Phylogenetic examination of female incorporation of ejaculate in Drosophila

Evolution

Volumn 51, Issue 3, 1997, Pages 833-845

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

^a SYRACUSE UNIVERSITY   (United States)

^b SAN FRANCISCO STATE UNIVERSITY   (United States)

^c ARIZONA STATE UNIVERSITY   (United States)

Author keywords

Accessory gland secretions; Comparative analysis; Ejaculate; Ejaculatory donation; Paternal investment; Phylogenetic constraint

Indexed keywords

EJACULATE; PHYLOGENY; PROTEIN;

DIPTERA; DROSOPHILA; DROSOPHILIDAE; INVERTEBRATA;

EID: 0030842126     PISSN: 00143820     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1558-5646.1997.tb03665.x     Document Type: Article

References (105)

1. ALEXANDER, R. D., AND G. BORGIA. 1979. On the origin and basis of the male-female phenomenon. Pp. 417-440 in M. S. Blum and N. A. Blum, eds. Sexual selection and reproductive competition in insects. Academic Press, London.
2. ALONSO-PIMENTEL, H., L. P. TOLBERT, AND W. B. HEED. 1994. Ultrastructural examination of the insemination reaction in Drosophila. Cell Tissue Res. 275:467-479.
3. ASHBURNER, M. 1989. Drosophila: a laboratory handbook. Cold Spring Harbor Laboratory Press, New York.
4. BATEMAN, A. J. 1948. Intrasexual selection in Drosophila. Heredity 2:349-368.
5. 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.
6. _. 1984. Molecular evolution in Drosophila and the higher Diptera. II. A time scale for fly evolution. J. Mol. Evol. 21:1-13.
7. 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.
8. BOGGS, C. L., AND L. E. GILBERT. 1979. Male contribution to egg production in butterflies: evidence for transfer of nutrients at mating. Science 206:83-84.
9. BOGGS, C. L., AND W. B. WATT. 1981. Population structure of pierid butterflies. IV. Genetics and physiological investment in offspring by male Colias. Oecologia 50:320-324.
10. BOUCHER, L., AND J. HUIGNARD. 1987. Transfer of male secretions from the spermatophore to the female insect in Caryedon serratus (OL.): analysis of the possible trophic role of these secretions. J. Insect Physiol. 33:949-957.
11. BOWEN, B. J., C. G. CODD, AND D. T. GWYNNE. 1984. The katydid spermatophore (Orthoptera: Tettigoniidae): male nutritional investment and its fate in the mated female. Aust. J. Zool. 32:23-31.
12. BOWNES, M., AND L. PARTRIDGE. 1987. Transfer of molecules from ejaculate to females in Drosophila melanogaster and Drosophila pseudoobscura. J. Insect Physiol. 33:941-947.
13. BRESSAC, C., A. FLEURY, AND D. LACHAISE. 1994. Another way of being anisogamous in Drosophila subgenus species: giant sperm, one-to-one gamete ratio, and high zygote provisioning. Proc. Nat. Acad. Sci. USA 91:10399-10402.
14. BUTLIN, R. K., C. W. WOODHATCH, AND G. M. HEWITT. 1987. Male spermatophore investment increases female fecundity in a grasshopper. Evolution 41:221-225.
15. CACCONE, A., J. M. GLEASON, AND J. R. POWELL. 1992. Complementary DNA-DNA hybridization in Drosophila. J. Mol. Evol. 34:130-140.
16. CHEESEMAN, M. T., AND C. GILLOTT. 1989. Long hyaline gland discharge and multiple spermatophore formation by the male grasshopper, Melanoplus sanguinipes. Physiol. Entomol. 14:257-264.
17. CHEN, P. S. 1984. The functional morphology and biochemistry of insect male accessory glands and their secretions. Annu. Rev. Entomol. 29:233-255.
18. CHEN, P. S., E. STUMM-ZOLLINGER, AND M. CALDELARI. 1985. Protein metabolism of Drosophila male accessory glands. II. Insect Biochem. 15:385-390.
19. DESALLE, R. 1992. The phylogenetic relationships of flies in the family Drosophilidae deduced from mtDNA sequences. Mol. Phylogenet. Evol. 1:31-40.
20. DODSON, G. N., G. K. MORRIS, AND D. T. GWYNNE. 1983. Mating behavior of the primitive Orthopteran genus Cyphoderris (Haglidae). Pp. 305-318 in D. T. Gwynne and G. K. Morris, eds. Orthopteran mating systems: sexual selection in a diverse group of insects. Westview Press, Boulder, CO.
21. EBERHARD, W. G. 1996. Female control: sexual selection by cryptic female choice. Princeton Univ. Press, Princeton, NJ.
