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Genetics. Dec 2000; 156(4): 1879–1888.
PMCID: PMC1461396

Molecular population genetics of male accessory gland proteins in Drosophila.

Abstract

Drosophila seminal proteins have an unusually high rate of molecular sequence evolution, suggesting either a high rate of neutral substitution or rapid adaptive evolution. To further quantify patterns of polymorphism and divergence in genes encoding seminal proteins, also called accessory gland proteins (Acp's), we conducted a sequencing survey of 10 Acp genes in samples of Drosophila melanogaster and D. simulans (Acp29AB, Acp32CD, Acp33A, Acp36DE, Acp53Ea, Acp62F, Acp63F, Acp76A, Acp95EF, and Acp98AB). Mean heterozygosity at replacement sites in D. simulans was 0.0074 for Acp genes and 0.0013 for a set of 19 non-Acp genes, and mean melanogaster-simulans divergence at replacement sites was 0.0497 for Acp genes and 0.0107 at non-Acp genes. The elevated divergence of Acp genes is thus accompanied by elevated within-species polymorphism. In addition to the already-reported departures of Acp26A, Acp29AB, and Acp70A from neutrality, our data reject neutrality at Acp29AB and Acp36DE in the direction of excess replacements in interspecific comparisons.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Aguadé M. Different forces drive the evolution of the Acp26Aa and Acp26Ab accessory gland genes in the Drosophila melanogaster species complex. Genetics. 1998 Nov;150(3):1079–1089. [PMC free article] [PubMed]
  • Aguadé M. Positive selection drives the evolution of the Acp29AB accessory gland protein in Drosophila. Genetics. 1999 Jun;152(2):543–551. [PMC free article] [PubMed]
  • Aguadé M, Miyashita N, Langley CH. Polymorphism and divergence in the Mst26A male accessory gland gene region in Drosophila. Genetics. 1992 Nov;132(3):755–770. [PMC free article] [PubMed]
  • Akashi H. Synonymous codon usage in Drosophila melanogaster: natural selection and translational accuracy. Genetics. 1994 Mar;136(3):927–935. [PMC free article] [PubMed]
  • Akashi H. Molecular evolution between Drosophila melanogaster and D. simulans: reduced codon bias, faster rates of amino acid substitution, and larger proteins in D. melanogaster. Genetics. 1996 Nov;144(3):1297–1307. [PMC free article] [PubMed]
  • Aquadro CF, Lado KM, Noon WA. The rosy region of Drosophila melanogaster and Drosophila simulans. I. Contrasting levels of naturally occurring DNA restriction map variation and divergence. Genetics. 1988 Aug;119(4):875–888. [PMC free article] [PubMed]
  • Bauer VL, Aquadro CF. Rates of DNA sequence evolution are not sex-biased in Drosophila melanogaster and D. simulans. Mol Biol Evol. 1997 Dec;14(12):1252–1257. [PubMed]
  • Begun DJ. Population genetics of silent and replacement variation in Drosophila simulans and D. melanogaster: X/autosome differences? Mol Biol Evol. 1996 Dec;13(10):1405–1407. [PubMed]
  • Begun DJ, Aquadro CF. African and North American populations of Drosophila melanogaster are very different at the DNA level. Nature. 1993 Oct 7;365(6446):548–550. [PubMed]
  • Begun DJ, Whitley P. Reduced X-linked nucleotide polymorphism in Drosophila simulans. Proc Natl Acad Sci U S A. 2000 May 23;97(11):5960–5965. [PMC free article] [PubMed]
  • Bertram MJ, Neubaum DM, Wolfner MF. Localization of the Drosophila male accessory gland protein Acp36DE in the mated female suggests a role in sperm storage. Insect Biochem Mol Biol. 1996 Sep-Oct;26(8-9):971–980. [PubMed]
  • Chapman T, Liddle LF, Kalb JM, Wolfner MF, Partridge L. Cost of mating in Drosophila melanogaster females is mediated by male accessory gland products. Nature. 1995 Jan 19;373(6511):241–244. [PubMed]
  • Chen PS. The accessory gland proteins in male Drosophila: structural, reproductive, and evolutionary aspects. Experientia. 1996 Jun 15;52(6):503–510. [PubMed]
  • Chen PS, Stumm-Zollinger E, Aigaki T, Balmer J, Bienz M, Böhlen P. A male accessory gland peptide that regulates reproductive behavior of female D. melanogaster. Cell. 1988 Jul 29;54(3):291–298. [PubMed]
  • Cirera S, Aguadé M. Evolutionary history of the sex-peptide (Acp70A) gene region in Drosophila melanogaster. Genetics. 1997 Sep;147(1):189–197. [PMC free article] [PubMed]
  • Civetta A, Singh RS. High divergence of reproductive tract proteins and their association with postzygotic reproductive isolation in Drosophila melanogaster and Drosophila virilis group species. J Mol Evol. 1995 Dec;41(6):1085–1095. [PubMed]
  • Clark AG, Begun DJ. Female genotypes affect sperm displacement in Drosophila. Genetics. 1998 Jul;149(3):1487–1493. [PMC free article] [PubMed]
