Evolutionary genetics and genetic variation of haplodiploids and X-linked genes

Annual Review of Ecology and Systematics

Volumn 28, Issue , 1997, Pages 55-83

  Hedrick, Philip W ^a   Parker, Joel D ^a  

^a ARIZONA STATE UNIVERSITY   (United States)

Author keywords

Effective population size; Heterozygosity; Inbreeding; Selection; X linked genes

Indexed keywords

EID: 0031436475     PISSN: 00664162     EISSN: None     Source Type: Journal    
DOI: 10.1146/annurev.ecolsys.28.1.55     Document Type: Review

References (174)

1. Aquadro CF, Begun BJ, Kindahl EC. 1994. Selection, recombination, and DNA polymorphism in Drosophila. In Non-Neutral Evolution, Theories and Molecular Data, ed. B Golding, pp. 46-56. New York: Chapman & Hall
2. Avery PJ. 1984. The population genetics of haplo-diploids and X-linked genes. Genet. Res. 44:321-41
3. Begun DJ. 1996. Population genetics of silent and replacement variation in Drosophila simulans and D. melanogaster: X/autosome differences? Mol. Biol. Evol. 13:1405-7
4. Begun DJ, Aquadro CF. 1991. Molecular population genetics of the distal portion of the X chromosome in Drosophila: evidence for genetic hitchhiking of the yellow-achaete region. Genetics 129:1147-58
5. Begun DJ, Aquadro CF. 1992. Levels of natural occurring DNA polymorphism correlate with recombination rate in Drosophila melanogaster. Nature 356:519-20
6. Belmont JW. 1996. Genetic control of X inactivation and processes leading to X-inactivation skewing. Am. J. Hum. Genet. 58:1101-8
7. Bennett JH, Oertel CR. 1965. The approach to random association of genotypes with random mating. J. Theor. Biol. 9:67-76
8. Berkelhamer RC. 1983. Intraspecific genetic variation and haplodiploidy, eusociality, and polygyny in the Hymenoptera. Evolution 37:540-45
9. Berry AJ, Ajiola JW, Kreitman M. 1991. Lack of polymorphism in the Drosophila fourth chromosome resulting from selection. Genetics 129:1111-17
10. Bijlsma R. 1982. Biochemical and physiological basis for fitness differences at allozyme loci in Drosophila melanogaster. In Advances in Genetics, Development, and Evolution of Drosophila, ed. S Lakovaara, pp. 297-308. New York: Plenum
11. Boato A, Battisti A. 1996. High genetic variability despite haplodiploidy in primitive sawflies of the genus Cephalcia (Hymenoptera, Pamphiliidae). Experientia 52:516-21
12. Boomsma JJ, Ratnieks FLW. 1996. Paternity in eusocial Hymenoptera. Philos. Trans. R. Soc. Lond. B. 351:947-75
13. Bregazzi V, Laverty T. 1992. Enzyme gene variation in five species of bumble bees (Hymenoptera: Apidae). Can. J. Zool. 70:1263-66
14. Bruckner C. 1976. The influence of genetic variation on wing symmetry on honeybees (Apis mellifera). Evolution 30:100-8
15. Bruckner C. 1978. Why are their inbreeding effects in haplodiploid systems? Evolution 32:230-33
16. Caballero A. 1995. On the effective size of populations with separate sexes, with particular reference to sex-linked genes. Genetics 139:1007-11
17. Caballero A, Hill WG. 1992. Effective size of non-random mating populations. Genetics 130:909-16
18. Carson HL. 1955. Variation in genetic recombination in natural populations. J. Cell. Compar. Physiol. 45:221-35
19. Chang H-J, Shimmin LC, Shyue S-K, Hewett-Emmett D, Li W-H. 1994. Weak male-driven molecular evolution in rodents. Proc. Natl. Acad. Sci. USA 91:827-31
20. Chapman TW, Stewart SC. 1996. Extremely high levels of inbreeding in a natural population of the free-living wasp Ancistrocerus antislope (Hymenoptera: Vespidea: Eumeninae). Heredity 76:65-69
