Maintenance of genetic variation in immune defense of a freshwater snail: role of environmental heterogeneity

Evolution

Volumn 64, Issue 8, 2010, Pages 2397-2407

  Seppälä, Otto ^a   Jokela, Jukka ^a  

^a ETH ZURICH   (Switzerland)

Author keywords

G E interaction; Genetic polymorphism; Immunocompetence; Life history trade offs; Lymnaea stagnalis; Pathogen resistance

Indexed keywords

FRESH WATER; MONOPHENOL MONOOXYGENASE; PLASMA PROTEIN;

DEFENSE MECHANISM; DISEASE RESISTANCE; ENVIRONMENTAL CONDITIONS; ENZYME ACTIVITY; FITNESS; FOOD AVAILABILITY; FRESHWATER ECOSYSTEM; GENETIC VARIATION; GENOTYPE-ENVIRONMENT INTERACTION; GROWTH RATE; HETEROGENEITY; IMMUNE SYSTEM; IMMUNOCOMPETENCE; LIFE HISTORY TRAIT; NATURAL SELECTION; POLYMORPHISM; SNAIL; TRADE-OFF;

ANIMAL; ARTICLE; BLOOD CELL; CYTOLOGY; DRUG EFFECT; ENVIRONMENT; ENZYMOLOGY; ESCHERICHIA COLI; FEEDING BEHAVIOR; GENETIC VARIABILITY; GENETICS; HEMOLYMPH; IMMUNOLOGY; INNATE IMMUNITY; LYMNAEA; METABOLISM; PHYSIOLOGY;

ANIMALS; BLOOD PROTEINS; ENVIRONMENT; ESCHERICHIA COLI; FEEDING BEHAVIOR; FRESH WATER; GENETIC VARIATION; HEMOCYTES; HEMOLYMPH; IMMUNITY, INNATE; LYMNAEA; MONOPHENOL MONOOXYGENASE;

BASOMMATOPHORA; GASTROPODA; LYMNAEA; LYMNAEA STAGNALIS;

EID: 77955233682     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/j.1558-5646.2010.00995.x     Document Type: Article

References (68)

