Indirect effects of parasitism: costs of infection to other individuals can be greater than direct costs borne by the host.

Parasitic infection has a direct physiological cost to hosts but may also alter how hosts interact with other individuals in their environment. Such indirect effects may alter both host fitness and the fitness of other individuals in the host's social network, yet the relative impact of direct and indirect effects of infection are rarely quantified. During reproduction, a host's social environment includes family members who may be in conflict over resource allocation. In such situations, infection may alter how resources are allocated, thereby redistributing the costs of parasitism between individuals. Here, we experimentally reduce parasite burdens of parent and/or nestling European shags (Phalacrocorax aristotelis) infected with Contracaecum nematodes in a factorial design, then simultaneously measure the impact of an individual's infection on all family members. We found no direct effect of infection on parent or offspring traits but indirect effects were detected in all group members, with both immediate effects (mass change and survival) and longer-term effects (timing of parents' subsequent breeding). Our results show that parasite infection can have a major impact on individuals other than the host, suggesting that the effect of parasites on population processes may be greater than previously thought.

Drug treatment of malaria infections can reduce levels of protection transferred to offspring via maternal immunity.

Maternally transferred immunity can have a fundamental effect on the ability of offspring to deal with infection. However, levels of antibodies in adults can vary both quantitatively and qualitatively between individuals and during the course of infection. How infection dynamics and their modification by drug treatment might affect the protection transferred to offspring remains poorly understood. Using the rodent malaria parasite Plasmodium chabaudi, we demonstrate that curing dams part way through infection prior to pregnancy can alter their immune response, with major consequences for offspring health and survival. In untreated maternal infections, maternally transferred protection suppressed parasitaemia and reduced pup mortality by 75 per cent compared with pups from naïve dams. However, when dams were treated with anti-malarial drugs, pups received fewer maternal antibodies, parasitaemia was only marginally suppressed, and mortality risk was 25 per cent higher than for pups from dams with full infections. We observed the same qualitative patterns across three different host strains and two parasite genotypes. This study reveals the role that within-host infection dynamics play in the fitness consequences of maternally transferred immunity. Furthermore, it highlights a potential trade-off between the health of mothers and offspring suggesting that anti-parasite treatment may significantly affect the outcome of infection in newborns.

Sublethal effects of natural parasitism act through maternal, but not paternal, reproductive success in a wild population.

Parasites are a major component of all animal populations. Males and females often differ in their levels of parasite prevalence, potentially leading to sex differences in the impact of parasitism on fitness, with important implications for the evolution of parasite and host traits including resistance, tolerance, and virulence. However, quantitative measures of the impact of parasitism under free-living conditions are extremely rare, as they require detailed host demographic data with measures of parasite burden over time. Here, we use endoscopy for direct quantification of natural-parasite burdens and relate these to reproductive success over 7 yr in a wild population of seabirds. Contrary to predictions, only female burdens were associated with negative impacts of parasitism on breeding success, despite males having significantly higher burdens. Female reproductive success declined by 30% across the range of natural parasite burdens. These effects persisted when accounting for interannual population differences in breeding success. Our results provide quantitative estimates of profound sub-lethal effects of parasitism on the population. Importantly, they highlight how parasites act unpredictably to shape ecological and evolutionary processes in different components of the same population, with implications for demography and selection on host and parasite traits.

Reproductive senescence in a long-lived seabird: rates of decline in late-life performance are associated with varying costs of early reproduction.

Evolutionary theories of senescence predict that rates of decline in performance parameters should be shaped by early-life trade-offs between reproduction and somatic maintenance. Here we investigate factors influencing the rate of reproductive senescence in a long-lived seabird, the common guillemot Uria aalge, using data collected over a 23-year period. In the last 3 years of life, individual guillemots had significantly reduced breeding success and were less likely to hold a site or attempt to breed. Females senesced at a significantly faster rate than males. At the individual level, high levels of reproductive output earlier in life were associated with increased senescence later in life. This trade-off between early- and late-life reproduction was evident independent of the fact that as birds age, they breed later in the season. The rate of senescence was additionally dependent on environmental conditions experienced earlier in life, with evidence that harsh conditions amplified later declines in breeding success. Overall, individuals with intermediate levels of early-life productivity lived longer. These results provide support for the antagonistic-pleiotropy and disposable-soma theories of senescence and demonstrate for the first time in a wild bird population that increased rates of senescence in reproductive performance are associated with varying costs of reproduction early in life.

