More than a colour change: Insect melanism, disease resistance and fecundity

Proceedings of the Royal Society B: Biological Sciences

Volumn 280, Issue 1763, 2013, Pages

  Dubovskiy, I M ^a   Whitten, M M A ^b   Kryukov, V Y ^a   Yaroslavtseva, O N ^a   Grizanova, E V ^a   Greig, C ^b   Mukherjee, K ^c   Vilcinskas, A ^c   Mitkovets, P V ^d   Glupov, V V ^a   Butt, T M ^b  

^a INSTITUTE OF SYSTEMATICS AND ECOLOGY OF ANIMALS   (Russian Federation)

^b SWANSEA UNIVERSITY   (United Kingdom)

^c JUSTUS LIEBIG UNIVERSITY   (Germany)

^d ALL RUSSIAN INSTITUTE OF PLANT PROTECTION   (Russian Federation)

Author keywords

Immunity; Insect; Insect pathogenic fungus; Melanism; Resistance; Stress

Indexed keywords

COLOR; CUTICLE; DISEASE RESISTANCE; ENTOMOPATHOGENIC ORGANISM; ENZYME ACTIVITY; FECUNDITY; FUNGUS; IMMUNITY; LARVAL DEVELOPMENT; LONGEVITY; MELANISM; MOTH; PATHOGEN; PHYSIOLOGICAL RESPONSE;

INSECT PROTEIN;

ANIMAL; BEAUVERIA; DISEASE RESISTANCE; FERTILITY; GENE EXPRESSION REGULATION; GENETICS; HOST PATHOGEN INTERACTION; IMMUNOLOGY; INSECT; LARVA; MELANOSIS; METABOLISM; MICROBIOLOGY; MOTH; PHYSIOLOGY;

ANIMALS; BEAUVERIA; DISEASE RESISTANCE; FERTILITY; GENE EXPRESSION REGULATION; HOST-PATHOGEN INTERACTIONS; INSECT PROTEINS; INSECTS; LARVA; MELANOSIS; MOTHS;

EID: 84892389775     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2013.0584     Document Type: Article

References (40)

