Downregulation of the evolutionary capacitor hsp90 is mediated by social cues

Proceedings of the Royal Society B: Biological Sciences

Volumn 282, Issue 1819, 2015, Pages

  Peuß, Robert ^a   Eggert, Hendrik ^a   Armitage, Sophie A O ^a   Kurtz, Joachim ^a  

^a UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

Canalization; Heat shock proteins; Hsp90; Immune defence; Stress; Tribolium castaneum

Indexed keywords

BEETLE; CANALIZATION (BIOLOGY); ENVIRONMENTAL CUE; ENVIRONMENTAL STRESS; ENZYME ACTIVITY; GENE EXPRESSION; GENETIC VARIATION; HEAT SHOCK; IMMUNE SYSTEM; MOLECULAR ANALYSIS; PROTEIN;

COLEOPTERA; HEXAPODA; TRIBOLIUM CASTANEUM;

HEAT SHOCK PROTEIN 90; INSECT PROTEIN; MONOPHENOL MONOOXYGENASE;

ANIMAL; ASSOCIATION; DOWN REGULATION; ENZYMOLOGY; FEMALE; GENETICS; MALE; METABOLISM; PHYSIOLOGY; SOCIAL BEHAVIOR; TRIBOLIUM;

ANIMALS; CUES; DOWN-REGULATION; FEMALE; HSP90 HEAT-SHOCK PROTEINS; INSECT PROTEINS; MALE; MONOPHENOL MONOOXYGENASE; SOCIAL BEHAVIOR; TRIBOLIUM;

EID: 84947570780     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2015.2041     Document Type: Article

References (57)