1. Allam B, Paillard C, Auffret M, Ford S E. Effects of the pathogenic Vibrio tapetis on defence factors of susceptible and non-susceptible bivalve species: II. Cellular and biochemical changes following in vivo challenge. Fish Shellfish Immun 2006, 20:384-397.
2. Barber I, Arnott S A, Braithwaite V, Andrew J, Huntingford F A. Indirect fitness consequences of mate choice in sticklebacks: offspring of brighter males grow slowly but resist parasite infection. Proc. R. Soc. B. 2001, 268:71-76.
3. Beninger P G, le Pennec G, le Pennec M. Demonstration of nutrient pathway from the digestive system to oocytes in the gonad intestinal loop of the scallop Pecten maximus L. Biol. Bull. 2003, 205:83-92.
4. Blanford S, Thomas M B, Pugh C, Pell J K. Temperature checks the Red Queen? Resistance and virulence in a fluctuating environment. Ecol. Lett. 2003, 6:2-5.
5. Boots M, Begon M. Trade-offs with resistance to a graulosis-virus in the Indian meal moth, examined by a laboratory evolution experiment. Funct. Ecol. 1993, 7:528-534.
6. Boycott A E, Diver C, Garstang S, Turner F M. The inheritance of sinistrality Limnea peregra. Philos. Trans. R. Soc. Lond. B 1930, 219:51-131.
7. Burdon J J, Jarosz A M. Host-pathogen interactions in natural populations of Linum marginale and Melampsora lini. I. Patterns of resistance and racial variation in a large host population. Evolution 1991, 45:205-217.
8. Butt D, Raftos A. Phenoloxidase-associated cellular defence in the Sydney rock oyster, Saccostrea glomerata, provides resistance against QX disease infections. Dev. Comp. Immunol. 2008, 32:299-306.
9. Butt D, Aladaileh S, O'Connor W A, Raftos D A. Effect of starvation on biological factors related to immunological defense in the Sydney rock oyster (Saccostrea glomerata). Aquaculture 2007, 264:82-91.
10. Carius H J, Little T J, Ebert D. Genetic variation in a host-parasite association: potential for coevolution and frequency-dependent selection. Evolution 2001, 55:1136-1145.
11. Cerenius L, Söderhäll K. The prophenoloxidase-activating system in invertebrates. Immunol. Rev. 2004, 198:116-126.
12. Cotter S C, Kruuk L E, Wilson K. Costs of resistance: genetic correlations and potential trade-offs in an insect immune system. J. Evol. Biol. 2004, 17:421-429.
13. Coutellec-Vreto M-A, Madec L, Guiller A. Selfing and biparental inbreeding: a mating system analysis in Lymnaea peregra (Gastropoda; Lymnaeidae). Heredity 1997, 79:277-285.
14. Dybdahl M F, Lively C M. Host-parasite coevolution: evidence for rare advantage and time-lagged selection in a natural population. Evolution 1998, 52:1057-1066.
15. Escobar J S, Facon B, Jarne P, Goudet J, David P. Correlated evolution of mating strategy and inbreeding depression within and among populations of the hermaphroditic snail Physa acuta. Evolution 2009, 63:2790-2804.
16. Feder D, Mello C B, Garcia E S, Azambuja P. Immune responses in Rhodnius prolixus: influence of nutrition and acdysone. J. Insect Physiol. 1997, 43:513-519.
17. Frank S A. Specific and non-specific defense against parasitic attack. J. Theor. Biol. 2000, 202:283-304.
18. Gillespie J H, Turelli M. Genotype-environment interactions and the maintenance of polygenic variation. Genetics 1989, 121:129-138.
19. Grosholz E D. The effects of host genotype and spatial distribution on trematode parasitism in a bivalve population. Evolution 1994, 48:1514-1524.
20. Hellio C, Bado-Nilles A, Gagnaire B, Renault T, Thomas-Guyon H. Demonstration of a true phenoloxidase activity and activation of a ProPO cascade in Pacific oyster, Crassostrea gigas (Thunberg) in vitro. Fish Shellfish Immun. 2007, 22:433-440.
21. Henry P-Y, Bousset L, Sourrouille P, Jarne P. Partial selfing, ecological disturbance and reproductive assurance in an invasive freshwater snail. Heredity 2005, 95:428-436.
22. Henter H J, Via S. The potential for coevolution in a host-parasitoid system. I. Genetic-variation within a population of wasps in the ability to parasitize an aphid host. Evolution 1995, 49:427-438.
23. Hernroth B. The influence of temperature and dose on antibacterial peptide response against lipopolysaccharide in the blue mussel, Mytilus edulis. Fish Shellfish Immun. 2003, 14:25-37.
24. Imler J L, Bulet P. Antimicrobial peptides in Drosophila: structures, activities and gene regulation. Chem. Rev. Ecol. Syst. 2005, 21:243-273.
25. Jokela J, Schmid-Hempel P, Rigby M C. Dr. Pangloss restrained by the Red Queen - steps towards a unified defense theory. Oikos 2000, 89:267-274.
26. Jokela J, Wiehn J, Kopp K. Among- and within-population variation in outcrossing rate of a mixed-mating freshwater snail. Heredity 2006, 97:275-282.
27. Karvonen A, Kirsi S, Hudson P J, Valtonen E T. Patterns of cercarial production from Diplostomum spathaceum: terminal investment or bet hedging?. Parasitology 2004, 129:87-92.
28. Kolluru G R, Grether G F, South S H, Dunlop E, Cardinali A, Liu L, Carapiet A. The effects of carotenoid and food availability on resistance to a naturally occurring parasite (Gyrodactylus turnbulli) in guppies (Poecilia reticulata). Biol. J. Linn. Soc. 2006, 89:301-309.
29. Kopp K C. Evolutionary ecology of introduced populations of the freshwater snail Lymnaea stagnalis (Gastropoda: Pulmonata). 2007, PhD-thesis, ETH-Zürich
30. Koskela T, Puustinen S, Salonen V, Mutikainen P. Resistance and tolerance in a host plant-holoparasitic plant interaction: genetic variation and costs. Evolution 2002, 56:899-908.
31. Kraaijeveld A R, Godfray H C J. Trade-off between parasitoid resistance and larval competitive ability in Drosophila melanogaster. Nature 1997, 389:278-280.
