Evolution of multiple kinds of female sperm-storage organs in Drosophila

Evolution

Volumn 53, Issue 6, 1999, Pages 1804-1822

  Pitnick, Scott ^a   Markow, Therese ^b,c   Spicer, Greg S ^d  

^a SYRACUSE UNIVERSITY   (United States)

^b ARIZONA STATE UNIVERSITY   (United States)

^c University of Arizona   (United States)

^d SAN FRANCISCO STATE UNIVERSITY   (United States)

Author keywords

Cryptic female choice; Reproduction; Sexual selection; Sperm; Sperm competition; Spermatheca; Vestigial

Indexed keywords

EVOLUTION; MORPHOLOGY; REPRODUCTIVE BIOLOGY;

DIPTERA; DROSOPHILA; DROSOPHILIDAE;

EID: 0033403583     PISSN: 00143820     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1558-5646.1999.tb04564.x     Document Type: Article

References (147)

1. Adiyodi, K. G. 1988. Annelida. Pp. 189-250 in K. G. Adiyodi and R. G. Adiyodi, eds. Reproductive biology of invertebrates. III. Accessory sex glands. Wiley, Chinchester, U.K.
2. Albuquerque, G. S., C. A. Tauber, and M. J. Tauber. 1996. Postmating reproductive isolation between Chrysopa quadripunctata and Chrysopa slonnae: mechanisms and geographic variation. Evolution 50:1598-1606.
3. Alexander, R. D., D. C. Marshall, and J. R. Cooley. 1997. Sexual conflict and the evolution of mating systems. Pp. 4-31 in J. C. Choe and B. J. Crespi, eds. The evolution of mating systems in insects and arachnids. Cambridge Univ. Press, Cambridge, U.K.
4. Anderson, R. C. 1945. A study of the factors affecting fertility of lozenge females of Drosophila melanogaster. Genetics 30:280-296.
5. Andersson, M. 1994. Sexual selection. Princeton Univ. Press, Princeton, NJ.
6. Ashburner, M. 1989. Drosophila: a laboratory handbook. Cold Spring Harbor Laboratory Press, New York.
7. Barrio, E., A. Latorre, and A. Moya. 1994. Phylogeny of the Drosophila obscura species group deduced from mitochondrial DNA sequences. J. Mol. Evol. 39:478-488.
8. Bauer, R. T., and J. W. Martin. 1991. Crustacean sexual biology. Columbia Univ. Press, New York.
9. Baur, B. 1998. Sperm competition in molluscs. Pp. 255-305 in T. R. Birkhead and A. P. Møller, eds. Sperm competition and sexual selection. Academic Press, San Diego, CA.
10. Bella, J. L., R. K. Butlin, and G. M. Hewitt. 1992. Asymmetrical homogamy and unequal sex ratio from reciprocal mating-order crosses between Chorthippus parallelus subspecies. Heredity 68: 345-352.
11. Beverley, S. M., and A. C. Wilson. 1982. Molecular evolution in Drosophila and the higher Diptera. I. Micro-complement fixation studies of a larval hemolymph protein. J. Mol. Evol. 18:251-264.
12. _. 1984. Molecular evolution in Drosophila and the higher Diptera. II. A time scale for fly evolution. J. Mol. Evol. 21:1-13.
13. Birkhead, T. R. 1998. Cryptic female choice: criteria for establishing female sperm choice. Evolution 52:1212-1218.
14. Birkhead, T. R., and A. P. Møller. 1992. Sperm competition in birds: evolutionary causes and consequences. Academic Press, London.
15. Birkhead, T. R., A. P. Møller, and W. J. Sutherland. 1993. Why do females make it so difficult for males to fertilize their eggs? J. Theor. Biol. 161:51-60.
16. Blaney, W. M. 1970. Some observations on the sperm tail of D. melanogaster. Dros. Info. Serv. 45:125-127.
17. Bloch Qazi, M. C., J. R. Aprille, and S. M. Lewis. 1998. Female role in sperm storage in the red flour beetle, Tribolium castaneum. Comp. Biochem. Physiol. A 120:641-647.
