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PMID: 16752217 Published · ppublish English Journal Article Research Support, U.S. Gov't, Non-P.H.S.

Positive selection on nucleotide substitutions and indels in accessory gland proteins of the Drosophila pseudoobscura subgroup.

Journal of molecular evolution ·Vol. 62 ·No. 6 ·2006-06-00 ·Pages 793-802

Schully SD, Hellberg ME

Abstract

Genes encoding reproductive proteins often diverge rapidly due to positive selection on nucleotide substitutions. While this general pattern is well established, the extent to which specific reproductive genes experience similar selection in different clades has been little explored, nor have possible targets of positive selection other than nucleotide substitutions, such as indels, received much attention. Here, we inspect for the signature of positive selection in the genes encoding five accessory gland proteins (Acps) (Acp26Aa, Acp32CD, Acp53Ea, Acp62F, and Acp70A) originally described from Drosophila melanogaster but with recognizable orthologues in the D. pseudoobscura subgroup. We compare patterns of selection within the D. psuedoobscura subgroup to those in the D. melanogaster subgroup. Similar patterns of positive selection were found in Acp26Aa and Acp62F in the two subgroups, while Acp53Ea and Acp70A experienced purifying selection in both subgroups. These proteins have thus remained targets for similar types of selection over long (>21-MY) periods of time. We also found several indel substitutions and polymorphisms in Acp26Aa and Acp32CD. These indels occur in the same regions as positively selected nucleotide substitutions for Acp26Aa in the D. pseudoobscura subgroup but not in the D. melanogaster subgroup. Rates of indel substitution within Acp26Aa in the D. pseudoobscura subgroup were up to several times those in noncoding regions of the Drosophila genome. This suggests that indel substitutions may be under positive selection and may play a key role in the divergence of some Acps.

