Consistent pattern of local adaptation during an experimental heat wave in a Pipefish-Trematode Host-Parasite system

PLoS ONE

Volumn 7, Issue 1, 2012, Pages

  Landis, Susanne H ^a   Kalbe, Martin ^b   Reusch, Thorsten B H ^a   Roth, Olivia ^a  

^a GEOMAR HELMHOLTZ CENTRE FOR OCEAN RESEARCH KIEL   (Germany)

^b MAX PLANCK INSTITUTE FOR EVOLUTIONARY BIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTIVE IMMUNITY; ALLOPATRY; ANIMAL EXPERIMENT; ARTICLE; CELL CYCLE PHASE; CERCARIA; CLIMATE CHANGE; CONTROLLED STUDY; CRYPTOCOTYLE LINGUA; DOWN REGULATION; ENVIRONMENTAL CHANGE; FISH; GEOGRAPHICAL VARIATION (SPECIES); GREENHOUSE EFFECT; HEAT ACCLIMATIZATION; HEAT STRESS; HEAT WAVE; HOST PARASITE INTERACTION; IMMUNOCOMPETENT CELL; INNATE IMMUNITY; LYMPHOCYTE; LYMPHOCYTE PROLIFERATION; MONOCYTE; NONHUMAN; PARASITE TRANSMISSION; PARASITE VIRULENCE; SYMPATRY; SYNGNATHUS TYPHIE; TREMATODE; WATER TEMPERATURE; ADAPTATION; ANALYSIS OF VARIANCE; ANIMAL; CYTOLOGY; ENVIRONMENT; HEAD KIDNEY; HEAT; PARASITOLOGY; PHYSIOLOGY; SMEGMAMORPHA; SPECIES DIFFERENCE;

CRYPTOCOTYLE LINGUA; SYNGNATHUS TYPHLE; TREMATODA;

ADAPTATION, PHYSIOLOGICAL; ANALYSIS OF VARIANCE; ANIMALS; ENVIRONMENT; HEAD KIDNEY; HOST-PARASITE INTERACTIONS; HOT TEMPERATURE; LYMPHOCYTES; MONOCYTES; SMEGMAMORPHA; SPECIES SPECIFICITY; TREMATODA;

EID: 84856382925     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0030658     Document Type: Article

References (58)

