Skip to main content

Advertisement

Log in

Male Sex Interspecies Divergence and Down Regulation of Expression of Spermatogenesis Genes in Drosophila Sterile Hybrids

  • Published:
Journal of Molecular Evolution Aims and scope Submit manuscript

Abstract

Male sex genes have shown a pattern of rapid interspecies divergence at both the coding and gene expression level. A common outcome from crosses between closely-related species is hybrid male sterility. Phenotypic and genetic studies in Drosophila sterile hybrid males have shown that spermatogenesis arrest is postmeiotic with few exceptions, and that most misregulated genes are involved in late stages of spermatogenesis. Comparative studies of gene regulation in sterile hybrids and parental species have mainly used microarrays providing a whole genome representation of regulatory problems in sterile hybrids. Real-time PCR studies can reject or reveal differences not observed in microarray assays. Moreover, differences in gene expression between samples can be dependant on the source of RNA (e.g., whole body vs. tissue). Here we survey expression in D. simulans, D. mauritiana and both intra and interspecies hybrids using a real-time PCR approach for eight genes expressed at the four main stages of sperm development. We find that all genes show a trend toward under expression in the testes of sterile hybrids relative to parental species with only the two proliferation genes (bam and bgcn) and the two meiotic class genes (can and sa) showing significant down regulation. The observed pattern of down regulation for the genes tested can not fully explain hybrid male sterility. We discuss the down regulation of spermatogenesis genes in hybrids between closely-related species within the contest of rapid divergence experienced by the male genome, hybrid sterility and possible allometric changes due to subtle testes-specific developmental abnormalities.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Allison DB, Cui X, Page GP, Sabripour M (2006) Microarray data analysis: from disarray to consolidation and consensus. Nat Rev Genet 7:55–65

    Article  CAS  PubMed  Google Scholar 

  • Artieri CG, Haerty W, Singh RS (2007) Association between levels of coding sequence divergence and gene misregulation in Drosophila male hybrids. J Mol Evol 65:697–704

    Article  CAS  PubMed  Google Scholar 

  • Barreau C, Benson E, Gudmannsdottir, Newton F, White-Cooper H (2008) Post-meiotic transcription in Drosophila testes. Development 135:1897–1902

    Article  CAS  PubMed  Google Scholar 

  • Bauer DuMont VL, Flores HA, Wright MH, Aquadro CF (2007) 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 24:182–191

    Article  PubMed  Google Scholar 

  • Catron DJ, Noor MAF (2008) Gene expression disruptions of organism versus organ in Drosophila species hybrids. PLoS ONE 3:e3009

    Article  PubMed  Google Scholar 

  • Civetta A, Singh RS (1995) High divergence of reproductive tract proteins and their association with postzygotic reproductive isolation in Drosophila melanogaster and Drosophila virilis group species. J Mol Evol 41:1085–1095

    Article  CAS  PubMed  Google Scholar 

  • Civetta A, Singh RS (1998) Sex-related genes, directional sexual selection, and speciation. Mol Biol Evol 15:901–909

    CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Coulthart MB, Singh RS (1988) High level of divergence of male-reproductive-tract proteins, between Drosophila melanogaster and its sibling species, D. simulans. Mol Biol Evol 5:182–191

    CAS  PubMed  Google Scholar 

  • Cox DN, Chao A, Lin H (2000) piwi encodes a nucleoplasmic factor whose activity modulates the number and division rate of germline stem cells. Development 127:503–514

    CAS  PubMed  Google Scholar 

  • Dobzhansky Th (1934) Studies on hybrid sterility. I. Spermatogenesis in pure and hybrid Drosophila pseudoobscura. 2 Zellf Mikr Anat 21:169–223

    Article  Google Scholar 

  • Fuller MT (1993) Spermatogenesis. In: Bate M, Martinez-Arias A (eds) The development of Drosophila melanogaster, vol 1. Cold Spring Harbor Press, Cold Spring Harbor, pp 71–147

    Google Scholar 

  • Fuller MT (1998) Genetic control of cell proliferation and differentiation in Drosophila spermatogenesis. Semin Cell Dev Biol 9:433–444

    Article  CAS  PubMed  Google Scholar 

  • Gould-Somero M, Holland L (1974) The timing of RNA synthesis for spermiogenesis in organ cultures of Drosophila melanogaster testes. Wilhelm Roux’s Arch Dev Biol 174:133–148

