Extensive homoplasy, nonstepwise mutations, and shared ancestral polymorphism at a complex microsatellite locus in Lake Malawi cichlids

Molecular Biology and Evolution

Volumn 17, Issue 4, 2000, Pages 489-498

  Van Oppen, Madeleine J H ^a,c   Rico, Ciro ^a   Turner, George F ^b   Hewitt, Godfrey M ^a  

^a UNIVERSITY OF EAST ANGLIA   (United Kingdom)

^b UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^c JAMES COOK UNIVERSITY   (Australia)

Author keywords

Cichlids; Evolution; Infinite allele model; Microsatellite; Model; Polymorphism; Shared ancestral; Stepwise mutation

Indexed keywords

MICROSATELLITE DNA;

AFRICA; ALLELE; ARTICLE; FISH; GENE DELETION; GENE FREQUENCY; GENE LOCUS; GENE MUTATION; GENETIC POLYMORPHISM; LAKE; MOLECULAR CLONING; MOLECULAR EVOLUTION; NONHUMAN; NUCLEOTIDE SEQUENCE; SEQUENCE ANALYSIS;

CICHLIDAE; COPADICHROMIS; METRIACLIMA ZEBRA; PISCES; PSEUDOTROPHEUS; PSEUDOTROPHEUS LUCERNA; PSEUDOTROPHEUS ZEBRA;

EID: 0034115982     PISSN: 07374038     EISSN: None     Source Type: Journal    
DOI: 10.1093/oxfordjournals.molbev.a026329     Document Type: Article

References (55)