22. ELGAR, M. A. 1992. Sexual cannibalism in spiders and other invertebrates. Pp. 129-156 in M. A. Elgar and B. J. Crespi, eds. Cannibalism: ecology and evolution among diverse taxa. Oxford Univ. Press, Oxford.
23. EMLEN, S. T., AND L. W. ORING. 1977. Ecology, sexual selection and the evolution of mating systems. Science 197:215-223.
24. FELSENSTEIN, J. 1985. Phylogenies and the comparative method. Am. Nat. 125:1-15.
25. FOGLEMAN, J. C., AND W.B. HEED. 1989. Columnar cacti and desert Drosophila: the chemistry of host plant specificity. Pp. 1-24 in J. Schmidt, ed. Special biotic relationships in the arid southwest. Univ. of New Mexico Press, Albuquerque.
26. GARLAND, T., JR., P. H. HARVEY, AND A. R. IVES. 1992. Procedures for the analysis of comparative data using phylogenetically independent contrasts. Syst. Biol. 41:18-32.
27. GARLAND, T., JR., A. W. DICKERMAN, C. M. JANIS, AND J. A. JONES. 1993. Phylogenetic analysis of covariance by computer simulation. Syst. Biol. 42:265-292.
28. GILLOTT, C. 1988. Arthropoda - Insecta. Pp. 319-471 in K. G. Adiyodi and R. G. Adiyodi, eds. Reproductive biology of invertebrates. Wiley, New York.
29. GREENFIELD, M. D. 1982. The question of paternal investment in Lepidoptera: male-contributed proteins in Plodia interpunctella. Int. J. Invertebr. Reprod. 5:323-330.
30. GRIMALDI, D. A. 1992. A phylogenetic, revised classification of genera in the Drosophilidae (Diptera). Bull. Am. Mus. Nat. Hist. 197:1-139.
31. GWYNNE, D. T. 1984. Courtship feeding increases female reproductive success in bushcrickets. Nature 307:361-363.
32. _. 1986a. Reply to: Stepfathers in insects and their psuedo-parental investment. Ethology 71:74-77.
33. _. 1986b. Courtship feeding in katydids (Orthoptera: Tettigoniidae): investment in offspring or in obtaining fertilizations? Am. Nat. 128:342-352.
34. _. 1988. Courtship feeding and the fitness of female katydids (Orthoptera: Tettigoniidae). Evolution 42:545-555.
35. GWYNNE, D. T., B. J. BOWEN, AND C. G. GODD. 1984. The function of the katydid spermatophore and its role in fecundity and insemination (Orthoptera: Tettigoniidae). Aust. J. Zool. 32:15-22.
36. HARVEY, P. H., AND M. D. PAGEL. 1991. The comparative method in evolutionary biology. Oxford Univ. Press, Oxford.
37. HEED, W. B. 1982. The origin of Drosophila in the Sonoran Desert. Pp. 65-80 in J. S. F. Barker and W. T. Starmer, eds. Ecological genetics and evolution. The cactus-yeast-Drosophila model system. Academic Press, Sydney, New South Wales, Australia.
38. HEED, W. B., AND D. A. GRIMALDI. 1991. Revision of the morphocryptic, Caribbean mayaguana species subcluster in the Drosophila repleta group (Diptera: Drosophilidae). Am. Mus. Novit. 2999:1-15.
39. 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.
40. JOLY, D., C. BRESSAC, J. DEVAUX, AND D. LACHAISE. 1991. Sperm length diversity in Drosophilidae. Drosophila Inf. Serv. 70:104-108.
41. JONES, K. N., F. J. ODENDAAL, AND P. R. EHRLICH. 1986. Evidence against the spermatophore as paternal investment in checkerspot butterflies (Euphydryas: Nymphalidae). Am. Midl. Nat. 116:1-6.
42. KARR, T. L. 1991. Intracellular sperm/egg interactions in Drosophila: a three-dimensional structural analysis of a paternal product in the developing egg. Mech. Dev. 34:101-112.
43. KARR, T. L., AND S. PITNICK. 1996. The ins and outs of fertilization. Nature 379:405-406.
44. 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.
45. LEE, H. T.-Y. 1950. A preliminary histological study of the insemination reaction in Drosophila gibberosa. Biol. Bull. 98:25-33.
46. LEOPOLD, R. A. 1976. The role of male accessory glands in insect reproduction. Annu. Rev. Entomol. 21:199-221.
47. Low, B. S. 1978. Environmental uncertainty and the parental strategies of marsupials and placentals. Am. Nat. 112:197-213.
48. MADDISON, W. P., AND D. R. MADDISON. 1992. MacClade: analysis of phylogeny and character evolution. Vers. 3.05. Sinauer, Sunderland, MA.