21. Chapuisat M. 1996. Characterization of microsatellite loci in Formica lugubris B and their variability in other ant species. Mol. Ecol. 5:599-601
22. Charlesworth B. 1996. Background selection and patterns of genetic diversity in Drosophila melanogaster. Genet. Res. 68:131-49
23. Charlesworth B, Coyne JA, Barton NH. 1987. The relative rates of evolution of sex chromosomes and autosomes. Am. Nat. 130:113-46
24. Charlesworth B, Langley CH. 1989. The population genetics of Drosophila transposable elements. Annu. Rev. Genet. 23:251-87
25. Charlesworth B, Morgan MT, Charlesworth D. 1993. The effect of deleterious mutations on neutral molecular variation. Genetics 134:1289-303
26. Choudary M, Strassmann JE, Sous CR, Queller DC. 1993. Microsatellite variation in a social insect. Biochem. Genet. 31:87-96
27. Clarke GM, Brand GW, Whitten MJ. 1986. Fluctuating asymmetry: a technique for measuring developmental stress caused by inbreeding. Aust. J. Biol. Sci. 39:143-53
28. Clarke GM, Oldroyd BP, Hunt P. 1992. The genetic basis of developmental stability in Apis mellifera: heterozygosity versus genic balance. Evolution 46:753-62
29. Clegg MT, Covener DR. 1982. Dynamics of correlated genetic systems. VII. Demographic aspects of sex-linked transmission. Am. Nat. 120:108-18
30. Comparini A, Biasiolo A. 1991. Genetic discrimination of Italian bee, Apis mellifem ligustica versus Carniolan bee. Apis mellifera carnica by allozyme variability analysis. Biochem. Syst. Ecol. 19:189-94
31. Cook JM. 1993. Sex determination in the Hymenoptera: a review of models and evidence. Heredity 71:421-35
32. Cook JM, Crozier RH. 1995. Sex determination and population biology in the Hymenoptera. Trends Ecol. Evol. 10:281-86
33. Cornette JL. 1978. Sex-linked genes in age-structured populations. Heredity 40:291-97
34. Crespi BJ. 1991. Heterozygosity in the haplodiploid Thysanoptera. Evolution 45:458-64
35. Crow JF, Roberts WC-1950. Inbreeding and homozygosity in bees. Genetics 35-613-21
36. Crozier RH. 1970. On the potential for genetic variability in haplo-diploidy. Genetica 41:551-56
37. Crozier RH. 1976. Counter-intuitive property of effective population size. Nature 262:384
38. Crozier RH. 1976. Why male-haploid and sex-linked genetic systems seem to have unusually sex-limited mutational genetic loads. Evolution 30:613-24
39. Crozier RH. 1985. Adaptive consequences of male-haploidy. In Spider Mites: Their Biology, Natural Enemies and Control, ed. W Helle, MW Sabelis, pp. 201-22. Amsterdam: Eisevier
40. 39a. Crozier RH, Pamilo P. 1996. Evolution of Social Insect Colonies. Sex Allocation and Kin Selection. Oxford, UK: Oxford Univ. Press. 320 pp.
41. Curtsinger JW. 1980. On the opportunity for polymorphism with sex-linkage or haplodiploidy. Genetics 96:995-1006
42. Curtsinger JW. 1984. Components of selection in X chromosome lines of Drosophila melanogaster: sex ratio modification by meiotic drive and viability selection. Genetics 108:941-52
43. Deitrich WF, Miller J, Steen R, Merchant MA, Damron-Boles D, et al. 1996. A comprehensive genetic map of the mouse genome. Nature 380:149-52
44. Dib C, Faure S, Fizames C, Samson D, Drouot N, et al. 1996. A comprehensive map of the human genome based on 5.264 microsatellites. Nature 380:152-54
45. Dickson Burkhart B, Montgomery E, Langley CH, Voelker RA. 1984. Characterization of allozyme null and low activity alleles from two natural populations of Drosophila melanogaster. Genetics 107:295-306
