Godefroy Devevey

An Experimental Test of the Dose-Dependent Effect of Carotenoids and Immune Activation on Sexual Signals and Antioxidant Activity

Carotenoid‐based sexual traits are thought to be reliable indicators of male quality because they might be scarce and therefore might indicate the ability of males to gather high‐quality food and because they are involved in important physiological functions (as immune enhancers and antioxidants). We performed an experiment where male and female zebra finches (Taeniopygia guttata) were provided with increasing carotenoid doses in the drinking water during 4 weeks (bill color of this species is a carotenoid‐based sexual signal). Simultaneously, birds were split into two groups: one receiving weekly injections of Escherichia coli lipopolysaccharide in order to activate the immune system, the other being injected with the same volume of phosphate buffered saline. We assessed how carotenoid availability and immune activation affected the amount of circulating plasma carotenoids, the beak color, and the antioxidant defenses (assessed as the resistance of red blood cells to a controlled free radical attack). Carotenoid availability affected the amount of circulating carotenoids and beak color; both variables reached a plateau at the highest carotenoid doses. Immune activation diverted carotenoids from plasma, and this in turn affected the expression of the sexual trait. Finally, we found a positive correlation between the change in circulating carotenoids and antioxidant defenses. These results support the idea that carotenoids have important physiological properties that ensure the honesty of carotenoid‐based sexual traits.

AN EXPERIMENTAL MANIPULATION OF LIFE-HISTORY TRAJECTORIES AND RESISTANCE TO OXIDATIVE STRESS

Abstract Optimal investment into life‐history traits depends on the environmental conditions that organisms are likely to experience during their life. Evolutionary theory tells us that optimal investment in reproduction versus maintenance is likely to shape the pattern of age‐associated decline in performance, also known as aging. The currency that is traded against different vital functions is, however, still debated. Here, we took advantage of a phenotypic manipulation of individual quality in early life to explore (1) long‐term consequences on life‐history trajectories, and (2) the possible physiological mechanism underlying the life‐history adjustments. We manipulated phenotypic quality of a cohort of captive zebra finches (Taeniopygia guttata) by assigning breeding pairs to either an enlarged or a reduced brood. Nestlings raised in enlarged broods were in poorer condition than nestlings raised in reduced broods. Interestingly, the effect of environmental conditions experienced during early life extended to the age at first reproduction. Birds from enlarged broods delayed reproduction. Birds that delayed reproduction produced less offspring but lived longer, although neither fecundity nor longevity were directly affected by the experimental brood size. Using the framework of the life‐table response experiment modeling, we also explored the effect of early environmental condition on population growth rate and aging. Birds raised in reduced broods tended to have a higher population growth rate, and a steeper decrease of reproductive value with age than birds reared in enlarged broods. Metabolic resources necessary to fight off the damaging effect of reactive oxygen species (ROS) could be the mechanism underlying the observed results, as (1) birds that engaged in a higher number of breeding events had a weaker red blood cell resistance to oxidative stress, (2) red blood cell resistance to oxidative stress predicted short‐term mortality (but not longevity), and (3) was related with a parabolic function to age. Overall, these results highlight that early condition can have long‐term effects on life‐history trajectories by affecting key life‐history traits such as age at first reproduction, and suggest that the trade‐off between reproduction and self‐maintenance might be mediated by the cumulative deleterious effect of ROS.

Neonatal nutrition, adult antioxidant defences and sexual attractiveness in the zebra finch

Early nutrition has recently been shown to have pervasive, downstream effects on adult life–history parameters including lifespan, but the underlying mechanisms remain poorly understood. Damage to biomolecules caused by oxidants, such as free radicals generated during metabolic processes, is widely recognized as a key contributor to somatic degeneration and the rate of ageing. Lipophilic antioxidants (carotenoids, vitamins A and E) are an important component of vertebrate defences against such damage. By using an avian model, we show here that independent of later nutrition, individuals experiencing a short period of low–quality nutrition during the nestling period had a twofold reduction in plasma levels of these antioxidants at adulthood. We found no effects on adult external morphology or sexual attractiveness: in mate–choice trials females did not discriminate between adult males that had received standard– or lower–quality diet as neonates. Our results suggest low–quality neonatal nutrition resulted in a long–term impairment in the capacity to assimilate dietary antioxidants, thereby setting up a need to trade off the requirement for antioxidant activity against the need to maintain morphological development and sexual attractiveness. Such state–dependent trade–offs could underpin the link between early nutrition and senescence.

Fecundity and survival in relation to resistance to oxidative stress in a free-living bird.