49. MARKOW, T. A. 1988. Drosophila males provide a material contribution to offspring sired by other males. Funct. Ecol. 2:77-79.
50. MARKOW, T. A., AND P. F. ANKNEY. 1984. Drosophila males contribute to oogenesis in a multiple mating species. Science 224: 302-303.
51. _. 1988. Insemination reaction in Drosophila: found in species whose males contribute material to oocytes before fertilization. Evolution 42:1097-1101.
52. MARKOW, T. A., P. D. GALLAGHER, AND R. A. KREBS. 1990. Ejaculate-derived nutritional contribution and female reproductive success in Drosophila mojavensis (Patterson and Crow). Funct. Ecol. 4:67-73.
53. MARSHALL, L. D. 1982. Male nutrient investment in the Lepidoptera: what nutrients should males invest? Am. Nat. 120:273-279.
54. MARSHALL, L. D., AND J. N. MCNEIL. 1989. Spermatophore mass as an estimate of male nutrient investment: a closer look in Pseudaletia unipuncta (Haworth) (Lepidoptera: Noctuidae). Funct. Ecol. 3:605-612.
55. MARTINS, E. P., AND T. GARLAND JR. 1991. Phylogenetic analyses of the correlated evolution of continuous characters: a simulation study. Evolution 45:534-557.
56. PARKER, G. A. 1970. Sperm competition and its evolutionary consequences in the insects. Biol. Rev. 45:525-567.
57. PARKER, G. A., AND L. W. SIMMONS. 1989. Nuptial feeding in insects: theoretical models of male and female interests. Ethology 82:3-26.
58. PATTERSON, J. T. 1946. A new type of isolating mechanism in Drosophila. Proc. Nat. Acad. Sci. USA 32:202-208.
59. _. 1947. The insemination reaction and its bearing on the problem of speciation in the mulleri subgroup. Univ. Texas Publ. 4720:41-77.
60. PATTERSON, J. T., AND W. S. STONE. 1952. Evolution in the genus Drosophila. Macmillan, New York.
61. PELANDAKIS, M., AND M. SOLIGNAC. 1993. Molecular phylogeny of Drosophila based on ribosomal RNA sequences. J. Mol. Evol. 37:525-543.
62. PITNICK, S. 1993. Operational sex ratios and sperm limitation in populations of Drosophila pachea. Behav. Ecol. Sociobiol. 33: 383-391.
63. _. 1996. Investment in testes and the cost of making long sperm in Drosophila. Am. Nat. 148:57-80.
64. PITNICK, S., AND T. A. MARKOW. 1994a. Large-male advantages associated with costs of sperm production in Drosophila hydei, a species with giant sperm. Proc. Nat. Acad. Sci. USA 91:9277-9281.
65. _. 1994b. 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.
66. 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.
67. PITNICK, S., G. S. SPICER, AND T. A. MARKOW. 1995a. How long is a giant sperm? Nature 375:109.
68. PITNICK, S., T. A. MARKOW, AND G. S. SPICER. 1995b. Delayed male maturity is a cost of producing large sperm in Drosophila. Proc. Nat. Acad. Sci. USA 92:10614-10618.
69. POLAK, M. 1993. Parasites increase fluctuating asymmetry of male Drosophila nigrospiracula: implications for sexual selection, Genetica 89:255-265.
70. POWELL, J. R., AND R. DESALLE. 1995. Drosophila molecular phylogenies and their uses. Evol. Biol. 28:87-138.
71. QUINN, J. S., AND S. K. SAKALUK. 1986. Prezygotic male reproductive effort in insects: why do males provide more than sperm? Fla. Entomol. 69:84-94.
72. REINHOLD, K., AND K.-G. HELLER. 1993. The ultimate function of nuptial feeding in the bushcricket Poecilimon veluchianus (Orthoptera: Tettigoniidae: Phaneropterinae). Behav. Ecol. Sociobiol. 32:55-60.
73. ROFF, D. A. 1992. The evolution of life histories: theories and analysis. Chapman and Hall, New York.
74. RUTOWSKI, R. L., G. W. GILCHRIST, AND B. TERKANIAN. 1987. Female butterflies mated with recently mated males show reduced reproductive output. Behav. Ecol. Sociobiol. 20:319-322.
75. SAKALUK, S. K. 1986. Is courtship feeding by male insects parental investment? Ethology 73:161-166.
76. SAKALUK, S. K., AND W. H. CADE. 1980. Female mating frequency and progeny production in singly and doubly mated house and field crickets. Can. J. Zool. 58:404-411.
77. SIMMONS, L. W. 1988. The contribution of multiple mating and spermatophore consumption to the lifetime reproductive success of female field crickets (Gryllus bimaculatus De Geer). Ecol., Entomol. 13:57-69.
