Olivier Chastel

Assessing the cost of mounting an immune response.

The evolution of parasite resistance has often been assumed to be governed by antagonistic selection pressures. Defense against pathogens, by mounting an immune response, confers evident benefits but may also incur costs, so that the optimal level of defense is expected to depend on the balance between benefits and costs. Although the benefits of immune surveillance are well known, estimates of costs are still equivocal. Here we studied the behavioral and physiological modifications associated with exposure to a nonreplicating antigen (lipopolysaccharide [LPS] of Escherichia coli) in a passerine species, the house sparrow (Passer domesticus). We further investigated whether the behavioral and physiological changes provoked by LPS induced measurable repercussions on life‐history traits, such as the breeding effort and reproductive success. Finally, we tested whether the trade‐off between immune activation and breeding effort was modulated by the workload required to feed the brood. Exposure to LPS reduced activity and increased body mass loss of captive individuals; similarly, LPS injection induced a dramatic drop in feeding rate and reproductive success of breeding females. However, this reduction depended on brood size, suggesting that the strength of the trade‐off between immune activation and reproduction was affected by the workload required to feed the brood. Overall, this study stresses the magnitude of costs associated with mounting immune responses and the ecological and evolutionary consequences for natural populations.

Testosterone and oxidative stress: the oxidation handicap hypothesis

Secondary sexual traits (SST) are usually thought to have evolved as honest signals of individual quality during mate choice. Honesty of SST is guaranteed by the cost of producing/maintaining them. In males, the expression of many SST is testosterone-dependent. The immunocompetence handicap hypothesis has been proposed as a possible mechanism ensuring honesty of SST on the basis that testosterone, in addition to its effect on sexual signals, also has an immunosuppressive effect. The immunocompetence handicap hypothesis has received mixed support. However, the cost of testosterone-based signalling is not limited to immunosuppression and might involve other physiological functions such as the antioxidant machinery. Here, we tested the hypothesis that testosterone depresses resistance to oxidative stress in a species with a testosterone-dependent sexual signal, the zebra finch. Male zebra finches received subcutaneous implants filled with flutamide (an anti-androgen) or testosterone, or kept empty (control). In agreement with the prediction, we found that red blood cell resistance to a free radical attack was the highest in males implanted with flutamide and the lowest in males implanted with testosterone. We also found that cell-mediated immune response was depressed in testosterone-treated birds, supporting the immunocompetence handicap hypothesis. The recent finding that red blood cell resistance to free radicals is negatively associated with mortality in this species suggests that benefits of sexual signalling might trade against the costs derived from oxidation.

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.

Stress Response and the Value of Reproduction : Are Birds Prudent Parents?

In vertebrates, stressors such as starvation or predator attacks stimulate the rapid elevation of circulating glucocorticoid hormones, triggering physiological and behavioral responses that aid immediate survival but simultaneously inhibit reproduction. This stress response has been proposed to serve as a physiological mediator of life‐history trade‐offs: when the value of current reproduction is high relative to the value of future reproduction and survival, a mitigated stress response is expected to enable successful breeding and maximize fitness. Using phylogenetic comparative analyses, we investigated baseline and peak stress‐induced plasma corticosterone levels during parental care in 64 bird species. We found that (1) species with a higher value of the current brood relative to future breeding mounted weaker corticosterone responses during acute stress, and (2) females in species with more female‐biased parental care had weaker corticosterone responses. These results support the brood value hypothesis, suggesting that the stress response evolves as an adaptive basis for life‐history strategies. Further, we found that (3) baseline corticosterone correlated positively with brood value and negatively with body mass, and (4) peak corticosterone was greater in species breeding at higher latitudes. The latter findings suggest that circulating corticosterone concentrations might be matched to the anticipated demands and risks during nesting.