    Article  CAS  Google Scholar 

  • Gonczy 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

    CAS  PubMed  Google Scholar 

  • Haerty W, Singh RS (2006) Gene regulation divergence is a major contributor to the evolution of Dobzhansky-Muller incompatibilities between species of Drosophila. Mol Biol Evol 23:1707–1714

    Article  CAS  PubMed  Google Scholar 

  • Haerty W, Jagadeeshan S, Kulathinal RJ, Wong A, Ravi Ram K, Sirot LK, Levesque L, Artieri CG, Wolfner MF, Civetta A, Singh RS (2007) Evolution in the fast lane: rapidly evolving sex-related genes in Drosophila. Genetics 177:1321–1335

    Article  CAS  PubMed  Google Scholar 

  • Haldane JBS (1922) Sex ratio and unisexual sterility in animal hybrids. J Genet 12:101–109

    Article  Google Scholar 

  • Hou YC, Chittaranjan S, Barbosa SG, McGall K, Gorski SM (2008) Effector caspase Dcp-1 and IAP protein Bruce regulate starvation-induced autophagy during Drosophila melanogaster oogenesis. J Cell Biol 182:1127–1139

    Article  CAS  PubMed  Google Scholar 

  • Jiang J, White-Cooper H (2003) Transcriptional activation in Drosophila spermatogenesis involves the mutually dependent function of aly and a novel meiotic arrest gene cookie monster. Development 130:563–573

    Article  CAS  PubMed  Google Scholar 

  • Kibbe WA (2007) OligoCalc: an online oligonucleotide properties calculator. Nucleic Acids Res 35:W43–W46

    Article  PubMed  Google Scholar 

  • Kulathinal R, Singh RS (1998) Cytological characterization of premeiotic versus postmeiotic defects producing hybrid male sterility among sibling species of the Drosophila melanogaster complex. Evolution 52:1067–1079

    Article  Google Scholar 

  • Lachaise D, David JR, Lemeunier F, Tsacas L, Asburner M (1986) The reproductive relationships of Drosophila sechellia with D. mauritiana, D. simulans and D. melanogaster from afrotropical regions. Evolution 40:262–271

    Article  Google Scholar 

  • Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948

    Article  CAS  PubMed  Google Scholar 

  • Lawniczak MK, Begun DJ (2004) A genome-wide analysis of courting and mating responses in Drosophila melanogaster females. Genome 47:900–910

    Article  CAS  PubMed  Google Scholar 

  • Lin T-Y, Viswanathan S, Wood C, Wilson PG, Wolf N, Fuller MT (1996) Coordinate developmental control of the meiotic cell cycle and spermatid differentiation in Drosophila males. Development 122:1331–1341

    CAS  PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Malone JH, Chrzanowski TH, Michalak P (2007) Sterility and gene expression in hybrid males of Xenopus laevis and X. muelleri. PLoS One 2:e781

    Article  PubMed  Google Scholar 

  • Manly BJF (1991) Randomization and Monte Carlo methods in biology. Chapman and Hall, London

    Google Scholar 

  • McGregor JR, Xi R, Harrison DA (2002) JAK signaling is somatically required for follicle cell differentiation in Drosophila. Development 129:705–717

    CAS  PubMed  Google Scholar 

  • Michalak P, Noor MAF (2003) Genome-wide patterns of expression in Drosophila pure species and hybrid males. Mol Biol Evol 20:1070–1076

    Article  CAS  PubMed  Google Scholar 

  • Michalak P, Noor MA (2004) Association of misexpression with sterility in hybrids of Drosophila simulans and D. mauritiana. J Mol Evol 59:277–282

    Article  CAS  PubMed  Google Scholar 

  • Michalak P, Ma D (2008) The acylphosphatase (Acyp) alleles associate with male hybrid sterility in Drosophila. Gene 416:61–65

    Article  CAS  PubMed  Google Scholar 

  • Moehring AJ, Teeter KC, Noor MAF (2007) Genome-wide patterns of expression in Drosophila pure species and hybrid males. II. Examination of multiple-species hybridizations, platforms, and life cycle stages. Mol Biol Evol 24:137–145

    Article  CAS  PubMed  Google Scholar 

  • Noor MAF (2005) Patterns of evolution of genes disrupted in expression in Drosophila species hybrids. Genet Res 85:119–125