78. SIMMONS, L. W., AND D. T. GWYNNE. 1993. Reproductive investment in bushcrickets: the allocation of male and female nutrients to offspring. Proc. R. Soc. Lond. B Biol. Sci. 252:1-5.
79. SIMMONS, L. W., AND G. A. PARKER. 1989. Nuptial feeding in insects: mating effort versus paternal investment. Ethology 81: 332-343.
80. SPICER, G. S. 1988. Molecular evolution among some Drosophila species groups as indicated by two-dimensional electrophoresis. J. Mol. Evol. 27:250-260.
81. _. 1991. Molecular evolution and phylogeny of the Dro- sophila virilis species group as inferred by two-dimensional electrophoresis. J. Mol. Evol. 33:379-394.
82. _. 1992. Reevaluation of the phylogeny of the Drosophila virilis species group. Ann. Entomol. Soc. Am. 85:11-25.
83. SPICER, G. S., AND J. JAENIKE. 1996. Phylogenetic analysis of breeding site use and α-amanitin tolerance within the Drosophila quinaria species group. Evolution 50:2328-2337.
84. SPICER, G. S., AND S. PITNICK. 1996. Molecular systematics of the Drosophila hydei subgroup inferred from mitochondrial DNA sequences. J. Mol. Evol. 43:281-286.
85. STEARNS, S. C. 1992. The evolution of life histories. Oxford Univ. Press, Oxford.
86. STEELE, R. H. 1986. Courtship feeding in Drosophila subobscura. I. The nutritional significance of courtship feeding. Anim. Behav. 34:1087-1098.
87. STUMM-ZOLLINGER, E., AND P. S. CHEN. 1988. Gene expression in male accessory glands of interspecific hybrids of Drosophila. J. Insect Physiol. 34:59-74.
88. 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.
89. SVÄRD, L., AND C. WIKLUND. 1988. Fecundity, egg weight and longevity in relation to multiple matings in females of the monarch butterfly. Behav. Ecol. Sociobiol. 23:39-43.
90. _. 1991. The effect of ejaculate mass on female reproductive output in the european swallowtail butterfly, Papilio machaon (L.) (Lepidoptera: Papilionidae). J. Insect Behav. 4:33-41.
91. SWOFFORD, D. L., AND W. P. MADDISON. 1987. Reconstructing ancestral characters state under wagner parsimony. Math. Biosci. 87:119-229.
92. THOMAS, S., AND R. S. SINGH. 1992. A comprehensive study of genic variation in natural populations of Drosophila melanogaster, VII. Varying rates of genic divergence as revealed by two-dimensional electrophoresis. Mol. Biol. Evol. 9:507-525.
93. THORNHILL, R. 1976. Sexual selection and nuptial feeding behavior in Bittacus apicalis (Insecta: Mecoptera). Am. Nat. 110:529-548.
94. _. 1983. Cryptic female choice and its implications in the scorpionfly Harpobittacus nigriceps. Am. Nat. 122:765-788.
95. THORNHILL, R., AND J. ALCOCK. 1983. The evolution of insect mating systems. Harvard Univ. Press, Cambridge, MA.
96. THROCKMORTON, L. H. 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.
97. _. 1982. The virilis species group. Pp. 227-297 in M. Ashburner and E. Novistky, eds. The genetics and biology of Drosophila. Vol. 3B. Academic Press, London.
98. TRIVERS, R. L. 1972. Parental investment and sexual selection. Pp. 136-179 in B. Campbell, ed. Sexual selection and the descent of man, 1871-1971. Aldine-Atherton, Chicago.
99. WASSERMAN, M. 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.
100. WEDELL, N. 1991. Sperm competition selects for nuptial feeding in a bushcricket. Evolution 45:1975-1978.
101. _. 1993. Spermatophore size in bushcrickets: comparative evidence for nuptial gifts as a sperm protection device. Evolution 47:1203-1212.
102. WEDELL, N., AND A. ARAK. 1989. The wartbiter spermatophore and its effect on female reproductive output (Orthoptera: Tettigoniidae, Decticus verrucivorus). Behav. Ecol. Sociobiol. 24: 117-125.
103. WHEELER, M. R. 1947. The insemination reaction in intraspecific matings of Drosophila. Univ. Texas Publ. 4720:78-115.
104. WICKLER, W. 1985. Stepfathers in insects and their pseudo-parental investment. Z. Tierpsychol. 69:72-78.
105. WICKLER, W. 1986. Mating costs versus parental investment: a reply to Gwynne. Ethology 71:78-79.