1. ALBERTSON, R. C., J. A. MARKERT, P. D. DANLEY, and T. D. KOCHER. 1999. Phylogeny of a rapidly evolving clade: the cichlid fishes of Lake Malawi, East Africa. Proc. Natl. Acad. Sci. USA 96:5107-5110.
2. ANGERS, B., and L. BERNATCHEZ. 1997. Complex evolution of a salmonid microsatellite locus and its consequences in inferring allelic divergence from size information. Mol. Biol. Evol. 14:230-238.
3. BLANQUER, A., and B. CROUAU-ROY. 1995. Polymorphism, monomorphism, and sequences in conserved microsatellites in primate species. J. Mol. Evol. 41:492-497.
4. BOWCOCK, A. M., A. RUIZ-LINARES, J. TOMFOHRDE, E. MINCH, J. R. KIDD, and L. L. CAVALLI-SFORZA. 1994. High resolution of human evolutionary trees with polymorphic microsatellites. Nature 386:455-457.
5. COLSON, I., and D. B. GOLDSTEIN. 1999. Evidence for complex mutations at microsatellite loci in Drosophila. Genetics 152:617-627.
6. CROW, J. F., and M. KIMURA. 1970. An introduction to population genetics theory. Harper and Row, New York, Evanston, and London.
7. CROZIER, R. H., B. KAUFMANN, M. E. CAREW, and Y. C. CROZIER. 1999. Mutability of microsatellites developed for the ant Camponotus consobrinus. Mol. Ecol. 8:271-276.
8. DI RIENZO, A., A. C. PETERSON, J. C. GARZA, A. M. VALDES, M. SLATKIN, and N. B. FREIMER. 1994. Mutational processes of simple-sequence: repeat loci in human populations. Proc. Natl. Acad. Sci. USA 91:3166-3170.
9. ESTOUP, A., and B. ANGERS. 1998. Microsatellites and mini-satellites for molecular ecology: theoretical and empirical considerations. Pp. 55-86 in G. R. CARVALHO, ed. Advances in molecular ecololgy. IOS Press.
10. ESTOUP, A., and J.-M. CORNUET. 1999. Microsatellite evolution: inferences from population data. Pp. 49-65 in D. B. GOLDSTEIN and C. SCHLÖTTERER, eds. Microsatellites: evolution and applications. Oxford University Press, Oxford, England.
11. ESTOUP, A., L. GARNERY, M. SOLIGNAC, and J.-M. CORNUET. 1995a. Microsatellite variation in honey bee (Apis mellifera L.) populations: hierarchical genetic structure and test of the infinite allele and stepwise mutation models. Genetics 140: 679-695.
12. ESTOUP, A., C. TAILLIEZ, J. M. CORNUET, and M. SOLIGNAC. 1995b. Size homoplasy and mutational processes of interrupted microsatellites in two bee species, Apis mellifera and Bombus terrestris (Apidae). Mol. Biol. Evol. 12:1074-1084.
13. GARZA, J. C., M. SLATKIN, and N. B. FREIMER. 1995. Microsatellite allele frequencies in humans and chimpanzees, with implications for constraints on allele size. Mol. Biol. Evol. 12:594-603.
14. GOLDSTEIN, D. B., A. R. LINARES, M. W. FELDMAN, and L. L. CAVALLI-SFORZA. 1995a. An evaluation of genetic distances for use with microsatellite loci. Genetics 139:463-471.
15. _. 1995b. Genetic absolute dating based on microsatellites and the origin of modern humans. Proc. Natl. Acad. Sci. USA 92:6723-6727.
16. GRIMALDI, M. C., and B. CROUAU-ROY. 1997. Microsatellite allelic homoplasy due to variable flanking sequences. J. Mol. Evol. 44:336-340.
17. HERT, E. 1991. Female choice based on egg-spots in Pseudotropheus aurora Burgess 1976, a rock-dwelling cichlid of Lake Malawi, Africa. J. Fish Biol. 38:951-953.
18. HOELZEL, A. R., J. V. LOPEZ, G. A. DOVER, and S. J. O'BRIEN. 1994. Rapid evolution of a heteroplasmic epetitive sequence in the mitochondrial DNA control region of carnivores. J. Mol. Evol. 39:191-199.
19. JARNE, P., and P. J. L. LAGODA. 1996. Microsatellites, from molecules to populations and back. Trends Ecol. Evol. 11: 424-429.
20. JONES, A. G., G. ROSENQUIST, A. BERGLUND, and J. C. AVISE. 1999. Clustered microsatellite mutations in the pipefish Syngnathus typhle. Genetics 152:1057-1063.
21. KIMURA, M., and J. F. CROW. 1964. The number of alleles that can be maintained in a finite population. Genetics 49:725-738.
22. KIMURA, M., and T. OHTA. 1978. Stepwise mutation model and distribution of allelic frequencies in a finite population. Proc. Natl. Acad. Sci. USA 75:2868-2872.
23. KLEIN, D., H. ONO, C. O'HUIGIN, V. VINCEK, T. GOLDSCHMIDT, and J. KLEIN. 1993. Extensive MHC variability in cichlid fishes of Lake Malawi. Nature 364:330-334.
24. MAHTANI, M. M., and H. F. WILLARD. 1993. A polymorphic X-linked tetranucleotide repeat locus displaying a high-rate of new mutation - implications for mechanisms of mutation at short tandem repeat loci. Hum. Mol. Genet. 2:431-437.
25. METZGAR, D., D. FIELD, R. HAUBRICH, and C. WILLS. 1998. Sequence analysis of a compound coding-region microsatellite in Candida albicans resolves homoplasies and provides a high-resolution tool for genotyping. FEMS Immunol. Med. Microbiol. 20:103-109.
26. MEYER, A. 1993. Phylogenetic relationships and evolutionary processes in cast-African cichlid fishes. Trends Ecol. Evol. 8:279-284.
27. MICHALAKIS, Y., and L. EXCOFFIER. 1996. A generic estimation of population subdivision using distances between alleles with special reference for microsatellite loci. Genetics 142: 1061-1064.