1. Lionakis MS. 2011 Drosophila and Galleria insect model hosts: new tools for the study of fungal virulence, pharmacology and immunology. Virulence 2, 521-527. (doi:10.4161/viru.2.6.18520)
2. Dubovskiy IM, Whitten MMA, Yaroslavtseva ON, Kryukov VY, Grizanova EV, Mukherjee K, Vilcinskas A, Glupov VV, Butt TM. 2013 Can insects develop resistance to insect pathogenic fungi? PLoS ONE 8, e60248. (doi:10.1371/journal.pone.0060248).
3. Cerenius L, Söderhäll K. 2004 The prophenoloxidase-activating system in invertebrates. Immunol. Rev. 198, 116-126. (doi:10.1111/j.0105-2896.2004. 00116.x)
4. Andersen SO. 2010 Insect cuticular sclerotization: a review. Insect Biochem. Mol. Biol. 40, 166-178. (doi:10.1016/j.ibmb.2009.10.007)
5. Butt TM, Wraight SP, Galaini-Wraight S, Humber RA, Roberts DW, Soper RS. 1988 Humoral encapsulation of the fungus Erynia radicans (Entomophthorales) by the potato leafhopper, Empoasca fabae (Homoptera: Cicadellidae). J. Invertebr. Pathol. 52, 49-56. (doi:10.1016/0022-2011(88)90101-2)
6. Wilson K, Cotter SC, Reeson AF, Pell JK. 2001 Melanism and disease resistance in insects. Ecol. Lett. 4, 637-649. (doi:10.1046/j.1461-0248.2001. 00279.x)
7. Cotter SC, Hails RS, Cory JS, Wilson K. 2004 Density-dependent prophylaxis and condition-dependent immune function in lepidopteran larvae: a multivariate approach. J. Anim. Ecol. 73, 283-293. (doi:10.1111/j.0021-8790.2004.00806.x)
8. Söderhäll K, Ajaxon R. 1982 Effect of quinones and melanin on mycelial growth of Aphanomyces spp. and extracellular protease of Aphanomyces astaci, a parasite on crayfish. J. Invertebr. Pathol. 39, 105-109.
9. Leger RJ, Cooper RM, Charnely AK. 1988 The effect of melanization of Manduca sexta cuticle on growth and infection by Metarhizium anisopliae. J. Invertebr. Pathol. 52, 459-470. (doi:10.1016/ 0022-2011(88)90059-6)
10. Barnes AI, Siva-Jothy MT. 2000 Density-dependent prophylaxis in the mealworm beetle Tenebrio molitor L. (Coleoptera: Tenebrionidae): cuticular melanization is an indicator of investment in immunity. Proc. R. Soc. Lond. B 267, 177-182. (doi:10.1098/rspb.2000.0984)
11. Wilson K, Thomas MB, Blanford S, Doggett M, Simpson SJ, Moore SL. 2002 Coping with crowds: density-dependent disease resistance in desert locusts. Proc. Natl Acad. Sci. USA 99, 5471-5475. (doi:10.1073/pnas.082461999)
12. Wilson K, Reeson AF. 1998 Density-dependent prophylaxis: evidence from Lepidoptera-baculovirus interactions? Ecol. Entomol. 23, 100-101. (doi:10.1046/j.1365-2311.1998. 00107.x)
13. Butt TM. 2002 Use of entomogenous fungi for the control of insect pests. In Mycota (eds K Esser, JW Bennett, F Kempken), pp. 111-134. Berlin, Germany: Springer.
14. Gillespie JP, Bailey AM, Cobb B, Vilcinskas A. 2000 Fungi as elicitors of insect immune responses. Arch. Insect Biochem. Physiol. 44, 49-68. (doi:10.1002/ 1520-6327(200006)44:2,49::AID-ARCH1.3.0. CO;2-F)
15. Roy BA, Kirchner JW. 2000 Evolutionary dynamics of pathogen resistance and tolerance. Evolution 54, 51-63. (doi:10.1111/j.0014-3820.2000. tb00007.x)
16. Sheldon BC, Verhulst S. 1996 Ecological immunology: costly parasite defences and tradeoffs in evolutionary ecology. Trends Ecol. Evol. 11, 317-321. (doi:10.1016/0169-5347(96)10039-2)
17. Schmid-Hempel P. 2005 Evolutionary ecology of insect immune defenses. Annu. Rev. Entomol. 50, 529-551. (doi:10.1146/annurev.ento.50.071803. 130420)
18. Cotter SC, Kruuk LEB, Wilson K. 2004 Costs of resistance: genetic correlations and potential trade-offs in an insect immune system. J. Evol. Biol. 17, 421-429. (doi:10.1046/j.1420-9101.2003. 00655.x)
19. Cotter SC, Myatt JP, Benskin CMH, Wilson K. 2008 Selection for cuticular melanism reveals immune function and life-history trade-offs in Spodoptera littoralis. J. Evol. Biol. 21, 1744-1754. (doi:10. 1111/j.1420-9101.2008.01587.x)
20. Lee KP, Wilson K. 2006 Melanism in a larval Lepidoptera: repeatability and heritability of a dynamic trait. Ecol. Entomol. 31, 196-205. (doi:10. 1111/j.0307-6946.2006.00780.x)
