Costs of mounting an immune response during pregnancy in a lizard

Physiological and Biochemical Zoology

Volumn 86, Issue 1, 2013, Pages 127-136

  Meylan, Sandrine ^a,b   Richard, Murielle ^a   Bauer, Sophie ^a   Haussy, Claudy ^a   Miles, Donald ^c  

^a SORBONNE UNIVERSITÉ   (France)

^b INSTITUT UNIVERSITAIRE DE FRANCE   (France)

^c OHIO UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BODY SIZE; BODY TEMPERATURE; CELL ORGANELLE; DEFENSE BEHAVIOR; DEVELOPMENTAL BIOLOGY; HOMEOSTASIS; IMMUNE RESPONSE; LIZARD; METABOLISM; PREGNANCY;

ANIMAL; ARTICLE; BASAL METABOLIC RATE; CELLULAR IMMUNITY; ERYTHROCYTE; FEMALE; FRANCE; IMMUNOLOGY; LITTER SIZE; LIZARD; MOTOR ACTIVITY; PHYSIOLOGY; REPRODUCTION; SHEEP; THERMOREGULATION; VIVIPARITY;

ANIMALS; BASAL METABOLISM; BODY TEMPERATURE REGULATION; ERYTHROCYTES; FEMALE; FRANCE; IMMUNITY, CELLULAR; LITTER SIZE; LIZARDS; MOTOR ACTIVITY; REPRODUCTION; SHEEP, DOMESTIC; VIVIPARITY, NONMAMMALIAN;

AVES; MAMMALIA; OVIS ARIES; SQUAMATA; VERTEBRATA; ZOOTOCA VIVIPARA;

EID: 84872331566     PISSN: 15222152     EISSN: None     Source Type: Journal    
DOI: 10.1086/668637     Document Type: Article

References (75)

