Developmental Link between Sex and Nutrition; Regulates Sex-Specific Mandible Growth via Juvenile Hormone Signaling in Stag Beetles

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Sexual dimorphisms in trait expression are widespread among animals and are especially pronounced in ornaments and weapons of sexual selection, which can attain exaggerated sizes. Expression of exaggerated traits is usually male-specific and nutrition sensitive. Consequently, the developmental mechanisms generating sexually dimorphic growth and nutrition-dependent phenotypic plasticity are each likely to regulate the expression of extreme structures. Yet we know little about how either of these mechanisms work, much less how they might interact with each other. We investigated the developmental mechanisms of sex-specific mandible growth in the stag beetle Cyclommatus metallifer, focusing on doublesex gene function and its interaction with juvenile hormone (JH) signaling. doublesex genes encode transcription factors that orchestrate male and female specific trait development, and JH acts as a mediator between nutrition and mandible growth. We found that the Cmdsx gene regulates sex differentiation in the stag beetle. Knockdown of Cmdsx by RNA-interference in both males and females produced intersex phenotypes, indicating a role for Cmdsx in sex-specific trait growth. By combining knockdown of Cmdsx with JH treatment, we showed that female-specific splice variants of Cmdsx contribute to the insensitivity of female mandibles to JH: knockdown of Cmdsx reversed this pattern, so that mandibles in knockdown females were stimulated to grow by JH treatment. In contrast, mandibles in knockdown males retained some sensitivity to JH, though mandibles in these individuals did not attain the full sizes of wild type males. We suggest that moderate JH sensitivity of mandibular cells may be the default developmental state for both sexes, with sex-specific Dsx protein decreasing sensitivity in females, and increasing it in males. This study is the first to demonstrate a causal link between the sex determination and JH signaling pathways, which clearly interact to determine the developmental fates and final sizes of nutrition-dependent secondary-sexual characters.

Vyšlo v časopise: Developmental Link between Sex and Nutrition; Regulates Sex-Specific Mandible Growth via Juvenile Hormone Signaling in Stag Beetles. PLoS Genet 10(1): e32767. doi:10.1371/journal.pgen.1004098
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004098

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Zdroje

1. WilliamsTM, CarrollSB (2009) Genetic and molecular insights into the development and evolution of sexual dimorphism. Nat Rev Genet 10: 797–804.

2. GempeT, BeyeM (2011) Function and evolution of sex determination mechanisms, genes and pathways in insects. Bioessays 33: 52–60.

3. EmlenDJ, WarrenIA, JohnsA, DworkinI, LavineLC (2012) A mechanism of extreme growth and reliable signaling in sexually selected ornaments and weapons. Science 337: 860–864.

4. EmlenDJ (2008) The evolution of animal weapons. Annu Rev Ecol Evol Syst 39: 387–413.

5. GotohH, CornetteR, KoshikawaS, OkadaY, LavineLC, et al. (2011) Juvenile hormone regulates extreme mandible growth in male stag beetles. PLoS ONE 6(6): e21139 Available: http://www.plosone.org/article/info%3Adoi%2F10.1371%2Fjournal.pone.0021139.

6. Andersson M (1994) Sexual Selection. Princeton: Princeton Univ. Press.

7. KnellRJ, FruhaufN, NorrisKA (1999) Conditional expression of a sexually selected trait in the stalk-eyed fly Diasemopsis aethiopica. Ecol Entomol 24: 323–328.

8. EmlenDJ, NijhoutHF (2000) The development and evolution of exaggerated morphologies in insects. Annu Rev Entomol 45: 661–708.

9. CottonS, FowlerK, PomiankowskiA (2004) Do sexual ornaments demonstrate heightened condition-dependent expression as predicted by the handicap hypothesis? Proc R Soc Lond B Biol Sci 271: 771–783.

10. EmlenDJ, SzafranQ, CorleyLS, DworkinI (2006) Insulin signaling and limb-patterning: candidate pathways for the origin and evolutionary diversification of beetle ‘horns’. Heredity 97: 179–191.

11. KotiahoJS (2000) Testing the assumptions of conditional handicap theory: costs and condition dependence of a sexually selected trait. Behav Ecol Sociobiol 48: 188–194.

12. BondurianskyR, RoweL (2005) Intralocus sexual conflict and the genetic architecture of sexually dimorphic traits in Prochyliza xanthostoma (Diptera: Piophilidae). Evolution 59: 1965–1975.

13. KoppA (2012) Dmrt genes in the development and evolution of sexual dimorphism. Trends Genet 28: 175–184.

14. MatsonCK, ZarkowerD (2012) Sex and the singular DM domain: insights into sexual regulation, evolution and plasticity. Nat Rev Genet 13: 163–174.

15. ClineTW, MeyerBJ (1996) Vive la difference: males vs females in flies vs worms. Annu Rev Genet 30: 637–702.

16. OhbayashiF, SuzukiMG, MitaK, OkanoK, ShimadaT (2001) A homologue of the Drosophila doublesex gene is transcribed into sex-specific mRNA isoforms in the silkworm, Bombyx mori. Comp Biochem Physiol B Biochem Mol Biol 128: 145–158.

17. SuzukiMG, FunagumaS, KandaT, TamuraT, ShimadaT (2005) Role of the male BmDSX protein in the sexual differentiation of Bombyx mori. Evol Dev 7: 58–68.

18. HasselmannM, GempeT, SchiøttM, Nunes-SilvaCG, OtteM, et al. (2008) Evidence for the evolutionary nascence of a novel sex determination pathway in honeybees. Nature 454: 519–522.

