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Differential Expression of Ecdysone Receptor Leads to Variation in Phenotypic Plasticity across Serial Homologs


One of the most exquisite types of organismal adaptations in nature occurs when organisms are able to change the way they develop in anticipation of the different selective environments they will experience as adults. This leads to variation in adult morphologies that are adaptive. Environmental cues experienced during development often lead to variation in hormonal titers that can have profound effect on the way genes are regulated and on the adult morphology. Here we examine the hormonal and molecular mechanisms that allow specific traits that are repeated in an organism (butterfly eyespots) to either be sensitive to environmental cues–and develop different morphologies—or insensitive to these cues and develop the same morphology. We discover that a specific gene, a hormone receptor, that is expressed in the sensitive eyespots but absent in the insensitive eyespots, is responsible for regulating the level of sensitivity of each of the eyespots to an environmental cue. We identify a molecule that is regulating levels of environmental sensitivity, or phenotypic plasticity, across repeated traits in an organism.


Vyšlo v časopise: Differential Expression of Ecdysone Receptor Leads to Variation in Phenotypic Plasticity across Serial Homologs. PLoS Genet 11(9): e32767. doi:10.1371/journal.pgen.1005529
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005529

Souhrn

One of the most exquisite types of organismal adaptations in nature occurs when organisms are able to change the way they develop in anticipation of the different selective environments they will experience as adults. This leads to variation in adult morphologies that are adaptive. Environmental cues experienced during development often lead to variation in hormonal titers that can have profound effect on the way genes are regulated and on the adult morphology. Here we examine the hormonal and molecular mechanisms that allow specific traits that are repeated in an organism (butterfly eyespots) to either be sensitive to environmental cues–and develop different morphologies—or insensitive to these cues and develop the same morphology. We discover that a specific gene, a hormone receptor, that is expressed in the sensitive eyespots but absent in the insensitive eyespots, is responsible for regulating the level of sensitivity of each of the eyespots to an environmental cue. We identify a molecule that is regulating levels of environmental sensitivity, or phenotypic plasticity, across repeated traits in an organism.


Zdroje

1. Rueffler C, Hermisson J, Wagner GP. Evolution of functional specialization and division of labor. Proc Natl Acad Sci U S A. 2012;109(6):E326–E35. doi: 10.1073/pnas.1110521109 22308336

2. Weatherbee SD, Halder G, Kim J, Hudson A, Carroll SB. Ultrabithorax regulates genes at several levels of the wing-patterning hierarchy to shape the development of the Drosophila haltere. Gen Dev. 1998;12(10):1474–82.

3. Averof M, Patel NH. Crustacean appendage evolution associated with changes in Hox gene expression. Nature. 1997;388(6643):682–6. ISI:A1997XQ86300051.

4. Liubicich DM, Serano JM, Pavlopoulos A, Kontarakis Z, Protas ME, Kwan E, et al. Knockdown of Parhyale Ultrabithorax recapitulates evolutionary changes in crustacean appendage morphology. Proc Natl Acad Sci U S A. 2009;106(33):13892–6. doi: 10.1073/pnas.0903105106 19666517

5. Moran NA. The evolutionary maintenance of alternative phenotypes. Am Nat. 1992;139(5):971–89. ISI:A1992HU07100005.

6. Oliver JC, Tong X, Gall LF, Piel WH, Monteiro A. A single origin for nymphalid butterfly eyespots followed by widespread loss of associated gene expression. PLoS Genet. 2012;8(8):e1002893. doi: 10.1371/journal.pgen.1002893 22916033

7. Oliver JC, Beaulieu JM, Gall LF, Piel WH, Monteiro A. Nymphalid eyespot serial homologs originate as a few individualized modules. Proc R Soc Lond B. in review.

8. Schachat SR, Oliver JC, Monteiro A. Nymphalid eyespots are co-opted to novel wing locations following a similar pattern in independent lineages. BMC Evol Biol. 2015;15(1):300.

9. Olofsson M, Vallin A, Jakobsson S, Wiklund C. Marginal eyespots on butterfly wings deflect bird attacks under low light intensities with UV wavelengths. PloS ONE. 2010;5(5):e10798. doi: 10.1371/journal.pone.0010798 20520736

10. Robertson KA, Monteiro A. Female Bicyclus anynana butterflies choose males on the basis of their UV-reflective dorsal eyespot pupils. Proc R Soc B. 2005;272 1541–6. 16048768

11. Vallin A, Jakobsson S, Lind J, Wiklund C. Prey survival by predator intimidation: an experimental study of peacock butterfly defence against blue tits. Proc R Soc B. 2005;272(1569):1203–7. ISI:000230563200002.

