Cytonuclear theory for haplodiploid species and X-linked genes. II. Stepping-stone models of gene flow and application to a fire ant hybrid zone

Evolution

Volumn 52, Issue 5, 1998, Pages 1423-1440

  Goodisman, Michael A D ^a   Dewayne Shoemaker, D ^b,c   Asmussen, Marjorie A ^a  

^a University of Georgia ^*  (United States)

^b UNIVERSITY OF ARIZONA   (United States)

^c WESTERN MICHIGAN UNIVERSITY   (United States)

Author keywords

Cytonuclear; Disequilibria; Fire ants; Haplodiploid; Hybrid zone; Solenopsis invicta; Solenopsis richteri; X linked

Indexed keywords

DIPLOIDY; GENE FLOW; HAPLOIDY; HYBRIDIZATION; MITOCHONDRIAL DNA; X CHROMOSOME;

GENE FLOW; HYBRID ZONE; MODEL;

FORMICIDAE; INSECTA; SOLENOPSIS GEMINATA; SOLENOPSIS INVICTA; SOLENOPSIS RICHTERI;

EID: 0031731813     PISSN: 00143820     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1558-5646.1998.tb02024.x     Document Type: Article

References (100)

1. ABERNETHY, K. 1994. The establishment of a hybrid zone between red and sika deer (genus Cervus). Mol. Ecol. 3:551-562.
2. ARNOLD, J. 1993. Cytonuclear disequilibria in hybrid zones. Annu. Rev. Ecol. Syst. 24:521-554.
3. ARNOLD, J., M. A. ASMUSSEN, AND J. C. AVISE. 1988. An epistatic mating system model can produce permanent cytonuclear disequilibrium in a hybrid zone. Proc. Nat. Acad. Sci. 85:1893-1896.
4. ARNOLD, M. L. 1997. Natural hybridization and evolution. Oxford Univ. Press, Oxford, U.K.
5. ARNOLD, M. L., AND S. A. HODGES. 1995. Are natural hybrids fit or unfit relative to their parents? Trends Ecol. Evol. 10:67-71.
6. ARNOLD, M. L., J. J. ROBINSON, C. M. BUCKNER, AND B. D. BENNETT. 1992. Pollen dispersal and interspecific gene flow in Louisiana irises. Heredity 68:399-404.
7. ASMUSSEN, M. A., AND J. ARNOLD. 1991. The effects of admixture and population subdivision on cytonuclear disequilibrium. Theor. Pop. Biol. 39:273-300.
8. ASMUSSEN, M. A., AND C. J. BASTEN. 1994. Sampling theory for cytonuclear disequilibria. Genetics 138:1351-1363.
9. _. 1996. Constraints and normalized measures for cytonuclear disequilibria. Heredity 76:207-214.
10. ASMUSSEN, M. A., AND A. SCHNABEL. 1991. Comparative effects of pollen and seed migration on the cytonuclear structure of plant populations. I. Maternal cytoplasmic inheritance. Genetics 128:639-654.
11. ASMUSSEN, M. A., J. ARNOLD, AND J. C. AVISE. 1987. Definition and properties of disequilibrium statistics for associations between nuclear and cytoplasmic genotypes. Genetics 115:755-768.
12. _. 1989. The effects of assortative mating and migration on cytonuclear associations in hybrid zones. Genetics 122:923-934.
13. AVISE, J. C., W. S. NELSON, J. ARNOLD, R. K. KOEHN, G. C. WILLIAMS, AND V. THORSTEINSSON. 1990. The evolutionary genetic status of Icelandic eels. Evolution 44:1254-1262.
14. AVISE, J. C., P. C. PIERCE, M. J. VAN DEN AVYLE, M. H. SMITH, W. S. NELSON, AND M. A. ASMUSSEN. 1997. Cytonuclear introgressive swamping and species turnover of bass after an introduction. J. Heredity 88:14-20.
15. BABCOCK, C. S., AND M. A. ASMUSSEN. 1996. Effects of differential selection in the sexes on cytonuclear polymorphism and disequilibria. Genetics 144:839-853.
16. _. 1998. Effects of differential selection in the sexes on cytonuclear dynamics: life stages with sex differences. Genetics 149:2063-2077.