1. Alonso-Alvarez C. and J.L. Tella. 2001. Effects of experimental food restriction and body-mass changes on the avian T-cellmediated immune response. Can J Zool 79:101-105.
2. Ardia D.R. 2007. The ability to mount multiple immune responses simultaneously varies across the range of the tree swallow. Ecography 30:23-30.
3. Avery R.A. 1982. Field studies of body temperatures and thermoregulation. Pp. 93-166 in C. Gans and F.H. Pough, eds. Biology of the reptilia. Vol. 12. Academic Press, New York.
4. Avery R.A. and B.H. McArdle. 1973. The morning emergence of the common lizard Lacerta vivipara Jacquin. Br J Herpetol 5:363-368.
5. Belliure J., S. Meylan, and J. Clobert. 2004. Prenatal and postnatal effects of corticosterone on behavior in juveniles of the common lizard, Lacerta vivipara. J Exp Zool 301A:401-410.
6. Bleu J., B. Heulin, C. Haussy, S. Meylan, and M. Massot. 2012. Experimental evidence of early costs of reproduction in conspecific viviparous and oviparous lizards. J Evol Biol 25: 1264-1274.
7. Bleu J., J.F. Le Galliard, S. Meylan, M. Massot, and P.S. Fitze. 2011. Mating does not influence reproductive investment, in a viviparous lizard. J Exp Zool 315A:458-464.
8. Bleu J., M. Massot, C. Haussy, and S. Meylan. 2012. Experimental litter size reduction reveals costs of gestation and delayed effects on offspring in a viviparous lizard. Proc R Soc B 279:489-498.
9. Blouin-Demers G. and P.J. Weatherhead. 2001. Thermal ecology of black rat snakes (Elaphe obsoleta) in a thermally challenging environment. Ecology 82:3025-3043.
10. Blount J.D., D.C. Houston, A.P. Møller, and J. Wright. 2003. Do individual branches of immune defence correlate? a comparative case study of scavenging and non-scavenging birds. Oikos 102:340-350.
11. Bonneaud C., J. Mazuc, G. Gonzalez, C. Haussy, O. Chastel, B. Faivre, and G. Sorci. 2003. Assessing the cost of mounting an immune response. Am Nat 161:367-379.
12. Carpenter C.C. and G.W. Ferguson. 1977. Variation and evolution of stereotyped behavior in reptiles. Pp. 335-554 in C.G.D.W. Tinkle, ed. Biology of the reptilia: ecology and behavior. Vol. 7. Academic Press, New York.
13. Clobert J., A. Oppliger, G. Sorci, B. Ernande, J.G. Swallow, and T. Garland Jr. 2000. Trade-offs in phenotypic traits: endurance at birth, growth, survival, predation and susceptibility to parasitism in a lizard, Lacerta vivipara. Funct Ecol 14:675-684.
14. Cote J., J. Clobert, L. Montes Poloni, C. Haussy, and S. Meylan. 2010. Food deprivation modifies corticosterone-dependent behavioural shifts in the common lizard. Gen Comp Endocrinol 166:142-151.
15. Deen C.M. and V.H. Hutchison. 2001. Effects of lipopolysaccharide and acclimation temperature on induced behavioral fever in juvenile Iguana iguana. J Therm Biol 26:55-63.
16. Eraud C., O. Duriez, O. Chastel, and B. Faivre. 2005. The energetic cost of humoral immunity in the collared dove, Streptopelia decaocto: is the magnitude sufficient to force energy-based trade-offs? Funct Ecol 19:110-118.
17. French S.S., D.F. DeNardo, and M.C. Moore. 2007. Trade-offs between the reproductive and immune systems: facultative responses to resources or obligate responses to reproduction? Am Nat 170:79-89.
18. French S.S., M.C. Moore, and G.E. Demas. 2009. Ecological immunology: the organism in context. Integr Comp Biol 49: 246-253.
19. Garland T., Jr., and J.B. Losos. 1994. Ecological morphology of locomotor performance in squamate reptiles. Pp. 240-302 in P.C. Wainwright and S.M. Reilly, eds. Ecological morphology: integrative organismal biology. University of Chicago Press, Chicago.
20. Gonzalez G., G. Sorci, A.P. Møller, P. Ninni, C. Haussy, and F. De Lope. 1999. Immunocompetence and condition-dependent sexual advertisement in male house sparrows (Passer domesticus). J Anim Ecol 68:1225-1234.
21. Graham A.L., D.M. Shuker, L.C. Pollitt, S.K.J.R. Auld, A.J. Wilson, and T.J. Little. 2011. Fitness consequences of immune responses: strengthening the empirical framework for ecoimmunology. Funct Ecol 25:5-17.
22. Hanssen S.A., D. Hasselquist, I. Folstad, and K.E. Erikstad. 2004. Costs of immunity: immune responsiveness reduces survival in a vertebrate. Proc R Soc B 271:925-930.