Major life history traits, such as fecundity and survival, have been consistently demonstrated to covary positively in nature, some individuals having more resources than others to allocate to all aspects of their life history. Yet, little is known about which resources (or state variables) may account for such covariation. Reactive oxygen species (ROS) are natural by-products of metabolism and, when ROS production exceeds antioxidant defenses, organisms are exposed to oxidative stress that can have deleterious effects on their fecundity and survival. Using a wild, long-lived bird, the Alpine Swift (Apus melba), we examined whether individual red cell resistance to oxidative stress covaried with fecundity and survival. We found that males that survived to the next breeding season tended to be more resistant to oxidative stress, and females with higher resistance to oxidative stress laid larger clutches. Furthermore, the eggs of females with low resistance to oxidative stress were less likely to hatch than those of females with high resistance to oxidative stress. By swapping entire clutches at clutch completion, we then demonstrated that hatching failure was related to the production of low-quality eggs by females with low resistance to oxidative stress, rather than to inadequate parental care during incubation. Although male and female resistance to oxidative stress covaried with age, the relationships among oxidative stress, survival, and fecundity occurred independently of chronological age. Overall, our study suggests that oxidative stress may play a significant role in shaping fecundity and survival in the wild. It further suggests that the nature of the covariation between resistance to oxidative stress and life history traits is sex specific, high resistance to oxidative stress covarying primarily with fecundity in females and with survival in males.

Carotenoids modulate the trade-off between egg production and resistance to oxidative stress in zebra finches

The allocation of resources to reproduction and survival is a central question of studies of life history evolution. Usually, increased allocation to current reproduction is paid in terms of reduced future reproduction and/or decreased survival. However, the proximal mechanisms underlying the cost of reproduction are poorly understood. Recently, it has been shown that increased susceptibility to oxidative stress might be one of such proximate links between reproduction and self-maintenance. Organisms possess a range of antioxidant defenses, including endogenously produced molecules (e.g., enzymes) and compounds ingested with food (e.g., carotenoids). If reproductive effort increases the production of reactive oxygen species, the availability of antioxidant defenses may partly or fully counteract the free-radical damages. One could, therefore, expect that the trade-off between reproduction and oxidative stress is modulated by the availability of antioxidant defenses. We tested this hypothesis in zebra finches. We manipulated reproductive effort by either allowing or preventing pairs to breed. Within each breeding or non-breeding group, the availability of antioxidant compounds was manipulated by supplementing or not supplementing the drinking water with carotenoids. We found that although birds in the breeding and non-breeding groups did not differ in their resistance to oxidative stress (the breakdown of red blood cells submitted to a controlled free-radical attack), one aspect of breeding effort (i.e., the number of eggs laid by birds in both breeding and non-breeding groups) was negatively correlated with resistance to oxidative stress only in birds that did not benefit from a carotenoid-supplemented diet. This result therefore suggests that carotenoid availability can modulate the trade-off between reproduction and resistance to oxidative stress.

Twofold cost of reproduction: an increase in parental effort leads to higher malarial parasitaemia and to a decrease in resistance to oxidative stress

Parental effort is usually associated with high metabolism that could lead to an increase in the production of reactive oxidative species giving rise to oxidative stress. Since many antioxidants involved in the resistance to oxidative stress can also enhance immune function, an increase in parental effort may diminish the level of antioxidants otherwise involved in parasite resistance. In the present study, we performed brood size manipulation in a population of great tits (Parus major) to create different levels of parental effort. We measured resistance to oxidative stress and used a newly developed quantitative PCR assay to quantify malarial parasitaemia. We found that males with an enlarged brood had significantly higher level of malarial parasites and lower red blood cell resistance to free radicals than males rearing control and reduced broods. Brood size manipulation did not affect female parasitaemia, although females with an enlarged brood had lower red blood cell resistance than females with control and reduced broods. However, for both sexes, there was no relationship between the level of parasitaemia and resistance to oxidative stress, suggesting a twofold cost of reproduction. Our results thus suggest the presence of two proximate and independent mechanisms for the well-documented trade-off between current reproductive effort and parental survival.

Environmental stress affects the expression of a carotenoid-based sexual trait in male zebra finches