32. Krasnov B R, Khokhlova I S, Arakelyan M S, Degen A A. Is a starving host tastier? Reproduction in fleas parasitizing food-limited redents. Funct. Ecol. 2005, 19:625-631.
33. Krebs C J. Ecological methodology 1989, Harper and Row, New York
34. Kurtz J, Sauer K P. The immunocompetence handicap hypothesis: testing the genetic predictions. Proc. R. Soc. Lond. B 1999, 266:2515-2522.
35. Lambrechts L, Chavette J-M, Snounou G, Koella J C. Environmental influence on the genetic basis of mosquito resistance to malaria parasites. Proc. R. Soc. B 2006, 273:1501-1506.
36. Lazzaro B P, Little T J. Immunity in a variable world. Phil. Trans. R. Soc. B 2009, 364:15-26.
37. Lee K P, Cory J S, Wilson K, Raubenheimer D, Simpson S J. Flexible diet choice offsets protein costs of pathogen resistance in a caterpillar. Proc. R. Soc. B 2006, 273:823-829.
38. Lloyd S. Environmental influences on host immunity. Ecology of infectious diseases in natural populations 1995, 327-361. Grenfell B TDobson A P.eds, Cambridge University Press, Cambridge
39. Luong L T, Polak M. Costs of resistance in the Drosophila-Macrocheles system: a negative genetic correlation between ectoparasite resistance and reproduction. Evolution 2007, 61:1391-1402.
40. Lynch M, Walsh B. Genetics and analysis of quantitative traits 1998, Sinauer Associaters Inc., Sunderland, MA
41. McKean K A, Yourth C P, Lazzaro B P, Clark A G. The evolutionary costs of immunological maintenance and deployment. BMC Evol. Biol. 2008, 8:76.
42. Mitchell S E, Rogers E S, Little T J, Read A F. Host-parasite and genotype-by-environment interactions: temperature modifies potential for selection by a sterilizing pathogen. Evolution 2005, 59:70-80.
43. Mitta G, Vandenbulcke F, Roch P. Original involvement of antimicrobial peptides in mussel innate immunity. FEBS Lett. 2000, 486:185-190.
44. Moret Y. Explaining variable costs of the immune response: selection for specific versus non-specific immunity and facultative life history change. Oikos 2003, 102:213-216.
45. Moret Y, Schmid-Hempel P. Survival for immunity: the price of immune system activation for bumblebee workers. Science 2000, 290:1166-1168.
46. Muñoz P, Meseguer J, Esteban M thomampersan. Phenoloxidase activity in three commercial bivalve species. Changes due to natural infestation with Perkinsus atlanticus. Fish Shellfish Immun. 2006, 20:12-19.
47. Murray D L, Keith L B, Cary J R. Do parasitism and nutritional status interact to affect production in snowshoe hares?. Ecology 1998, 79:1209-1222.
48. Reznick D, Nunney L, Tessier A. Big houses, big cars, superfleas and the costs of reproduction. Trends. Ecol. Evol. 2000, 15:421-425.
49. Richards C S. Schistosoma mansoni: susceptibility reversal with age in the snail host Biomphalaria glabrata. Exp. Parasitol. 1977, 42:165-168.
50. Roff D A. Evolutionary quantitative genetics 1997, Chapman and Hall, New York
51. Ryder J J, Siva-Jothy M T. Quantitative genetics of immune function and body size in the house cricket, Acheta domesticus. J. Evol. Biol. 2001, 14:646-653.
52. Salvaudon L, Héraudet V, Shykoff J A. Parasite-host fitness trade-offs change with parasite identity: genotype-specific interactions in a plant-pathogen system. Evolution 2005, 59:2518-2524.
53. Schlichting C D, Pigliucci M. Phenotypic evolution: a reaction norm perspective 1998, Sinauer Association, Sunderland, MA
54. Schmid-Hempel P, Ebert D. On the evolutionary ecology of specific immune defense. Trends Ecol. Evol. 2003, 18:27-32.
55. Schwarzenbach G A, Hosken D J, Ward P I. Sex and immunity in the yellow dung fly Scathophaga stercoraria. J. Evol. Biol. 2005, 18:455-463.
56. Sgró C M, Hoffmann A A. Genetic correlations, tradeoffs and environmental variation. Heredity 2004, 93:241-248.
57. Sheldon B C, Verhulst S. Ecological immunology: costly parasite defenses and trade offs in evolutionary ecology. Trends. Ecol. Evol. 1996, 11:317-321.
58. Siva-Jothy M T, Thompson J J W. Short-term nutrient deprivation affects immune function. Physiol. Entomol. 2002, 27:206-212.
59. Slater A F G, Keymer A E. Heligmosomoides polygurus (Nematoda): the influence of dietary protein on the dynamics of repeated infection. Proc. R. Soc. Lond. B 1986, 229:69-83.
60. Sminia T. Gastropods. Invertebrate blood cells 1981, 1:191-232. Ratcliffe N ARowley A F.eds, Academic Press, London
61. Sokal R R, Rohlf F J. Biometry 1994, Freeman, New York
62. Uttenweiler-Joseph S, Moniatte M, Lagueux M, Van Dorsselaer A, Hoffmann J A, Bulet P. Differential display of peptides induced during the immune response of Drosophila: a matrix-assisted laser desorption ionization time-of-flight mass spectrometry study. Proc. Natl. Acad. Sci. USA 1998, 95:11342-11347.
63. Väyrynen T, Siddall R, Valtonen E T, Taskinen J. Patterns of trematode parasitism in lymnaeid snails from northern and central Finland. Ann. Zool. Fennici. 2000, 37:189-199.
64. Wakelin D. Nature and nurture: overcoming constrains on immunity. Parasitology 1989, 99:S21-S35.
65. Wiehn J, Korpimäki E. Resource levels, reproduction and resistance to haematozoan infections. Proc. R. Soc. Lond. B 1998, 265:1197-1201.
66. Wiehn J, Kopp K, Rezzonico S, Karttunen S, Jokela J. Family-level covariation between parasite resistance and mating system in a hermaphroditic freshwater snail. Evolution 2002, 56:1454-1461.
67. Xu B, Chen M, Yang H, Zhao S. Starvation-induced changes of hemocyte parameters in the zhikong scallop Chlamys farreri. J. Shellfish Res. 2008, 27:1195-1199.
68. Zhong D, Pai A, Yan G. Costly resistance to parasitism: evidence from simultaneous quantitative trait loci mapping for resistance and fitness in Tribolium castaneum. Genetics 2005, 169:2127-2135.