17. BAKER, R. J., AND S. K. DAVIS. 1989. Ribosomal-DNA, mitochondrial-DNA, chromosomal, and allozymic studies on a contact zone in the pocket gopher, Geomys. Evolution 43:63-75.
18. BARTON, N. H. 1979a. Gene flow past a cline. Heredity 43:333-339.
19. _. 1979b. The dynamics of hybrid zones. Heredity 43:341-359.
20. _. 1983. Multilocus clines. Evolution 37:454-471.
21. BARTON, N. H., AND A. CLARK. 1990. Population structure and processes in evolution. Pp. 115-173 in K. Wöhrmann and S. K. Jain, eds. Population biology: ecological and evolutionary viewpoints. Springer, Berlin.
22. BARTON, N. H., AND K. S. GALE. 1993. Genetic analysis of hybrid zones. Pp. 13-45 in R. G. Harrison, ed. Hybrid zones and the evolutionary process. Oxford Univ. Press, Oxford, U.K.
23. BARTON, N. H., AND G. M. HEWITT. 1985. Analysis of hybrid zones. Annu. Rev. Ecol. Syst. 16:113-148.
24. _. 1989. Adaptation, speciation and hybrid zones. Nature 341:497-503.
25. BASTEN, C. J., AND M. A. ASMUSSEN. 1997. The exact test for cytonuclear disequilibria. Genetics 146:1165-1171.
26. BAZYKIN, A. D. 1969. Hypothetical mechanism of speciation. Evolution 23:685-687.
27. CELLINO, M. L., AND J. ARNOLD. 1993. The effects of cytoplasmic male sterility on cytonuclear disequilibria in hybrid zones. Genetica 88:37-50.
28. CLARK, A. G. 1984. Natural selection with nuclear and cytoplasmic transmission. I. A deterministic model. Genetics 107:679-701.
29. COYNE, J. A. 1992. Genetics and speciation. Nature 355:511-515.
30. _. 1994. Rules for Haldane's rules. Nature 369:189-190.
31. COYNE, J. A., AND H. A. ORR. 1989. Two rules of speciation. Pp. 180-207 in D. Otte and J. A. Endler, eds. Speciation and its consequences. Sinaur, Sunderland, MA.
32. CROZIER, R. H., AND P. PAMILO. 1996. Evolution of social insect colonies: sex allocation and kin selection. Oxford Univ. Press, Oxford, U.K.
33. CRUZAN, M. B., AND M. L. ARNOLD. 1993. Ecological and genetic associations in an Iris hybrid zone. Evolution 47:1432-1445.
34. _. 1994. Assortative mating and natural selection in an Iris hybrid zone. Evolution 48:1946-1958.
35. DATTA, S., AND J. ARNOLD. 1996. Diagnostics and a statistical test of neutrality hypotheses using the dynamics of cytonuclear disequilibria. Biometrics 52:1042-1054.
36. DATTA, S., Y.-X. FU, AND J. ARNOLD. 1996a. Dynamics and equilibrium behavior of cytonuclear disequilibria under genetic drift, mutation, and migration. Theor. Pop. Biol. 50:298-324.
37. DATTA, S., M. KIPARSKY, D. M. RAND, AND J. ARNOLD. 1996b. A statistical test of a neutral model using the dynamics of cytonuclear disequilibria. Genetics 144:1985-1992.
38. DEAN, R., AND J. ARNOLD. 1996. Cytonuclear disequilibria in hybrid zones using RAPD markers. Evolution 50:1702-1705.
39. DIFFIE, S., R. K. VANDER MEER, AND M. H. BASS. 1988. Discovery of hybrid fire ant populations in Georgia and Alabama. J. Entomol. Sci. 23:187-191.
40. DOD, B., L. S. JERMIIN, P. BOURSOT, V. H. CHAPMAN, J. T. NELSON, AND F. BONHOMME. 1993. Counterselection on sex chromosomes in the Mus musculus European hybrid zone. J. Evol. Biol. 6: 529-546.
41. DOWLING, T. E., AND W. R. HOEH. 1991. The extent of introgression outside the contact zone between Notropis cornutus and Notropis chrysocephalus (Teleostei: Cyprinidae). Evolution 45:944-956.