Body Condition and Seabird Reproductive Performance: A Study of Three Petrel Species

We investigated relationships between body condition (body mass scaled by body size) early in the breeding season and reproductive performance of three seabird species showing various life history traits. The study was conducted at Kerguelen Island from 1987 to 1994 on the Blue Petrel (Halobaena caerulea, an oceanic feeder), the Thin- billed Prion (Pachyptila belcheri, a neritic feeder), and the Common Diving Petrel (Pe- lecanoides urinatrix, a coastal feeder). Breeding success was highly variable among years in the three species, but the proportion of nonbreeding experienced breeders varied sig- nificantly only in the Blue Petrel. In the three species, body condition showed considerable year-to-year variation, suggesting substantial fluctuation in the availability of prey early in the breeding season. Relationships between early body condition and reproductive perfor- mance differed among the species. Reproductive success was significantly influenced by early condition in the Blue Petrel but not in the Thin-billed Prion and the Common Diving Petrel. In the long-lived Blue Petrel, depletion of body condition early in the breeding season resulted in a high proportion of nonbreeders and massive egg desertion. On the other hand, the shorter lived Thin-billed Prion and Common Diving Petrel seemed to respond by maintaining their reproductive output during poor years, probably investing more in the reproductive episode. Such contrasted patterns are analyzed in the light of reproductive effort and optimal clutch size theory.

MAJOR HISTOCOMPATIBILITY ALLELES ASSOCIATED WITH LOCAL RESISTANCE TO MALARIA IN A PASSERINE

Abstract Malaria parasites are a major cause of human mortality in tropical countries and a potential threat for wildlife, as witnessed by the malaria‐induced extinction of naive Hawaiian avifauna. Identifying resistance mechanisms is therefore crucial both for human health and wildlife conservation. Patterns of malaria resistance are known to be highly polygenic in both humans and mice, with marked contributions attributed to major histocompatibility (Mhc) genes. Here we show that specific Mhc variants are linked to both increased resistance and susceptibility to malaria infection in a wild passerine species, the house sparrow (Passer domesticus). In addition, links between host immunogenetics and resistance to malaria involved population‐specific alleles, suggesting local adaptationn in this host‐parasite interaction. This is the first evidence for a population‐specific genetic control of resistance to malaria in a wild species.

Complex Mhc-based mate choice in a wild passerine

The extreme polymorphism of the vertebrate major histocompatibility complex (Mhc) is famous for protecting hosts against constantly evolving pathogens. Mate choice is often evoked as a means of maintaining Mhc variability through avoidance of partners with similar Mhc alleles or preference for heterozygotes. Evidence for these two hypotheses mostly comes from studies on humans and laboratory mice. Here, we tested these hypotheses in a wild outbred population of house sparrows (Passer domesticus). Females were not more or less closely related to the males they paired with when considering neutral genetic variation. However, males failed to form breeding pairs when they had too few Mhc alleles and when they were too dissimilar from females at Mhc loci (i.e. had no common alleles). Furthermore, pairs did not form at random as Mhc diversity positively correlated in mating pairs. These results suggest that mate choice evolves in response to (i) benefits in terms of parasite resistance acquired from allelic diversity, and (ii) costs associated with the disruption of co-adapted genes.

Terminal investment induced by immune challenge and fitness traits associated with major histocompatibility complex in the house sparrow

Abstract The terminal investment hypothesis predicts that individuals should invest more in their present reproduction if they are less likely to survive to future reproductive events. Infections, which reduce viability, may be used by individuals as a cue of a diminishing residual reproductive value and could therefore theoretically trigger an intensification of breeding effort. We tested this hypothesis in a natural population of house sparrows (Passer domesticus). We manipulated the immune system of breeding females by injecting them with a vaccine against the Paramyxo virus, the agent of Newcastle disease. Females were captured and treated immediately after completion of their first clutch either with the vaccine (NDV) or with phosphate buffered saline (PBS). The entire clutch was subsequently removed. We also screened Mhc class I genes of females to assess possible genotype‐by‐immune treatment interactions on reproductive investment. Our results indicate that vaccinated females were more likely to lay replacement clutches and that the difference in number of eggs between first and replacement clutches was greater for NDV females than for controls. In addition, chick size, both in terms of tarsus length and body mass, was affected by immune activation but in interaction with nestling age and female body mass, respectively. Mhc genotype‐by‐immune treatment interactions were never significant; however, allelic diversity was positively correlated with nestling survival. These results show that immune system activation is potentially used as a cue of reduced survival prospect and appears to induce a costly terminal investment behavior, and Mhc diversity might be under selection in a natural population of house sparrows.