46. Dobzhansky T. 1970. Genetics of the Evolutionary Process. New York: Columbia Univ. Press. 505 pp.
47. Drescher W. 1964. The sex limited genetic load in natural populations of Drosophila melanogaster. Am. Nat. 98:167-81
48. Eanes WF, Hey J, Houle D. 1985. Homozygous and hemizygous viability variation on the X chromosome of Drosophila melanogaster. Genetics 111:831-44
49. Eanes WF, Wesley C, Hey J, Houle D, Ajioka JW. 1988. The fitness consequences of P element insertion in Drosophila melanogaster. Genet. Res. 52:17-26
50. England PR, Briscoe DA, Frankham R. 1996. Microsatellite polymorphisms in a wild population of Drosophila melanogaster. Genet. Res. 67:285-90
51. Estoup A, Garney L, Solignac M, Cornuet JM. 1995. Microsatellite variation in Honey Bee (Apis mellifera L.) populations: hierarchical genetic structure and test of the infinite allele and stepwise mutation models. Genetics 140:679-95
52. Estoup A, Tailliez C, Cornuet JM, Solignac M. 1995. Size homoplasy and mutational processes of interrupted microsatellites in two bee species. Apis mellifera and Bombus terrestris (Apidae). Mol. Biol. Evol. 12:1074-84
53. Evans JD. 1993. Parentage analyses in ant colonies using simple sequence repeat loci. Mol. Ecol. 2:393-97
54. Fain PR, Kort EN, Chance PF, Nguyen K, Redd DF, et al 1995. A 2D crossoverbased map of the human X chromosome for map integration. Nat. Gener. 9:261-66
55. Gallo AJ. 1978. Genetic load of the X-chromosome in natural populations of Drosophila melanogaster. Genetica 49:153-57
56. Gertsch P, Pamilo P, Varvio SL. 1995. Microsatellites reveal high genetic diversity within colonies of Campunotus ants. Mol. Ecol. 4:257-60
57. Goldstein DB, Clark AG. 1995. Microsatellite variation in North American populations of Drosophila melanogaster. Nucleic Acids Res. 23:3882-86
58. Graur D. 1985. Gene diversity in Hymenoptera. Evolution 39:190-99
59. Haldane JBS. 1926. A mathematical theory of natural and artificial selection. Part III. Proc. Cambridge Philos. Soc. 23:363-72
60. Haldane JBS. 1935. The rate of spontaneous mutation of a human gene. J. Genet. 31:317-26
61. Haldane JBS, Jayakar SD. 1964. Equilibria under natural selection at a sex-linked locus. J. Genet. 59:29-36
62. Halliday RB. 1981. Heterozygosity and genetic distance in sibling species of meat ants (Iridomyrmex purpureus group). Evolution 35:234-42
63. Harnaguchi K, Ito Y. 1993. GT dinucleotide repeat polymorphisms in a polygynous ant. Leptothorax spinosior and their use for measurement of relatedness. Naturwissenschaften 80:179-81
64. Hamilton WD. 1964. The genetical evolution of social behavior. I. J. Theor. Biol. 7:1-16
65. Hamilton WD. 1964. The genetical evolution of social behavior. II. J. Theor. Biol. 7:17-52
66. Hamilton WD. 1967. Extraordinary sex ratios. Science 156:477-88
67. Hamilton WD. 1979. Wingless and fighting males in fig wasps and other insects. In Sexual Selection and Reproductive Competition in Insects, ed. MS Blum, NA Blum, pp. 167-220. New York: Academic