23. Herczeg G., A. Gonda, J. Saarikivi, and J. Merilä. 2006. Experimental support for the cost-benefit model of lizard thermoregulation. Behav Ecol Sociobiol 60:405-414.
24. Hertz P.E., R.B. Huey, and E. Nevo. 1982. Fight versus flight: body temperature influences defensive responses of lizards. Anim Behav 30:676-679.
25. Horak P., L. Saks, I. Ots, T. Kullissaar, H. Kollist, and M. Zilmer. 2003. Physiological effects of immune challenge in captive greenfinches (Carduelis chloris). Can J Zool 81:371-379.
26. Horak P., M. Zilmer, L. Saks, I. Ots, U. Karu, and K. Zilmer. 2006. Antioxidant protection, carotenoids and the costs of immune challenge in greenfinches. J Exp Biol 209:4329-4338.
27. Hudson L. and F.C. Hay. 1989. Practical immunology. Blackwell Scientific, Oxford.
28. Huey R.B. 1982a. Phylogenetic and ontogenetic determinants of sprint performance in some diurnal Kalahari lizards. Koedoe 25:43-48.
29. Huey R.B. 1982b. Temperature, physiology and the ecology of reptiles. Pp. 25-91 in C. Gans and F.H. Pough, eds. Biology of the reptilia. Vol. 12. Academic Press, New York.
30. Huyghe K., J.F. Husak, A. Herrel, Z. Tadic, I.T. Moore, R. Van Damme, and B. Vanhooydonck. 2009. Relationships between hormones, physiological performance and immunocompetence in a color-polymorphic lizard species, Podarcis melisellensis. Horm Behav 55:488-494.
31. Ilmonen P., T. Taarna, and D. Hasselquist. 2000. Experimentally activated immune defence in female pied flycatchers results in reduced breeding success. Proc R Soc B 267:665-670.
32. Lecomte J. 1993. Comportements du lézard vivipare. Université Paris Sud, Paris.
33. Lefranc A. and J. Bundgaard. 2000. The influence of male and female body size on copulation duration and fecundity in Drosophila melanogaster. Hereditas 132:243-247.
34. Le Galliard J.F., M. Massot, M.M. Landys, S. Meylan, and J. Clobert. 2006. Ontogenic sources of variation in sexual size dimorphism in a viviparous lizard. J Evol Biol 19:690-704.
35. Lewis L.Y. and R.E. Gatten. 1985. Aerobic metabolism of American alligators, Alligator mississippiensis, under standard conditions and during voluntary activity. Comp Biochem Physiol A 80:441-447.
36. Lochmiller R.L. and C. Deerenberg. 2000. Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos 88:87-98.
37. Lorenzon P., J. Clobert, and M. Massot. 2001. The contribution of phenotypic plasticity to adaptation in Lacerta vivipara. Evolution 55:392-404.
38. Martin L.B., D.M. Hawley, and D.R. Ardia. 2011. An introduction to ecological immunology. Funct Ecol 25:1-4.
39. Martin L.B., A. Scheuerlein, and M. Wikelski. 2003. Immune activity elevates energy expenditure of house sparrows: a link between direct and indirect costs? Proc R Soc B 270:153-158.
40. Massot M. and J. Clobert. 1995. Influence of maternal food availability on offspring dispersal. Behav Ecol Sociobiol 37: 413-418.
41. Massot M., J. Clobert, L. Montes-Poloni, C. Haussy, J. Cubo, and S. Meylan. 2011. An integrative study of ageing in a wild population of common lizards (Lacerta vivipara). Funct Ecol 25:848-858.
42. Meylan S., J. Belliure, J. Clobert, and M. de Fraipont. 2002. Stress and body condition as prenatal and postnatal determinants of dispersal in the common lizard (Lacerta vivipara). Horm Behav 42:319-326.
43. Meylan S. and J. Clobert. 2005. Is corticosterone-mediated phenotype development adaptive? maternal corticosterone treatment enhances survival in male lizards. Horm Behav 48:44-52.
44. Meylan S., J. Clobert, and B. Sinervo. 2007. Adaptive significance of maternal induction of density-dependent phenotypes. Oikos 116:650-661.
45. Meylan S., M. De Fraipont, P. Aragon, E. Vercken, and J. Clobert. 2009. Are dispersal-dependent behavioural traits produced by phenotypic plasticity? J Exp Zool 311A:377-388.
46. Meylan S., M. De Fraipont, and J. Clobert. 2004. Maternal size and stress and offspring philopatry: an experimental study in the common lizard (Lacerta vivipara). Ecoscience 11:123-129.
47. Meylan S., A. M. Duffy, and J. Clobert. 2003. The effect of transdermal corticosterone application on plasma corticosterone levels in pregnant Lacerta vivipara. Comp Biochem Physiol 134:497-503.