1. Darwin C. 1859 On the origin of species by means of natural selection, or the preservation of favoured races in the struggle for life. London, UK: John Murray
2. Fisher RA. 1930 The genetical theory of natural selection. Oxford, UK: Clarendon Press
3. Waddington CH. 1942 Canalization of development and the inheritance of acquired characters. Nature 150, 563–565. (doi:10.1038/150563a0)
4. Wagner GP, Altenberg L. 1996 Perspective: complex adaptations and the evolution of evolvability. Evolution 50, 967–976. (doi:10.2307/2410639)
5. Wagner A. 2008 Robustness and evolvability: a paradox resolved. Proc. R. Soc. B 275, 91–100. (doi:10.1098/rspb.2007.1137)
6. Masel J, Trotter MV. 2010 Robustness and evolvability. Trends Genet. 26, 406–414. (doi:10.1016/j.tig.2010.06.002)
7. Pigliucci M. 2008 Is evolvability evolvable? Nat. Rev. Genet. 9, 75–82. (doi:10.1038/nrg2278)
8. Becker J, Craig EA. 1994 Heat-shock proteins as molecular chaperones. Eur. J. Biochem. 219, 11–23. (doi:10.1111/j.1432-1033.1994.tb19910.x)
9. Feder ME, Hofmann GE. 1999 Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu. Rev. Physiol. 61, 243–282. (doi:10.1146/annurev.physiol.61.1.243)
10. Benoit JB, Lopez-Martinez G. 2012 Role of conventional and unconventional stress proteins during the response of insects to traumatic environmental conditions, pp. 128–160. Sharjah, United Arab Emirates: Bentham Science Publishers
11. Rutherford SL. 2003 Between genotype and phenotype: protein chaperones and evolvability. Nature Rev. Genet. 4, 263–274. (doi:10.1038/nrg1041)
12. Le Rouzic A, Carlborg Ö. 2008 Evolutionary potential of hidden genetic variation. Trends Ecol. Evol. 23, 33–37. (doi:10.1016/j.tree.2007.09.014)
13. Rutherford SL, Lindquist S. 1998 Hsp90 as a capacitor for morphological evolution. Nature 396, 336–342. (doi:10.1038/24550)
14. Rohner N, Jarosz DF, Kowalko JE, Yoshizawa M, Jeffery WR, Borowsky RL, Lindquist S, Tabin CJ. 2013 Cryptic variation in morphological evolution: HSP90 as a capacitor for loss of eyes in cavefish. Science 342, 1372–1375. (doi:10.1126/science.1240276)
15. Specchia V, Piacentini L, Tritto P, Fanti L, D’Alessandro R, Palumbo G, Pimpinelli S, Bozzetti MP. 2010 Hsp90 prevents phenotypic variation by suppressing the mutagenic activity of transposons. Nature 463, 662–665. (doi:10.1038/nature08739)
16. Chen B, Wagner A. 2012 Hsp90 is important for fecundity, longevity, and buffering of cryptic deleterious variation in wild fly populations. BMC Evol. Biol. 12, 25. (doi:10.1186/1471-2148-12-25)
17. Sgró CM, Wegener B, Hoffmann A. 2010 A naturally occurring variant of Hsp90 that is associated with decanalization. Proc. R. Soc. B 277, 2049–2057. (doi:10.1098/rspb.2010.0008)
18. Siegal ML, Masel J. 2012 Hsp90 depletion goes wild. BMC Biol. 10, 14. (doi:10.1186/1741-7007-10-14)
19. Ketola T, Laakso J, Kaitala V, Airaksinen S. 2004 Evolution of Hsp90 expression in Tetrahymena thermophila (Protozoa, Ciliata) populations exposed to thermally variable environments. Evolution 58, 741–748. (doi:10.1111/j.0014-3820.2004.tb00407.x)
20. Rutherford S, Hirate Y, Swalla BJ. 2007 The Hsp90 capacitor, developmental remodeling, and evolution: the robustness of gene networks and the curious evolvability of metamorphosis. Crit. Rev. Biochem. Mol. Biol. 42, 355–372. (doi:10.1080/10409230701597782)
21. Altincicek B, Knorr E, Vilcinskas A. 2008 Beetle immunity: identification of immune-inducible genes from the model insect Tribolium castaneum. Dev. Comp. Immunol. 32, 585–595. (doi:10.1016/j.dci.2007.09.005)
22. Masri L, Cremer S. 2014 Individual and social immunisation in insects. Trends Immunol. 35, 471–482. (doi:10.1016/j.it.2014.08.005)
23. Cremer S, Armitage SAO, Schmid-Hempel P. 2007 Social immunity. Curr. Biol. 17, 693–702. (doi:10.1016/j.cub.2007.06.008)
24. Cotter SC, Kilner RM. 2010 Personal immunity versus social immunity. Behav. Ecol. 21, 663–668. (doi:10.1093/beheco/arq070)
25. Brown SJ et al. 2009 The red flour beetle, Tribolium castaneum (Coleoptera): a model for studies of development and pest biology. Cold Spring Harb. Protoc. 4, 1–12. (doi:10.1101/sqb.2009.74.047)
26. Milutinovic´ B, Stolpe C, Peuß R, Armitage SAO, Kurtz J. 2013 The red flour beetle as a model for bacterial oral infections. PLoS ONE 8, e64638. (doi:10.1371/journal.pone.0064638)
27. Roth O, Joop G, Eggert H, Hilbert J, Daniel J, Schmid-Hempel P, Kurtz J. 2010 Paternally derived immune priming for offspring in the red flour beetle, Tribolium castaneum. J. Anim. Ecol. 79, 403–413. (doi:10.1111/j.1365-2656.2009.01617.x)
28. Behrens S, Peuß R, Milutinović B, Eggert H, Esser D, Rosenstiel P, Schulenburg H, Bornberg-Bauer E, Kurtz J. 2014 Infection routes matter in populationspecific responses of the red flour beetle to the entomopathogen Bacillus thuringiensis. BMC Genomics 15, 445. (doi:10.1186/1471-2164-15-445)
29. Sokoloff A. 1974 The biology of Tribolium. London, UK: Oxford University Pess
30. Lemaitre B, Hoffmann JA. 2007 The host defense of Drosophila melanogaster. Annu. Rev. Immunol. 25, 697–743. (doi:10.1146/annurev.immunol.25.022106.141615)