68. Haiti DL. 1971. Some aspects of natural selection in arrhenotokous populations. Am. Zool. 11:309-25
69. Hartl DL. 1972. A fundamental theorem of natural selection for sex linkage or arrhenotoky. Am. Nat. 106:516-24
70. Hedrick PW. 1976. Simulation of X-linked selection in Drosophila. Genetics 83:551-71
71. Hedrick PW. 1980. Selection in finite populations. III. An experimental examination. Genetics 96:297-313
72. Hedrick PW. 1982. Genetic hitchhiking: a new factor in evolution. Bioscience 32:845-53
73. Hedrick PW. 1985. Genetic of Populations. Boston: Jones & Bartlett. 629 pp.
74. Hedrick PW, Cockerham CC. 1986. Partial inbreeding: equilibrium heterozygosity and the heterozygosity paradox. Evolution 40:856-61
75. Hill WG. 1974. Estimation of linkage disequilibrium in randomly mating populations. Heredity 33:229-39
76. Hill WG. 1979. A note on effective population size with overlapping generations. Genetics 92:317-22
77. Hofker MH, Skaastad MI, Bergen AAB, Wapenaar MC, Bakker E, et al. 1986. The X chromosome shows less genetic variation at restriction sites than the autosomes. Am. J. Hum. Genet. 39:438-51
78. Hollocher H, Wu C-I. 1996. The genetics of reproductive isolation in the Drosophila simulans clade: X vs. autosomal effects and male vs. female effects. Genetics 143:1243-55
79. Hughes CR, Queller DC. 1993. Detection of highly polymorphic microsatellite loci in a species with little allozyme polymorphism. Mol. Ecol. 2:131-37
80. Hunt GJ, Page RE, Fondrk MK, Dullum CJ. 1995. Major quantitative trait loci affecting honey bee foraging behavior. Genetics 141:1537-45
81. Janecek LL, Honeycutt IL, Rautenbach BH, Erasmus SR, Schitter DA. 1992. Allozyme variation and systematics of African mole-rats (Rodentia: Bathyergidae). Biochem. Syst. Ecol. 20:401-16
82. Jennings HS. 1916. The numerical results of diverse systems of breeding. Genetics 1:53-89
83. Keller L, Passera L. 1993. Incest avoidance, fluctuation asymmetry, and the consequences of inbreeding in Iridomyrmex humilis, an ant with multiple queen colonies. Behav. Ecol. Sociobiol. 233:191-99
84. Kerr WE. 1976. Population genetic studies in bees. 2. sex-limited genes. Evolution 30:94-99
85. Kerr WE, Kerr LS. 1952. Concealed variability in the X-chromosome of Drosophila melanogaster. Am. Nat. 86:405-07
86. Kidwell JF, Clegg MT, Stewart FM, Prout T. 1977. Regions of stable equilibria for models of differential selection in the two sexes under random mating. Genetics 85:171-83
87. Kimura M. 1969. The number of heterozygous nucleotide sites maintained in a finite population due to steady flux of mutation. Genetics 61:893-903
88. Kimura M, Crow JF. 1964. The number of alleles that can be maintained in a finite population. Genetics 49:725-38
89. Kukuk PF, May B. 1985. A reexamination of genetic variability in Ditalictus zephyrus (Hymenoptera: Halictidae). Evolution 39:226-28
90. LaMunyon CW, Ward S. 1997. Increased competitiveness of nematode sperm bearing the male X chromosome. Proc. Natl Acad. Sci. USA 94:185-89
91. Langley CH, Voelker RA, Leigh Brown AJ, Ohnishi S, Dickson B, Montgomery E. 1981. Null allele frequencies at allozyme loci in natural populations of Drosophila melanogaster. Genetics 99:151-56
92. Lester LJ, Selander RK. 1979. Population genetics of haplodiploid insects. Genetics 92:1329-43
93. Li CC. 1976. First Course in Population Genetics. Pacific Grove, CA: Boxwood. 631 pp.
94. Li W-H, Ellsworth DL, Krushkal J, Chang BH-J, Hewett-Emmett D. 1996. Rates of nucleotide substitution in primates and rodents and the generation-time effect hypothesis. Mol. Phylogenet. Evol. 5:182-87
95. Li W-H, Sadler LA. 1991. Low nucleotide diversity in man. Genetics 129:513-23
96. Lisker R, Motulsky AG. 1967. Computer simulation of evolutionary trends in an X linked trait, application to glucose-6-phosphate dehydrogenase deficiency in man. Acta Genet. 17:465-74
