Genetics, Vol 139, 189-201, Copyright © 1995


INVESTIGATIONS

Variation in Sperm Displacement and Its Association with Accessory Gland Protein Loci in Drosophila melanogaster

A. G. Clark, M. Aguade, T. Prout, L. G. Harshman and C. H. Langley
Department of Biology, Pennsylvania State University, University Park, Pennsylvania 16802

Genes that influence mating and/or fertilization success may be targets for strong natural selection. If females remate frequently relative to the duration of sperm storage and rate of sperm use, sperm displacement may be an important component of male reproductive success. Although it has long been known that mutant laboratory stocks of Drosophila differ in sperm displacement, the magnitude of the naturally occurring genetic variation in this character has not been systematically quantified. Here we report the results of a screen for variation in sperm displacement among 152 lines of Drosophilia melanogaster that were made homozygous for second and/or third chromosomes recovered from natural populations. Sperm displacement was assayed by scoring the progeny of cn;bw females that had been mated sequentially to cn;bw and tested males in either order. Highly significant differences were seen in both the ability to displace sperm that is resident in the female's reproductive tract and in the ability to resist displacement by subsequent sperm. Most lines exhibited nearly complete displacement, having nearly all progeny sired by the second male, but several lines had as few as half the progeny fathered by the second male. Lines that were identified in the screen for naturally occurring variation in sperm displacement were also characterized for single-strand conformation polymorphisms (SSCP) at seven accessory gland protein (Acp) genes, Glucose dehydrogenase (Gld), and Esterase-6 (Est-6). Acp genes encode proteins that are in some cases known to be transmitted to the female in the seminal fluid and are likely candidates for genes that might mediate the phenomenon of sperm displacement. Significant associations were found between particular Acp alleles at four different loci (Acp26Aa/Ab, Acp29B, Acp36DE and Acp53E) and the ability of males to resist displacement by subsequent sperm. There was no correlation between the ability to displace resident sperm and the ability to resist being displaced by subsequent sperm. This lack of correlation, and the association of Acp alleles with resisting subsequent sperm only, suggests that different mechanisms mediate the two components of sperm displacement.


This article has been cited by other articles:


Home page
GeneticsHome page
L. A. McGraw, A. G. Clark, and M. F. Wolfner
Post-mating Gene Expression Profiles of Female Drosophila melanogaster in Response to Time and to Four Male Accessory Gland Proteins
Genetics, July 1, 2008; 179(3): 1395 - 1408.
[Abstract] [Full Text] [PDF]


Home page
Proc. Natl. Acad. Sci. USAHome page
H. Dai, Y. Chen, S. Chen, Q. Mao, D. Kennedy, P. Landback, A. Eyre-Walker, W. Du, and M. Long
The evolution of courtship behaviors through the origination of a new gene in Drosophila
PNAS, May 27, 2008; 105(21): 7478 - 7483.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
J. L. Mueller, J. R. Linklater, K. Ravi Ram, T. Chapman, and M. F. Wolfner
Targeted Gene Deletion and Phenotypic Analysis of the Drosophila melanogaster Seminal Fluid Protease Inhibitor Acp62F
Genetics, March 1, 2008; 178(3): 1605 - 1614.
[Abstract] [Full Text] [PDF]


Home page
Mol Biol EvolHome page
A. Wong, M. C. Turchin, M. F. Wolfner, and C. F. Aquadro
Evidence for Positive Selection on Drosophila melanogaster Seminal Fluid Protease Homologs
Mol. Biol. Evol., March 1, 2008; 25(3): 497 - 506.
[Abstract] [Full Text] [PDF]


Home page
Proc. Natl. Acad. Sci. USAHome page
T. Dottorini, L. Nicolaides, H. Ranson, D. W. Rogers, A. Crisanti, and F. Catteruccia
A genome-wide analysis in Anopheles gambiae mosquitoes reveals 46 male accessory gland genes, possible modulators of female behavior
PNAS, October 9, 2007; 104(41): 16215 - 16220.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
B. J. Wagstaff and D. J. Begun
Adaptive Evolution of Recently Duplicated Accessory Gland Protein Genes in Desert Drosophila
Genetics, October 1, 2007; 177(2): 1023 - 1030.
[Abstract] [Full Text] [PDF]


