspecies of tsetse fly,Glossina morsitans centralis andG. morsitans morsitans. Unexpectedly high levels of variation were found within each subspecies, averaging 24% and 31%, respectively. Contiguous repeats and repeats cloned at random were comparably divergent. Nevertheless, it was possible to identify three instances of apparent homogenisation, each being, remarkably, of an insertion/deletion nature. We conclude that the rate of turnover in the tsetse families is comparable to that of most mutations, and discuss the possible parameters affecting flux in these families.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Amos CA, Dover GA (1981) The distribution of repetitive DNAs between regular and supernumerary chromosomes in species ofGlossina: a two-step process in the origin of supernumeraries. Chromosoma 81:673–690
Arnheim N (1983) Concerted evolution of multigene families. In: Koehn R, Nei M (eds) Evolution of genes and proteins. Sinauer Associates, Sunderland, Massachusetts, pp 38–61
Bentley DL, Rabbitts TH (1983) Evolution of immunoglobulin V genes: evidence indicating that recently duplicated human Vk sequences have diverged by gene conversion. Cell 32:181–189
Brown SDM, Piechaczyk M (1983) Insertion sequences and tandem repetitions as sources of variation in a dispersed repeat family. J Mol Biol 165:249–256
Brutlag DL (1981) Molecular arrangements and evolution of heterochromatic DNA. Annu Rev Genet 14:121–144
Coen ES, Dover GA (1983) Unequal exchanges and the coevolution of X and Y rDNA arrays inD. melanogaster. Cell 33:849–855
Coen ES, Thoday JM, Dover GA (1982) Rate of turnover of structural variants in the rDNA gene family ofDrosophila melanogaster. Nature 295:564–568
Curtis CF (1972) Sterility from crosses between sub-species of the tsetse flyGlossina morsitans. Acta Trop (Basel) 29:250–268
Daniels GR, Fox GM, Loewensteiner D, Schmid CW, Deininger PL (1983) Species-specific homogeneity of the primate Alu family of repeated DNA sequences. Nucleic Acids Res 11: 7579–7593
Dover, GA (1982) Molecular drive: a cohesive mode of species evolution. Nature 299:111–117
Dover GA, Brown SDM, Coen ES, Dallas J, Strachan T, trick M (1982) The dynamics of genome evolution and species differentiation. In: Dover GA, Flavell RB (eds) Genome evolution. Academic Press, London, pp 343–374
Dover GA, Trick M, Strachan T, Coen ES, Brown SDM (1984) DNA family turnover and the coevolution of chromosomes. In: Bennett MD, Gropp A and Wolf U (eds) Chromosomes Today, vol 8. Allen & Unwin, London, pp 229–240
Grimaldi G, Queen C, Singer MF (1981) Interspersed repeated sequences in the African Green Monkey genome that are homologous to the human Alu family. Nucleic Acids Res 9:5553–5568
Grunstein M, Hogness DS (1975) Colony hybridisation: a method for the isolation of cloned DNAs that contain a specific gene. Proc Natl Acad Sci USA 72:3961–3965
Hood L, Campbell JH, Elgin SCR (1975) The organisation, expression and evolution of antibody genes and other multigene families. Annu Rev Genet 9:305–353
Hörz W, Altenburger W (1981) Nucleotide sequence of mouse satellite DNA. Nucleic Acids Res 9:683–696
Hsieh T-S, Brutlag D (1979) Sequence and sequence variation within the 1.688 g/cm3 satellite DNA ofDrosophila melanogaster. J Mol Biol 135:465–481
Itard J (1973) Revue des connaissances actuelles sur la cytogenetique des Glossines (Diptera). Rev Elev Med Vet Pays Trop 26:151–167
Jelinek WR, Schmid CW (1982) Repetitive sequences in eukaryotic DNA and their expression. Annu Rev Biochem 51: 813–844
Jones CW, Kafatos FC (1982) Accepted mutations in a gene family: evolutionary diversification of duplicated DNA. J Mol Evol 19:87–103
Kedes LH (1979) Histone genes and histone messengers. Annu Rev Biochem 48:837–870
McCutchan T, Hsu H, Thayer RE, Singer MF (1982) Organisation of African Green Monkey DNA at junctions between α-satellite and other DNA sequences. J Mol Biol 157:195–211
McDonell MW, Simon MN, Studier FW (1977) Analysis of restriction fragments of T7 DNA and determination of molecular weights by electrophoresis in neutral and alkaline gels. J Mol Biol 110:119–146