42. EDWARDS, A. W. F. 1992. Likelihood. Johns Hopkins Univ. Press, Baltimore, MD.
43. ENDLER, J. A. 1973. Gene flow and population differentiation. Science 179:243-250.
44. _. 1977. Geographic variation, speciation, and clines. Princeton Univ. Press. Princeton, NJ.
45. FELSENSTEIN, J. 1976. The theoretical population genetics of variable selection and migration. Annu. Rev. Ecol. Syst. 10:253-280.
46. FERRIS, S. D., R. D. SAGE, C.-M. HUANG, J. T. NIELSEN, U. RITTE, AND A. C. WILSON. 1983. Flow of mitochondrial DNA across a species boundary. Proc. Nat. Acad. Sci. 80:2290-2294.
47. FORBES, S. H., AND F. W. ALLENDORF. 1991. Associations between mitochondrial and nuclear genotypes in cutthroat trout hybrid swarms. Evolution 45:1332-1349.
48. Fu, Y.-X., AND J. ARNOLD. 1991. On the association of restriction fragment length polymorphisms across species boundaries. Proc. Nat. Acad. Sci. 88:3967-3971.
49. _. 1992. Dynamics of cytonuclear disequilibria in finite populations and comparison with a two-locus nuclear system. Theor. Pop. Biol. 41:1-25.
50. GILL, F. B. 1997. Local cytonuclear extinction of the golden winged warbler. Evolution 51:519-525.
51. GOODISMAN, M. A. D., AND M. A. ASMUSSEN. 1997. Cytonuclear theory for haplodiploid species and X-linked genes. I. Hardy-Weinberg dynamics and continent-island model. Genetics 147: 321-338.
52. HAGEN, R. H. 1990. Population structure and host use in hybridizing subspecies of Papilio glaucus (Lepidoptera: Papilionidae). Evolution 44:1914-1930.
53. HARE, M. P., AND J. C. AVISE. 1996. Molecular genetic analysis of a stepped multilocus cline in the American oyster (Crassostrea virginica). Evolution 50:2305-2315.
54. HARRISON, R. G. 1990. Hybrid zones: Windows on evolutionary process. Pp. 69-128 in D. Futuyma and J. Antonovics, eds. Oxford surveys in evolutionary biology. Oxford Univ. Press, Oxford, U.K.
55. HARRISON, R. G., AND S. M. BOGDANOWICZ. 1997. Patterns of variation and linkage disequilibrium in a field cricket hybrid zone. Evolution 51:493-505.
56. HEWITT, G. M. 1988. Hybrid zones-natural laboratories for evolutionary studies. Trends Ecol. Evol. 3:158-167.
57. HEWITT, G. M., J. GOSALVEZ, C. LOPEZ-FERNANDEZ, M. G. RITCHIE, W. NICHOLS, AND R. K. BUTLIN. 1988. Differences in the nucleolar organisers on sex chromosomes and Haldane's rule in a hybrid zone. Pp. 109-119. in P. E. Brandham, ed. Kew chromosome conference III. HMSO, London.
58. JAAROLA, M., H. TEGELSTRÖM, AND K. FREDGA. 1997. A contact zone with noncoincident clines for sex-specific markers in the field vole (Microtus agrestis). Evolution 51:241-249.
59. JERVIS, M., AND N. KIDD, EDS. 1996. Insect natural enemies: practical approaches to their study and evaluation. Chapman and Hall, London.
60. KIMURA, M., AND G. H. WEISS. 1964. The stepping stone model of population structure and the decrease of genetic correlation with distance. Genetics 49:561-576.
61. LAMB, T., AND J. C. AVISE. 1986. Directional introgression of mitochondrial DNA in a hybrid population of tree frogs: the influence of mating behavior. Proc. Nat. Acad. Sci. 83:2526-2530.