High annual variability in reproductive success and survival of an Antarctic seabird, the snow petrel Pagodroma nivea

Demographic parameters were estimated for snow petrels Pagodroma nivea nesting at Pointe Géologie Archipelago, Adélie Land, Antarctica between 1963 and 1990; 21 years of data on adult survival and 27 years of data on breeding success are available. The average age of first return and first breeding were 8.1 and 9.9 years respectively and there was no signifcant difference between the sexes. The overall breeding success averaged 51.3% and was very variable between years (21–80%). Breeding failure was mostly due to incubation failure and annual breeding success was negatively correlated with average snow falls in October–November and October–March. Breeding frequency was very low, averaging 52% of seasons during a reproductive lifetime. Good quality sites, with high occupancy rate and high breeding success were few in the study plots. Poor years in 1966–1967, 1976–1977 and 1983–1984, with low breeding success, very low proportions of nets with breeding attempts and high numbers of non-breeders, occurred 1 year after large-scale El Niño Southern Oscillation (ENSO) events. Snow petrels exhibited very low philopatry. Only 45 birds have been recovered in the study plots from a total of 1115 banded fledglings giving an estimated rate of return of 12.9% between fledging and 3 years old. Annual survival between 3 and 10 years was 91.4%. Annual adult survival (93.4%), though variable, was low during poor years of 1977–1978 and 1983–1984. Adult survival of males (94.7%) was not significantly different from that of females (93.9%). Over the study period, the population of Pointe Géologie was stable. Using the estimated parameters, a Leslie model gave a growth rate of 0.948%, which was probably compensated by immigration (5.7% per year). Restricted numbers of good-quality sites at the place of birth could have led young birds to prospect other colonies and could have selected low philopatry. High adult survival, strong site tenacity and capacity to spread breeding over a long lifetime are probably part of the adaptive strategy of this small fulmarine petrel facing highly variable environmental conditions.

Patterns of aging in the long-lived wandering albatross

How does an animal age in natural conditions? Given the multifaceted nature of senescence, identifying the effects of age on physiology and behavior remains challenging. We investigated the effects of age on a broad array of phenotypic traits in a wild, long-lived animal, the wandering albatross. We studied foraging behavior using satellite tracking and activity loggers in males and females (age 6–48+ years), and monitored reproductive performance and nine markers of baseline physiology known to reflect senescence in vertebrates (humoral immunity, oxidative stress, antioxidant defenses, and hormone levels). Age strongly affected foraging behavior and reproductive performance, but not baseline physiology. Consistent with results of mammal and human studies, age affected males and females differently. Overall, our findings demonstrate that age, sex, and foraging ability interact in shaping aging patterns in natural conditions. Specifically, we found an unexpected pattern of spatial segregation by age; old males foraged in remote Antarctica waters, whereas young and middle-aged males never foraged south of the Polar Front. Old males traveled a greater distance but were less active at the sea surface, and returned from sea with elevated levels of stress hormone (corticosterone), mirroring a low foraging efficiency. In contrast to findings in captive animals and short-lived birds, and consistent with disposable soma theory, we found no detectable age-related deterioration of baseline physiology in albatrosses. We propose that foraging efficiency (i.e., the ability of individuals to extract energy from their environment) might play a central role in shaping aging patterns in natural conditions.