Interpreting immunological indices: The importance of taking parasite community into account. An example in blackbirds<i>Turdus merula</i>

Biard, Clotilde; Monceau, Karine; Motreuil, Sébastien; Moreau, Jérôme

doi:10.1111/2041-210x.12371

Cited by 38 publications

(44 citation statements)

References 102 publications

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“…Furthermore, some parasites can manipulate the immune responses of their host and facilitate infections by other species of parasites (Biard et al . ). Thus, host species that invest more into reproduction are likely less able to mount effective immune responses against a variety of parasites, and end up acquiring a richer nematode community.…”

Section: Discussionmentioning

confidence: 97%

Nematode parasite diversity in birds: the role of host ecology, life history and migration

Leung

Koprivnikar

2016

Journal of Animal Ecology

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Previous studies have found that migratory birds generally have a more diverse array of pathogens such as parasites, as well as higher intensities of infection. However, it is not clear whether this is driven by the metabolic and physiological demands of migration, differential selection on host life-history traits or basic ecological differences between migratory and non-migratory species. Parasitic helminths can cause significant pathology in their hosts, and many are trophically transmitted such that host diet and habitat use play key roles in the acquisition of infections. Given the concurrent changes in avian habitats and migratory behaviour, it is critical to understand the degree to which host ecology influences their parasite communities. We examined nematode parasite diversity in 153 species of Anseriformes (water birds) and Accipitriformes (predatory birds) in relation to their migratory behaviour, diet, habitat use, geographic distribution and life history using previously published data. Overall, migrators, host species with wide geographic distributions and those utilizing multiple aquatic habitats had greater nematode richness (number of species), and birds with large clutches harboured more diverse nematode fauna with respect to number of superfamilies. Separate analyses for each host order found similar results related to distribution, habitat use and migration; however, herbivorous water birds played host to a less diverse nematode community compared to those that consume some animals. Birds using multiple aquatic habitats have a more diverse nematode fauna relative to primarily terrestrial species, likely because there is greater opportunity for contact with parasite infectious stages and/or consumption of infected hosts. As such, omnivorous and carnivorous birds using aquatic habitats may be more affected by environmental changes that alter their diet and range. Even though there were no overall differences in their ecology and life history compared with non-migrators, migratory bird species still harboured a more diverse array of nematodes, suggesting that this behaviour places unique demands on these hosts and warrants further study.

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Section: Discussionmentioning

confidence: 97%

Nematode parasite diversity in birds: the role of host ecology, life history and migration

Leung

Koprivnikar

2016

Journal of Animal Ecology

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“…We recommend that future research on the link between immunity and behavioural syndrome control for sex differences to take into account the differences between sexes for evolutionary trajectories and we urge researchers to pay attention to the choice of the proxy used to test POLS hypothesis to avoid misleading results (Biard et al . ).…”

Section: Discussionmentioning

confidence: 97%

“…Indeed, caution should be taken in the way immunological proxies are interpreted because immunity is also a multidimensional function (Biard et al . ) and might not be sufficient to actually predict immune efficacy (Pham & Schneider ). In the present study, we assessed the relationship between (i) personality and fitness and (ii) personality and immunity.…”

Section: Introductionmentioning

confidence: 99%

Personality, immune response and reproductive success: an appraisal of the pace‐of‐life syndrome hypothesis

Monceau

Dechaume-Moncharmont

Moreau

et al. 2017

Journal of Animal Ecology

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The pace-of-life syndrome (POLS) hypothesis is an extended concept of the life-history theory that includes behavioural traits. The studies challenging the POLS hypothesis often focus on the relationships between a single personality trait and a physiological and/or life-history trait. While pathogens represent a major selective pressure, few studies have been interested in testing relationships between behavioural syndrome, and several fitness components including immunity. The aim of this study was to address this question in the mealworm beetle, Tenebrio molitor, a model species in immunity studies. The personality score was estimated from a multidimensional syndrome based of four repeatable behavioural traits. In a first experiment, we investigated its relationship with two measures of fitness (reproduction and survival) and three components of the innate immunity (haemocyte concentration, and levels of activity of the phenoloxidase including the total proenzyme and the naturally activated one) to challenge the POLS hypothesis in T. molitor. Overall, we found a relationship between behavioural syndrome and reproductive success in this species, thus supporting the POLS hypothesis. We also showed a sex-specific relationship between behavioural syndrome and basal immune parameters. In a second experiment, we tested whether this observed relationship with innate immunity could be confirmed in term of differential survival after challenging by entomopathogenic bacteria, Bacillus thuringiensis. In this case, no significant relationship was evidenced. We recommend that future researchers on the POLS should control for differences in evolutionary trajectory between sexes and to pay attention to the choice of the proxy used, especially when looking at immune traits.

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“…This pattern could arise because of lower parental quality, since high-quality birds breed earlier in the season and are probably less likely to lose their first-laid clutches (Brinkhof et al 1999;Verhulst and Nilsson 2008). In addition, differences can arise because of differences in overall food quantity and quality or differential exposure to parasites and pathogens (Sorci et al 1997;Biard et al 2015;Muriel et al 2015b). In agreement with this possibility, we found an increase of trypanosomes and coccidia in replacement broods compared to first broods.…”

Section: Discussionmentioning

confidence: 99%

Sex-Specific Effects of High Yolk Androgen Levels on Constitutive and Cell-Mediated Immune Responses in Nestlings of an Altricial Passerine

Muriel

Pérez‐Rodríguez

Ortiz‐Santaliestra

et al. 2017

Physiological and Biochemical Zoology

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Avian embryos are exposed to yolk androgens that are incorporated into the egg by the ovulating female. These steroids can affect several aspects of embryo development, often resulting in increases in overall size or the speed of growth of different traits. However, several studies suggest that they also entail immune costs to the offspring. In this study, we explored whether variation in yolk androgen concentration affected several measures of the constitutive and cell-mediated immune axes in the spotless starling (Sturnus unicolor). Using a within-brood design, we injected different doses of androgens (testosterone and androstenedione) into the eggs. Our study showed that experimentally increased yolk androgens led to sex-specific immunosuppression in both the innate and adaptive axes of the immune system. Both cell-mediated immune response (CMI) and lysozyme activity decreased with increasing androgen levels injected into the egg in the case of male nestlings, whereas there were no effects on females. The effects that we found were always linear: no quadratic or threshold patterns were detected. We found no effects of the experimental treatment in hemolysis or agglutination capacity, but these measures were negatively correlated with CMI, suggesting negative correlation among different branches of the immune system. Blood (trypanosomes and hemosporidians) and intestinal (coccidia) parasites were not affected by the experimental increase of yolk androgen levels. Our results show that in our study species yolk androgens induce immunosuppression in some axes of the male nestling immune system. Further studies should analyze the proximate causes for these contrasting effects in different axes of the immune system and the reason for the differential impact on males and females.

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Interpreting immunological indices: The importance of taking parasite community into account. An example in blackbirdsTurdus merula

Cited by 38 publications

References 102 publications

Nematode parasite diversity in birds: the role of host ecology, life history and migration

Nematode parasite diversity in birds: the role of host ecology, life history and migration

Personality, immune response and reproductive success: an appraisal of the pace‐of‐life syndrome hypothesis

Sex-Specific Effects of High Yolk Androgen Levels on Constitutive and Cell-Mediated Immune Responses in Nestlings of an Altricial Passerine

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