Gene expression differences underlying genotype-bygenotype specificity in a host-parasite system

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 9, 2014, Pages 3496-3501

  Barribeau, Seth M ^a,c   Sadd, Ben M ^a,b   Du Plessis, Louis ^a   Schmid Hempel, Paul ^a  

^a ETH ZURICH   (Switzerland)

^b ILLINOIS STATE UNIVERSITY   (United States)

^c Institute for Advanced Study Berlin   (Germany)

Author keywords

Coevolution; Manipulation; Red Queen

Indexed keywords

TRANSCRIPTOME;

ARTICLE; BOMBUS TERRESTRIS; CRITHIDIA; GENE EXPRESSION; GENE ONTOLOGY; GENOTYPE; HOST PARASITE INTERACTION; NONHUMAN; PRIORITY JOURNAL; RNA SEQUENCE; SEQUENCE ANALYSIS;

COEVOLUTION; MANIPULATION; RED QUEEN;

ANALYSIS OF VARIANCE; ANIMALS; BASE SEQUENCE; BEES; BIOLOGICAL EVOLUTION; COMPUTATIONAL BIOLOGY; CRITHIDIA; DNA PRIMERS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE ONTOLOGY; GENOTYPE; HOST-PARASITE INTERACTIONS; MOLECULAR SEQUENCE DATA; SEQUENCE ANALYSIS, RNA; SPECIES SPECIFICITY; SWITZERLAND;

EID: 84895804955     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1318628111     Document Type: Article

References (70)