18. Boisseau, C., and J. Joly. 1975. Transport and survival of spermatozoa in female amphibia. Pp. 94-104 in E. S. E. Hafez and C. G. Thibault, eds. The biology of spermatozoa. Karger, Basel, Switzerland.
19. Boulétreau-Merle, J. 1977. Rôle des spermathéques dans l'utilisation du sperme et la stimulation de l'ovogenese chez Drosophila melanogaster. J. Insect Physiol. 23:1099-1104.
20. Bressac, C., and E. Hauschteck-Jungen. 1996. Drosophila subobscura females preferentially select long sperm for storage and use. J. Insect Physiol. 42:323-328.
21. Briskie, J. V., and R. Montogomerie. 1992. Sperm size and sperm competition in birds. Proc. R. Soc. Lond. B Biol. Sci. 247:89-95.
22. _. 1993. Patterns of sperm storage in relation to sperm competition in passerine birds. Condor 95:442-454.
23. Briskie, J. V., R. Montgomerie, and T. R. Birkhead. 1997. The evolution of sperm size in birds. Evolution 51:937-945.
24. Brown, W. D., B. J. Crespi, and J. C. Choe. 1997. Sexual conflict and the evolution of mating systems. Pp. 352-377 in J. C. Choe and B. J. Crespi, eds. The evolution of mating systems in insects and arachnids. Cambridge Univ. Press, Cambridge, U.K.
25. Caccone, A., J. M. Gleason, and J. R. Powell. 1992. Complementary DNA-DNA hybridization in Drosophila. J. Mol. Evol. 34: 130-140.
26. Callahan, P. S., and T. Cascio. 1963. Histology of the reproductive tracts and transmission of sperm in the corn earworm, Heliothis zea. Ann. Entomol. Soc. Am. 56:535-556.
27. Carayon, J. 1966. Traumatic insemination and the paragenital system. Pp. 81-166 in R. Usinger, ed. Monograph of Cimicidae. Thomas Say Foundation 7, Entomological Society of America, Philadelphia, PA.
28. Chapman, T., L. F. Liddle, J. M. Kalb, M. F. Wolfner, and L. Partridge. 1995. Cost of mating Drosophila melanogaster females is mediated by male accessory gland products. Nature 373:241-244.
29. Clarke, M. R. B. 1980. The reduced major axis of a bivariate sample. Biometrika 67:441-446.
30. Cunningham, C. W., K. E. Omland, and T. H. Oakley. 1998. Reconstructing ancestral character states: a critical reappraisal. Trends Ecol. Evol. 13:361-366.
31. Davey, K. G. 1958. The migration of spermatozoa in the female of Rhodnius prolixus Stal. J. Exp. Biol. 30:694-701.
32. _. 1965. Reproduction in insects. Oliver and Boyd, London.
33. Davies, N. B. 1989. Sexual conflict and the polygamy threshold. Anim. Behav. 38:226-234.
34. DeSalle, R. 1992. The phylogenetic relationships of flies in the family Drosophilidae deduced from mtDNA sequences. Mol. Phylog. Evol. 1:31-40.
35. Donoghue, M. J., and D. D. Ackerly. 1996. Phylogenetic uncertainties and sensitivity analysis in comparative biology. Phil. Trans. R. Soc. Lond. B Biol. Sci. 351:1241-1249.
36. Downes, J. A. 1968. Notes on the organs of processes of sperm-transfer in the lower Diptera. Can. Entomol. 100:608-617.
37. Dybas, L. K., and H. S. Dybas. 1981. Coadaptation and taxonomic differentiation of sperm and spermathecae in featherwing beetles. Evolution 35:168-174.
38. Eberhard, W. G. 1985. Sexual selection and animal genitalia. Harvard Univ. Press, Cambridge, MA.
39. _. 1996. Female control: sexual selection by cryptic female choice. Princeton University Press, Princeton, NJ.