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Oliveri G, Oliveri A (1965) Autoradiographic study of nucleic acid synthesis during spermatogenesis in Drosophila melanogaster. Mutat Res 2:366–380

    Google Scholar 

  • Pavlidis P, Li Q, Noble WS (2003) The effect of replication on gene expression microarray experiments. Bioinformatics 19:1620–16207

    Article  CAS  PubMed  Google Scholar 

  • Price CS, Kim CH, Gronlund CJ, Coyne JA (2001) Cryptic reproductive isolation in the Drosophila simulans species complex. Evolution 55:81–92

    CAS  PubMed  Google Scholar 

  • Ranz JM, Namgyal K, Gibson G, Hartl DL (2004) Anomalies in the expression profile of interspecific hybrids of Drosophila melanogaster and Drosophila simulans. Genome Res 14:373–379

    Article  CAS  PubMed  Google Scholar 

  • Silver DL, Montell DJ (2001) Paracrine signaling through the JAK/STAT pathway activates invasive behavior of ovarian epithelial cells in Drosophila. Cell 107:831–841

    Article  CAS  PubMed  Google Scholar 

  • Singh RS, Kulathinal RJ (2005) Male sex drive and the masculinization of the genome. Bioessays 27:518–525

    Article  CAS  PubMed  Google Scholar 

  • Thomas S, Singh RS (1992) A comprehensive study of genic variation in natural populations of Drosophila melanogaster. VII. Varying rates of genic divergence as revealed by two-dimensional electrophoresis. Mol Biol Evol 9:507–525

    CAS  PubMed  Google Scholar 

  • Wakimoto BT, Lindsley DL, Herrera C (2004) Toward a comprehensive genetic analysis of male fertility in Drosophila melanogaster. Genetics 167:207–216

    Article  CAS  PubMed  Google Scholar 

  • White-Cooper H, Leroy D, MacQueen A, Fuller MT (2000) Transcription of meiotic cell cycle and terminal differentiation genes depends on a conserved chromatin associated protein, whose nuclear localisation is regulated. Development 127:5463–5473

    CAS  PubMed  Google Scholar 

  • White-Cooper H, Doggett K, Ellis RE (2009) The evolution of spermatogenesis. In: Birkhead TR, Hosken DJ, Pitnick S (eds) Sperm biology: an evolutionary perspective. Elsevier, Oxford, pp 151–183

    Google Scholar 

  • Wong MD, Jin Z, Xie T (2005) Molecular mechanisms of germline stem cell regulation. Annu Rev Genet 39:173–195

    Article  CAS  PubMed  Google Scholar 

  • Wu CI, Perez DE, Davis AW, Johnson NA, Cabot EL et al (1992) Molecular genetic studies of postmating reproductive isolation in Drosophila. In: Takahata N, Clark AG (eds) Molecular Paleo-population biology. Springer, Berlin, pp 191–212

    Google Scholar 

  • You FM, Huo N, Gu YQ, Luo MC, Ma Y, Hane D, Lazo GR, Dvorak J, Anderson OD (2008) BatchPrimer3: a high throughput web application for PCR and sequencing primer design. BMC Bioinformatics 9:253

    Article  PubMed  Google Scholar 

  • Zeng LW, Singh RS (1993) The genetic basis of Haldane’s rule and the nature of asymmetric hybrid male sterility among Drosophila simulans, Drosophila mauritiana and Drosophila sechellia. Genetics 134:251–260

    CAS  PubMed  Google Scholar 

  • Zhang Y, Sturgill D, Parisi M, Kumar S, Oliver B (2007) Constraint and turnover in sex-biased gene expression in the genus Drosophila. Nature 450:233–237

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by funds from a New Opportunities Grant (CFI), an individual Discovery Grant (NSERC) and an RTI Grant (NSERC) to Alberto Civetta. Vignesh Sundararajan was partially supported by University of Winnipeg Graduate Student Assistantship (UWGA) and Manitoba Graduate Scholarship (MGS).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Alberto Civetta.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 9 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sundararajan, V., Civetta, A. Male Sex Interspecies Divergence and Down Regulation of Expression of Spermatogenesis Genes in Drosophila Sterile Hybrids. J Mol Evol 72, 80–89 (2011). https://doi.org/10.1007/s00239-010-9404-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00239-010-9404-5

Keywords

Navigation