97. Lyon MF. 1992. Some milestones in the history of X-chromosome inactivation. Annu. Rev. Genet. 26:17-28
98. Lyttle TW. 1991. Segregation distorters. Annu. Rev. Genet. 25:511-37
99. Mayo O. 1976. Neutral alleles at X-linked loci: a cautionary note. Hum. Hered 26:49-63.
100. McKusick V. 1994. Mendelian Inheritance in Man. Baltimore, MD: Johns Hopkins Univ. Press. 3009 pp. 11 ed.
101. 99a. McVean GT, Hurst LD. 1997. Evidence for a selectively favorable reduction in the mutation rate of the X chromosome. Nature 386:388-92
102. Menken SJB. 1982. Enzymatic characterization of nine endoparasite species of small Ermine moths (Yponomeutidae). Experientia 38:1461-62
103. Metcalf RA, Marlin JC, Whitt GS. 1975. Low levels of genetic heterozygosity in Hymenoptera. Nature 257:792-93
104. Michalakis Y, Veuille M. 1996. Length variation of CAG/CAA trinucleotide repeats in natural populations of Drosophila melanogaster and its relation to the recombination rate. Genetics 143:1713-25
105. Montgomery E, Charlesworth B, Langley CH. 1987. A test for the role of natural selection in the stabilization of transposable element copy number in a population of Drosophila melanogaster. Genet. Res. 49:31-41
106. Moriyama EN, Powell JR. 1996. Intraspecific nuclear DNA variation in Drosophila. Mol Biol Evol. 13:261-77
107. Motulsky AG. 1960. Metabolic polymorphism and the role of infectious disease in human evolution. Hum. Biol. 32:28-62
108. Nagylaki T. 1975. A continuous selective model for a X-linked locus. Heredity 34:273-78
109. Nagylaki T. 1979. Selection in dioecious populations. Ann. Hum Genet. 43:143-50
110. Nagylaki T. 1981. The inbreeding effective population number and the expected homozygosity for an X-linked locus. Genetics 47:731-37
111. Nagylaki T. 1995. The inbreeding effective population number in dioecious populations. Genetics 139:473-85
112. Nei M. 1978. Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583-90
113. Nunney L. 1993. The influence of mating system and overlapping generations on effective population size. Evolution 47:389-92
114. Owen RE. 1985. Difficulties with the interpretation of patterns of genetic variation in the eusocial Hymenoptera. Evolution 39:205-10
115. Owen RE. 1986. Colony-level selection in the social insects: single locus additive and nonadditive models. Theor. Pop. Biol. 29:198-234
116. Owen RE. 1986. Gene frequency clines at X-linked orhaplodiploid loci. Heredity 57:209-19
117. Owen RE. 1988. Selection at two sexlinked loci. Heredity 60:415-25
118. Owen RE. 1989. Differential size variation of male and female bumblebees. J. Hered. 80:39-43
119. Owen RE. 1993. Genetics of parasitic hymenoptera. In Applications of Genetics to Arthropods of Biological Control Significance, ed. SK Narang, AC Bartlett, RM Faust, pp. 69-89. Boca Raton, FL: CRC
120. Owen RE, Mydynnski LJ, Packer L, McCorquodale DB. 1992. Allozyme variation in Bumble Bees (Hymenoptera: Apidae). Biochem. Syst. 30:443-53
121. Owen RE, Owen ARG. 1989. Effective population size in social Hymenoptera with worker-produced males. Heredity 63:59-65
122. Owen RE, Packer L. 1994. Estimation of the proportion of diploid males in populations of Hymenoptera. Heredity 72:219-27
123. Packer L, Owen RE. 1989. Allozyme variation in Halictus rubicundus (Christ): a primitively social Halictine Bee (Hymenoptera: Halictidae). Can. Entomol. 121:1049-57
124. Packer L, Owen RE. 1990. Allozyme variation, linkage disequilibrium and diploid male production in a primitively social bee Augochorella striate (Hymenoptera; Halictidae). Heredity 65:241-48