40. Felsenstein, J. 1985. Phylogenies and the comparative method. Am. Nat. 125:1-15.
41. Filosi, M., and M. E. Perotti. 1975. Fine structure of the spermatheca of Drosophila melanogaster. J. Submicr. Cytol. 7:259-270.
42. Fowler, G. L. 1973. Some aspects of the reproductive biology of Drosophila: sperm transfer, sperm storage, and sperm utilization. Adv. Genet. 17:293-360.
43. Gack, C., and K. Peschke. 1994. Spermathecal morphology, sperm transfer and a novel mechanism of sperm displacement in the rove beetle, Aleochara curtula (Coleoptera, Staphylinidae). Zoomorphology 114:227-237.
44. Gage, M. J. G. 1994. Associations between body size, mating pattern, testis size, and sperm lengths across butterflies. Proc. R. Soc. Lond. B Biol. Sci. 258:247-254.
45. Garland, T. 1985. Ontogenetic and individual variation in size, shape and speed in the Australian agamid lizard Amphibolurus nuchalis. J. Zool. 207:425-439.
46. Garland, T., P. H. Harvey, and A. R. Ives. 1992. Procedures for the analysis of comparative data using phylogenetically independent contrasts. Syst. Biol. 41:18-32.
47. Garland, T., A. W. Dickerman, C. M. Janis, and J. A. Jones. 1993. Phylogenetic analysis of covariance by computer simulation. Syst. Biol. 42:265-292.
48. Gilbert, D. G. 1981. Ejaculate esterase-6 and initial sperm use by female Drosophila melanogaster. J. Insect Physiol. 27:641-650.
49. Gomendio, M., and E. R. S. Roldan. 1991. Sperm competition influences sperm size in mammals. Proc. R. Soc. Lond. B Biol. Sci. 243:181-185.
50. Gowaty, P. A. 1997. Sexual dialectics, sexual selection, and variation in reproductive behavior. Pp. 351-384 in P. A. Gowaty, ed. Feminism and evolutionary biology. Chapman and Hall, New York.
51. Gowaty, P. A., and N. Buschhaus. 1998. Ultimate causation of aggressive and forced copulation in birds: female resistance, the CODE hypothesis, and social monogamy. Am. Zool. 38:207-225.
52. Gregory, P. G., and D. J. Howard. 1993. Laboratory hybridization studies of Allonemobius fasciatus and A. socius (Orthoptera: Gryllidae). Ann. Entomol. Soc. Am. 86:694-701.
53. _. 1994. A postinsemination barrier to fertilization isolates two closely related ground crickets. Evolution 48:705-710.
54. Grimaldi, D., A. C. James, and J. Jaenike. 1992. Systematics and modes of reproductive isolation in the holarctic Drosophila testacea species group (Diptera: Drosophildae). Ann. Entomol. Soc. Am. 85:671-685.
55. Harvey, P. H., and M. D. Pagel. 1991. The comparative method in evolutionary biology. Oxford Univ. Press, Oxford, U.K.
56. Hellriegel, B., and P. I. Ward. 1998. Complex female reproductive tract morphology: its possible use in postcopulatory female choice. J. Theor. Biol. 190:179-186.
57. Hewitt, G. M., P. Mason, and R. A. Nichols. 1989. Sperm precedence and homogamy across a hybrid zone in the alpine grasshopper Podisma pedestris. Heredity 62:343-353.
58. Hihara, F., and H. Kurokawa. 1987. The sperm length and the internal reproductive organs of Drosophila with special references to phylogenetic relationships. Zool. Sci. 4:167-174.
59. Holland, B., and W. R. Rice. 1998. Chase-away sexual selection: antagonistic seduction versus resistance. Evolution 52:1-7.
60. Jefferson, M. C. 1977. Breeding biology of Drosophila pachea and its relatives. Ph.D. diss., University of Arizona, Tucson, AZ.