Home page
Integr. Comp. Biol.Home page
K. Ravi Ram and M. F. Wolfner
Seminal influences: Drosophila Acps and the molecular interplay between males and females during reproduction
Integr. Comp. Biol., September 1, 2007; 47(3): 427 - 445.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
A. C. Fiumera, B. L. Dumont, and A. G. Clark
Associations Between Sperm Competition and Natural Variation in Male Reproductive Genes on the Third Chromosome of Drosophila melanogaster
Genetics, June 1, 2007; 176(2): 1245 - 1260.
[Abstract] [Full Text] [PDF]


Home page
J HeredHome page
C. W. LaMunyon, O. Bouban, and A. D. Cutter
Postcopulatory Sexual Selection Reduces Genetic Diversity in Experimental Populations of Caenorhabditis elegans
J. Hered., January 1, 2007; 98(1): 67 - 72.
[Abstract] [Full Text] [PDF]


Home page
Proc. Natl. Acad. Sci. USAHome page
A. Wong, S. N. Albright, and M. F. Wolfner
Evidence for structural constraint on ovulin, a rapidly evolving Drosophila melanogaster seminal protein
PNAS, December 5, 2006; 103(49): 18644 - 18649.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
M. Proschel, Z. Zhang, and J. Parsch
Widespread Adaptive Evolution of Drosophila Genes With Sex-Biased Expression
Genetics, October 1, 2006; 174(2): 893 - 900.
[Abstract] [Full Text] [PDF]


Home page
Behav EcolHome page
E. J. Wenninger and A. L. Averill
Influence of body and genital morphology on relative male fertilization success in oriental beetle
Behav. Ecol., July 1, 2006; 17(4): 656 - 663.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
J. L. Mueller, K. R. Ram, L. A. McGraw, M. C. Bloch Qazi, E. D. Siggia, A. G. Clark, C. F. Aquadro, and M. F. Wolfner
Cross-Species Comparison of Drosophila Male Accessory Gland Protein Genes
Genetics, September 1, 2005; 171(1): 131 - 143.
[Abstract] [Full Text] [PDF]


Home page
Proc. Natl. Acad. Sci. USAHome page
T. F. C. Mackay, S. L. Heinsohn, R. F. Lyman, A. J. Moehring, T. J. Morgan, and S. M. Rollmann
Genetics and genomics of Drosophila mating behavior
PNAS, May 3, 2005; 102(suppl_1): 6622 - 6629.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
A. C. Fiumera, B. L. Dumont, and A. G. Clark
Sperm Competitive Ability in Drosophila melanogaster Associated With Variation in Male Reproductive Proteins
Genetics, January 1, 2005; 169(1): 243 - 257.
[Abstract] [Full Text] [PDF]


Home page
Proc. Natl. Acad. Sci. USAHome page
J. L. Mueller, D. R. Ripoll, C. F. Aquadro, and M. F. Wolfner
Comparative structural modeling and inference of conserved protein classes in Drosophila seminal fluid
PNAS, September 14, 2004; 101(37): 13542 - 13547.
[Abstract] [Full Text] [PDF]


Home page
Mol Biol EvolHome page
S. V. Nuzhdin, M. L. Wayne, K. L. Harmon, and L. M. McIntyre
Common Pattern of Evolution of Gene Expression Level and Protein Sequence in Drosophila
Mol. Biol. Evol., July 1, 2004; 21(7): 1308 - 1317.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
A. D. Kern, C. D. Jones, and D. J. Begun
Molecular Population Genetics of Male Accessory Gland Proteins in the Drosophila simulans Complex
Genetics, June 1, 2004; 167(2): 725 - 735.
[Abstract] [Full Text] [PDF]


Home page
J HeredHome page
L. S. Stevison, B. A. Counterman, and M. A. F. Noor
Molecular Evolution of X-linked Accessory Gland Proteins in Drosophila pseudoobscura
J. Hered., March 1, 2004; 95(2): 114 - 118.
[Abstract] [Full Text] [PDF]


Home page
Mol Biol EvolHome page
M. H. Kohn, S. Fang, and C.-I Wu
Inference of Positive and Negative Selection on the 5' Regulatory Regions of Drosophila Genes
Mol. Biol. Evol., February 1, 2004; 21(2): 374 - 383.
[Abstract] [Full Text] [PDF]


