Sperm Competitive Ability in Drosophila melanogaster Associated With Variation in Male Reproductive Proteins

Multiple mating by females establishes the opportunity for postcopulatory sexual selection favoring males whose sperm is preferentially employed in fertilizations. Here we use natural variation in a wild population of Drosophila melanogaster to investigate the genetic basis of sperm competitive ability. Approximately 101 chromosome 2 substitution lines were scored for components of sperm competitive ability (P1′, P2′, fecundity, remating rate, and refractoriness), genotyped at 70 polymorphic markers in 10 male reproductive genes, and measured for transcript abundance of those genes. Permutation tests were applied to quantify the statistical significance of associations between genotype and phenotype. Nine significant associations were identified between polymorphisms in the male reproductive genes and sperm competitive ability and 13 were identified between genotype and transcript abundance, but no significant associations were found between transcript abundance and sperm competitive ability. Pleiotropy was evident in two genes: a polymorphism in Acp33A associated with both P1′ and P2′ and a polymorphism in CG17331 associated with both elevated P2′ and reduced refractoriness. The latter case is consistent with antagonistic pleiotropy and may serve as a mechanism maintaining genetic variation.

[1]  M. Wolfner,et al.  Comparative structural modeling and inference of conserved protein classes in Drosophila seminal fluid. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[2]  A. Clark,et al.  Genetic Basis of Natural Variation in D. melanogaster Antibacterial Immunity , 2004, Science.

[3]  D. Milewicz,et al.  Methodology for using a universal primer to label amplified DNA segments for molecular analysis , 2003, Biotechnology Letters.

[4]  C. Gillott Male accessory gland secretions: modulators of female reproductive physiology and behavior. , 2003, Annual review of entomology.

[5]  M. Wolfner,et al.  An early role for the Drosophila melanogaster male seminal protein Acp36DE in female sperm storage , 2003, Journal of Experimental Biology.

[6]  Matthew W. Hahn,et al.  The evolution of transcriptional regulation in eukaryotes. , 2003, Molecular biology and evolution.

[7]  John Parsch,et al.  Rapid evolution of male-biased gene expression in Drosophila , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[8]  E. Kubli,et al.  Sex-peptide is the molecular basis of the sperm effect in Drosophila melanogaster , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[9]  L. Partridge,et al.  The sex peptide of Drosophila melanogaster: Female post-mating responses analyzed by using RNA interference , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[10]  John D. Storey,et al.  Statistical significance for genomewide studies , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[11]  C. Fricke,et al.  The effects of male and female genotype on variance in male fertilization success in the red flour beetle (Tribolium castaneum) , 2003, Behavioral Ecology and Sociobiology.

[12]  G. Churchill,et al.  Variation in gene expression within and among natural populations , 2002, Nature Genetics.

[13]  Stephen G Oliver,et al.  Dynamics of Protein Turnover, a Missing Dimension in Proteomics* , 2002, Molecular & Cellular Proteomics.

[14]  L. Simmons,et al.  EVOLUTION OF EJACULATES: PATTERNS OF PHENOTYPIC AND GENOTYPIC VARIATION AND CONDITION DEPENDENCE IN SPERM COMPETITION TRAITS , 2002, Evolution; international journal of organic evolution.

[15]  S. Pääbo,et al.  Intra- and Interspecific Variation in Primate Gene Expression Patterns , 2002, Science.

[16]  L. Hood,et al.  Complementary Profiling of Gene Expression at the Transcriptome and Proteome Levels in Saccharomyces cerevisiae*S , 2002, Molecular & Cellular Proteomics.

[17]  T. Birkhead,et al.  Evolution of sex: Postcopulatory sexual selection , 2002, Nature Reviews Genetics.

[18]  W. Swanson,et al.  The rapid evolution of reproductive proteins , 2002, Nature Reviews Genetics.

[19]  A. Clark,et al.  Sperm competition and the maintenance of polymorphism , 2002, Heredity.

[20]  M. Wolfner The gifts that keep on giving: physiological functions and evolutionary dynamics of male seminal proteins in Drosophila , 2002, Heredity.

[21]  M. Noll,et al.  Dual role of the Pax gene paired in accessory gland development of Drosophila. , 2002, Development.

[22]  D. Roff Life History, Evolution of , 2001 .

[23]  E S Buckler,et al.  Structure of linkage disequilibrium and phenotypic associations in the maize genome , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[24]  L. Partridge,et al.  The Acp26Aa seminal fluid protein is a modulator of early egg hatchability in Drosophila melanogaster , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[25]  T. Tregenza,et al.  Sexual selection and speciation. , 2001, Trends in ecology & evolution.