61. Joly, D., and C. Bressac. 1994. Sperm length in Drosophildae (Diptera): estimation by testis and receptacle lengths. Int. J. Insect Morphol. Embryol. 23:85-92.
62. Kadow, P. E. 1954. An analysis of sexual behavior and reproductive physiology in the guppy, Lebistes reticulatus (Peters). Ph.D. diss., New York University, New York.
63. Karr, T. L., and S. Pitnick. 1996. The ins and outs of fertilization. Nature 379:405-406.
64. Keller, L., and H. Reeve. 1995. Why do females mate with multiple males? The sexually selected sperm hypothesis. Adv. Study Behav. 24:291-315.
65. Knowlton, N., and S. R. Greenwell. 1984. Male sperm competition avoidance mechanisms: The influence of female interests. Pp. 61-84 in R. L. Smith, ed. Sperm competition and the evolution of animal mating systems. Academic Press, New York.
66. Kwiatowski, J., D. Skarecky, K. Bailey, and F. J. Ayala. 1994. Phylogeny of Drosophila and related genera inferred from the nucleotide sequence of the Cu, Zn Sod gene. J. Mol. Evol. 38: 443-454.
67. LaMunyon, C. W., and T. Eisner. 1993. Postcopulatory sexual selection in an arctiid moth (Utetheisa ornatrix). Proc. Natl. Acad. Sci. USA 90:4689-4692.
68. LaMunyon, C., and S. Ward. 1998. Larger sperm outcompete smaller sperm in the nematode C. elegans. Proc. R. Soc. Lond. B Biol. Sci. 265:1-6.
69. LeCato, G. L., and R. L. Pienkowski. 1973. Insemination and sperm storage in the alfalfa weevil, Hypera postica (Gyllenhal) (Coleoptera: Curculionidae). Int. J. Insect Morphol. Embryol. 2: 257-263.
70. Linley, J. R. 1981. Emptying of the spermatophore and spermathecal filling in Culicoides melleus (Coq.)(Diptera: Ceratopogonidae). Can. J. Zool. 59:347-356.
71. Linley, J. R., and K. R. Simmons. 1981. Sperm motility and spermathecal filling in lower Diptera. Int. J. Invert. Repro. 4:137-146.
72. _. 1983. Quantitative aspects of sperm transfer in Simulium decorum (Diptera: Simuliidae). J. Insect Physiol. 9:581-584.
73. Maddison, D. R. 1994. Phylogenetic methods for inferring the evolutionary history and processes of change in discretely valued characters. Annu. Rev. Entomol. 39:267-292.
74. Maddison, W. P., and D. R. Maddison. 1997. MacClade: analysis of phylogeny and character evolution. Vers. 3.05. Sinauer, Sunderland, MA.
75. Markow, T. A. 1996. Evolution of Drosophila mating systems. Pp. 73-106 in M. K. Hecht, ed. Evolutionary biology. Vol. 29. Plenum Press, New York.
76. _. 1997. Assortative fertilization in Drosophila. Proc. Natl. Acad. Sci. USA 94:7756-7760.
77. Martins, E. P., and T. Garland. 1991. Phylogenetic analyses of the correlated evolution of continuous characters: a simulation study. Evolution 45:534-557.
78. Miller, A. 1950. The internal anatomy and histology of the imago of Drosophila melanogaster. Pp. 420-534 in M. Demerec, ed. Biology of Drosophila. Hafner, New York.
79. Moore, J. A. 1949. Patterns of evolution in the genus Rana. Pp. 315-338 in G. L. Jepsen, E. Mayr and G. G. Simpson, eds. Genetics, paleontology, and evolution. Princeton Univ. Press, Princeton, NJ.
80. Nonidez, J. F. 1920. The internal phenomena of reproduction in Drosophila. Biol. Bull. 39:207-230.
81. Olsson, M., and T. Madsen. 1998. Sexual selection and sperm competition in reptiles. Pp. 503-577 in T. R. Birkhead and A. P. Møller, eds. Sperm competition and sexual selection. Academic Press, San Diego, CA.