62. LARRUGA, J. M., J. ROZAS, M. HERNANDEZ, A. M. GONZALEZ, AND V. M. CABERA. 1993. Latitudinal differences in sex chromosome inversions, sex linked allozymes, and mitochondrial DNA variation in Drosophila subobscura. Genetica 92:67-74.
63. LASALLE, J., AND I. D. GAULD, EDS. 1993. Hymenoptera and biodiversity. Wallingford, Oxon, U.K.
64. LATORRE, A., C. HERNANDEZ, D. MARTINEZ, J. A. CASTRO, M. RAMON, AND A. MOYA. 1992. Population structure and mitochondrial DNA gene flow in Old World populations of Drosophila subobscura. Heredity 68:15-24.
65. LOFGREN, C. S. 1986. History of imported fire ants in the United States. Pp. 36-47 in C. S. Lofgren and R. K. Vander Meer, eds. Fire ants and leaf-cutting ants: biology and management. Westview Press, Boulder, CO.
66. MALLET, J., AND N. BARTON. 1989. Inference from clines stabilized by frequency-dependent selection. Genetics 122:967-976.
67. MALLET, J., N. BARTON, G. M. LAMAS, J. C. SANTISTEBAN, M. M. MUEDAS, AND H. EELEY. 1990. Estimates of selection and gene flow from measures of cline width and linkage disequilibrium in heliconius hybrid zones. Genetics 124:921-936.
68. MARKIN, G. P., J. H. DILLIER, S. O. HILL, M. S. BLUM, AND H. R. HERMANN. 1971. Nuptial flight and flight ranges of the imported fire ant, Solenopsis saevissima richteri (Hymenoptera: Formicidae). J. Georgia Entomol. Soc. 6:137-144.
69. MARUYAMA, T. 1970a. Analysis of population structure. I. One-dimensional stepping-stone models of finite length. Ann. Hum. Genet. 34:201-219.
70. _. 1970b. Stepping stone models of finite length. Adv. Appl. Prob. 2:229-258.
71. _. 1971. Analysis of population structure. II. Two-dimensional stepping stone models of finite length and other geographically structured populations. Ann. Hum. Genet. 35:179-196.
72. MAY, R. M., J. A. ENDLER, AND R. E. MCMURTRIE. 1975. Gene frequency clines in the presence of selection opposed by gene flow. Am. Nat. 109:659-676.
73. MOORE, W. S. 1977. An evaluation of narrow hybrid zones in vertebrates. Q. Rev. Biol. 52:263-277.
74. MORAN, C. 1979. The structure of the hybrid zone in Caledia captiva. Heredity 42:13-32.
75. MOYA, A., E. BARRIO, D. MARTINEZ, A. LATORRE, F. CONZALEZ CANDELAS, M. RAMON, AND J. A. CASTRO. 1993. Molecular characterization and cytonuclear disequilibria of two Drosophila subobscura mitochondrial haplotypes. Genome 36:890-898.
76. NAGYLAKI, T. 1975. Conditions for the existence of clines. Genetics 80:595-615.
77. _. 1976. Clines with variable migration. Genetics 83:867-886.
78. OLDROYD, B. P., J. M. CORNUET, D. ROWE, T. E. RINDERER, AND R. H. CROZIER. 1995. Racial admixture of Apis mellifera in Tasmania, Australia: similarities and differences with natural hybrid zones in Europe. Heredity 74:315-325.
79. OWEN, R. E. 1986. Gene frequency clines at X-linked or haplodiploid loci. Heredity 57:209-219.
80. PAIGE, K. N., W. C. CAPMAN, AND P. JENNETTEN. 1991. Mitochondrial inheritance patterns across a cottonwood hybrid zone: cytonuclear disequilibrium and hybrid zone dynamics. Evolution 45:1360-1369.
81. RICE, W. R. 1989. Analyzing tables of statistical tests. Evolution 43:223-225.
82. RIESEBERG, L. H., AND J. F. WENDEL. 1993. Introgression and its consequences in plants. Pp. 70-109 in R. G. Harrison, ed. Hybrid zones and the evolutionary process. Oxford Univ. Press, Oxford, U.K.