1. Lambrechts L, Halbert J, Durand P, Gouagna LC, Koella JC (2005) Host genotype by parasite genotype interactions underlying the resistance of anopheline mosquitoes to Plasmodium falciparum. Malar J 4(1):3.
2. Carius HJ, Little TJ, Ebert D (2001) Genetic variation in a host-parasite association: Potential for coevolution and frequency-dependent selection. Evolution 55(6): 1136-1145.
3. Schmid-Hempel P (2001) On the evolutionary ecology of host-parasite interactions: Addressing the question with regard to bumblebees and their parasites. Naturwissenschaften 88(4):147-158.
4. Mallon EB, Loosli R, Schmid-Hempel P (2003) Specific versus nonspecific immune defense in the bumblebee, Bombus terrestris L. Evolution 57(6):1444-1447.
5. Schulenburg H, Ewbank JJ (2004) Diversity and specificity in the interaction between Caenorhabditis elegans and the pathogen Serratia marcescens. BMC Evol Biol 4:49.
6. Hamilton WD (1980) Sex versus non-sex versus parasite. Oikos 35(2):282-290.
7. Jaenike J (1978) An hypothesis to account for the maintenance of sex within populations. Evol Theory 3:191-194.
8. Schulte RD, Makus C, Schulenburg H (2013) Host-parasite coevolution favours parasite genetic diversity and horizontal gene transfer. J Evol Biol 26(8):1836-1840.
9. Hamilton WD (1982) Pathogens as causes of genetic diversity in their host populations. Population Biology of Infectious Diseases, eds Anderson R, May R (Springer, Berlin), pp 269-296.
10. Sackton TB, et al. (2007) Dynamic evolution of the innate immune system in Drosophila. Nat Genet 39(12):1461-1468.
11. Waterhouse RM, et al. (2007) Evolutionary dynamics of immune-related genes and pathways in disease-vector mosquitoes. Science 316(5832):1738-1743.
12. Viljakainen L, et al. (2009) Rapid evolution of immune proteins in social insects. Mol Biol Evol 26(8):1791-1801.
13. Lazzaro B, Clark A (2012) Rapid evolution of innate immune response genes. Rapidly Evolving Genes and Genetic Systems, eds Singh R, Xu J, Kulathinal R (Oxford Univ Press, Oxford), pp 203-222.
14. Tiffin P, Moeller DA (2006) Molecular evolution of plant immune system genes. Trends Genet 22(12):662-670.
15. Lazzaro B, Sackton T, Clark A (2006) Genetic variation in Drosophila melanogaster resistance to infection: A comparison across bacteria. Genetics 174(3):1539-1554.
16. Rottschaefer SM, et al. (2011) Exceptional diversity, maintenance of polymorphism, and recent directional selection on the APL1 malaria resistance genes of Anopheles gambiae. PLoS Biol 9(3):e1000600.
17. Harris C, et al. (2010) Polymorphisms in Anopheles gambiae immune genes associated with natural resistance to Plasmodium falciparum. PLoS Pathog 6(9):e1001112.
18. Obbard DJ, Jiggins FM, Halligan DL, Little TJ (2006) Natural selection drives extremely rapid evolution in antiviral RNAi genes. Curr Biol 16(6):580-585.
19. Belvin MP, Anderson KV (1996) A conserved signaling pathway: The Drosophila tolldorsal pathway. Annu Rev Cell Dev Biol 12:393-416.
20. Lemaitre B, Nicolas E, Michaut L, Reichhart JM, Hoffmann JA (1996) The dorsoventral regulatory gene cassette spätzle/Toll/cactus controls the potent antifungal response in Drosophila adults. Cell 86(6):973-983.
21. Medzhitov R (2001) Toll-like receptors and innate immunity. Nat Rev Immunol 1(2): 135-145.
22. Sadd BM (2011) Food-environment mediates the outcome of specific interactions between a bumblebee and its trypanosome parasite. Evolution 65(10):2995-3001.
23. Lazzaro BP, Little TJ (2009) Immunity in a variable world. Philos Trans R Soc Lond B Biol Sci 364(1513):15-26.
24. Raberg L, Grahn M, Hasselquist D, Svensson E (1998) On the adaptive significance of stress-induced immunosuppression. Proc Biol Sci 265(1406):1637-1641.
25. Nuismer SL, Otto SP (2005) Host-parasite interactions and the evolution of gene expression. PLoS Biol 3(7):e203.
26. Bonneaud C, et al. (2011) Rapid evolution of disease resistance is accompanied by functional changes in gene expression in a wild bird. Proc Natl Acad Sci USA 108(19): 7866-7871.
27. Wayne ML, et al. (2011) Expression of defense genes in Drosophila evolves under a different selective regime from expression of other genes. Evolution 65(4): 1068-1078.
28. Sackton TB, Lazzaro BP, Clark AG (2010) Genotype and gene expression associations with immune function in Drosophila. PLoS Genet 6(1):e1000797.
29. Navajas M, et al. (2008) Differential gene expression of the honey bee Apis mellifera associated with Varroa destructor infection. BMC Genomics 9:301.
30. Schlüns H, Sadd BM, Schmid-Hempel P, Crozier RH (2010) Infection with the trypanosome Crithidia bombi and expression of immune-related genes in the bumblebee Bombus terrestris. Dev Comp Immunol 34(7):705-709.
31. Brunner FS, Schmid-Hempel P, Barribeau SM (2013) Immune gene expression in Bombus terrestris: Signatures of infection despite strong variation among populations, colonies, and sister workers. PLoS ONE 8(7):e68181.
32. Lovegrove FE, et al. (2006) Simultaneous host and parasite expression profiling identifies tissue-specific transcriptional programs associated with susceptibility or resistance to experimental cerebral malaria. BMC Genomics 7:295.
33. Bozdech Z, et al. (2008) The transcriptome of Plasmodium vivax reveals divergence and diversity of transcriptional regulation in malaria parasites. Proc Natl Acad Sci USA 105(42):16290-16295.
34. Barribeau SM, Schmid-Hempel P (2013) Qualitatively different immune response of the bumblebee host, Bombus terrestris, to infection by different genotypes of the trypanosome gut parasite, Crithidia bombi. Infect Genet Evol 20:249-256.
35. Riddell CE, Adams S, Schmid-Hempel P, Mallon EB (2009) Differential expression of immune defences is associated with specific host-parasite interactions in insects. PLoS ONE 4(10):e7621.