82. Omland, K. E. 1997. Examining two standard assumptions of ancestral reconstructions: repeated loss of dichromatism in dabbling ducks (Anatini). Evolution 51:1636-1646.
83. Otronen, M., P. Reguera, and P. I. Ward. 1997. Sperm storage in the yellow dung fly Scathophaga stercoraria: identifying the sperm of competing males in separate female spermathecae. Ethnology 103:844-854.
84. Parker, G. A. 1970. Sperm competition and its evolutionary consequences in the insects. Biol. Rev. 45:525-567.
85. _. 1984. Sperm competition and the evolution of animal mating strategies. Pp. 1-60 in R. L. Smith, ed. Sperm competition and the evolution of animal mating systems. Academic Press, New York.
86. _. 1993. Sperm competition games: Sperm size and sperm number under adult control. Proc. R. Soc. Lond. B Biol. Sci. 253:245-254.
87. Partridge, L., and M. Farquhar. 1981. Sexual activity reduces lifespan of male fruitflies. Nature 294:580-582.
88. Patterson, J. T. 1943. Studies in the genetics of Drosophila. III. The Drosophilidae of the southwest. Univ. Texas Publ. 4313:7-203.
89. _. 1947. II. Sexual isolation in the mulleri subgroup. Univ. Texas Publ. 4720:32-40.
90. _. 1954. Fate of the sperm in the reproductive tract of the Drosophila female in homogamic matings. Univ. Texas Publ. 5422:19-37.
91. Pelandakis, M., and M. Solignac. 1993. Molecular phylogeny of Drosophila based on ribosomal RNA sequences. J. Mol. Evol. 37:525-543.
92. Pitnick, S. 1996. Investment in testes and the cost of making long sperm in Drosophila. Am. Nat. 148:57-80.
93. Pitnick, S., and T. A. Markow. 1994a. Male gametic strategies: Sperm size, testes size, and the allocation of ejaculate among successive mates by the sperm-limited fly Drosophila pachea and its relatives. Am. Nat. 143:785-819.
94. _. 1994b. Large-male advantages associated with costs of sperm production in Drosophila hydei, a species with giant sperm. Proc. Natl. Acad. Sci. USA 91:9277-9281.
95. Pitnick, S., T. A. Markow, and M. F. Riedy. 1991. Transfer of ejaculate and incorporation of male-derived substances by females in the nannoptera species group (Diptera: Drosophilidae). Evolution 45:774-780.
96. Pitnick, S., T. A. Markow, and G. S. Spicer. 1995a. Delayed male maturity is a cost of producing large sperm in Drosophila. Proc. Natl. Acad. Sci. USA 92:10614-10618.
97. Pitnick, S., G. S. Spicer, and T. A. Markow. 1995b. How long is a giant sperm? Nature 375:109.
98. _. 1997. Phylogenetic examination of female incorporation of ejaculate in Drosophila. Evolution 51:833-845.
99. Polak, M. 1993. Parasites increase fluctuating asymmetry of male Drosophila nigrospiracula: implications for sexual selection. Genetica 89:255-265.
100. Powell, J. R. 1997. Progress and prospects in evolutionary biology: the Drosophila model. Oxford Univ. Press, New York.
101. Powell, J. R., and R. DeSalle. 1995. Drosophila molecular phylogenies and their uses. Evol. Biol. 28:87-138.
102. Presgraves, D. C., R. H. Baker, and G. S. Wilkinson. 1999. Coevolution of sperm and female reproductive tract morphology in stalk-eyed flies. Proc. R. Soc. Lond. B Biol. Sci. 266:1041-1047.
103. Price, C. S. C. 1997. Conspecific sperm precedence in Drosophila. Nature 388:663-666.
