Masculinization of Gene Expression Is Associated with Exaggeration of Male Sexual Dimorphism

English version České info

Gene expression differences between the sexes account for the majority of sexually dimorphic phenotypes, and the study of sex-biased gene expression is important for understanding the genetic basis of complex sexual dimorphisms. However, it has been difficult to test the nature of this relationship due to the fact that sexual dimorphism has traditionally been conceptualized as a dichotomy between males and females, rather than an axis with individuals distributed at intermediate points. The wild turkey (Meleagris gallopavo) exhibits just this sort of continuum, with dominant and subordinate males forming a gradient in male secondary sexual characteristics. This makes it possible for the first time to test the correlation between sex-biased gene expression and sexually dimorphic phenotypes, a relationship crucial to molecular studies of sexual selection and sexual conflict. Here, we show that subordinate male transcriptomes show striking multiple concordances with their relative phenotypic sexual dimorphism. Subordinate males were clearly male rather than intersex, and when compared to dominant males, their transcriptomes were simultaneously demasculinized for male-biased genes and feminized for female-biased genes across the majority of the transcriptome. These results provide the first evidence linking sexually dimorphic transcription and sexually dimorphic phenotypes. More importantly, they indicate that evolutionary changes in sexual dimorphism can be achieved by varying the magnitude of sex-bias in expression across a large proportion of the coding content of a genome.

Vyšlo v časopise: Masculinization of Gene Expression Is Associated with Exaggeration of Male Sexual Dimorphism. PLoS Genet 9(8): e32767. doi:10.1371/journal.pgen.1003697
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003697

Souhrn

Zdroje

1. MankJE (2009) Sex chromosomes and the evolution of sexual dimorphism: Lessons from the genome. Am Nat 173(2): 141–150.

2. EllegrenH, ParschJ (2007) The evolution of sex-biased genes and sex-biased gene expression. Nat Rev Genet 8(9): 689–698.

3. CutterAD, WardS (2005) Sexual and temporal dynamics of molecular evolution in C. elegans development. Mol Biol Evol 22 : 178–188.

4. MankJE, Hultin-RosenbergL, AxelssonE, EllegrenH (2007) Rapid evolution of female-biased, but not male-biased, genes expressed in the avian brain. Mol Biol Evol 24(12): 2698–2706.

5. RanzJM, Castillo-DavisCI, MeiklejohnCD, HartlDL (1997) Sex-dependent gene expression and the evolution of the Drosophila transcriptome. Science 300 : 1742–1745.

6. ReiniusB, SaetreP, LeonardJA, BlekhmanR, Merino-MartinezR, et al. (2008) An evolutionary conserved sexual signature in the primate brain. PLoS Genet 4(6): e1000100.

7. YangX, SchadtEE, WangS, WangH, ArnoldAP, et al. (2006) Tissue-specific expression and regulation of sexually dimorphic genes in mice. Genome Res 16(8): 995–1004.

8. MagnussonK, MendesAM, WindbichlerN, PapathanosP-A, NolanT, et al. (2011) Transcription regulation of sex-biased genes during ontogeny in the malaria vector Anopheles gambiae. PLoS One 6(6): e21572.

9. MankJE, NamK, BrunströmB, EllegrenH (2010) Ontogenetic complexity of sexual dimorphism and sex-specific selection. Mol Biol Evol 27(7): 1570–1578.

10. OmettoL, ShoemakerD, RossKG, KellerL (2011) Evolution of gene expression in fire ants: the effects of developmental stage, caste, and species. Mol Biol Evol 28(4): 1381–1392.

11. ZhangY, SturgillD, ParisiM, KumarS, OliverB (2007) Constraint and turnover in sex-biased gene expression in the genus Drosophila. Nature 450 : 233–238.

12. BuchholzR (1995) Female choice, parasite load and male ornamentation in Wild Turkeys. Anim Behav 50 : 929–943.

13. BuchholzR (1997) Male dominance and variation in fleshy head ornamentation in Wild Turkeys. J Avian Biol 28 : 223–230.

14. HillG, DoucetS, BuchholzR (1997) The effect of coccidial infection on iridescent plumage coloration in wild turkeys. Anim Behav 69 : 387–394.

15. WattsCR, StokesAW (1971) The social order of turkeys. Science 224 : 112–118.

16. KrakauerAH (2005) Kin selection and cooperative courtship in wild turkeys. Nature 434 : 69–72.

17. KrakauerAH (2008) Sexual selection and the genetic mating system of Wild Turkeys. Condor 110(1): 1–12.

18. HamiltonWD (1964) The genetical evolution of social behaviour. I J Theor Biol 7(1): 1–16.

19. MankJE, Hultin-RosenbergL, WebsterMT, EllegrenH (2008) The unique genomic properties of sex-biased genes: Insights from avian microarray data. BMC Genomics 9 : 148.

20. KirkpatrickM, HallDW (2004) Male-biased mutation, sex linkage, and the rate of adaptive evolution. Evolution 58(2): 437–440.

21. ItohY, ReplogleK, KimYH, WadeJ, ClaytonDF, et al. (2010) Sex bias and dosage compensation in the zebra finch versus chicken genomes: general and specialized patterns among birds. Genome Res 20(4): 512–518.

22. ConnallonT, KnowlesLL (2005) Intergenomic conflict revealed by patterns of sex-biased gene expression. Trends Genet 21(9): 495–499.