12. Oliver JC, Robertson KA, Monteiro A. Accomodating natural and sexual selection in butterfly wing pattern evolution. Proc R Soc B. 2009;276:2369–75. doi: 10.1098/rspb.2009.0182 19364741

13. Kodandaramaiah U. The evolutionary significance of butterfly eyespots. Behav Ecol. 2011.

14. Brakefield PM, Larsen TB. The evolutionary significance of dry and wet season forms in some tropical butterflies. Biol J Linn Soc. 1984;22:1–12.

15. Brakefield PM, Reitsma N. Phenotypic plasticity, seasonal climate and the population biology of Bicyclus butterflies (Satyridae) in Malawi. Ecol Entomol. 1991;16:291–303.

16. Brakefield PM, Frankino WA. Polyphenisms in Lepidoptera: Multidisciplinary approaches to studies of evolution and development. In: Whitman DW, Ananthakrishnan TN, editors. Phenotypic Plasticity in Insects Mechanisms and Consequences. Plymouth: Science Publishers; 2009. p. 281–312.

17. Prudic KL, Stoehr AM, Wasik BW, Monteiro A. Invertebrate predators attack eyespots and promote the evolution of phenotypic plasticity. Proc Biol Sci. 2015;282(1798):20141531. doi: 10.1098/rspb.2014.1531 25392465

18. Nijhout HF. Control mechanisms of polyphenic development in insects. Bioscience. 1999;49(3):181–92.

19. Simpson SJ, Sword GA, Lo N. Polyphenism in Insects. Curr Biol. 2011;21(18):R738–R49. doi: 10.1016/j.cub.2011.06.006 21959164

20. Windig JJ. Reaction norms and the genetic-basis of phenotypic plasticity in the wing pattern of the butterfly Bicyclus anynana. J Evol Biol. 1994;7(6):665–95.

21. Ghiradella H. Structure and Development of Iridescent Butterfly Scales—Lattices and Laminae. J Morphol. 1989;202(1):69–88. ISI:A1989AV85800005.

22. Vukusic P, Sambles JR, Lawrence CR, Wootton RJ. Quantified interference and diffraction in single Morpho butterfly scales. Proc R Soc B. 1999;266(1427):1403–11. ISI:000081833200001.

23. Jindra M, Malone F, Hiruma K, Riddiford LM. Developmental profiles and ecdysteroid regulation of the mRNAs for two ecdysone receptor isoforms in the epidermis and wings of the tobacco hornworm, Manduca sexta. Dev Biol. 1996;180(1):258–72. ISI:A1996VW70000020.

24. Koch PB, Merk R, Reinhardt R, Weber P. Localization of ecdysone receptor protein during colour pattern formation in wings of the butterfly Precis coenia (Lepidoptera: Nymphalidae) and co-expression with Distal-less protein. Dev Genes Evol. 2003;212(12):571–84. 12536321.

25. Zera AJ. Endocrine analysis in evolutionary-developmental studies of insect polymorphism: hormone manipulation versus direct measurement of hormonal regulators. Evol Dev. 2007;9(5):499–513. ISI:000249321200009.

26. Dinan L, Whiting P, Girault JP, Lafont R, Dhadialla TS, Cress DE, et al. Cucurbitacins are insect steroid hormone antagonists acting at the ecdysteroid receptor. Biochem J. 1997;327:643–50. ISI:A1997YF86500003.

27. Oliver JC, Ramos DM, Prudic KL, Monteiro A. Temporal gene expression variation associated with eyespot size plasticity in Bicyclus anynana. PloS ONE. 2013;8(6):e65830. doi: 10.1371/journal.pone.0065830 23762437

28. Snell-Rood EC, Moczek AP. Insulin Signaling as a Mechanism Underlying Developmental Plasticity: The Role of FOXO in a Nutritional Polyphenism. PloS ONE. 2012;7(4).

29. Tang HY, Smith-Caldas MSB, Driscoll MV, Salhadar S, Shingleton AW. FOXO Regulates Organ-Specific Phenotypic Plasticity In Drosophila. PLoS Genet. 2011;7(11).