104. Racey, P. A. 1979. The prolonged storage and survival of spermatoazoa in Chiroptera. J. Repro. Fert. 56:391-402.
105. Radwan, J. 1996. Intraspecific variation in sperm competition success in the bulb mite: a role of sperm size. Proc. R. Soc. Lond. B Biol. Sci. 263:855-859.
106. Ree, R. H., and M. J. Donoghue. 1998. Step matrices and the interpretation of homoplasy. Syst. Biol. 47:582-588.
107. Rice, W. R. 1996. Sexually antagonistic male adaptation triggered by experimental arrest of female evolution. Nature 381:232-234.
108. _. 1997. Intergenomic conflict, interlocus antagonistic evolution, and the evolution of reproductive isolation. Pp. 261-270 in D. J. Howard and S. H. Berlocher, eds. Endless forms: species and speciation. Oxford Univ. Press, Oxford, U.K.
109. Rice, W. R., and B. Holland. 1997. The enemies within: intergenomic conflict, interlocus contest evolution (ICE), and the intraspecific Red Queen. Behav. Ecol. Sociobiol. 41:1-10.
110. Rice, W. R., and E. E. Hostert. 1993. Laboratory experiments on speciation: what have we learned in 40 years? Evolution 47: 1637-1653.
111. Robinson, T., N. A. Johnson, and M J. Wade. 1994. Postcopulatory, prezygotic isolation: intraspecific and interspecific sperm precedence in Tribolium spp. flour beetles. Heredity 73:155-159.
112. Rodríguez, V. 1994. Function of the spermathecal muscle in Chelymorpha alternans Boheman (Coleoptera: Chrysomelidae: Cassidinae). Physiol. Entomol. 19:198-202.
113. Rowe, L., G. Arnqvist, A. Sih, and J. J. Krupa. 1994. Sexual conflict and the evolutionary ecology of mating patterns: water striders as a model system. Trends Ecol. Evol. 9:289-293.
114. Russell, J. S., B. L. Ward, and W. B. Heed. 1977. Sperm storage and hybridization in D. nannoptera and related species. Dros. Info. Serv. 52:70.
115. Russo, C. A. M., N. Takezaki, and M. Nei. 1995. Molecular phylogeny and divergence times of Drosophilid species. Mol. Biol. Evol. 12:391-404.
116. Shugart, G. W. 1988. Uterovaginal sperm-storage glands in sixteen species with comments on morphological differences. Auk 105: 379-385.
117. Siva-Jothy, M. T. 1987. The structure and function of the female sperm-storage organs in libellulid dragonflies. J. Insect Physiol. 33:559-567.
118. Siva-Jothy, M. T., and R. E. Hooper. 1995. The disposition and genetic diversity of stored sperm in females of the damselfly Calopteryx splendens xanthostoma (Charpentier). Proc. R. Soc. Lond. B Biol. Sci. 259 313-318.
119. Smuts, B. B., and R. W. Smuts. 1993. Male aggression and sexual coercion of females in nonhuman primates and other mammals: evidence and theoretical implications. Adv. Study Behav. 22:1-63.
120. Snodgrass, R. E. 1935. The principles of insect morphology. McGraw Hill, New York.
121. Snook, R. R. 1995. The evolution of sperm polymorphism in the Drosophila obscura group, Ph.D. diss. Arizona State University, Tempe, AZ.
122. Snook, R. R., T. A. Markow, and T. L. Karr. 1994. Functional nonequivalence of sperm in Drosophila psuedoobscura. Proc. Natl. Acad. Sci. USA 91:11222-11226.
123. Spicer, G. 1988. Molecular evolution among some Drosophila species groups as indicated by two-dimensional electrophoresis. J. Mol. Evol. 27:250-260.
124. _. 1991. Molecular evolution and phylogeny of the Drosophila virilis species group as inferred by two-dimensional electrophoresis. J. Mol. Evol. 1991:379-394.
