Recurrent positive selection at Bgcn, a key determinant of germ line differentiation, does not appear to be driven by simple coevolution with its partner protein bam

Molecular Biology and Evolution

Volumn 24, Issue 1, 2007, Pages 182-191

  Bauer DuMont, Vanessa L ^a   Flores, Heather A ^a   Wright, Mark H ^a   Aquadro, Charles F ^a  

^a Department of Obstetrics Gynecology   (United States)

Author keywords

bam; bgcn; Drosophila; Nonsynonymous; Positive selection

Indexed keywords

ARTICLE; BAG OF MARBLE; BENIGN GONIAL CELL NEOPLASM; CONTROLLED STUDY; DROSOPHILA SIMULANS; GAMETOGENESIS; GENE LOCUS; GENE MUTATION; GENETIC POLYMORPHISM; GENETIC SELECTION; GENETIC VARIABILITY; GERM LINE; MOLECULAR EVOLUTION; NONHUMAN; NUCLEOTIDE SEQUENCE;

ANIMALS; CELL DIFFERENTIATION; DNA HELICASES; DROSOPHILA; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EVOLUTION, MOLECULAR; FEMALE; GAMETOGENESIS; GERM CELLS; MALE; MOLECULAR SEQUENCE DATA; PHYLOGENY; SELECTION (GENETICS);

DROSOPHILA MELANOGASTER; DROSOPHILA SIMULANS;

EID: 33845868780     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msl141     Document Type: Article

References (56)