Messing J (1981) MI 3mp2 and derivatives: a molecular cloning system for DNA sequencing, strand-specific hybridisation andin vitro mutagenesis. In: Walton A (ed) Third Cleveland symposium on macromolecules, recombinant DNA. Elsevier, Amsterdam, pp 143–153
Mews AR, Langley PA, Pimley RW, Flood MET (1977) Largescale rearing of tsetse flies (Glossina spp.) in the absence of a living host. Bull Entomol Res 67:119–128
Miklos GLG, Gill AC (1981) The DNA sequences of cloned complex satellite DNAs from HawaiianDrosophila and their bearing on satellite DNA sequence conservation. Chromosoma 82:409–427
Ohta T (1980) Evolution and variation in multigene families. Springer-Verlag, New York (Lecture notes in biomathematics, vol 37)
Ohta T, Dover GA (1983) Population genetics of multigene families that are dispersed into two or more chromosomes. Proc Natl Acad Sci USA 80:4079–4083
Ohta T, Dover GA (1984) The cohesive population genetics of molecular drive. Genetics (in press)
Peacock WJ, Lohe AR, Gerlach WL, Dunsmuir P, Dennis ES, Appels R (1977) Fine structure and evolution of DNA in heterochromatin. Cold Spring Harbor Symp Quant Biol 43: 1121–1135
Petes TD (1980) Unequal meiotic recombination within tandem arrays of yeast ribosomal RNA genes. Cell 19:765–774
Potts WH (1970) Systematics and identification ofGlossina. In: Mulligan HW (ed) The African trypanosomiases. Allen and Unwin, London, pp 243–273
Rigby PWJ, Dickmann M, Rhodes C, Berg P (1977) Labelling deoxyribonucleic acid to high specific activityin vitro by nick translation with DNA polymerase I. J Mol Biol 113:237–251
Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain terminating inhibitors. Proc Natl Acad Sci USA 74: 5463–5467
Smith GP (1976) Evolution of repeated DNA sequences by unequal crossover, Science 191:528–535
Southern DI (1980) Chromosome diversity in tsetse flies. In: Blackman RL, Hewitt GM, Ashburner M (eds) Insect cytogenetics. Blackwell, London, pp 225–243
Southern DI, Pell PE (1973) Chromosome relationships and meiotic mechanisms of certainmorsitans group tsetse flies and their hybrids. Chromosoma 44:319–334
Southern EM (1975) Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol 98:505–517
Strachan T, Coen ES, Webb DA, Dover GA (1982) Modes and rates of change of complex DNA families ofDrosophila. J Mol Biol 158:37–54
Szostak JW, Wu R (1980) Unequal crossing over in the ribosomal DNA ofSaccharomyces cerevisiae. Nature 284:426–430
Tartof K (1974) Unequal mitotic sister chromatid exchange and disproportionate replication as mechanisms regulating ribosomal RNA gene redundancies. Cold Spring Harbor Symp Quant Biol 38:491–500
Thayer RE, Singer MF, McCutchan TF (1981) Sequence relationships between single repeat units of highly reiterated African Green Monkey DNA. Nucleic Acids Res 9:169–181
Trick M (1983) Aspects of genome evolution in tsetse fly species. Ph.D. thesis, University of Cambridge, Cambridge, England
Trick M, Dover GA (1984) Genetic relationships between subspecies of the tsetse flyGlossina morsitans inferred from variation in mitochondrial sequences. Can J Gen Cytol (in press)
Twigg AJ, Sherratt D (1980) Trans-complementable copynumber mutants of plasmid ColEl. Nature 283:216–218
Vanderplank FL (1944) Hybridisation betweenGlossina species and suggested new method for control of certain species of tsetse. Nature 154:607–608
Vanderplank FL (1947) Experiments on the hybridisation of tsetse flies (Glossina, Diptera) and the possibility of a new method of control. Trans R Entomol Soc Lond 98:1–18
Wahl GM, Stern M, Stark G (1979) Efficient transfer of large DNA fragments from agarose gels to diazobenzyloxymethyl-paper and rapid hybridisation by using dextran sulphate. Proc Natl Acad Sci USA 76:3683–3687
Yamamoto M, Miklos GLG (1978) Genetic studies on the heterochromation inD. melanogaster and their implication for the function of satellite DNA. Chromosoma 66:71–98
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Trick, M., Dover, G.A. Unexpectedly slow homogenisation within a repetitive DNA family shared between two subspecies of tsetse fly. J Mol Evol 20, 322–329 (1984). https://doi.org/10.1007/BF02104738
Issue Date:
DOI: https://doi.org/10.1007/BF02104738