Responding to environmental change: plastic responses vary little in a synchronous breeder.

The impact of environmental change on animal populations is strongly influenced by the ability of individuals to plastically adjust key life-history events. There is therefore considerable interest in establishing the degree of plasticity in traits and how selection acts on plasticity in natural populations. Breeding time is a key life-history trait that affects fitness and recent studies have found that females vary significantly in their breeding time-environment relationships, with selection often favouring individuals exhibiting stronger plastic responses. In contrast, here, we show that although breeding time in the common guillemot, Uria aalge, is highly plastic at the population level in response to a large-scale environmental cue (the North Atlantic Oscillation, NAO), there is very little between-individual variation-most individuals respond to this climate cue very similarly. We demonstrate strong stabilizing selection against individuals who deviate from the average population-level response to NAO. This species differs significantly from those previously studied in being a colonial breeder, in which reproductive synchrony has a substantial impact on fitness; we suggest that counter selection imposed by a need for synchrony could limit individuals in their response and potential for directional selection to act. This demonstrates the importance of considering the relative costs and benefits of highly plastic responses in assessing the likely response of a population to the environmental change.

Parasitism in early life: environmental conditions shape within-brood variation in responses to infection.

Parasites play key ecological and evolutionary roles through the costs they impose on their host. In wild populations, the effect of parasitism is likely to vary considerably with environmental conditions, which may affect the availability of resources to hosts for defense. However, the interaction between parasitism and prevailing conditions is rarely quantified. In addition to environmental variation acting on hosts, individuals are likely to vary in their response to parasitism, and the combined effect of both may increase heterogeneity in host responses. Offspring hierarchies, established by parents in response to uncertain rearing conditions, may be an important source of variation between individuals. Here, we use experimental antiparasite treatment across 5 years of variable conditions to test how annual population productivity (a proxy for environmental conditions) and parasitism interact to affect growth and survival of different brood members in juvenile European shags (Phalacrocorax aristotelis). In control broods, last-hatched chicks had more plastic growth rates, growing faster in more productive years. Older siblings grew at a similar rate in all years. Treatment removed the effect of environment on last-hatched chicks, such that all siblings in treated broods grew at a similar rate across environmental conditions. There were no differences in nematode burden between years or siblings, suggesting that variation in responses arose from intrinsic differences between chicks. Whole-brood growth rate was not affected by treatment, indicating that within-brood differences were driven by a change in resource allocation between siblings rather than a change in overall parental provisioning. We show that gastrointestinal parasites can be a key component of offspring's developmental environment. Our results also demonstrate the value of considering prevailing conditions for our understanding of parasite effects on host life-history traits. Establishing how environmental conditions shape responses to parasitism is important as environmental variability is predicted to increase.

Impacts of parasites in early life: contrasting effects on juvenile growth for different family members.

Parasitism experienced early in ontogeny can have a major impact on host growth, development and future fitness, but whether siblings are affected equally by parasitism is poorly understood. In birds, hatching asynchrony induced by hormonal or behavioural mechanisms largely under parental control might predispose young to respond to infection in different ways. Here we show that parasites can have different consequences for offspring depending on their position in the family hierarchy. We experimentally treated European Shag (Phalacrocorax aristoteli) nestlings with the broad-spectrum anti-parasite drug ivermectin and compared their growth rates with nestlings from control broods. Average growth rates measured over the period of linear growth (10 days to 30 days of age) and survival did not differ for nestlings from treated and control broods. However, when considering individuals within broods, parasite treatment reversed the patterns of growth for individual family members: last-hatched nestlings grew significantly slower than their siblings in control nests but grew faster in treated nests. This was at the expense of their earlier-hatched brood-mates, who showed an overall growth rate reduction relative to last-hatched nestlings in treated nests. These results highlight the importance of exploring individual variation in the costs of infection and suggest that parasites could be a key factor modulating within-family dynamics, sibling competition and developmental trajectories from an early age.