  • Clark AG, Aguadé M, Prout T, Harshman LG, Langley CH. Variation in sperm displacement and its association with accessory gland protein loci in Drosophila melanogaster. Genetics. 1995 Jan;139(1):189–201. [PMC free article] [PubMed]
  • Clark AG, Begun DJ, Prout T. Female x male interactions in Drosophila sperm competition. Science. 1999 Jan 8;283(5399):217–220. [PubMed]
  • Coulthart MB, Singh RS. Differing amounts of genetic polymorphism in testes and male accessory glands of Drosophila melanogaster and Drosophila simulans. Biochem Genet. 1988 Feb;26(1-2):153–164. [PubMed]
  • DiBenedetto AJ, Harada HA, Wolfner MF. Structure, cell-specific expression, and mating-induced regulation of a Drosophila melanogaster male accessory gland gene. Dev Biol. 1990 May;139(1):134–148. [PubMed]
  • Gillespie JH. Junk ain't what junk does: neutral alleles in a selected context. Gene. 1997 Dec 31;205(1-2):291–299. [PubMed]
  • Moriyama EN, Powell JR. Intraspecific nuclear DNA variation in Drosophila. Mol Biol Evol. 1996 Jan;13(1):261–277. [PubMed]
  • Neubaum DM, Wolfner MF. Mated Drosophila melanogaster females require a seminal fluid protein, Acp36DE, to store sperm efficiently. Genetics. 1999 Oct;153(2):845–857. [PMC free article] [PubMed]
  • Powell JR, Moriyama EN. Evolution of codon usage bias in Drosophila. Proc Natl Acad Sci U S A. 1997 Jul 22;94(15):7784–7790. [PMC free article] [PubMed]
  • Prout T, Clark AG. Polymorphism in genes that influence sperm displacement. Genetics. 1996 Sep;144(1):401–408. [PMC free article] [PubMed]
  • Richmond RC, Gilbert DG, Sheehan KB, Gromko MH, Butterworth FM. Esterase 6 and reproduction in Drosophila melanogaster. Science. 1980 Mar 28;207(4438):1483–1485. [PubMed]
  • Rice WR. Sexually antagonistic male adaptation triggered by experimental arrest of female evolution. Nature. 1996 May 16;381(6579):232–234. [PubMed]
  • Richmond RC, Gilbert DG, Sheehan KB, Gromko MH, Butterworth FM. Esterase 6 and reproduction in Drosophila melanogaster. Science. 1980 Mar 28;207(4438):1483–1485. [PubMed]
  • Rozas J, Rozas R. DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics. 1999 Feb;15(2):174–175. [PubMed]
  • Hey J, Wakeley J. A coalescent estimator of the population recombination rate. Genetics. 1997 Mar;145(3):833–846. [PMC free article] [PubMed]
  • Holland B, Rice WR. Experimental removal of sexual selection reverses intersexual antagonistic coevolution and removes a reproductive load. Proc Natl Acad Sci U S A. 1999 Apr 27;96(9):5083–5088. [PMC free article] [PubMed]
  • Hudson RR, Kaplan NL. The coalescent process in models with selection and recombination. Genetics. 1988 Nov;120(3):831–840. [PMC free article] [PubMed]
  • Hudson RR, Kreitman M, Aguadé M. A test of neutral molecular evolution based on nucleotide data. Genetics. 1987 May;116(1):153–159. [PMC free article] [PubMed]
  • Tram U, Wolfner MF. Male seminal fluid proteins are essential for sperm storage in Drosophila melanogaster. Genetics. 1999 Oct;153(2):837–844. [PMC free article] [PubMed]
  • Hudson RR, Boos DD, Kaplan NL. A statistical test for detecting geographic subdivision. Mol Biol Evol. 1992 Jan;9(1):138–151. [PubMed]
  • Steyerberg EW, Kievit J, de Mol Van Otterloo JC, van Bockel JH, Eijkemans MJ, Habbema JD. Perioperative mortality of elective abdominal aortic aneurysm surgery. A clinical prediction rule based on literature and individual patient data. Arch Intern Med. 1995 Oct 9;155(18):1998–2004. [PubMed]
  • Tsaur SC, Ting CT, Wu CI. Positive selection driving the evolution of a gene of male reproduction, Acp26Aa, of Drosophila: II. Divergence versus polymorphism. Mol Biol Evol. 1998 Aug;15(8):1040–1046. [PubMed]
  • Imhof M, Harr B, Brem G, Schlötterer C. Multiple mating in wild Drosophila melanogaster revisited by microsatellite analysis. Mol Ecol. 1998 Jul;7(7):915–917. [PubMed]
  • Watterson GA. On the number of segregating sites in genetical models without recombination. Theor Popul Biol. 1975 Apr;7(2):256–276. [PubMed]
  • Kreitman M, Hudson RR. Inferring the evolutionary histories of the Adh and Adh-dup loci in Drosophila melanogaster from patterns of polymorphism and divergence. Genetics. 1991 Mar;127(3):565–582. [PMC free article] [PubMed]
  • Wolfner MF, Harada HA, Bertram MJ, Stelick TJ, Kraus KW, Kalb JM, Lung YO, Neubaum DM, Park M, Tram U. New genes for male accessory gland proteins in Drosophila melanogaster. Insect Biochem Mol Biol. 1997 Oct;27(10):825–834. [PubMed]
  • Wright F. The 'effective number of codons' used in a gene. Gene. 1990 Mar 1;87(1):23–29. [PubMed]
  • McDonald JH, Kreitman M. Adaptive protein evolution at the Adh locus in Drosophila. Nature. 1991 Jun 20;351(6328):652–654. [PubMed]

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