23. StoneD, HechterO (1055) Studies on ACTH action in perfused bovine adrenals: aspects of progesterone as an intermediary in corticosteroidogenesis. Arch Biochem Biophys 54 : 121.

24. HalkerstonIDK, EichhornJ, HechterOA (1961) Requirement for reduced triphosphopyridine nucleotide for cholesterol side-chain cleavage by mitochondrial fractions of bovine adrenal cortex. J Biol Chem 236 : 374.

25. GharaniN, WaterworthDM, BattyS, WhiteD, Gilling-SmithC, et al. (1997) Association of the steroid synthesis gene CYP11a with polycystic ovary syndrome and hyperandrogenism. Hum Mol Genet 6 : 397–402.

26. KatsumataN, OhtakeM, HojoT, OgawaE, HaraT, et al. (2002) Compound heterozygous mutations in the cholesterol side-chain cleavage enxyme gene (CYP11A) cause congential adrenal insufficiency in humans. J Clin Endocrinol Metab 87 : 3808–3813.

27. StewartAD, PischeddaA, RiceWR (2010) Resolving intralocus sexual conflict: genetic chanisms and time frame. J Heredity 101: S94–S99.

28. LuP, VogelC, WangR, YaoX, MarcotteEM (2007) Absolute protein expression profiling estimates the relative contribution of transcriptional and translational regulation. Nature Biotechnology 25 : 117–124.

29. MankJE, AviseJC (2006) Comparative phylogenetic analysis of male alternative reproductive tactics. Evolution 60 : 1311–1316.

30. LohseM, BolgerAM, NagelA, FernieAR, LunnJE, et al. (2012) RobiNA: a user-friendly, integrated software solution for RNA-Seq-based transcriptomics. Nucleic Acids Res 40 : 622–627.

31. DalloulRA, LongJA, ZiminAV, AslamL, BealK, et al. (2012) Multi-Platform Next-Generation Sequencing of the Domestic Turkey Meleagris gallopavo: Genome Assembly and Analysis. PLoS Biol 8(9): e1000475.

32. FlicekP, AmodeMR, BarrellD, BealK, BrentS, et al. (2012) Ensembl 2012. Nucleic Acids Res 40(D1): D84–D90.

33. LiB, DeweyC (2011) RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics 12(1): 323.

34. LangmeadB, TrapnellC, PopM, SalzbergS (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Gen Biol 10(3): R25.

35. HarrisonPW, MankJE, WedellN (2012) Incomplete sex chromosome dosage compensation in the Indian meal moth Plodia interpunctella, based on de novo transcriptome assembly. Genome Biol Evol 4 : 1118–1126.

36. MoghadamHK, HarrisonPW, ZacharG, SzekelyT, MankJE (2013) The plover neurotranscriptome assembly: Transcriptomic analysis in an ecological model species without a reference genome. Molecular Ecology Resources 3 : 696–705.

37. MortazaviA, WilliamsBA, McCueK, SchaefferL, WoldB (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Meth 5 : 621–628.

38. AndersS, HuberW (2010) Differential expression analysis for sequence count data. Genome Biol 11: R106.

39. de HoonMJ, ImotoS, NolanJ, MiyanoS (2004) Open source clustering software. Bioinformatics 20 : 1453–1454.

40. SaldanhaAJ (2004) Java Treeview -⁠ extensible visualization of microarray data. Bioinformatics 20 : 3246–3248.

41. SuzukiR, ShimodairaH (2006) Pvclust: An R package for assessing the uncertainty in hierarchical clustering. Bioinformatics 22 : 1540–1542.

42. WrightAE, MoghadamHK, MankJE (2012) Trade-off between selection for dosage compensation and masculinisation on the avian Z chromosome. Genetics 192 : 1433–1445.

43. MankJE, EllegrenH (2009) Sex-linkage of sexually antagonistic genes is predicted by female, but not male, effects in birds. Evolution 63(6): 1464–1472.

44. BenjaminiY, HochbergY (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Roy Stat Soc B 57(1): 289–300.

45. EdenE, NavonR, SteinfeldI, LipsonD, YakhiniZ (2009) GOrilla: A tool for discovery and visualization of enriched GO terms in ranked gene lists. BMC Bioinformatics 10 : 48.

46. EdenE, LipsonD, YogevS, YakhiniZ (2007) Discovering motifs in ranked lists of DNA sequences. PLoS Computational Biol 3(3): e39.

47. LechnerM, FindeiβS, SteinerL, MarzM, StadlerPF, et al. (2011) Proteinortho: Detection of (Co-)orthologs in large-scale analysis. BMC Bioinformatics 12 : 124.

48. GoughJ, KarplusK, HughevR, ChothiaC (2001) Assignment of homology to genome sequences using a library of hidden markov models that represent all proteins of known structure. J Mol Biol 313(4): 903–919.

49. YangZ (2007) PAML 4: Phylogenetic analysis by maximum likelihood. Mol Biol Evol 24 : 1586–1591.

50. AxelssonE, Hultin-RosenbergL, BrandströmM, ZwahlénM, ClaytonDF, et al. (2008) Natural selection in avian protein-coding genes expressed in brain. Mol Ecol 17(12): 3008–3017.

51. SubramanianA, TamayoP, MoothaVK, MukherjeeS, EbertBL, et al. Gene set enrichment analysis: A knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci USA 102(48): 15545–15550.