MBE Advance Access originally published online on December 15, 2005
Molecular Biology and Evolution 2006 23(3):655-662; doi:10.1093/molbev/msj074
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
Research Article |
Rapid Evolution and Gene-Specific Patterns of Selection for Three Genes of Spermatogenesis in Drosophila
,1
* Department of Biology, University of Winnipeg, Winnipeg, Manitoba, Canada; and Department of Biochemistry and Medical Genetics, University of Manitoba, Winnipeg, Manitoba, Canada
E-mail: a.civetta{at}uwinnipeg.ca.
Hybrid males resulting from crosses between closely related species of Drosophila are sterile. The F1 hybrid sterility phenotype is mainly due to defects occurring during late stages of development that relate to sperm individualization, and so genes controlling sperm development may have been subjected to selective diversification between species. It is also possible that genes of spermatogenesis experience selective constraints given their role in a developmental pathway. We analyzed the molecular evolution of three genes playing a role during the sperm developmental pathway in Drosophila at an early (bam), a mid (aly), and a late (dj) stage. The complete coding region of these genes was sequenced in different strains of Drosophila melanogaster and Drosophila simulans. All three genes showed rapid divergence between species, with larger numbers of nonsynonymous to synonymous differences between species than polymorphisms. Although this could be interpreted as evidence for positive selection at all three genes, formal tests of selection do not support such a conclusion. Departures from neutrality were detected only for dj and bam but not aly. The role played by selection is unique and determined by gene-specific characteristics rather than site of expression. In dj, the departure was due to a high proportion of neutral synonymous polymorphisms in D. simulans, and there was evidence of purifying selection maintaining a high lysine amino acid protein content that is characteristic of other DNA-binding proteins. The earliest spermatogenesis gene surveyed, which plays a role in both male and female gametogenesis, was bam, and its significant departure from neutrality was due to an excess of nonsynonymous substitutions between species. Bam is degraded at the end of mitosis, and rapid evolutionary changes among species might be a characteristic shared with other degradable transient proteins. However, the large number of nonsynonymous changes between D. melanogaster and D. simulans and a phylogenetic comparative analysis among species confirms evidence of positive selection driving the evolution of Bam and suggests an yet unknown germ cell line developmental adaptive change between these two species.
Key Words: population genetics • spermatogenesis • Drosophila • selection
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  Y. Li, N. T. Minor, J. K. Park, D. M. McKearin, and J. Z. Maines Bam and Bgcn antagonize Nanos-dependent germ-line stem cell maintenance PNAS, June 9, 2009; 106(23): 9304 - 9309. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. Llopart and J. M. Comeron Recurrent Events of Positive Selection in Independent Drosophila Lineages at the Spermatogenesis Gene roughex Genetics, June 1, 2008; 179(2): 1009 - 1020. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
H. S. Makinen, T. Shikano, J. M. Cano, and J. Merila Hitchhiking Mapping Reveals a Candidate Genomic Region for Natural Selection in Three-Spined Stickleback Chromosome VIII Genetics, January 1, 2008; 178(1): 453 - 465. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
W. Haerty, S. Jagadeeshan, R. J. Kulathinal, A. Wong, K. Ravi Ram, L. K. Sirot, L. Levesque, C. G. Artieri, M. F. Wolfner, A. Civetta, et al. Evolution in the Fast Lane: Rapidly Evolving Sex-Related Genes in Drosophila Genetics, November 1, 2007; 177(3): 1321 - 1335. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 V. L. Bauer DuMont, H. A. Flores, M. H. Wright, and C. F. Aquadro 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 Mol. Biol. Evol., January 1, 2007; 24(1): 182 - 191. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Metta, R. Gudavalli, J.-M. Gibert, and C. Schlotterer No Accelerated Rate of Protein Evolution in Male-Biased Drosophila pseudoobscura Genes Genetics, September 1, 2006; 174(1): 411 - 420. [Abstract] [Full Text] [PDF]
|
|