1. Aquadro CF, Lado KM, Noon WA. 1988. The rosy region of Drosophila melanogaster and Drosophila simulans. I. Contrasting levels of naturally occurring DNA restriction map variation and divergence. Genetics. 119:875-888.
2. Bauer DuMont V, Fay JC, Calabrese PP, Aquadro CF. 2004. DNA variability and divergence at the Notch locus in Drosophila melanogaster and D. simulans: a case of accelerated synonymous site divergence. Genetics. 167:171-185.
3. Begun DJ, Aquadro CF. 1994. Evolutionary inferences from DNA variation at the 6-phosphogluconate dehydrogenase locus in natural populations of Drosophila: selection and geographic differentiation. Genetics. 136:155-171.
4. Benjamini Y, Hochberg Y. 1995. Controlling the false discovery rate - a practical and powerful approach to multiple testing. J R Stat Soc Ser B (Methodol). 57:289-300.
5. Betancourt AJ, Presgraves DC. 2002. Linkage limits the power of natural selection in Drosophila. Proc Natl Acad Sci. 99:13616-13620.
6. Braun RE, Behringer RR, Peschon JJ, Brinster RL, Palmiter RD. 1989. Genetically haploid spermatids are phenotypically diploid. Nature. 337:373-376.
7. Castillo-Davis CI, Kondrashov FA, Hartl DL, Kulathinal RJ. 2004. The functional genomic distribution of protein divergence in two animal phyla: coevolution, genomic conflict, and constraint. Genome Res. 14:802-811.
8. Chen D, McKearin D. 2005. Gene circuitry controlling a stem cell niche. Curr Biol. 15:179-184.
9. Civetta A, Rajakumar SA, Brouwers B, Bacik JP. 2006. Rapid evolution and gene-specific patterns of selection for three genes of spermatogenesis in Drosophila. Mol Biol Evol. 23:655-662.
10. Clark ME, Veneti Z, Bourtzis K, Karr TL. 2002. The distribution and proliferation of the intracellular bacteria Wolbachia during spermatogenesis in Drosophila. Mech Dev. 111:3-15.
11. Cooley L, Theurkauf WE. 1994. Cytoskeletal functions during Drosophila oogenesis. Science. 266:590-596.
12. Cox RT, Spradling AC. 2003. A Balbiani body and the fusome mediate mitochondrial inheritance during Drosophila oogenesis. Development. 130:1579-1590.
13. Cutter AD, Ward S. 2005. Sexual and temporal dynamics of molecular evolution in C. elegans development. Mol Biol Evol. 22:178-188.
14. de Cuevas M, Lilly MA, Spradling AC. 1997. Germline cyst formation in Drosophila. Annu Rev Genet. 31:405-428.
15. DePristo MA, Weinreich DM, Hartl DL. 2005. Missense meanderings in sequence space: a biophysical view of protein evolution. Nat Rev Genet. 6:678-687.
16. Eanes WF, Kirchner M, Yoon J, Biermann CH, Wang I-N, McCartney MF, Verrelli BC. 1996. Historical selection, amino acid polmorphism and lineage-specific divergence at the G6pd locus in Drosophila melanogaster and D. simulans. Genetics. 144:1027-1041.
17. Eyre-Walker A. 2002. Changing effective population size and the McDonald-Kreitman test. Genetics. 162:2017-2024.
18. Fay JC, Wu C-I. 2000. Hitchhiking under positive Darwinian selection. Genetics. 155:1405-1413.
19. Fay JC, Wyckoff GJ, Wu C-I. 2001. Positive and negative selection on the human genome. Genetics. 158:1227-1234.
20. Fu Y-X, Li W-H. 1993. Statistical tests of neutrality of mutations. Genetics. 133:693-709.
21. Fuller MT. 1998. Genetic control of cell proliferation and differentiation in Drosophila spermatogenesis. Semin Cell Dev Biol. 9:433-444.
22. Glassey B, Civetta A. 2004. Positive selection at reproductive ADAM genes with potential intercellular binding activity. Mol Biol Evol. 21:851-859.
23. Gönczy P, Matunis E, DiNardo S. 1997. bag-of-marbles and benign gonial cell neoplasm act in the germline to restrict proliferation during Drosophila spermatogenesis. Development. 124:4361-4371.
24. Haag ES, Molla MN. 2005. Compensatory evolution of interacting gene products through multifunctional intermediates. Evolution. 59:1620-1632.
25. Hamblin MT, Aquadro CF. 1996. High nucleotide sequence variation in a region of low recombination in Drosophila simulans is consistent with the background selection model. Mol Biol Evol. 13:1133-1140.
26. Hamblin MT, Veuille M. 1999. Population structure among African and derived populations of Drosophila simulans: evidence for ancient subdivision and recent admixture. Genetics. 153:305-317.
27. Hey J, Kliman RM. 2002. Interactions between natural selection, recombination and gene density in the genes of Drosophila. Genetics. 160:595-608.