19. HedigerM, HenggelerC, MeierN, PerezR, SacconeG, et al. (2010) Molecular characterization of the key switch F provides a basis for understanding the rapid divergence of the sex-determining pathway in the housefly. Genetics 184: 155–170.

20. KijimotoT, MoczekAP, AndrewsJ (2012) Diversification of doublesex function underlies morph-, sex-, and species-specific development of beetle horns. Proc Natl Acad Sci U S A 109: 20526–20531.

21. ShuklaJN, PalliSR (2012) Doublesex target genes in the red flour beetle, Tribolium castaneum. Sci Rep 2: 00948 Available: http://www.nature.com/srep/2012/121210/srep00948/full/srep00948.html.

22. ItoY, HarigaiA, NakataM, HosoyaT, ArayaK, et al. (2013) The role of doublesex in the evolution of exaggerated horns in the Japanese rhinoceros beetle. EMBO Rep 14: 561–567.

23. ErdmanSE, ChenHJ, BurtisKC (1996) Functional and genetic characterization of the oligomerization and DNA binding properties of the Drosophila doublesex proteins. Genetics 144: 1639–1652.

24. BakerBS, WolfnerMF (1988) A molecular analysis of doublesex, a bifunctional gene that controls both male and female sexual differentiation in Drosophila melanogaster. Genes Dev 2: 477–489.

25. BurtisKC, BakerBS (1989) Drosophila doublesex gene controls somatic sexual differentiation by producing alternatively spliced mRNAs encoding related sex-specific polypeptides. Cell 56: 997–1010.

26. ValenaS, MoczekAP (2012) Epigenetic mechanisms underlying developmental plasticity in horned beetles. Genet Res Int 2012 Article ID 576303. Available: http://dx.doi.org/10.1155/2012/576303.

27. Darwin C (1871) The descent of man and selection in relation to sex. London: John Murray.

28. HuxleyJS (1931) Relative growth of mandibles in stag beetles (Lucanidae). J Linn Soc Lond 37: 675–703.

29. HosoyaT, ArayaK (2005) Phylogeny of Japanese stag beetle (Coleoptera: Lucanidae) inferred from 16S mtrRNA gene sequences, with reference to the evolution of sexual dimorphism of mandibles. Zool Sci 22: 1305–1318.

30. KawanoK (2006) Sexual dimorphism and the making of oversized male characters in beetles (Coleoptera). Ann Entomol Soc Am 99: 327–341.

31. Kodric-BrownA, SiblyRM, BrownJH (2006) The allometry of ornaments and weapons. Proc Natl Acad Sci U S A 103: 8733–8738.

32. Fujita H (2010) The Lucanid Beetles of the world. Tokyo: Mushi-sha. (In Japanese).

33. GotohH, FukayaK, MiuraT (2012) Heritability of male mandible length in the stag beetle Cyclommatus metallifer. Entomol Sci 15: 430–433.

34. OliveiraDCSG, WerrenJH, VerhulstEC, GiebelJD, KampingA, et al. (2009) Identification and characterization of the doublesex gene on Nasonia. Insect Mol Biol 18: 315–324.

35. BayrerJR, ZhangW, WeissMA (2005) Dimerization of doublesex is mediated by a cryptic ubiquitin-associated domain fold: implications for sex-specific gene regulation. J Biol Chem 280: 32989–32996.

36. RobinettCC, VaughanAG, KnappJM, BakerBS (2010) Sex and the single cell. II. There is a time and place for sex. PLoS Biol 8(5): e1000365 Available: http://www.plosbiology.org/article/info%3Adoi%2F10.1371%2Fjournal.pbio.1000365.

37. TanakaK, BarminaO, SandersLE, ArbeitmanMN, KoppA (2011) Evolution of sex-specific traits through changes in HOX-Dependent doublesex expression. PLoS Biol 9(8): e1001131 Available: http://www.plosbiology.org/article/info%3Adoi%2F10.1371%2Fjournal.pbio.1001131.

38. Nijhout HF (1994) Insect hormones. Princeton: Princeton Univ. Press.

39. EmlenDJ, NijhoutHF (1999) Hormonal control of male horn length dimorphism in the dung beetle Onthophagus Taurus (Coleoptera: Scarabaeidae). J Insect Physiol 45: 45–53.

40. FryCL (2006) Juvenile hormone mediates a trade-off between primary and secondary sexual traits in stalk-eyed flies. Evol Dev 8: 191–201.

41. NiitsuS, LobbiaS, KamitoT (2011) In vitro effects of juvenile hormone analog on wing disc morphogenesis under ecdysteroid treatment in the female-wingless bagworm moth Eumeta variegate (Insecta: Lepidoptera, Psychidae). Tissue Cell 43: 143–150.

42. ShingletonAW, DasJ, ViniciusL, SternDL (2005) The temporal requirements for insulin signaling during development in Drosophila. PLoS Biol 3(9): e289 Available: http://www.plosbiology.org/article/info%3Adoi%2F10.1371%2Fjournal.pbio.0030289.

43. EdgarBA (2006) How flies get their size: Genetics meets physiology. Nat Rev Genet 7: 907–916.

44. TangHY, Smith-CaldasMSB, DriscollMV, SalhadarS, ShingletonAW (2011) FOXO regulates organ-specific phenotypic plasticity in Drosophila. PLoS Genet 7(11): e1002373 Available: http://www.plosgenetics.org/article/info%3Adoi%2F10.1371%2Fjournal.pgen.1002373.

45. LarkinMA, BlackshieldsG, BrownNP, ChennaR, McGettiganPA, et al. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947–2948.

46. R Core Team (2012) R: A language and environment for statistical computing, R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0. Available: http://R-project.org/.

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