31. Bulet P, Stocklin R. 2005 Insect antimicrobial peptides: structures, properties and gene regulation. Protein Pept. Lett. 12, 3–11. (doi:10.2174/0929866053406011)
32. Hoffmann JA, Kafatos FC, Janeway CA, Ezekowitz RA. 1999 Phylogenetic perspectives in innate immunity. Science 284, 1313–1318. (doi:10.1126/science.284.5418.1313)
33. Freitak D, Knorr E, Vogel H, Vilcinskas A. 2012 Gender- and stressor-specific microRNA expression in Tribolium castaneum. Biol. Lett. 8, 860–863. (doi:10.1098/rsbl.2012.0273)
34. Zhang Y et al. 2013 Identification and characterization of novel ER-based hsp90 gene in the red flour beetle, Tribolium castaneum. Cell Stress Chaperones 19, 623–633. (doi:10.s12192-013-0487-y)
35. Knorr E, Vilcinskas A. 2011 Post-embryonic functions of HSP90 in Tribolium castaneum include the regulation of compound eye development. Dev. Genes Evol. 221, 357–362. (doi:10.1007/s00427-011-0379-z)
36. Luu-The V, Paquet N, Calvo E, Cumps J. 2005 Improved real-time RT-PCR method for highthroughput measurements using second derivative calculation and double correction. Biotechniques 38, 287–293. (doi:10.2144/05382RR05)
37. Pfaffl MW. 2001 A new mathematical model for relative quantification in real-time RT–PCR. Nucleic Acids Res. 29, e45. (doi:10.1093/nar/29.9.e45)
38. Cerenius L, Lee BL, Söderhäll K. 2008 The proPOsystem: pros and cons for its role in invertebrate immunity. Trends Immunol. 29, 263–271. (doi:10.1016/j.it.2008.02.009)
39. Cerenius L, Söderhäll K. 2004 The prophenoloxidaseactivating system in invertebrates. Immunol. Rev. 198, 116–126. (doi:10.1111/j.0105-2896.2004.00116.x)
40. Roth O, Sadd BM, Schmid-Hempel P, Kurtz J. 2009 Strain-specific priming of resistance in the red flour beetle, Tribolium castaneum. Proc. R. Soc. B 276, 145–151. (doi:10.1098/rspb.2008.1157)
41. Baracchi D, Mazza G, Turillazzi S. 2012 From individual to collective immunity: the role of the venom as antimicrobial agent in the Stenogastrinae wasp societies. J. Insect Physiol. 58, 188–193. (doi:10.1016/j.jinsphys.2011.11.007)
42. Tschinkel WR. 1975 A comparative study of the chemical defensive system of tenebrionid beetles: chemistry of the secretions. J. Insect Physiol. 21, 753–783. (doi:10.1016/0022-1910(75)90008-6)
43. Yezerski A, Gilmor TP, Stevens L. 2004 Genetic analysis of benzoquinone production in Tribolium confusum. J. Chem. Ecol. 30, 1035–1044. (doi:10.1023/B:JOEC.0000028465.37658.ae)
44. Joop G, Roth O, Schmid-Hempel P, Kurtz J. 2014 Experimental evolution of external immune defences in the red flour beetle. J. Evol. Biol. 27, 1562–1571. (doi:10.1111/jeb.12406)
45. Lewis SM. 2004 Multiple mating and repeated copulations: effects on male reproductive success in red flour beetles. Anim. Behav. 67, 799–804. (doi:10.1016/j.anbehav.2003.05.013)
46. Wojcik DP. 1969 Mating behavior of 8 storedproduct beetles (Coleoptera: Dermestidae, Tenebrionidae, Cucujidae, and Curculionidae). Florida Entomol. 52, 171–197. (doi:10.2307/3493853)
47. Pfaffl MW, Horgan GW, Dempfle L. 2002 Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res. 30, e36. (doi:10.1093/nar/30.9.e36)
48. Benjamini Y, Hochberg Y. 1995 Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Statist. Soc. B 57, 289–300
49. Georgel P et al. 2001 Drosophila immune deficiency (IMD) is a death domain protein that activates antibacterial defense and can promote apoptosis. Dev. Cell 1, 503–514. (doi:10.1016/S1534-5807(01)00059-4)
50. Binggeli O, Neyen C, Poidevin M, Lemaitre B. 2014 Prophenoloxidase activation is required for survival to microbial infections in Drosophila. PLoS Pathog. 10, e1004067. (doi:10.1371/journal.ppat.1004067)
51. Prendeville HR, Stevens L. 2002 Microbe inhibition by Tribolium flour beetles varies with beetle species, strain, sex, and microbe group. J. Chem. Ecol. 28, 1183–1190. (doi:10.1023/A:1016281600915)
52. Otti O, Tragust S, Feldhaar H. 2014 Unifying external and internal immune defences. Trends Ecol. Evol. 29, 625–634. (doi:10.1016/j.tree.2014.09.002)
53. Xu J, Shu J, Qiu X, Wang Z, Zhao F, Zhang Z, Zhang Q. 2009 Effects of heat shock on ovary development and hsp83 expression in Tribolium castaneum (Coleoptera: Tenebrionidae). Arch. Insect Biochem. Physiol. 70, 204–216. (doi:10.1002/arch.20294)
54. Xu J, Shu J, Zhang Q. 2010 Expression of the Tribolium castaneum (Coleoptera: Tenebrionidae) hsp83 gene and its relation to oogenesis during ovarian maturation. J. Genet. Genomics 37, 513–522. (doi:10.1016/S1673-8527(09)60071-0)
55. Eggert H, Kurtz J, Diddens-de Buhr MF. 2014 Different effects of paternal trans-generational immune priming on survival and immunity in step and genetic offspring. Proc. R. Soc. B 281, 20142089. (doi:10.1098/rspb.2014.2089)
56. Plaistow SJ, Outreman Y, Moret Y, Rigaud T. 2003 Variation in the risk of being wounded: an overlooked factor in studies of invertebrate immune function? Ecol. Lett. 6, 489–494. (doi:10.1046/j.1461-0248.2003.00455.x)
57. Ebert D, Hamilton WD. 1996 Sex against virulence: the coevolution of parasitic diseases. Trends Ecol. Evol. 11, 79–82. (doi:10.1016/0169-5347(96)81047-0)