Home page
J. Exp. Biol.Home page
M. C. B. Qazi and M. F. Wolfner
An early role for the Drosophila melanogaster male seminal protein Acp36DE in female sperm storage
J. Exp. Biol., October 1, 2003; 206(19): 3521 - 3528.
[Abstract] [Full Text] [PDF]


Home page
Proc. Natl. Acad. Sci. USAHome page
W. J. Swanson
Sex peptide and the sperm effect in Drosophila melanogaster
PNAS, August 19, 2003; 100(17): 9643 - 9644.
[Full Text] [PDF]


Home page
GeneticsHome page
B. Jones and A. G. Clark
Bayesian Sperm Competition Estimates
Genetics, March 1, 2003; 163(3): 1193 - 1199.
[Abstract] [Full Text] [PDF]


Home page
Mol Biol EvolHome page
D. G. Torgerson, R. J. Kulathinal, and R. S. Singh
Mammalian Sperm Proteins Are Rapidly Evolving: Evidence of Positive Selection in Functionally Diverse Genes
Mol. Biol. Evol., November 1, 2002; 19(11): 1973 - 1980.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
O. Lung, U. Tram, C. M. Finnerty, M. A. Eipper-Mains, J. M. Kalb, and M. F. Wolfner
The Drosophila melanogaster Seminal Fluid Protein Acp62F Is a Protease Inhibitor That Is Toxic Upon Ectopic Expression
Genetics, January 1, 2002; 160(1): 211 - 224.
[Abstract] [Full Text] [PDF]


Home page
Proc. Natl. Acad. Sci. USAHome page
L. L. Knowles and T. A. Markow
Sexually antagonistic coevolution of a postmating-prezygotic reproductive character in desert Drosophila
PNAS, July 5, 2001; (2001) 151123998.
[Abstract] [Full Text] [PDF]


Home page
Proc. Natl. Acad. Sci. USAHome page
W. J. Swanson, A. G. Clark, H. M. Waldrip-Dail, M. F. Wolfner, and C. F. Aquadro
Evolutionary EST analysis identifies rapidly evolving male reproductive proteins in Drosophila
PNAS, June 7, 2001; (2001) 131568198.
[Abstract] [Full Text] [PDF]


Home page
Proc. Natl. Acad. Sci. USAHome page
A. D. Stutt and M. T. Siva-Jothy
Traumatic insemination and sexual conflict in the bed bug Cimexlectularius
PNAS, April 25, 2001; (2001) 101440698.
[Abstract] [Full Text]


Home page
GeneticsHome page
D. J. Begun, P. Whitley, B. L. Todd, H. M. Waldrip-Dail, and A. G. Clark
Molecular Population Genetics of Male Accessory Gland Proteins in Drosophila
Genetics, December 1, 2000; 156(4): 1879 - 1888.
[Abstract] [Full Text]


Home page
Proc. Natl. Acad. Sci. USAHome page
W. R. Rice
Dangerous liaisons
PNAS, November 21, 2000; 97(24): 12953 - 12955.
[Full Text] [PDF]


Home page
Proc. Natl. Acad. Sci. USAHome page
A. Civetta and A. G. Clark
Correlated effects of sperm competition and postmating female mortality
PNAS, November 8, 2000; (2000) 230305397.
[Abstract] [Full Text]


Home page
Proc. Natl. Acad. Sci. USAHome page
A. B. Carvalho, B. P. Lazzaro, and A. G. Clark
Y chromosomal fertility factors kl-2 and kl-3 of Drosophila melanogaster encode dynein heavy chain polypeptides
PNAS, November 2, 2000; (2000) 230438397.
[Abstract] [Full Text]


Home page
GeneticsHome page
C. Green, E. Levashina, C. McKimmie, T. Dafforn, J.-M. Reichhart, and D. Gubb
The necrotic Gene in Drosophila Corresponds to One of a Cluster of Three Serpin Transcripts Mapping at 43A1.2
Genetics, November 1, 2000; 156(3): 1117 - 1127.
[Abstract] [Full Text]


Home page
GeneticsHome page
R. R. Snook, S. Y. Cleland, M. F. Wolfner, and T. L. Karr
Offsetting Effects of Wolbachia Infection and Heat Shock on Sperm Production in Drosophila simulans: Analyses of Fecundity, Fertility and Accessory Gland Proteins
Genetics, May 1, 2000; 155(1): 167 - 178.
[Abstract] [Full Text]