1. Van Valen L, (1973) A new evolutionary law. Evol Theo 1: 1-30.
2. Lively CM, (1989) Adaptation by a Parasitic Trematode to Local Populations of Its Snail Host. Evolution 43: 1663-1671.
3. Ebert D, Hamilton WD, (1996) Sex against virulence: The coevolution of parasitic diseases. Trends Ecol Evol 11: 79-82.
4. Kaltz O, Shykoff JA, (1998) Local adaptation in host-parasite systems. Heredity 81: 361-370.
5. Carius HJ, Little TJ, Ebert D, (2001) Genetic variation in a host-parasite association: potential for coevolution and freqency-dependent selection. Evolution 55: 1136-1145.
6. Lazzaro BP, Sackton TB, Clark AG, (2006) Genetic variation in Drosophila melanogaster resistance to infection: a comparison across bacteria. Genetics 174: 1539-1554.
7. Antonovics J, Thrall PH, (1994) Cost of resistance and the maintenance of genetic-polymorphism in host-pathogen systems. Proc R Soc B 257: 105-110.
8. McClelland EE, Penn DJ, Potts WK, (2003) Major histocompatibility complex heterozygote superiority during coinfection. Infect Immun 71: 2079-2086.
9. Rauch G, Kalbe M, Reusch TBH, (2006) One day is enough: rapid and specific host-parasite interactions in a stickleback-trematode system. Biol Lett 2: 382-384.
10. Gandon S, (2002) Local adaptation and the geometry of host-parasite coevolution. Ecol Lett 5: 246-256.
11. Schmid-Hempel P, Ebert D, (2003) On the evolutionary ecology of specific immune defence. Trends Ecol Evol 18: 27-32.
12. Thompson JN, (1994) The coevolutionary process Chicago University of Chicago Press.
13. Thompson JN, (1997) Evaluating the dynamics of coevolution among geographically structured populations. Ecology 78: 1619-1623.
14. Gomez JM, Abdelaziz M, Camacho JPM, Munoz-Pajares AJ, Perfectti F, (2009) Local adaptation and maladaptation to pollinators in a generalist geographic mosaic. Ecol Lett 12: 672-682.
15. Enfield DB, (1988) Is El Niño Becoming More Common? Oceanography 1: 23-27.
16. Ebert D, Zschokke-Rohringer CD, Carius HJ, (1998) Within- and between-population variation for resistance of Daphnia magna to the bacterial endoparasite Pasteuria ramosa. Proc R Soc B 265: 2127-2134.
17. Seppälä O, Jokela J, (2010) Immune defence under extreme ambient temperature. Biol Lett 7: 119-122.
18. Wegner KM, Kalbe M, Milinski M, Reusch TBH, (2008) Mortality selection during the 2003 European heat wave in three-spined sticklebacks: effect of parasites and MHC genotype. BMC Evol Biol 8: 1-12.
19. Blanford S, Thomas MT, Pugh C, Pell JK, (2003) Temperature checks the Red Queen? Resistance and virulence in a fluctuating environment. Ecol Lett 6: 2-5.
20. IPCC (2007) Summary for Policymakers. Parry OFC ML, Palutikof JP, Linden PJvd, Hanson CE, eds. Cambridge, UK, 7-22 Cambridge University Press pp. 8-13 Climate Change 2007: Impacts, Adaptation and Vulnerability. Contribution of Working Group II to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change.
21. Reusch TBH, Ehlers A, Hammerli A, Worm B, (2005) Ecosystem recovery after climatic extremes enhanced by genotypic diversity. P Natl Acad Sci USA 102: 2826-2831.
22. Roth O, Kurtz J, Reusch TBH, (2010) A summer heat wave decreases the immunocompetence of the mesograzer, Idotea baltica. Mar Biol 157: 1605-1611.
23. Easterling DR, Meehl GA, Parmesan C, Changnon SA, Karl TR, et al. (2000) Climate extremes: Observations, modeling, and impacts. Science 289: 2068-2074.
24. Thomas MB, Blanford S, (2003) Thermal bioloy in insect-parasite interactions. Trends Ecol Evol 18: 344-350.
25. Belkin IM, (2009) Rapid warming of Large Marine Ecosystems. Prog Oceanogr 81: 207-213.
26. Harvell CD, Mitchell CE, Ward JR, Altizer S, Dobson AP, et al. (2002) Climate warming and disease risks for terrestrial and marine biota. Science 296: 2158-2162.
27. Fellowes MDE, Kraaijeveld AR, Godfray H, (1999) Cross resistance following artificial selection for increased host defence against parasitoids in Drosophila melanogaster. Evolution 53: 966-972.
28. Lazzaro BP, Little TJ, (2009) Immunity in a variable world. Philos T Roy Soc B 364: 15-26.
29. Mydlarz LD, Jones LE, Harvell CD, (2006) Innate immunity environmental drivers and disease ecology of marine and freshwater invertebrates. Annu Rev Ecol Evol S 37: 251-288.
30. Ahnesjo I, (1995) Temperature affects male and female potential reproductive rates differently in the sex-role reversed pipefish, Syngnathus typhle. Behav Ecol 6: 229-233.