125. Page RE. 1986. Sperm utilization in social insects. Annu. Rev. Ecol. Svst. 31:297-320
126. Pamilo P. 1979. Genie variation at sexlinked loci: quantification of regular selection models. Hereditas 91:129-33
127. Pamilo P. 1991. Evolution of colony characteristics in social insects. I. Sex allocation. Am. Nat. 137:83-107
128. Pamilo P. 1991. Evolution of colony characteristics in social insects. II. Number of reproductive individuals. Am. Nat. 138:412-33
129. Pamilo P. 1993. Polyandry and allele frequency differences between the sexes in the ant Formica aquilonia. Heredity 70:472-80
130. Pamilo P, Crozier RH. 1981. Genie variation in male haploids under deterministic selection. Genetics 98:199-214
131. Pamilo P, Gertsch P, Thorén P, Seppä P. 1997. Molecular population genetics of social insects. Annu. Rev. Ecol. Syst. 28:1-26
132. Pamilo P, Sundstrom L, Fortelius W, Rosengren R. 1994. Diploid males and colony-level selection in Formica ants. Ethol. Ecol. Evol. 6:221-35
133. Pamilo P, Varvio-Aho S, Pekkarinen A. 1978. Low enzyme gene variability in Hymenoptera as a consequence of haplodiploidy. Hereditas 88:93-99
134. Pamilo P, Varvio-Aho S, Pekkarinen A. 1984. Genetic variation in bumblebee s (Bombus, Psithyrus) and putative sibling species of Bombus lucorum. Hereditas 101:245-51
135. Pamilo P, Vepsalainen K, Rosengren R. 1975. Low allozymic variability in Formica ants. Hereditas 80:293-96
136. Passera L, Keller L, Suzzoni J. 1988. Queen replacement in dequeened colonies of the Argentine ant Iridomyrmex humilis (Mayr). Psyche 95:59-63
137. Pollak E. 1984. Gamete frequencies at two sex-linked loci in random mating age-structured populations. Math. Biosci. 70:217-35
138. Pollak E. 1990. The effective population size of an age-structured population with a sex-linked locus. Math. Biosci. 101:121-30
139. Queller DC. 1993. Worker control of sex ratio and selection for extreme multiple mating by queens. Am. Nat. 142:346-51
140. Rao SSR. 1983. Religion and intensity of inbreeding in Tamil Nadu, South India. Soc. Biol. 30:413-22
141. Reeve HK, Sherman-Reeve J, Pfennig DW. 1985. Eusociality and genetic variability: a re-evaluation. Evolution 39:200-1
142. Rosemeier L, Packer L. 1993. A comparison of genetic variation in two sibling species pair of Haplodiploid insects. Biochem. Genet. 31:185-200
143. Ross KG. 1992. Strong selection on a gene that influences reproductive competition in a social insect. Nature 355:347-49
144. Ross KG, Keller L 1995. Ecology and evolution of social organization: insights from fire ants and other highly eusocial insects. Annu. Rev. Ecol. Syst. 26:631-56
145. Ross KG, Keller L. 1995. Joint influence of gene flow and selection on a reproductively important genetic polymorphism in the fire ant Solenopsis invicta. Am. Nat. 146:325-48
146. Ruwende C, Khoo SC, Snow RW, Yates SNR, Kwiatowski D, et al. 1995. Natural selection of hemizygotes for G6PD deficiency in Africa by resistance to severe malaria. Nature 376:246-49
147. Sanghvi LD. 1966. Inbreeding in India. Eugen. Q. 13:291-301
148. Schug MD, Mackay TFC, Aquadro CF. 1997. Low mutation rates of microsatellite loci in Drosophila melanogaster. Nat. Genet. 15:99-102
149. Schug MD, Wettstrand KA, Gaudette MS, Lim RH, Hutter CM, Aquadro CF. 1997. The distribution and frequency of microsatellite loci in Drosophila melanogaster. Nucleic Acids Res. In press
