Positive correlations between heterozygosity and fitness traits are frequently observed, and it has been hypothesized, but rarely tested experimentally, that parasites play a key role in mediating the heterozygosity–fitness association. We evaluated this hypothesis in a wild great tit (Parus major) population by testing the prediction that the heterozygosity–fitness association would appear in broods experimentally infested with a common ectoparasite, but not in parasite‐free broods. We simultaneously assessed the effects of parental and offspring heterozygosity on nestling growth and found that body mass of nestlings close to independence, which is a strong predictor of post‐fledging survival, increased significantly with nestling levels of heterozygosity in experimentally infested nests, but not in parasite‐free nests. Heterozygosity level of the fathers also showed a significant positive correlation with offspring body mass under an experimental parasite load, whereas there was no correlation with the mothers’ level of heterozygosity. Thus, our results indicate a key role for parasites as mediators of the heterozygosity–fitness correlations.

No abstract

Life-history theory predicts a trade-off for allocation of limited resources to reproduction and self-maintenance; however, many of the underlying physiological mechanisms remain elusive. There is growing evidence for oxidative stress to play an essential role in this trade-off because some by-products from the immune system and from normal metabolism generate reactive oxygen species that can cause oxidative damage. We manipulated reproductive effort of male and female great tits shortly before reproduction by clipping feathers of either the male or female parent of pairs of known age, given that parental effort may differ between the sexes and change over the lifetime of an individual. We quantified the effect of the treatment on morphological, physiological, behavioral, and reproductive traits. We found that feather clipping led to a decrease in parental body mass and to a reduced clutch size. Nestlings raised by clipped fathers showed reduced body mass although feeding rate was equally high between clipped and control individuals. In contrast to our predictions, we found that the feather clipping did not affect oxidative status. However, independently of the treatment, adult males had higher antioxidant capacity than females and older males showed higher oxidative damage compared with yearlings. Thus, our results suggest that the self-maintenance was prioritized over reproduction. It suggests that males are more susceptible to increased workload than females and thus more likely to reduce allocation of resources to reproduction.

There is growing evidence that heterozygosity–fitness correlations (HFCs) are more pronounced under harsh conditions. Empirical evidence suggests a mediating effect of parasite infestation on the occurrence of HFCs. Parasites have the potential to mediate HFCs not only by generally causing high stress levels but also by inducing resource allocation tradeoffs between the necessary investments in immunity and other costly functions. To investigate the relative importance of these two mechanisms, we manipulated growth conditions of great tit nestlings by brood size manipulation, which modifies nestling competition, and simultaneously infested broods with ectoparasites. We investigated under which treatment conditions HFCs arise and, second, whether heterozygosity is linked to tradeoff decisions between immunity and growth. We classified microsatellites as neutral or presumed functional and analyzed these effects separately. Neutral heterozygosity was positively related to the immune response to a novel antigen in parasite-free nests, but not in infested nests. For nestlings with lower heterozygosity levels, the investments in immunity under parasite pressure came at the expenses of reduced feather growth, survival, and female body condition. Functional heterozygosity was negatively related to nestling immune response regardless of the growth conditions. These contrasting effects of functional and neutral markers might indicate different underlying mechanisms causing the HFCs. Our results confirm the importance of considering marker functionality in HFC studies and indicate that parasites mediate HFCs by influencing the costs of immune defense rather than by a general increase in environmental harshness levels.

After birth, an organism needs to invest both in somatic growth and in the development of efficient immune functions to counter the effects of pathogens, and hence an investment trade-off is predicted. To explore this trade-off, we simultaneously exposed nestling great tits (Parus major) to a common ectoparasite, while stimulating immune function. Using a 2 × 2 experimental design, we first infested half of the nests with hen fleas (Ceratophyllus gallinae) on day 3 post-hatch and later, on day 9-13 post-hatch, and then supplemented half of the nestlings within each nest with an immuno-enhancing amino acid (methionine). We then assessed the non-specific immune response by measuring both the inflammatory response to a lipopolysaccharide (LPS) and assessing the levels of acute phase proteins (APP). In parasite-infested nestlings, methionine had a negative effect on body mass close to fledging. Methionine had an immune-enhancing effect in the absence of ectoparasites only. The inflammatory response to LPS was significantly lower in nestlings infested with fleas and was also lower in nestlings supplemented with methionine. These patterns of immune responses suggest an immunosuppressive effect of ectoparasites that could neutralise the immune-enhancing effect of methionine. Our study thus suggests that the trade-off between investment in life history traits and immune function is only partly dependent on available resources, but shows that parasites may influence this trade-off in a more complex way, by also inhibiting important physiological functions.