30. Emlen DJ, Warren IA, Johns A, Dworkin I, Lavine LC. A Mechanism of Extreme Growth and Reliable Signaling in Sexually Selected Ornaments and Weapons. Science. 2012;337(6096):860–4. doi: 10.1126/science.1224286 22837386

31. Hyun S. Body size regulation and insulin-like growth factor signaling. Cellular and Molecular Life Sciences. 2013;70(13):2351–65. doi: 10.1007/s00018-013-1313-5 23508807

32. Koch PB, Buckmann D. Hormonal-control of seasonal morphs by the timing of ecdysteroid release in Arashnia levana L (Nymphalidae, Lepidoptera). J Insect Physiol. 1987;33(11):823–9. ISI:A1987K176700006.

33. Rountree DB, Nijhout HF. Hormonal control of a seasonal polyphenism in Precis coenia (Lepidoptera: Nymphalidae). J Insect Physiol. 1995;41(11):987–92.

34. Brakefield PM, Kesbeke F, Koch PB. The regulation of phenotypic plasticity of eyespots in the butterfly Bicyclus anynana. Am Nat. 1998;152:853–60. doi: 10.1086/286213 18811432

35. Koch PB, Brakefield PM, Kesbeke F. Ecdysteroids control eyespot size and wing color pattern in the polyphenic butterfly Bicyclus anynana (Lepidoptera, Satyridae). J Insect Physiol. 1996;42:223–30.

36. Kooi RE, Brakefield PM. The critical period for wing pattern induction in the polyphenic tropical butterfly Bicyclus anynana (Satyrinae). J Insect Physiol. 1999;45(3):201–12. 12770367.

37. Oostra V, de Jong MA, Invergo BM, Kesbeke F, Wende F, Brakefield PM, et al. Translating environmental gradients into discontinuous reaction norms via hormone signalling in a polyphenic butterfly. Proceedings of the Royal Society B-Biological Sciences. 2011;278(1706):789–97.

38. Zijlstra WG, Steigenga MJ, Koch PB, Zwaan BJ, Brakefield PM. Butterfly selected lines explore the hormonal basis of interactions between life histories and morphology. Am Nat. 2004;163(5):E76–87. 15122496

39. Mateus ARA, Marques-Pita M, Oostra V, Lafuente E, Brakefield PM, Zwaan BJ, et al. Adaptive developmental plasticity: Compartmentalized responses to environmental cues and to corresponding internal signals provide phenotypic flexibility. Bmc Biology. 2014;12.

40. Monteiro A, Prudic KL. Multiple approaches to study color pattern evolution in butterflies. Trends in Evolutionary Biology. 2010;2:e2.

41. Monteiro A, Chen B, Ramos DM, Oliver JC, Tong X, Guo M, et al. Distal-less regulates eyespot patterns and melanization in Bicyclus butterflies. J Exp Zool Part B. 2013;320(5):321–31.

42. Tomoyasu Y, Wheeler SR, Denell RE. Ultrabithorax is required for membranous wing identity in the beetle Tribolium castaneum. Nature. 2005;433(7026):643–7. 15703749

43. Weatherbee SD, Halder G, Kim J, Hudson A, Carroll S. Ultrabithorax regulates genes at several levels of the wing-patterning hierarchy to shape the development of the Drosophila haltere. Gen Dev. 1998;12(10):1474–82.

44. Cherbas L, Lee K, Cherbas P. Identification of ecdysone response elements by analysis of the Drosophila Eip28/29 gene. Genes Dev. 1991;5(1):120–31. 1899227

45. Zera AJ, Zhao ZW. Morph-associated JH titer diel rhythm in Gryllus firmus: Experimental verification of its circadian basis and cycle characterization in artificially selected lines raised in the field. J Insect Physiol. 2009;55(5):450–8. doi: 10.1016/j.jinsphys.2008.11.012 19100744

46. Davidowitz G, Nijhout HF. The physiological basis of reaction norms: The interaction among growth rate, the duration of growth and body size. Integrative and Comparative Biology. 2004;44(6):443–9. doi: 10.1093/icb/44.6.443 21676730

47. Westerlund SA, Hoffmann KH. Rapid quantification of juvenile hormones and their metabolites in insect haemolymph by liquid chromatography-mass spectrometry (LC-MS). Anal Bioanal Chem. 2004;379(3):540–3. 15057500

48. Brunetti CR, Selegue JE, Monteiro A, French V, Brakefield PM, Carroll SB. The generation and diversification of butterfly eyespot color patterns. Curr Biol. 2001;11:1578–85. 11676917

49. Stoehr AM, Walker JF, Monteiro A. Spalt expression and the development of melanic color patterns in pierid butterflies. EvoDevo 2013;4:6 doi: 10.1186/2041-9139-4-6 23419038

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Genetika Reprodukčná medicína

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PLOS Genetics


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