MeSH Terms
Amino Acid Sequence Animals Base Sequence Drosophila/classification,genetics Drosophila Proteins/classification,genetics Intercellular Signaling Peptides and Proteins Molecular Sequence Data Mutation Peptides/classification,genetics Selection, Genetic Seminal Plasma Proteins/classification,genetics Sequence Alignment Sequence Deletion Species Specificity
Chemicals
Acp26Aa protein, Drosophila Drosophila Proteins Intercellular Signaling Peptides and Proteins Peptides Seminal Plasma Proteins accessory gland peptide 62F, Drosophila
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Schully Sheri Dixon
Department of Biological Sciences, Louisiana State University, Baton Rouge, LA 70803, USA.
Hellberg Michael E
References (55)
55 references, click to expand
  1. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism.
    Genetics. 1989 Nov;123(3):585-95 PMID: 2513255
  2. Positive selection and sequence rearrangements generate extensive polymorphism in the gamete recognition protein bindin.
    Mol Biol Evol. 1996 Feb;13(2):397-406 PMID: 8587504
  3. Codon-substitution models for heterogeneous selection pressure at amino acid sites.
    Genetics. 2000 May;155(1):431-49 PMID: 10790415
  4. 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):1085-95 PMID: 8587107
  5. Codon-substitution models to detect adaptive evolution that account for heterogeneous selective pressures among site classes.
    Mol Biol Evol. 2002 Jan;19(1):49-57 PMID: 11752189
  6. The neighbor-joining method: a new method for reconstructing phylogenetic trees.
    Mol Biol Evol. 1987 Jul;4(4):406-25 PMID: 3447015
  7. Patterns of positive selection in the complete NBS-LRR gene family of Arabidopsis thaliana.
    Genome Res. 2002 Sep;12(9):1305-15 PMID: 12213767
  8. Likelihood models for detecting positively selected amino acid sites and applications to the HIV-1 envelope gene.
    Genetics. 1998 Mar;148(3):929-36 PMID: 9539414
  9. Molecular evolution of X-linked accessory gland proteins in Drosophila pseudoobscura.
    J Hered. 2004 Mar-Apr;95(2):114-8 PMID: 15073226
  10. Adaptive protein evolution at the Adh locus in Drosophila.
    Nature. 1991 Jun 20;351(6328):652-4 PMID: 1904993
  11. Variation in sperm displacement and its association with accessory gland protein loci in Drosophila melanogaster.
    Genetics. 1995 Jan;139(1):189-201 PMID: 7705622
  12. Accuracy and power of statistical methods for detecting adaptive evolution in protein coding sequences and for identifying positively selected sites.
    Genetics. 2004 Oct;168(2):1041-51 PMID: 15514074
  13. Statistical properties of the number of recombination events in the history of a sample of DNA sequences.
    Genetics. 1985 Sep;111(1):147-64 PMID: 4029609
  14. Mated Drosophila melanogaster females require a seminal fluid protein, Acp36DE, to store sperm efficiently.
    Genetics. 1999 Oct;153(2):845-57 PMID: 10511562
  15. The Acp26Aa seminal fluid protein is a modulator of early egg hatchability in Drosophila melanogaster.
    Proc Biol Sci. 2001 Aug 22;268(1477):1647-54 PMID: 11506676
  16. Majority of divergence between closely related DNA samples is due to indels.
    Proc Natl Acad Sci U S A. 2003 Apr 15;100(8):4661-5 PMID: 12672966
  17. Speciation on the coasts of the new world: phylogeography and the evolution of bindin in the sea urchin genus Lytechinus.
    Evolution. 2004 Jun;58(6):1225-41 PMID: 15266972
  18. A Drosophila seminal fluid protein, Acp26Aa, stimulates egg laying in females for 1 day after mating.
    Proc Natl Acad Sci U S A. 1995 Oct 24;92(22):10114-8 PMID: 7479736
  19. Positive selection for indel substitutions in the rodent sperm protein catsper1.
    Mol Biol Evol. 2005 Sep;22(9):1845-52 PMID: 15930155
  20. SPERM DISPLACEMENT WITHOUT SPERM TRANSFER IN DROSOPHILA MELANOGASTER.
    Evolution. 1994 Jun;48(3):758-766 PMID: 28568282
  21. Adaptive evolution of sperm bindin tracks egg incompatibility in neotropical sea urchins of the genus Echinometra.
    Mol Biol Evol. 2004 Apr;21(4):732-45 PMID: 14963103
  22. Pervasive adaptive evolution in mammalian fertilization proteins.
    Mol Biol Evol. 2003 Jan;20(1):18-20 PMID: 12519901
  23. Bayes empirical bayes inference of amino acid sites under positive selection.
    Mol Biol Evol. 2005 Apr;22(4):1107-18 PMID: 15689528
  24. Positive selection and propeptide repeats promote rapid interspecific divergence of a gastropod sperm protein.
    Mol Biol Evol. 2000 Mar;17(3):458-66 PMID: 10723746
  25. Concerted evolution in an egg receptor for a rapidly evolving abalone sperm protein.
    Science. 1998 Jul 31;281(5377):710-2 PMID: 9685267
  26. Relationships in the Drosophila obscura species group, inferred from mitochondrial cytochrome oxidase II sequences.
    Mol Biol Evol. 1993 May;10(3):619-34 PMID: 8393127