36. Sadd BM, Barribeau SM (2013) Heterogeneity in infection outcome: Lessons from a bumblebee-trypanosome system. Parasite Immunol 35(11):339-349.
37. Schmid-Hempel P, Reber Funk C (2004) The distribution of genotypes of the trypanosome parasite, Crithidia bombi, in populations of its host, Bombus terrestris. Parasitology 129(Pt 2):147-158.
38. Salathé RM, Schmid-Hempel P (2011) The genotypic structure of a multi-host bumblebee parasite suggests a role for ecological niche overlap. PLoS ONE 6(8):e22054.
39. Tognazzo M, Schmid-Hempel R, Schmid-Hempel P (2012) Probing mixed-genotype infections II: High multiplicity in natural infections of the trypanosomatid, Crithidia bombi, in its host, Bombus spp. PLoS ONE 7(11):e49137.
40. Ruiz-González MX, et al. (2012) Dynamic transmission, host quality, and population structure in a multihost parasite of bumblebees. Evolution 66(10):3053-3066.
41. Shykoff JA, Schmid-Hempel P (1991) Incidence and effects of four parasites in natural populations of bumble bees in Switzerland. Apidologie 22:117-125.
42. Imhoof B, Schmid-Hempel P (1999) Colony success of the bumble bee, Bombus terrestris, in relation to infections by two protozoan parasites, Crithidia bombi and Nosema bombi. Insectes Soc 46(3):233-238.
43. Schmid-Hempel P, Puhr K, Kruger N, Reber C, Schmid-Hempel R (1999) Dynamic and genetic consequences of variation in horizontal transmission for a microparasitic infection. Evolution 53(2):426-434.
44. Gerardo NM, et al. (2010) Immunity and other defenses in pea aphids, Acyrthosiphon pisum. Genome Biol 11(2):R21.
45. Evans JD, et al. (2006) Immune pathways and defence mechanisms in honey bees Apis mellifera. Insect Mol Biol 15(5):645-656.
46. Lemaitre B (2012) The drosophila gut: A new paradigm for epithelial immune response. Cytokine 59(3):494.
47. Otterstatter MC, Thomson JD (2006) Within-host dynamics of an intestinal pathogen of bumble bees. Parasitology 133(Pt 6):749-761.
48. Schmid-Hempel P, Schmid-Hempel R (1993) Transmission of a pathogen in Bombus terrestris, with a note on division of labour in social insects. Behav Ecol Sociobiol 33(5): 319-327.
49. Brown MJF, Loosli R, Schmid-Hempel P (2000) Condition-dependent expression of virulence in a trypanosome infecting bumblebees. Oikos 91(3):421-427.
50. Apidianakis Y, et al. (2005) Profiling early infection responses: Pseudomonas aeruginosa eludes host defenses by suppressing antimicrobial peptide gene expression. Proc Natl Acad Sci USA 102(7):2573-2578.
51. Schmid-Hempel P (2008) Parasite immune evasion: A momentous molecular war. Trends Ecol Evol 23(6):318-326.
52. Lefèvre T, et al. (2009) Invasion of the body snatchers: The diversity and evolution of manipulative strategies in host-parasite interactions. Adv Parasitol 68:45-83.
53. Ji D, Kim Y (2004) An entomopathogenic bacterium, Xenorhabdus nematophila, inhibits the expression of an antibacterial peptide, cecropin, of the beet armyworm, Spodoptera exigua. J Insect Physiol 50(6):489-496.
54. Vallet-Gely I, Lemaitre B, Boccard F (2008) Bacterial strategies to overcome insect defences. Nat Rev Microbiol 6(4):302-313.
55. Deshwal S, Mallon EB (2014) Antimicrobial peptides play a functional role in bumblebee anti-trypanosome defense. Dev Comp Immunol 42(2):240-243.
56. Hu C, Aksoy S (2006) Innate immune responses regulate trypanosome parasite infection of the tsetse fly Glossina morsitans morsitans. Mol Microbiol 60(5):1194-1204.
57. Olivier M, Gregory DJ, Forget G (2005) Subversion mechanisms by which Leishmania parasites can escape the host immune response: A signaling point of view. Clin Microbiol Rev 18(2):293-305.
58. Telleria EL, et al. (2012) Caspar-like gene depletion reduces Leishmania infection in sand fly host Lutzomyia longipalpis. J Biol Chem 287(16):12985-12993.
59. Telleria EL, et al. (2013) Bacterial feeding, Leishmania infection and distinct infection routes induce differential defensin expression in Lutzomyia longipalpis. Parasit Vectors 6:12.
60. Bonneaud C, Balenger SL, Zhang JW, Edwards SV, Hill GE (2012) Innate immunity and the evolution of resistance to an emerging infectious disease in a wild bird. Mol Ecol 21(11):2628-2639.
61. Saeij JPJ, et al. (2007) Toxoplasma co-opts host gene expression by injection of a polymorphic kinase homologue. Nature 445(7125):324-327.
62. Kucharski R, Maleszka J, Maleszka R (2007) Novel cuticular proteins revealed by the honey bee genome. Insect Biochem Mol Biol 37(2):128-134.
63. Chen YX, et al. (2007) Role of peptide hydrophobicity in the mechanism of action of alpha-helical antimicrobial peptides. Antimicrob Agents Chemother 51(4):1398-1406.
64. Simonet G, Claeys I, Broeck JV (2002) Structural and functional properties of a novel serine protease inhibiting peptide family in arthropods. Comp Biochem Physiol B Biochem Mol Biol 132(1):247-255.
65. Poirie M, et al. (2000) Drosophila resistance genes to parasitoids: Chromosomal location and linkage analysis. Proc Biol Sci 267(1451):1417-1421.
66. Luijckx P, Fienberg H, Duneau D, Ebert D (2013) A matching-allele model explains host resistance to parasites. Curr Biol 23(12):1085-1088.
67. Schmid-Hempel P (2011) Evolutionary Parasitology: The Integrated Study of Infections, Immunology, Ecology, and Genetics (Oxford Univ Press, Oxford).
68. Sadd BM, Schmid-Hempel P (2007) Facultative but persistent trans-generational immunity via the mother's eggs in bumblebees. Curr Biol 17(24):R1046-R1047.
69. Sadd BM, Schmid-Hempel P (2009) A distinct infection cost associated with transgenerational priming of antibacterial immunity in bumble-bees. Biol Lett 5(6): 798-801.
70. Conesa A, et al. (2005) Blast2GO: A universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21(18):3674-3676.