Do individual branches of immune defence correlate? A comparative case study of scavenging and non-scavenging birds

Costs of immunity are widely believed to play an important role in life history evolution, but most studies of ecological immunology have considered only single aspects of immune function. It is unclear whether we should expect correlated responses in other aspects of immune function not measured, b...

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Published inOikos Vol. 102; no. 2; pp. 340 - 350
Main Authors Blount, Jonathan D., Houston, David C., Møller, Anders Pape, Wright, Jonathan
Format Journal Article
LanguageEnglish
Published Copenhagen Munksgaard International Publishers 01.08.2003
Blackwell Publishers
Blackwell
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ISSN0030-1299
1600-0706
DOI10.1034/j.1600-0706.2003.12413.x

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Abstract Costs of immunity are widely believed to play an important role in life history evolution, but most studies of ecological immunology have considered only single aspects of immune function. It is unclear whether we should expect correlated responses in other aspects of immune function not measured, because individual branches of immune defence may differ in their running costs and thus may compete unequally for limiting resources, resulting in negatively correlated evolution. In theory such selection pressure may be most intense where species are hosts to more virulent parasites, thus facing a higher potential cost of parasitism. These issues are relatively unstudied, but could influence the efficiacy of attempting to estimate the scale and cost of host investment in immune defence. Here, in a comparative study of birds we found that species that scavenge at carcasses, that were hypothesised to be hosts to virulent parasites, had larger spleens for their body size and higher blood total leukocyte concentrations (general measures of immune function) than non-scavengers. These results support the hypothesis that scavengers are subject to strong parasite-mediated selection on immune defences. However, measures of specific branches of immune function revealed that scavengers had a relatively lower proportion of lymphocytes than phagocytic types of leukocytes, suggesting robust front line immune defences that could potentially reduce the need for mounting relatively energetically costly lymphocyte-dependent immune responses. Following experimental inoculation, scavengers produced significantly larger humoral immune responses, but not cell-mediated immune responses, than non-scavengers. However, the sizes of cell-mediated and humoral immune responses were not correlated across species. These results suggest that single measures of immune defence may not characterise the overall immune strategy, or reveal the likely costs involved.
AbstractList Costs of immunity are widely believed to play an important role in life history evolution, but most studies of ecological immunology have considered only single aspects of immune function. It is unclear whether we should expect correlated responses in other aspects of immune function not measured, because individual branches of immune defence may differ in their running costs and thus may compete unequally for limiting resources, resulting in negatively correlated evolution. In theory such selection pressure may be most intense where species are hosts to more virulent parasites, thus facing a higher potential cost of parasitism. These issues are relatively unstudied, but could influence the efficiacy of attempting to estimate the scale and cost of host investment in immune defence. Here, in a comparative study of birds we found that species that scavenge at carcasses, that were hypothesised to be hosts to virulent parasites, had larger spleens for their body size and higher blood total leukocyte concentrations (general measures of immune function) than non-scavengers. These results support the hypothesis that scavengers are subject to strong parasite-mediated selection on immune defences. However, measures of specific branches of immune function revealed that scavengers had a relatively lower proportion of lymphocytes than phagocytic types of leukocytes, suggesting robust front line immune defences that could potentially reduce the need for mounting relatively energetically costly lymphocyte-dependent immune responses. Following experimental inoculation, scavengers produced significantly larger humoral immune responses, but not cell-mediated immune responses, than non-scavengers. However, the sizes of cell-mediated and humoral immune responses were not correlated across species. These results suggest that single measures of immune defence may not characterise the overall immune strategy, or reveal the likely costs involved.
Costs of immunity are widely believed to play an important role in life history evolution, but most studies of ecological immunology have considered only single aspects of immune function. It is unclear whether we should expect correlated responses in other aspects of immune function not measured, because individual branches of immune defence may differ in their running costs and thus may compete unequally for limiting resources, resulting in negatively correlated evolution. In theory such selection pressure may be most intense where species are hosts to more virulent parasites, thus facing a higher potential cost of parasitism. These issues are relatively unstudied, but could influence the efficacy of attempting to estimate the scale and cost of host investment in immune defence. Here, in a comparative study of birds we found that species that scavenge at carcasses, that were hypothesised to be hosts to virulent parasites, had larger spleens for their body size and higher blood total leukocyte concentrations (general measures of immune function) than non‐scavengers. These results support the hypothesis that scavengers are subject to strong parasite‐mediated selection on immune defences. However, measures of specific branches of immune function revealed that scavengers had a relatively lower proportion of lymphocytes than phagocytic types of leukocytes, suggesting robust front line immune defences that could potentially reduce the need for mounting relatively energetically costly lymphocyte‐dependent immune responses. Following experimental inoculation, scavengers produced significantly larger humoral immune responses, but not cell‐mediated immune responses, than non‐scavengers. However, the sizes of cell‐mediated and humoral immune responses were not correlated across species. These results suggest that single measures of immune defence may not characterise the overall immune strategy, or reveal the likely costs involved.
Author Møller, Anders Pape
Blount, Jonathan D.
Houston, David C.
Wright, Jonathan
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Keywords Trophic group
Infection
Necrophagous
Vertebrata
Immune response
Interspecific comparison
Virulence
Defense mechanism
Selection pressure
Detritivorous
Aves
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1997; 114
1997; 150
2000; 89
1987; 104
2000; 88
1996; 71
1985; 125
1994; 69
1998; 83
1998; 82
1996; 32
1998; 44
2000; 290
1997; 8
1990
1967; 55
2000; 54
1997; 264
2000; 11
1997; 12
1999; 14
1985
2002; 269
1988; 130
1981
1998; 12
2001; 98
1976; 263
1997; 20
1992; 103
1995; 10
1999; 68
1996; 50
1998
1997
1995
1999; 141
1994
1994; 48
1993
1992
1999; 266
1991
1995; 350
1996; 59
1999; 9
1972; 3
1996; 11
1998; 191
1980; 59
1982; 85
1999; 39
1991; 70
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1992, 1994, 1996, 1997
1998; 265
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1991; 128
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Snippet Costs of immunity are widely believed to play an important role in life history evolution, but most studies of ecological immunology have considered only...
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SubjectTerms Animal and plant ecology
Animal, plant and microbial ecology
Animals
Autoecology
Aves
Biological and medical sciences
Biological taxonomies
Birds
Evolution
Fundamental and applied biological sciences. Psychology
Leukocytes
Lymphocytes
Parasite hosts
Parasites
Phylogeny
Spleen
Vertebrata
Wild birds
Title Do individual branches of immune defence correlate? A comparative case study of scavenging and non-scavenging birds
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Volume 102
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