  27. False-positive selection identified by ML-based methods: examples from the Sig1 gene of the diatom Thalassiosira weissflogii and the tax gene of a human T-cell lymphotropic virus.
    Mol Biol Evol. 2004 May;21(5):914-21 PMID: 15014169
  28. The gifts that keep on giving: physiological functions and evolutionary dynamics of male seminal proteins in Drosophila.
    Heredity (Edinb). 2002 Feb;88(2):85-93 PMID: 11932766
  29. A sperm ion channel required for sperm motility and male fertility.
    Nature. 2001 Oct 11;413(6856):603-9 PMID: 11595941
  30. High mutation rate and predominance of insertions in the Caenorhabditis elegans nuclear genome.
    Nature. 2004 Aug 5;430(7000):679-82 PMID: 15295601
  31. DnaSP, DNA polymorphism analyses by the coalescent and other methods.
    Bioinformatics. 2003 Dec 12;19(18):2496-7 PMID: 14668244
  32. Sex gene pool evolution and speciation: a new paradigm.
    Genes Genet Syst. 2000 Jun;75(3):119-30 PMID: 10984836
  33. Comparative genome sequencing of Drosophila pseudoobscura: chromosomal, gene, and cis-element evolution.
    Genome Res. 2005 Jan;15(1):1-18 PMID: 15632085
  34. Comparative genomics of accessory gland protein genes in Drosophila melanogaster and D. pseudoobscura.
    Mol Biol Evol. 2005 Apr;22(4):818-32 PMID: 15601888
  35. Sex in Drosophila mauritiana: a very high level of amino acid polymorphism in a male reproductive protein gene, Acp26Aa.
    Mol Biol Evol. 2001 Jan;18(1):22-6 PMID: 11141189
  36. Molecular population genetics of male accessory gland proteins in the Drosophila simulans complex.
    Genetics. 2004 Jun;167(2):725-35 PMID: 15238524
  37. Drosophila female sexual behavior induced by sterile males showing copulation complementation.
    Proc Natl Acad Sci U S A. 2000 Mar 28;97(7):3272-5 PMID: 10725377
  38. Male contributions to egg production: the role of accessory gland products and sperm in Drosophila melanogaster.
    Proc Biol Sci. 2001 Jan 22;268(1463):175-80 PMID: 11209888
  39. Sex-related genes, directional sexual selection, and speciation.
    Mol Biol Evol. 1998 Jul;15(7):901-9 PMID: 9656489
  40. Patterns of evolutionary constraints in intronic and intergenic DNA of Drosophila.
    Genome Res. 2004 Feb;14(2):273-9 PMID: 14762063
  41. On the evolution of codon volatility.
    Genetics. 2005 Jan;169(1):495-501 PMID: 15466418
  42. Inferring the history of speciation from multilocus DNA sequence data: the case of Drosophila pseudoobscura and close relatives.
    Mol Biol Evol. 2002 Apr;19(4):472-88 PMID: 11919289
  43. Molecular population genetics of male accessory gland proteins in Drosophila.
    Genetics. 2000 Dec;156(4):1879-88 PMID: 11102381
  44. The Drosophila melanogaster seminal fluid protein Acp62F is a protease inhibitor that is toxic upon ectopic expression.
    Genetics. 2002 Jan;160(1):211-24 PMID: 11805057
  45. Cross-species comparison of Drosophila male accessory gland protein genes.
    Genetics. 2005 Sep;171(1):131-43 PMID: 15944345
  46. Molecular evolution and population genetics of duplicated accessory gland protein genes in Drosophila.
    Mol Biol Evol. 2004 Sep;21(9):1625-8 PMID: 15215320
  47. Cost of mating in Drosophila melanogaster females is mediated by male accessory gland products.
    Nature. 1995 Jan 19;373(6511):241-4 PMID: 7816137
  48. Positive selection on protein-length in the evolution of a primate sperm ion channel.
    Proc Natl Acad Sci U S A. 2003 Oct 14;100(21):12241-6 PMID: 14523237
  49. The evolution of conspecific sperm precedence in Drosophila.
    Mol Ecol. 2003 May;12(5):1179-84 PMID: 12694281
  50. Population genetics of accessory gland proteins and sexual behavior in Drosophila melanogaster populations from Evolution Canyon.
    Evolution. 2003 Dec;57(12):2785-91 PMID: 14761057
  51. Ectopic expression of sex peptide alters reproductive behavior of female D. melanogaster.
    Neuron. 1991 Oct;7(4):557-63 PMID: 1931051
  52. Pattern of nucleotide substitution at major histocompatibility complex class I loci reveals overdominant selection.
    Nature. 1988 Sep 8;335(6186):167-70 PMID: 3412472
  53. A male accessory gland peptide that regulates reproductive behavior of female D. melanogaster.
    Cell. 1988 Jul 29;54(3):291-8 PMID: 3135120
  54. Evolutionary EST analysis identifies rapidly evolving male reproductive proteins in Drosophila.
    Proc Natl Acad Sci U S A. 2001 Jun 19;98(13):7375-9 PMID: 11404480
  55. Positive selection and the molecular evolution of a gene of male reproduction, Acp26Aa of Drosophila.
    Mol Biol Evol. 1997 May;14(5):544-9 PMID: 9159932
Article Info
Journal
Journal of molecular evolution
Abbr.
J Mol Evol
ISSN
0022-2844
Published
2006-06-00
Epub
2006-00-28
Pages
793-802
Language
English
Region
Germany
NLM ID
0360051
Subset
IM
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