48. Meylan S., C. Haussy, and Y. Voituron. 2010. Physiological actions of corticosterone and its modulation by an immune challenge in reptiles. Gen Comp Endocrinol 169:158-166.
49. Miles D.B., R. Calsbeek, and B. Sinervo. 2007a. Corticosterone, locomotor performance, and metabolism in side-blotched lizards (Uta stansburiana). Horm Behav 51:548-554.
50. Miles D.B., B. Sinervo, L. Hazard, E. Svensson, and D. Costa. 2007b. Alternative mating strategies: integrating hormones, physiology and behavior. Funct Ecol 21:653-665.
51. Moret Y. and P. Schmid-Hempel. 2000. Survival for immunity: the price of immune system activation for bumblebee workers. Science 290:1166-1168.
52. Munoz F.A., S. Estrada-Parra, A. Romero-Rojas, T.M. Work, E. Gonzalez-Ballesteros, and I. Estrada-Garcia. 2009. Identification of CD3_T lymphocytes in the green turtle Chelonia mydas. Vet Immunol Immunopathol 131:211-217.
53. Ots I., A.B. Kerimov, E.V. Ivankina, T.A. Ilyina, and P. Horak. 2001. Immune challenge affects basal metabolic activity in wintering great tits. Proc R Soc B 268:1175-1181.
54. Partridge L. and M. Farquhar. 1983. Lifetime mating success of male fruitflies (Drosphilia melanogaster) is related to their size. Anim Behav 31:871-877.
55. Patterson J.W. and P.M.C. Davies. 1978. Preferred body temperature: seasonal and sexual differences in the lizard Lacerta vivipara. J Therm Biol 3:39-41.
56. Richard M., M. Massot, J. Clobert, and S. Meylan. 2012. Litter quality and inflammatory response are dependent on mating strategy in a reptile. Oecologia 170:39-46.
57. Roff D.A. and D.J. Fairbairn. 2007. The evolution of trade-offs: where are we? J Evol Biol 20:433-447.
58. Roitt I., J. Brostoff, and D. Male. 1998. Immunology. Gower Medical, London.
59. Schulenburg H., J. Kurtz, Y. Moret, and M.T. Siva-Jothy. 2009. Introduction. Ecological immunology. Philos Trans R Soc B 364:3-14.
60. Sheldon B.C. and S. Verhulst. 1996. Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol Evol 11:317-321.
61. Sherman E. and A. Stephens. 1998. Fever and metabolic rate in the toad Bufo marinus. J Therm Biol 23:49-52.
62. Sorci G. and B. Faivre. 2009. Inflammation and oxidative stress in vertebrate host-parasite systems. Philos Trans R Soc B 364: 71-83.
63. Sorci G., M. Massot, and J. Clobert. 1994. Maternal parasite load increases sprint speed and philopatry in female offspring of the common lizard. Am Nat 144:153-164.
64. Stearns S.C. 1992. The evolution of life histories. Oxford University Press, Oxford.
65. Stevenson R.D. 1985. The relative importance of behavioral and physiological adjustments controlling body temperature in terrestrial ectotherms. Am Nat 126:362-386.
66. Svensson E., L. Raberg, C. Koch, and D. Hasselquist. 1998. Energetic stress, immunosuppression and the costs of an antibody response. Funct Ecol 12:912-919.
67. Svensson E., B. Sinervo, and T. Comendant. 2001. Densitydependent competition and selection on immune function in genetic lizard morphs. Proc Natl Acad USA 98:12561-12565.
68. Tella J.L., J.A. Lemus, M. Carrete, and G. Blanco. 2008. The PHA test reflects acquired t-cell mediated immunocompetence in birds. PLoS ONE 3:e3295.
69. Uller T., C. Isaksson, and M. Olsson. 2006. Immune challenge reduces reproductive output and growth in a lizard. Funct Ecol 20:873-879.
70. Van Damme R., D. Bauwens, A.M. Castilla, and R.F. Verheyen. 1990. Comparative thermal ecology of the sympatric lizards Podarcis tiliguerta and Podarcis sicula. Acta Oecol 11:503-512.
71. Van Damme R., D. Bauwens, and R.F. Verheyen. 1986. Selected body temperatures in the lizard Lacerta vivipara: variation within and between populations. J Therm Biol 11:219-222.
72. Viney M.E., E.M. Riley, and K.L. Buchanan. 2005. Optimal immune responses: immunocompetence revisited. Trends Ecol Evol 20:665-669.
73. Vinkler M., H. Bainová, and T. Albrecht. 2010. Functional analysis of the skin-swelling response to phytohaemagglutinin. Funct Ecol 24:1081-1086.
74. Withers P.C. 1992. Comparative animal physiology. Saunders College, Philadelphia.
75. Zimmerman L.M., L.A. Vogel, and R.M. Bowden. 2010. Understanding the vertebrate immune system: insights from the reptilian perspective. J Exp Biol 213:661-671.