28. MORAN, P, and I. KORNFIELD. 1993. Retention of an ancestral polymorphism in the mbuna species flock (Teleostei, Cichlidae) of Lake Malawi. Mol. Biol. Evol. 10:1015-1029.
29. _. 1995. Were population bottlenecks associated with the radiation of the mbuna species flock (Teleostei, Cichlidae) of Lake Malawi. Mol. Biol. Evol. 12:1085-1093.
30. PARKER, A., and I. KORNFIELD. 1997. Evolution of the mitochondrial DNA control region in the mbuna (Cichlidae) species flock of Lake Malawi, East Africa. J. Mol. Evol. 45:70-83.
31. POWELL, W., M. MORGANTE, C. ANDRE, J. W. MCNICOL, G. C. MACHRAY, J. J. DOYLE, S. V. TINGEY, and J. A. RAFALSKI. 1995. Hypervariable microsatellites provide a general source of polymorphic DNA markers for the chloroplast genome. Curr. Biol. 5:1023-1029.
32. PRIMMER, C. R., and H. ELLEGREN. 1998. Patterns of molecular evolution in avian microsatellites. Mol. Biol. Evol. 15:997-1008.
33. PRIMMER, C. R., N. SAINO, A. P. MOLLER, and H. ELLEGREN. 1998. Unraveling the processes of microsatellite evolution through analysis of germ line mutations in barn swallows Hirundo rustica. Mol. Biol. Evol. 15:1047-1054.
34. PROCACCINI, G., and L. MAZZELLA. 1998. Population genetic structure and gene flow in the seagrass Posidonia oceanica assessed using microsatellite analysis. Mar. Ecol. Prog. Ser. 169:133-141.
35. PROVAN, J., G. CORBETT, R. WAUGH, J. W. MCNICOL, M. MORGANTE, and W. POWELL. 1996. DNA fingerprints of rice (Oryza sativa) obtained from hypervariable chloroplast simple sequence repeats. Proc. R. Soc. Lond. B Biol. Sci. 263:1275-1281.
36. RIBBINK, A. J., B. A. MARSH, A. C. MARSH, A. C. RIBBINK, and B. J. SHARP. 1983. A preliminary survey of the cichlid fishes of rocky habitats in Lake Malawi. S. Afr. J. Zool. 18: 149-310.
37. RICE, W. R. 1989. Analyzing tables of statistical tests. Evolution 43:223-225.
38. ROUSSET, F. 1996. Equilibrium values of measures of population subdivision for stepwise mutation processes. Genetics 142:1357-1362.
39. SAMBROOK, J., E. F. FRITCH, and T. MANIATIS. 1989. Molecular cloning: a laboratory manual. 2nd edition (3 volumes). Cold Spring Harbor Laboratory Press, New York.
40. SCHLÖTTERER, C., R. RITTER, B. HARR, and G. BREM. 1998. High mutation rate of a long microsatellite allele in Drosophila melanogaster provides evidence for allele-specific mutation rates. Mol. Biol. Evol. 15:1269-1274.
41. SEEHAUSEN, O., and J. J. VAN ALPHEN. 1998. The effect of male coloration on female mate choice in closely related Lake Victoria cichlids (Haplochromis nyererei complex). Behav. Ecol. Sociobiol. 42:1-8.
42. SHRIVER, M. D., L. JIN, R. CHAKRABORTY, and E. BOERWINKLE. 1993. VNTR allele frequency distribution under the stepwise mutation model. Genetics 134:983-993.
43. SLATKIN, M. 1995. A measure of population subdivision based on microsatellite allele frequencies. Genetics 139:457-462.
44. SORANZO, N., J. PROVAN, and W. POWELL. 1999. An example of microsatellite length variation in the mitochondrial genome of conifers. Genome 42:158-161.
45. TAYLOR, J. S., P. SANNY, and F. BREDEN. 1999. Microsatellite allele size homoplasy in the guppy (Poecilia reticulata). J. Mol. Evol. 48:245-247.
46. VALDES, A. M., M. SLATKIN, and N. B. FREIMER. 1993. Allele frequencies at microsatellite loci: the stepwise mutation model revised. Genetics 133:737-749.
47. VAN OPPEN, M. J. H., C. RICO, J. DEUTSCH, G. F. TURNER, and G. M. HEWITT. 1997a. Isolation and characterisation of microsatellite loci in the cichlid fish Pseudotropheus zebra. Mol. Ecol. 6:387-388.
48. VAN OPPEN, M. J. H., G. F. TURNER, C. RICO, J. C. DEUTSCH, K. M. IBRAHIM, R. L. ROBINSON, and G. M. HEWITT. 1997b. Unusually fine-scale genetic structuring found in rapidly speciating Malawi cichlid fishes. Proc. R. Soc. Lond. B Biol. Sci. 264:1803-1812.
49. VAN OPPEN, M. J. H., G. F. TURNER, C. RICO, R. L. ROBINSON, J. C. DEUTSCH, M. J. GENNER, and G. M. HEWITT. 1998. Assortative mating among rock-dwelling cichlid fishes supports high estimates of species richness from lake Malawi. Mol. Ecol. 7:991-1001.
50. VIARD, F., P. FRANCK, M.-P. DUBOIS, A. ESTOUP, and P. JARNE. 1998. Variation of microsatellite size homoplasy across electromorphs, loci and populations in three invertebrate species. J. Mol. Evol. 47:42-51.
51. WEBER, J. L., and C. WONG. 1993. Mutation of human short tandem repeats. Hum. Mol. Genet. 2:1123-1128.
52. WEIR, B. S., and C. C. COCKERHAM. 1984. Estimating F-statistics for the analysis of population structure. Evolution 38: 1358-1370.
53. WHITTON, J., L. H. RIESEBERG, and M. C. UNGERER. 1997. Microsatellite loci are not conserved across the Asteraceae. Mol. Biol. Evol. 14:204-209.
54. WRIGHT, S. 1951. The genetical structure of populations. Ann. Eugenics 15:323-354.
55. ZARDOYA, R., D. M. VOLLMER, C. CRADDOCK, J. T. STREELMAN, S. KARL, and A. MEYER. 1996. Evolutionary conservation of microsatellite flanking regions and their use in resolving the phylogeny of cichlid fishes (Pisces: Perciformes). Proc. R. Soc. Lond. B Biol. Sci. 263:1589-1598.