SUMMARY Abiotic factors including thermal stress are suggested to exert constrains on sexual ornaments through trade-offs between sexual displays and physiological functions related to self-maintenance. Given the health properties of carotenoid pigments, carotenoid-based ornaments offer a relevant context in which to investigate the effect of environmental stress, such as ambient temperature, on the production and maintenance of secondary sexual traits and, also, to explore the proximate mechanisms shaping their expression. In this study, we exposed male zebra finches (Taeniopygia guttata) to environmental stress by exposing them to two temperature regimes (6 and 26°C) over a 4 week period. Simultaneously, half of the males in each temperature group were supplemented with carotenoids, whereas the other half were not. The expression of a carotenoid-based sexual trait (bill colour) and the amount of circulating carotenoids were assessed before and at the end of the experiment. Carotenoid-supplemented males developed a redder bill, but the effect of supplementation was reduced under cold exposure. However, we found evidence that birds facing a cold stress were carotenoid limited, since supplemented males developed redder bills than the non-supplemented ones. Interestingly, while cold-exposed and non-supplemented males developed duller bills, they circulated a higher amount of carotenoids at the end of the experiment compared to the pre-experimental values. Together, these results suggest that ambient temperature might contribute to the modulation of the expression of carotenoid-based ornaments. Our findings suggest that carotenoids are a limiting resource under cold exposure and that they might be prioritized for self-maintenance at the expense of the ornament. The physiological functions related to self-maintenance that might have benefited from carotenoid saving are discussed.

First arrived takes all: inhibitory priority effects dominate competition between co-infecting Borrelia burgdorferi strains

BackgroundWithin-host microbial communities and interactions among microbes are increasingly recognized as important factors influencing host health and pathogen transmission. The microbial community associated with a host is indeed influenced by a complex network of direct and indirect interactions between the host and the lineages of microbes it harbors, but the mechanisms are rarely established. We investigated the within-host interactions among strains of Borrelia burgdorferi, the causative agent of Lyme disease, using experimental infections in mice. We used a fully crossed-design with three distinct strains, each group of hosts receiving two sequential inoculations. We used data from these experimental infections to assess the effect of coinfection on bacterial dissemination and fitness (by measuring the transmission of bacteria to xenodiagnostic ticks) as well as the effect of coinfection on host immune response compared to single infection.ResultsThe infection and transmission data strongly indicate a competitive interaction among B. burgdorferi strains within a host in which the order of appearance of the strain is the main determinant of the competitive outcome. This pattern is well described by the classic priority effect in the ecological literature. In all cases, the primary strain a mouse was infected with had an absolute fitness advantage primarily since it was transmitted an order of magnitude more than the secondary strain. The mechanism of exclusion of the secondary strain is an inhibition of the colonization of mouse tissues, even though 29% of mice showed some evidence of infection by secondary strain. Contrary to expectation, the strong and specific adaptive immune response evoked against the primary strain was not followed by production of immunoglobulins after the inoculation of the secondary strain, neither against strain-specific antigen nor against antigens common to all strains. Hence, the data do not support a major role of the immune response in the observed priority effect.ConclusionThe strong inhibitory priority effect is a dominant mechanism underlying competition for transmission between coinfecting B. burgdorferi strains, most likely through resource exploitation. The observed priority effect could shape bacterial diversity in nature, with consequences in epidemiology and evolution of the disease.

The effect of spatial heterogenity on the aggregation of ticks on white-footed mice.

Parasites are often aggregated on a minority of the individuals in their host populations. Although host characteristics are commonly presumed to explain parasite aggregation on hosts, spatio-temporal aggregation of parasites during their host-seeking stages may have a dominant effect on the aggregation on hosts. We aimed to quantify, using mixed models, repeatability and autocorrelation analyses, the degree to which the aggregation of blacklegged ticks (Ixodes scapularis) on white-footed mice (Peromyscus leucopus) is influenced by spatio-temporal distributions of the host-seeking ticks and by heterogeneity among mice. Host-seeking ticks were spatially aggregated at both the larval and nymphal life-stages. However, this spatial aggregation accounted for little of the variation in larval and nymphal burdens observed on mice (3% and 0%, respectively). Conversely, mouse identity accounted for a substantial proportion of the variance in tick burdens. Mouse identity was a significant explanatory factor as the majority of ticks parasitized a consistent set of mice throughout the activity seasons. Of the characteristics associated with mouse identity investigated, only gender affected larval burdens, and body mass and home range sizes in males were correlated with nymphal burdens. These analyses suggest that aggregation of ticks on a minority of mice does not result from the distribution of host-seeking ticks but from characteristics of the hosts.

Flea infestation reduces the life span of the common vole.

Parasitism is often a source of variation in hosts fitness components. Understanding and estimating its relative importance for fitness components of hosts is fundamental from physiological, ecological and evolutionary perspectives. Host-parasite studies have often reported parasite-induced reduction of host fecundity, whereas the effect of parasitism on host survival has been largely neglected. Here, we experimentally investigated the effect of infestation by rat fleas (Nosopsyllus fasciatus) on the life span of wild-derived male common voles (Microtus arvalis) bred in captivity. We found that the mean life span of parasitized voles was reduced by 36% compared to control voles. Parasitized voles had a smaller body size, but a relatively larger heart and spleen than control voles. These results indicate an effect of flea infestation on host life span and our findings strongly suggest that ectoparasites should be taken into account in the studies of host population dynamics.