[26]  A. Clark,et al.  Evolutionary EST analysis identifies rapidly evolving male reproductive proteins in Drosophila , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[27]  S. Pitnick,et al.  Males' evolutionary responses to experimental removal of sexual selection , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[28]  W. D. Brown,et al.  Evolution of female remating behaviour following experimental removal of sexual selection , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[29]  B. Sinervo,et al.  Polygyny, mate-guarding, and posthumous fertilization as alternative male mating strategies. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[30]  A. Clark,et al.  Molecular population genetics of male accessory gland proteins in Drosophila. , 2000, Genetics.

[31]  M. Purugganan The molecular population genetics of regulatory genes , 2000, Molecular ecology.

[32]  L M McIntyre,et al.  Circumventing multiple testing: A multilocus Monte Carlo approach to testing for association , 2000, Genetic epidemiology.

[33]  L. Partridge,et al.  The role of male accessory gland protein Acp36DE in sperm competition in Drosophila melanogaster , 2000, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[34]  A. Clark,et al.  NONTRANSITIVITY OF SPERM PRECEDENCE IN DROSOPHILA , 2000, Evolution; international journal of organic evolution.

[35]  G. Cha,et al.  Regulation of Mst57Dc Expression in Male Accessory Glands of Dorsophila melanogaster , 2000, Molecules and cells.

[36]  M. Uhlén,et al.  Single-nucleotide polymorphism analysis by pyrosequencing. , 2000, Analytical biochemistry.

[37]  A. Clark,et al.  Chromosomal effects on male and female components of sperm precedence in Drosophila. , 2000, Genetical research.

[38]  M. Gage,et al.  The evolution of sperm length in moths , 2000, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[39]  M. Petrie,et al.  Why do females mate multiply? A review of the genetic benefits , 2000, Biological reviews of the Cambridge Philosophical Society.

[40]  M. Wolfner,et al.  The Drosophila seminal fluid protein Acp26Aa stimulates release of oocytes by the ovary , 2000, Current Biology.

[41]  B. Futcher,et al.  A Sampling of the Yeast Proteome , 1999, Molecular and Cellular Biology.

[42]  M. Wolfner,et al.  Mated Drosophila melanogaster females require a seminal fluid protein, Acp36DE, to store sperm efficiently. , 1999, Genetics.

[43]  M. Aguadé Positive selection drives the evolution of the Acp29AB accessory gland protein in Drosophila. , 1999, Genetics.

[44]  M. Bownes,et al.  Control of oocyte maturation in sexually mature Drosophila females. , 1999, Developmental biology.

[45]  A. Clark,et al.  Female x male interactions in Drosophila sperm competition. , 1999, Science.

[46]  M. Aguadé Different forces drive the evolution of the Acp26Aa and Acp26Ab accessory gland genes in the Drosophila melanogaster species complex. , 1998, Genetics.

[47]  A. Clark,et al.  INFERENCE OF SPERM COMPETITION FROM BROODS OF FIELD‐CAUGHT DROSOPHILA , 1998, Evolution; international journal of organic evolution.

[48]  Chung-I Wu,et al.  Positive selection driving the evolution of a gene of male reproduction, Acp26Aa, of Drosophila: II. Divergence versus polymorphism. , 1998, Molecular biology and evolution.

[49]  A. Clark,et al.  Female genotypes affect sperm displacement in Drosophila. , 1998, Genetics.

[50]  A. Civetta,et al.  Sex-related genes, directional sexual selection, and speciation. , 1998, Molecular biology and evolution.

[51]  L. Partridge,et al.  Mating and hormonal triggers regulate accessory gland gene expression in male Drosophila. , 1997, Journal of insect physiology.

[52]  M. Wolfner,et al.  New genes for male accessory gland proteins in Drosophila melanogaster. , 1997, Insect biochemistry and molecular biology.

[53]  W. Rice,et al.  The enemies within: intergenomic conflict, interlocus contest evolution (ICE), and the intraspecific Red Queen , 1997, Behavioral Ecology and Sociobiology.

[54]  G. Parker,et al.  Sperm Competition in Fishes: The Evolution of Testis Size and Ejaculate Characteristics , 1997, The American Naturalist.

[55]  A. Reyes,et al.  Multiple paternity in two natural populations (orchard and vineyard) of Drosophila. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[56]  A. Clark,et al.  Polymorphism in genes that influence sperm displacement. , 1996, Genetics.

[57]  M. Wolfner,et al.  Localization of the Drosophila male accessory gland protein Acp36DE in the mated female suggests a role in sperm storage. , 1996, Insect Biochemistry and Molecular Biology.