Home page
Proc. Natl. Acad. Sci. USAHome page
S. R. Palumbi
All males are not created equal: Fertility differences depend on gamete recognition polymorphisms in sea urchins
PNAS, October 26, 1999; 96(22): 12632 - 12637.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
U. Tram and M. F. Wolfner
Male Seminal Fluid Proteins Are Essential for Sperm Storage in Drosophila melanogaster
Genetics, October 1, 1999; 153(2): 837 - 844.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
D. M. Neubaum and M. F. Wolfner
Mated Drosophila melanogaster Females Require a Seminal Fluid Protein, Acp36DE, to Store Sperm Efficiently
Genetics, October 1, 1999; 153(2): 845 - 857.
[Abstract] [Full Text] [PDF]


Home page
Behav EcolHome page
G. Arnqvist and I. Danielsson
Postmating sexual selection: the effects of male body size and recovery period on paternity and egg production rate in a water strider
Behav. Ecol., July 1, 1999; 10(4): 358 - 365.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
M. Aguadé
Positive Selection Drives the Evolution of the Acp29AB Accessory Gland Protein in Drosophila
Genetics, June 1, 1999; 152(2): 543 - 551.
[Abstract] [Full Text]


Home page
Proc. Natl. Acad. Sci. USAHome page
B. Holland and W. R. Rice
Experimental removal of sexual selection reverses intersexual antagonistic coevolution and removes a reproductive load
PNAS, April 27, 1999; 96(9): 5083 - 5088.
[Abstract] [Full Text] [PDF]


Home page
ScienceHome page
A. G. Clark, D. J. Begun, and T. Prout
Female × Male Interactions in Drosophila Sperm Competition
Science, January 8, 1999; 283(5399): 217 - 220.
[Abstract] [Full Text]


Home page
GeneticsHome page
M. Aguadé
Different Forces Drive the Evolution of the Acp26Aa and Acp26Ab Accessory Gland Genes in the Drosophila melanogaster Species Complex
Genetics, November 1, 1998; 150(3): 1079 - 1089.
[Abstract] [Full Text]


Home page
GeneticsHome page
A. G. Clark and D. J. Begun
Female Genotypes Affect Sperm Displacement in Drosophila
Genetics, July 1, 1998; 149(3): 1487 - 1493.
[Abstract] [Full Text] [PDF]


Home page
Proc. Natl. Acad. Sci. USAHome page
T. A. Markow
Assortative fertilization in Drosophila
PNAS, July 22, 1997; 94(15): 7756 - 7760.
[Abstract] [Full Text] [PDF]


Home page
Proc. Natl. Acad. Sci. USAHome page
A. D. Stutt and M. T. Siva-Jothy
Traumatic insemination and sexual conflict in the bed bug Cimexlectularius
PNAS, May 8, 2001; 98(10): 5683 - 5687.
[Abstract] [Full Text] [PDF]


Home page
Proc. Natl. Acad. Sci. USAHome page
W. J. Swanson, A. G. Clark, H. M. Waldrip-Dail, M. F. Wolfner, and C. F. Aquadro
Evolutionary EST analysis identifies rapidly evolving male reproductive proteins in Drosophila
PNAS, June 19, 2001; 98(13): 7375 - 7379.
[Abstract] [Full Text] [PDF]


Home page
Proc. Natl. Acad. Sci. USAHome page
L. L. Knowles and T. A. Markow
Sexually antagonistic coevolution of a postmating-prezygotic reproductive character in desert Drosophila
PNAS, July 17, 2001; 98(15): 8692 - 8696.
[Abstract] [Full Text] [PDF]


Home page
Proc. Natl. Acad. Sci. USAHome page
A. Civetta and A. G. Clark
Correlated effects of sperm competition and postmating female mortality
PNAS, November 21, 2000; 97(24): 13162 - 13165.
[Abstract] [Full Text] [PDF]


Home page
Proc. Natl. Acad. Sci. USAHome page
A. B. Carvalho, B. P. Lazzaro, and A. G. Clark
Y chromosomal fertility factors kl-2 and kl-3 of Drosophila melanogaster encode dynein heavy chain polypeptides
PNAS, November 21, 2000; 97(24): 13239 - 13244.
[Abstract] [Full Text] [PDF]