125. _. 1992. Reevaluation of the phylogeny of the Drosophila virilis species group (Diptera: Drosophilidae). Ann. Entomol. Soc. Am. 85:11-25.
126. Spicer, G. S., and J. Jaenike. 1996. Phylogenetic analysis of breeding site use and a-amanitin tolerance within the Drosophila quinaria species group. Evolution 50:2328-2337.
127. Spicer, G. S., and S. Pitnick. 1996. Molecular systematics of the Drosophila hydei subgroup as inferred from mitochondrial DNA sequences. J. Mol. Evol. 43:281-286.
128. Stockley, P. 1997. Sexual conflict resulting from adaptations to sperm competition. Trends Ecol. Evol. 12:154-159.
129. Stone, W. S., and J. T. Patterson. 1954. III. Fertilizations in multiple matings between species of the virilis group. Univ. Texas Publ. 5422:38-45.
130. Sturtevant, A. H. 1925. The seminal receptacles and accessory glands of the Diptera, with special reference to the Acalypterae. J. New York Entomol. Soc. 33:195-215.
131. _. 1926. The seminal receptacles and accessory glands of the Diptera, with special reference to the Acalypterae. J. New York Entomol. Soc. 34:1-22.
132. Sullivan, D. T., P. W. Atkinson, and W. T. Starmer. 1990. Molecular evolution of the alcohol dehydrogenase genes in the genus Drosophila. Evol. Biol. 24:107-147.
133. Swofford, D. L., and W. P. Maddison. 1987. Reconstructing ancestral characters state under wagner parsimony. Math. Biosci. 87:119-199.
134. Thomas, R. H., and D. W. Zeh. 1984. Sperm transfer and utilization strategies in arachnids: ecological and morphological constraints. Pp. 179-221 in R. L. Smith, ed. Sperm competition and the evolution of animal mating systems. Academic Press, New York.
135. Throckmorton, L. H. 1962. The problem of phylogeny in the genus Drosophila. Univ. Texas Publ. 6205:207-343.
136. _. 1975. The phylogeny, ecology and geography of Drosophila. Pp. 421-469 in R. C. King, ed. Handbook of genetics. Vol. 3. Plenum Press, New York.
137. Villavaso, E. J. 1975. The role of the spermathecal gland of the boll weevil, Anthonomus grandis. J. Insect Physiol. 21:1457-1462.
138. Wade, M. J., H. Patterson, N. W. Chang, and N. A. Johnson. 1994. Postcopulatory, prezygotic isolation in flour beetles. Heredity 72:163-167.
139. Walker, W. F. 1980. Sperm utilization strategies in nonsocial insects. Am. Nat. 115:780-799.
140. Ward, P. I. 1993. Females influence sperm storage and use in the yellow dung fly Scathophaga stercoraria (L.). Behav. Ecol. Sociobiol. 32:313-319.
141. _. 1998. A possible explanation for cryptic female choice in the yellow dung fly. Scathophaga stercoraria (L.). Ethol. 104: 97-110.
142. Wasserman, M. 1962. Cytological studies of the repleta group of the genus Drosophila: V. The mulleri subgroup. Univ. Texas Publ. 6205:85-117.
143. _. 1992. Cytological evolution of the Drosophila repleta species group. Pp. 455-552 in C. B. Krimbas and J. R. Powell, eds. Drosophila inversion polymorphism. CRC Press, Boca Raton, FL.
144. Wheeler, M. R. 1947. IV. The insemination reaction in intraspecific matings of Drosophila. Univ. Texas Publ. 4720:78-115.
145. _. 1949. Taxonomic studies on the Drophilidae. Univ. Texas Publ. 4920:157-195.
146. _. 1954. Taxonomic studies on American Drosophila. Univ. Texas Publ. 4720:47-64.
147. Wigglesworth, V. B. 1965. The principles of insect physiology. Methuen, London.