83. Ross, K. G., AND J. L. ROBERTSON. 1990. Developmental stability, heterozygosity, and fitness in two introduced fire ants (Solenopsis invicta and 5. richteri) and their hybrid. Heredity 64:93-103.
84. ROSS, K. G., AND D. D. SHOEMAKER. 1997. Nuclear and mitochondrial genetic structure in two social forms of the fire ant Solenopsis invicta: insights into transitions to an alternate social organization. Heredity 78:590-602.
85. Ross, K. G., AND J. C. TRAGER. 1990. Systematics and population genetics of fire ants (Solenopsis saevissima complex) from Argentina. Evolution 44:2113-2134.
86. Ross, K. G., R. K. VANDER MEER, D. J. C. FLETCHER, AND E. L. VARGO. 1987. Biochemical phenotypic and genetic studies of two introduced fire ants and their hybrid (Hymenoptera: Formicidae). Evolution 41:280-293.
87. SCHNABEL, A., AND M. A. ASMUSSEN. 1992. Comparative effects of pollen and seed migration on the cytonuclear structure of plant populations. II Paternal cytoplasmic inheritance. Genetics 132:253-267.
88. SCRIBNER, K. T., AND J. C. AVISE. 1993. Cytonuclear genetic architecture in mosquitofish populations and the possible roles of introgressive hybridization. Mol. Ecol. 2:139-149.
89. SHAW, D. D., A. D. MARCHANT, M. L. ARNOLD, AND N. COTRERAS. 1988. Chromosomal rearrangements, ribosomal genes and mitochondrial DNA: contrasting patterns of introgression across a narrow hybrid zone. Pp. 121-129 in P. E. Brandham, ed. Kew chromosome conference III. HMSO, London.
90. SHOEMAKER, D. D., K. G. ROSS, AND M. L. ARNOLD. 1994, Development of RAPD markers in two introduced fire ants, Solenopsis invicta and S. richteri, and their application to the study of a hybrid zone. Mol. Ecol. 3:531-539.
91. _. 1996. Genetic structure and evolution of a fire ant hybrid zone. Evolution 50:1958-1976.
92. SIMON, C., F. FRATI, A. BECKENBACH, B. CRESPI, H. LIU, AND P. FLOOK. 1994. Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Ann. Entomol. Soc. Am. 87: 651-701.
93. SITES, J. W., JR., C. J. BASTEN, AND M. A. ASMUSSEN. 1996. Cytonuclear genetic structure of a hybrid zone in lizards of the Sceloporus grammicus complex (Sauria, Phrynosomatidae). Mol. Ecol. 5:379-392.
94. SLATKIN, M. 1973. Gene flow and selection in a cline. Genetics 75:733-756.
95. SPERLING, F. A., AND J. R. SPENCE. 1991. Structure of an asymmetric hybrid zone between two water strider species (Hemiptera: Gerridae: Limnoporus). Evolution 45:1370-1383.
96. SPERLING, F. A. H. 1994. Sex-linked genes and species differences in Lepidoptera. Can. Entomol. 126:807-818.
97. TUCKER, P. K., R. D. SAGE, J. WARNER, A. C. WILSON, AND E. M. EICHER. 1992. Abrupt cline for sex chromosomes in a hybrid zone between two species of mice. Evolution 46:1146-1163.
98. VANDER MEER, R. K., AND C. S. LOFGREN. 1989. Biochemical and behavioral evidence for hybridization between fire ants, Solenopsis invicta and Solenopsis richteri (Hymenoptera: Formicidae). J. Chem. Ecol. 15:1757-1765.
99. VANDER MEER, R. K., C. S. LOFGREN, AND F. M. ALVEREZ. 1985. Biochemical evidence for hybridization in fire ants. Fla. Entomol. 68:501-506.
100. VINSON, S. B., AND L. GREENBERG. 1986. The biology, physiology, and ecology of imported fire ants. Pp. 193-226 in S. B. Vinson, ed. Economic impact and control of social insects. Praeger, New York.