150. Sheppard WS, Heydon SL. 1986. High levels of genetic variability in three male-haploid species (Hymenoptera: Argidae, Tenthredinidae). Evolution 40:1350-53
151. Shimmin LC, Chang BH-W, Li W-H. 1993. Male driven evolution of DNA sequences. Nature 362:745-47
152. Shoemaker DD, Ross KG. 1992. Estimates of heterozygosity in two social insects using a large number of electrophoretic markers. Heredity 69:573-82
153. Simmons MJ, Crow JF. 1977. Mutations affecting fitness in Drosophila populations. Annu. Rev. Genet. 11:49-78
154. Singh RS, Rhomberg LR. 1987. A comprehensive study of genic variation in natural populations of Drosophila melanogaster. II. Estimates of heterozygosity and patterns of geographic differentiation. Genetics 117:255-71
155. Slatkin N. 1995. A measure of population subdivision based on microsatellite allele frequencies. Genetics 139:457-62
156. Slatkin M, Excoffier L. 1996. Testing for linkage disequilibrium in genotypic data using the Expectation-Maximization algorithm. Heredity 76:377-83
157. Snyder TP. 1974. Lack of allozymic variability in three bee species. Evolution 28:687-89
158. Strassmarm JE, Barefield K, Solis CR, Hughes CR, Queller DC. 1997. Trinucleotide microsatellite loci for a social wasp, Polistes. Mol. Ecol. 6:97-100
159. Thomson G. 1977. The effects of a selected locus on linked neutral loci. Genetics 85:753-88
160. n microsatellite loci in a yellowjacket wasp, Vespula rufa (L.) (Hymenoptera: Vespidae). Biochem. Genet. 4:141-48
161. Turelli M, Orr HA. 1995. The dominance theory of Haldane's rule. Genetics 140:389-402
162. Voelker RA, Langley CH, Leigh Brown AJ, Ohnishi S, Dickson B. et al. 1980. Enzyme null alleles in natural population of Drosophila melanogaster: frequencies in a North Carolina population. Proc. Natl. Acad. Sci. USA 77:1091-95
163. Waage JK. 1986. Family planning in parasitoids: adaptive patterns of progeny and sex allocation. In Insect Parasitoids, ed. JK Waage, D Greathead, pp. 63-95. London: Academic
164. Wagner AE, Briscoe DA. 1983. An absence of enzyme variation within two species of Trigona (Hymenoptera). Heredity 50:97-103
165. Wang J. 1996. Inbreeding coefficient and effective size for an X-linked locus in nonrandom mating populations. Heredity 76:569-77
166. Ward PS. 1980. Genetic variation and population differentiation in the Rhytidoponera impressa group, a species complex of ponerine ants (Hymenoptera: Formicidae), Evolution 34:1060-76
167. Ward PS, Taylor RW 1981. Allozyme variation, colony structure and genetic relatedness in the primitive ant Nothomyrmecia macrops Clark (Hymenoptera: Formicidae). J. Aust. Entomol. Soc. 20:177-83
168. Werren JH. 1993. The evolution of inbreeding in haplodiploid organisms. In The Natural History of Inbreeding and Outbreeding: Theoretical and Empirical Perspectives, ed. NW Thornhill, pp. 42-59, Chicago: Univ. Chicago Press
169. Wilton AD, Sved JA. 1979. X chromosomal heterosis in Drosophila melanogaster. Genet. Res. 34:303-15
170. Whitlock MC, Wade MJ. 1995. Speciation: founder events and their effects on X-linked and autosomal genes. Am. Nat. 145:676-85
171. Wright S. 1922. Coefficients of inbreeding and relationship. Am. Nat. 56:330-38
172. Wright S. 1933. Inbreeding and homozygosis. Proc. Natl. Acad. Sci. USA 19:411-20
173. Wright S. 1969. Evolution and Genetics of Populations. Vol. II. The Theory of Gene Frequencies. Chicago: Univ. Chicago Press. 511 pp.
174. Wu C-l, Davis AW. 1993. Evolution of postmating reproductive isolation: the composite nature of Haldane's rule and its genetic bases. Am. Nat. 142:187-212