21. Butt TM, Ibrahim L, Clark SJ, Beckett A. 1995 The germination behaviour of Metarhizium anisopliae on the surface of aphid and flea beetle cuticles. Mycol. Res. 99, 945-950. (doi:10.1016/S0953-7562(09)80754-5)
22. Ment D, Gindin G, Soroker V, Glazer I, Rot A, Samish M. 2010 Metarhizium anisopliae conidial responses to lipids from tick cuticle and tick mammalian host surface. J. Invertebr. Pathol. 103, 132-139. (doi: 10.1016/j.jip.2009.12.010)
23. Kraaijeveld AR, Elrayes NP, Schuppe HR, Newland PL. 2011 L-arginine enhances immunity to parasitoids in Drosophila melanogaster and increases NO production in lamellocytes. Dev. Comp. Immunol. 35, 857-864. (doi:10.1016/j.dci.2011.03. 019)
24. Yan XD, Scherphof GL, Kamps J. 2005 Liposome opsonization. J. Liposome Res. 15, 109-139.
25. Schuhmann B, Seitz V, Vilcinskas A, Podsiadlowski L. 2003 Cloning and expression of gallerimycin, an antifungal peptide expressed in immune response of greater wax moth larvae, Galleria mellonella. Arch. Insect Biochem. Physiol. 53, 125-133. (doi:10. 1002/arch.10091)
26. Vogel H, Altincicek B, Glockner G, Vilcinskas A. 2011 A comprehensive transcriptome and immune-gene repertoire of the lepidopteran model host Galleria mellonella. BMC Genomics 12, 308. (doi:10.1186/ 1471-2164-12-308)
27. Semighini CP, Heitman J. 2009 Dynamic duo takes down fungal villains. Proc. Natl Acad. Sci. USA 106, 2971-2972. (doi:10.1073/pnas. 0900801106)
28. Xu PJ, Li T, Xiao JH, Murphy RW, Huang DW. 2011 Universal primers for amplifying the complete coding sequence of cytoplasmic heat shock protein 90 (HSP90) in Lepidoptera. Eur. J. Entomol. 108, 164-168.
29. Sweeney AW, Inman AO, Bland CE, Wright RG. 1983 The fine structure of Culicinomyces clavisporus invading mosquito larvae. J. Invertebr. Pathol. 42, 224-243. (doi:10.1016/0022-2011(83)90065-4)
30. Shiao S-H, Whitten MMA, Zachary D, Hoffmann JA, Levashina EL. 2006 Fz2 and Cdc42 mediate melanization and actin polymerization but are dispensable for Plasmodium killing in the mosquito midgut. PLoS Pathog. 2, e133. (doi:10.1371/journal. ppat.0020133)
31. Fullaondo A, García-Sánchez S, Sanz-Parra A, Recio E, Lee SY, Gubb D. 2011 Spn1 Regulates the GNBP3-Dependent Toll Signaling Pathway in Drosophila melanogaster. Mol. Cell Biol. 31, 2960-2972. (doi:10.1128/MCB. 01397-10)
32. Zhang ZT, Zhu SY. 2009 Drosomycin, an essential component of antifungal defence in Drosophila. Insect Mol. Biol. 18, 549-556. (doi:10.1111/j.1365-2583.2009.00907.x)
33. Mak P, Zdybicka-Barabas A, Cytrynska M. 2010 A different repertoire of Galleria mellonella antimicrobial peptides in larvae challenged with bacteria and fungi. Dev. Comp. Immunol. 34, 1129-1136. (doi:10.1016/j.dci. 2010.06.005)
34. Wojda I, Kowalski P, Jakubowicz T. 2009 Humoral immune response of Galleria mellonella larvae after infection by Beauveria bassiana under optimal and heat-shock conditions. J. Insect Physiol. 55, 525-531. (doi:10.1016/j.jinsphys. 2009.01.014)
35. Xu X-X, Zhong X, Yi H-Y, Yu X-Q. 2012 Manduca sexta gloverin binds microbial components and is active against bacteria and fungi. Dev. Comp. Immunol. 38, 275-284. (doi:10.1016/j.dci.2012. 06.012)
36. Bandani AR, Khambay BPS, Faull JL, Newton R, Deadman M, Butt TM. 2000 Production of efrapeptins by Tolypocladium species and evaluation of their insecticidal and antimicrobial properties. Mycol. Res. 104, 537-544. (doi:10.1017/S0953756299001859)
37. Wedde M, Weise C, Kopacek P, Franke P, Vilcinskas A. 1998 Purification and characterization of an inducible metalloprotease inhibitor from the hemolymph of greater wax moth larvae, Galleria mellonella. Eur. J. Biochem. 255, 534-543. (doi:10. 1046/j.1432-1327.1998.2550535.x)
38. True JR. 2003 Insect melanism: the molecules matter. Trends Ecol. Evol. 18, 640-647. (doi:10. 1016/j.tree.2003.09.006)
39. Ferrari J, Muller CB, Kraaijeveld AR, Godfray CJ. 2001 Clonal variation and covariation in aphid resistance to parasitoids and a pathogen. Evolution 55, 1805-1814. (doi:10.1111/j.0014-3820.2001.tb00829.x)
40. Labbé P, Vale PF, Little TJ. 2010 Successfully resisting a pathogen is rarely costly in Daphnia magna. BMC Evol. Biol. 10, 355. (doi:10.1186/1471-2148-10-355)