Effects of experimental brood size manipulation and gender on carotenoid levels of Eurasian kestrels Falco tinnunculus.

BACKGROUND: Animals use carotenoid-pigments for coloration, as antioxidants and as enhancers of the immune system. Carotenoid-dependent colours can thus signal individual quality and carotenoids have also been suggested to mediate life-history trade-offs. METHODOLOGY: To examine trade-offs in carotenoid allocation between parents and the young, or between skin coloration and plasma of the parents at different levels of brood demand, we manipulated brood sizes of Eurasian kestrels (Falco tinnunculus). PRINCIPAL FINDINGS: Brood size manipulation had no overall effect on plasma carotenoid levels or skin hue of parents, but female parents had twice the plasma carotenoid levels of males. Males work physically harder than females and they might thus also use more carotenoids against oxidative stress than females. Alternatively, females could be gaining back the carotenoid stores they depleted during egg-laying by eating primarily carotenoid-rich food items during the early nestling stage. Fledglings in enlarged broods had higher plasma carotenoid concentrations than those in reduced broods. This difference was not explained by diet. In light of recent evidence from other species, we suggest it might instead be due to fledglings in enlarged broods having higher testosterone levels, which in turn increased plasma carotenoid levels. The partial cross-foster design of our experiment revealed evidence for origin effects (genetic or maternal) on carotenoid levels of fledglings, but no origin-environment interaction. SIGNIFICANCE: These results from wild birds differ from studies in captivity, and thus offer new insights into carotenoid physiology in relation to division of parental care and demands of the brood.

Antioxidant protection, carotenoids and the costs of immune challenge in greenfinches.

Costs accompanying immune challenges are believed to play an important role in life-history trade-offs and warranting the honesty of signal traits. We performed an experiment in captive greenfinches (Carduelis chloris L.) in order to test whether and how humoral immune challenge with non-pathogenic antigen [sheep red blood cells (SRBC)] affects parameters of individual condition including intensity of coccidian infection, estimates of total antioxidant protection, plasma carotenoids and ability to mount a cell-mediated immune response. We also asked whether the potential costs of immune challenge can be alleviated by dietary carotenoid supplementation. None of the treatments affected intensity of coccidiosis. Humoral immune challenge suppressed the cell-mediated response to phytohemagglutinin (PHA), suggesting a trade-off between the uses of different arms of the immune system. Immune challenge reduced body-mass gain, but only among the carotenoid-depleted birds, indicating that certain somatic costs associated with immune system activation can be alleviated by carotenoids. No evidence for oxidative stress-induced immunopathological damages could be found because immune activation did not affect total antioxidant protection or carotenoid levels. Carotenoid supplementation inclined birds to fattening, indicating that lutein interfered with lipid metabolism. Altogether, our results support the hypotheses of biological importance of carotenoids and exemplify the overwhelming complexity of their integrated ecophysiological functions.

When not to avoid inbreeding.

Avoidance of incestuous matings is widely reported across many animal taxa, and the adaptive value of such behavior is explained through inbreeding depression. However, an old and somewhat neglected theoretical result predicts that inbred matings offer another, positive effect on the inclusive fitness of parents: an individual who mates with a relative will help that relative to spread genes identical by descent. This benefit can be substantial, if the additional mating achieved by the relative does not harm his mating success otherwise, and in the context of selfing in plants the phenomenon is well known. Here, we develop a model that derives expected values of inbreeding tolerance, that is, the magnitude of inbreeding depression that is required to make individuals avoid inbreeding, for different animal life histories and parental investment patterns. We also distinguish between simultaneous and sequential mate choice, and show that inbreeding tolerance should often be remarkably high in the latter scenario in particular, although egalitarian parental care will lead to lower tolerance. There is a mismatch between theory and data: the almost complete lack of cases where individuals prefer to mate incestuously is at odds with a large overlap between the predicted range of inbreeding tolerance and estimates of inbreeding depression found in nature. We discuss four different solutions to this enigma, and suggest that inbreeding tolerance, where it is found, should not always be attributed to a simple constraint that has prevented finding any other mate.

Immune response is energetically costly in white cabbage butterfly pupae.

Parasite-driven coevolution has led hosts to develop a complicated and potentially costly defence machinery, consisting mainly of the immune system. Despite the evidence for the trade-offs between immune function and life-history traits, it is still obscure how the costs of using and maintaining the immune function are paid. We tested whether immune challenge is energetically costly for white cabbage butterfly (Pieris brassicae L.) diapausing pupa. Individuals challenged with nylon implant raised their standard metabolic rate nearly 8% compared to the controls. Hence, costs of activation of immune system in insect pupa can be expressed in energetic currency.

Carotenoid-based plumage coloration of male greenfinches reflects health and immunocompetence.

Hypotheses of parasite-mediated sexual selection (PMSS) propose that elaborate male ornaments have evolved due to female preferences. Females would benefit from mating with more ornamental males if males' ornamentation signals their health status and ability to provide parasite resistance genes for the offspring. Carotenoid-based plumage coloration of birds has been hypothesised to honestly reflect an individual's health status due to trade-off in allocation of carotenoids between maintenance and signalling functions. The prediction of this hypothesis, namely that individuals with brighter plumage are able to mount stronger immune responses against novel antigens and reveal generally better health state, was tested in captive male greenfinches (Carduelis chloris). Greenfinches with brighter yellow breast feathers showed stronger humoral immune response against novel antigen (SRBC) while no relationship between plumage coloration and an estimate of cell-mediated immune responsiveness (PHA response) was detected. Elaborately ornamental individuals had better general health state as indicated by the negative correlations between plumage brightness and heterophil haemoconcentration. Consistent with the concept of PMSS, these results suggest that carotenoid-based plumage coloration in greenfinches honestly signals immunocompetence and health status.