31. Kirby RR, Johns DG, Lindley JA, (2006) Fathers in hot water: rising sea temperatures and a Northeastern Atlantic pipefish baby boom. Biol Lett 2: 597-600.
32. Poulin R, (2006) Global warming and temperature-mediated increases in cercarial emergence in tramtode parasites. Parasitology 132: 143-151.
33. Studer A, Thieltges DW, Poulin R, (2010) Parasites and global warming: net effects of temperature on an intertidal host-parasite system. Mar Ecol-Prog Ser 415: 11-22.
34. Schulte RD, Makus C, Hasert B, Michiels NK, Schulenburg H, (2011) Host-parasite local adaptation after experimental coevolution of Caenorhabditis elegans and its microparasite Bacillus thuringiensis. Proc R Soc B 278: 2832-2839.
35. Berglund A, Rosenqvist G, Svensson I, (1986) Mate choice, fecundity and sexual dimorphism in two pipefish species (Syntnathidae). Behav Ecol Sociobiol 19: 301-307.
36. Zander CD, (1998) Ecology of Host Parasite Relationships in the Baltic Sea. Naturwissenschaften 85: 426-436.
37. Zander CD, Reimer LW, Barz K, (1999) Parasite communities of the Salzhaff (Northwest Mecklenburg, Baltic Sea). I. Structure and dynamics of communities of littoral fish, especially small-sized fish. Parasitol Res 85: 356-372.
38. Blakeslee AMH, Byers JE, Lesser MP, (2008) Solving cryptogenic histories using host and parasite molecular genetics: the resolution of Littorina littorea's North American origin. Mol Ecol 17: 3684-3696.
39. Granovitch A, Johannesson K, (2000) Digenetic trematodes in four species of Littorina from the west coast of Sweden. Ophelia 53: 55-65.
40. Stunkard HW, (1930) The life history of Cryptocotyle lingua (Creplin), with notes on the physiology of the metacercariae. J Morphol 50: 143-191.
41. Bergmann N, Winters G, Rauch G, Eizaguirre C, Gu J, et al. (2010) Population-specificity of heat stress gene induction in northern and southern eelgrass Zostera marina populations under simulated global warming. Mol Ecol 19: 2870-2883.
42. Belkin S, Colwell RR, eds. (2005) Oceans and Health: Pathogens in the Marine Environment 1. ed New York Springer Science+Business Media, Inc.
43. Roth O, Scharsack J, I K, TBH R, (2011) Bateman's principle and immunity in a sex-role reversed pipefish. J Evol Biol 24: 1410-1420.
44. Tort L BJ, Mackenzie S, (2003) Fish immune system: A crossroads between immune and adaptive responses. Immunologia 22: 277-286.
45. Matsunaga T, Rahman A, (1998) What brought the adaptive immune system to vertebrates?- The jaw hypothesis and the seahorse. Immunol Rev 166: 177-186.
46. Mazzi D, (2004) Parasites make male pipefish careless. J Evol Biol 17: 519-527.
47. Moret Y, Schmid-Hempel P, (2000) Survival for immunity: The price of immune system activation for bumblebee workers. Science 290: 1166-1168.
48. Read AF, Allen JE, (2000) Evolution and immunology- The economics of immunity. Science 290: 1104-1105.
49. Schmid-Hempel P, Ebert D, (2003) On the evolutionary ecology of specific immune defence. Trends Ecol Evol 18: 27-32.
50. Wegner KM, Kalbe M, Reusch TBH, (2007) Innate versus adaptive immunity in sticklebacks: evidence for trade-offs from a selection experiment. Evol Ecol 21: 473-483.
51. Braude S, Tang-Martinez Z, Taylor GT, (1999) Stress, testosterone, and the immunoredistribution hypothesis. Behav Ecol 10: 345-350.
52. Thieltges DW, Rick J, (2006) Effect of temperature on emergence, survival and infectivity of cercariae of the marine trematode Renicola roscovita (Digenea: Renicolidae). Dis Aquat Organ 73: 63-68.
53. Laine AL, (2008) Temperature-mediated patterns of local adaptation in a natural plant-pathogen metapopulation. Ecol Lett 11: 327-337.
54. McCoy KD, Boulinier T, Tirard C, Michalakis Y, (2001) Host specificity of a generalist parasite: genetic evidence of sympatric host races in the seabird tick Ixodes uriae. J Evol Biol 14: 395-405.
55. Gandon S, Capowiez Y, Dubois Y, Michalakis Y, Olivieri I, (1996) Local adaptation and gene-for-gene coevolution in a metapopulation model. Proc R Soc B 263: 1003-1009.
56. Ardia DR, Parmentier HK, Vogel LA, (2011) The role of constraints and limitation in driving individual variation in immune response. Funct Ecol 25: 61-73.
57. Baucom RS, de Roode JC, (2011) Ecological immunology and tolerance in plants and animals. Funct Ecol 25: 18-28.
58. Hawley DM, Altizer SM, (2011) Disease ecology meets ecological immunology: understanding the links between organismal immunity and infection dynamics in natural populations. Funct Ecol 25: 48-60.