28. Jagadeeshan S, Singh RS. 2005. Rapidly evolving genes of Drosophila: differing levels of selective pressure in testis, ovary, and head tissues between sibling species. Mol Biol Evol. 22:1793-1801.
29. Kosakovsky Pond SL, Frost SDW. 2005. A genetic algorithm approach to detecting lineage-specific variation in selection pressure. Mol Biol Evol. 22:478-485.
30. Kosakovsky Pond SL, Frost SDW, Muse SV. 2005. HyPhy: hypothesis testing using phylogenies. Bioinformatics. 21:676-679.
31. Kreitman M. 1983. Nucleotide polymorphismat the alcohol dehydrogenase locus of Drosophila melanogaster. Nature. 304:412-417.
32. Labate JA, Bierman CH, Eanes WF. 1999. Nucleotide variation at the runt locus in Drosophila melanogaster and Drosophila simulans. Mol Biol Evol. 16:724-731.
33. Lavoie CA, Ohlstein B, McKearin DM. 1999. Localization and function of Bam protein require the benign gonial cell neoplasm gene product. Dev Biol. 212:405-413.
34. Lazzaro BP, Clark AG. 2001. Evidence for recurrent paralogous gene conversion and exceptional allelic divergence in the Attacin genes of Drosophila melanogaster. Genetics. 159:659-671.
35. León A, McKearin D. 1999. Identification of TER94, an AAA ATPase protein, as a Bam-dependent component of the Drosophila fusome. Mol Biol Cell. 10:3825-3834.
36. McDonald JH, Kreitman M. 1991. Adaptive protein evolution at the Adh locus in Drosophila. Nature. 20:652-654.
37. Moriyama EN, Powell JR. 1996. Intraspecific nuclear DNA variation in Drosophila. Mol Biol Evol. 13:261-277.
38. Nielsen R, Bustamante C, Clark AG, et al. (13 co-authors). 2005. A scan for positively selected genes in the genomes of humans and chimpanzees. Plos Biol. 6:976-985.
39. Ohlstein B, Lavoie CA, Vef O, Gateff E, McKearin DM. 2000. The Drosophila cystoblast differentiation factor, benign gonial cell neoplasm, is related to DExH-box proteins and interacts genetically with bag-of-marbles. Genetics. 155:1809-1819.
40. Poirot O, Suhre K, Abergel C, O'Toole E, Notredame C. 2004. 3DCoffee: a web server for mixing sequences and structure into multiple sequence alignments. Nucleic Acids Res. 32:W37-W40.
41. Rodgers S, Wells R, Rechsteiner M. 1986. Amino acid sequences common to rapidly degraded proteins: the PEST hypothesis. Science. 234:364-368.
42. Rozas J, Sánchez-DelBarrio JC, Messeguer X, Rozas R. 2003. DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics. 19:2496-2497.
43. Schulz C, Kiger AA, Tazuke SI, Yamashita YM, Pantalena-Filho LC, Jones DL, Wood CG, Fuller MT. 2004. A misexpression screen reveals effects of bag-of-marbles and TGFβ class signaling on the Drosophila male germ-line stem cell lineage. Genetics. 167:707-723.
44. Snook RR, Cleland SY, Wolfner MF, Karr TL. 2000. Offsetting effects of Wolbachia infection and heat shock on sperm production in Drosophila simulans: comparative analyses of fecundity, fertility and accessory gland proteins. Genetics. 155:167-178.
45. Spradling A, Drummond-Barbosa D, Kai T. 2001. Stem cells find their niche. Nature. 414:98-104.
46. Stephens M, Smith NJ, Donnelly P. 2001. A new statistical method for haplotype reconstruction from population data. Am J Hum Genet. 68:978-989.
47. Stephens M, Donnelly P. 2003. Inference in molecular population genetics. J R Stat Soc Ser B. 62:605-655.
48. Swanson WJ, Vacquier VD. 2002. The rapid evolution of reproductive proteins. Nat Rev Genet. 3:137-144.
49. Swanson WJ, Wong A, Wolfner MF, Aquadro CF. 2004. Evolutionary expressed sequence tag analysis of Drosophila female reproductive tracts identifies genes subjected to positive selection. Genetics. 168:1457-1465.
50. Szakmary A, Cox DN, Wang Z, Lin H. 2005. Regulatory relationship among piwi, pumilio, and bag-of-marbles in Drosophila germline stem cell self-renewal and differentiation. Curr Biol. 15:171-178.
51. Tajima F. 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics. 123:585-595.
52. Tajima F. 1993. Simple methods for testing the molecular evolutionary clock hypothesis. Genetics. 135:599-607.
53. Torgerson DG, Kulathinal RJ, Singh RS. 2002. Mammalian sperm proteins are rapidly evolving: evidence of positive selection in functionally diverse genes. Mol Biol Evol. 19:1973-1980.
54. Wakeley J. 2003. Polymorphism and divergence for island-model species. Genetics. 163:411-420.
55. Yang Z. 1997. PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci. 13:555-556.
56. Yang Z, Nielsen R. 2002. Codon-substitution models for detecting molecular adaptation at individual sites along specific lineages. Mol Biol Evol. 19:908-917.