Carotenoid-based plumage coloration reflects hemoparasite infection and local survival in breeding great tits.

Carotenoid-based sexual coloration has been hypothesised to be prevalent across many vertebrate taxa because it reliably reflects individual phenotypic quality in terms of foraging efficiency or health status due to the trade-off between signal colour and use of carotenoids for immune function and detoxification. We investigated the ventral, yellow coloration of breeding adult great tits (Parus major L.) in relation to sex, age, breeding habitat, local survival and infection status with respect to Haemoproteus blood parasites. The extent of plumage coloration (estimated as hue and lutein absorbance) was generally higher in rural than in urban birds. Males had higher values of hue than females. In both male and female yearlings, the plumage of unparasitised individuals had a greater hue of yellow than parasitised ones, while older males revealed the opposite pattern. The survival of infected yearlings was worse than that of uninfected yearlings, while the opposite was true for old breeders. Survivors had generally higher values of hue than non-survivors. These results are consistent with predictions of functional hypotheses, suggesting that carotenoid-based plumage coloration serves as a signal reflecting individual quality in terms of health status and local survival.

Do great tits (Parus major) starve to reproduce?

To test whether nest abandonment is associated with parental health state, reproductive parameters and parental condition indices were examined in relation to brood desertion in great tits. Before desertion, pairs that abandoned their broods in the second half of the nestling period had significantly higher nestling mortality as well as lower average weight of nestlings and entire broods. Independently of brood size, female great tits that deserted their broods on average weighed 1 g (>5%) more than non-deserters. Comparison of metabolic profiles revealed that deserting females were in better nutritional condition (inclined to fat deposition) than non-deserters, which showed symptoms of postresorptive catabolic state, as indicated by a lower level of plasma triglycerides, very low density lipoproteins, and a higher level of free fatty acids and ß-hydroxy-butyrate. These results suggest that desertion can be regarded as a reproductive restraint and that non-deserting females invested at least some of their maintenance resources on brood rearing. We found no evidence that desertion or non-desertion was associated with age- or disease-related differences in residual reproductive values. Male condition was not related to brood abandonment, suggesting that desertions were primarily initiated by females.

Immune function and survival of great tit nestlings in relation to growth conditions.

Life history theory predicts a trade-off between number and quality of offspring. Reduced quality with increasing brood size may arise from a decrease in body condition or in immunocompetence that would be important in fighting off virulent parasites by immunologically naive offspring. We tested the effect of rearing conditions on immune function of nestling great tits (Parus major) by reducing or increasing broods by two hatchlings. In the middle of the nestling period (on day 8), nestlings from enlarged broods developed lower T cell responses [as measured from the cutaneous swelling reaction to injection with phytohaemagglutinin (PHA)] and tended to have lower total leukocyte and lymphocyte concentrations in their peripheral blood than nestlings from reduced broods. Brood size manipulation affected the PHA response of nestlings most strongly in small clutches, suggesting that nestling immune function was dependent on their parents' condition, as estimated by original clutch size. Intra-brood differences in nestling mortality were unrelated to immune parameters, but nestlings in broods without mortality had a stronger PHA response, higher concentration of lymphocytes and higher body mass on day 15 than nestlings in broods with mortality. These results support the prediction that the immune function of altricial birds is affected by rearing conditions, and that growth and immune parameters are related to inter-brood differences in nestling survival.

Health impact of blood parasites in breeding great tits.

Hypotheses of hemoparasite-mediated sexual selection and reproductive costs rely on the assumption that avian blood parasite infections are harmful to their hosts. To test the validity of this assumption, we examined the health impact of Haemoproteus blood parasites on their great tit (Parus major) host. We hypothesised that if blood parasites impose any serious health impact on their avian hosts, then infected individuals must differ from uninfected ones in respect to hemato-serological general health and immune parameters. A 3-year study of two great tit populations, breeding in contrasting (urban and rural) habitats in south-east Estonia, revealed that Haemoproteus blood parasites affected the health state of their avian hosts. Infected individuals had elevated lymphocyte hemoconcentration and plasma gamma-globulin levels, indicating that both cell-mediated and humoral immune response mechanisms are involved in host defence. The effect of parasites on cell-mediated immunity was both age- and sex-specific, as infection status affected peripheral blood lymphocyte counts only in males, and among these, the magnitude of response was greater in old individuals than yearlings. Heterophile hemoconcentration and plasma albumin levels were not affected by infection status, suggesting that blood stages of Haemoproteus infection do not cause a severe inflammatory response. Parasitism was not related to hematocrit values, indicating that Haemoproteus infection does not cause anemia. In two years, infected individuals were heavier than uninfected ones in the urban but not in the rural study area. This suggests, that under certain circumstances (possibly related to reproductive tactics), breeding great tits may avoid losing body mass in order to save resources for an anti-parasite immune response.