[58]  W. Rice Sexually antagonistic male adaptation triggered by experimental arrest of female evolution , 1996, Nature.

[59]  M. Wolfner,et al.  A Drosophila seminal fluid protein, Acp26Aa, stimulates egg laying in females for 1 day after mating. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[60]  Dyanov Hm,et al.  Method for attachment of microscopic preparations on glass for in situ hybridization, PRINS and in situ PCR studies. , 1995 .

[61]  François Rousset,et al.  GENEPOP (version 1.2): population genetic software for exact tests and ecumenicism , 1995 .

[62]  G. Petersen,et al.  A Drosophila male accessory gland protein that is a member of the serpin superfamily of proteinase inhibitors is transferred to females during mating. , 1995, Insect biochemistry and molecular biology.

[63]  M. Gage Associations between body size, mating pattern, testis size and sperm lengths across butterflies , 1994, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[64]  R. Parkash,et al.  Parallel selection of ethanol and acetic-acid tolerance in Drosophila melanogaster populations from India , 1994, Genetics Selection Evolution.

[65]  R. Doerge,et al.  Empirical threshold values for quantitative trait mapping. , 1994, Genetics.

[66]  B. Sheldon Male phenotype, fertility, and the pursuit of extra-pair copulations by female birds , 1994, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[67]  M. Wolfner,et al.  Cell type-specific gene expression in the Drosophila melanogaster male accessory gland , 1992, Mechanisms of Development.

[68]  T. Aigaki,et al.  Ectopic expression of sex peptide alters reproductive behavior of female D. melanogaster , 1991, Neuron.

[69]  M. Wolfner,et al.  Synthesis of two Drosophila male accessory gland proteins and their fate after transfer to the female during mating. , 1990, Developmental biology.

[70]  G. Parker Sperm competition games: raffles and roles , 1990, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[71]  G. Parker Sperm competition games: sneaks and extra-pair copulations , 1990, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[72]  M. Wolfner,et al.  Structure, cell-specific expression, and mating-induced regulation of a Drosophila melanogaster male accessory gland gene. , 1990, Developmental biology.

[73]  M. Wolfner,et al.  Structure and expression of a Drosophila male accessory gland gene whose product resembles a peptide pheromone precursor. , 1988, Genes & development.

[74]  M. Bienz,et al.  A male accessory gland peptide that regulates reproductive behavior of female D. melanogaster , 1988, Cell.

[75]  S. Larson,et al.  Testis weight, body weight and breeding system in primates , 1981, Nature.

[76]  T. Prout,et al.  The population genetics of sperm displacement. , 1977, Genetics.

[77]  Bateman Aj Intra-sexual selection in Drosophila. , 1948 .

[78]  M. Wolfner,et al.  The Drosophila melanogaster seminal fluid protein Acp62F is a protease inhibitor that is toxic upon ectopic expression. , 2002, Genetics.

[79]  C. Wu,et al.  Sex in Drosophila mauritiana: a very high level of amino acid polymorphism in a male reproductive protein gene, Acp26Aa. , 2001, Molecular biology and evolution.

[80]  A. Møller,et al.  Sperm competition and sexual selection , 1998 .

[81]  K. Hughes,et al.  Quantitative genetics of sperm precedence in Drosophila melanogaster. , 1997, Genetics.

[82]  P. Service,et al.  Genetic variation in “first” male effects on egg laying and remating by femaleDrosophila melanogaster , 1996, Behavior genetics.

[83]  R. Doerge,et al.  Permutation tests for multiple loci affecting a quantitative character. , 1996, Genetics.

[84]  A. Clark,et al.  Variation in sperm displacement and its association with accessory gland protein loci in Drosophila melanogaster. , 1995, Genetics.

[85]  H. Dyanov,et al.  Method for attachment of microscopic preparations on glass for in situ hybridization, PRINS and in situ PCR studies. , 1995, BioTechniques.

[86]  P. S. Chen,et al.  Protein metabolism of Drosophila melanogaster male accessory glands—III: Stimulation of protein synthesis following copulation , 1985 .

[87]  P. S. Chen,et al.  Protein metabolism of Drosophila melanogaster male accessory glands—I: Characterization of secretory proteins , 1985 .

[88]  T. Halliday Behavioural ecology: Do frogs and toads choose their mates? , 1983, Nature.

[89]  Geoffrey Parker,et al.  SEXUAL SELECTION AND SEXUAL CONFLICT , 1979 .

[90]  B. Bainbridge,et al.  Genetics , 1981, Experientia.