Does coping style predict optimization? An experimental test in a wild passerine bird

A number of studies have suggested that avian brood size is individually optimized. Yet, optimal reproductive decisions likely vary owing to among-individual differences in environmental sensitivity. Specifically, ‘proactive’ individuals who do not track environmental changes may be less able to produce optimal brood sizes than ‘reactive’ individuals who have more precise local environmental knowledge. To test this, we quantified exploratory behaviour (a proxy for proactivity) in a great tit (Parus major) population, manipulated brood sizes (reduced, control, enlarged) and evaluated whether individuals of dissimilar coping style differed in their level of optimization. If reactive females behaved optimally, any deviation from their original brood size should lower fitness, whereas this should not be the case for proactive females. Reactive females indeed performed best at their natural brood size, whereas proactive females performed best when raising an enlarged brood. These findings imply that proactive females produced sub-optimal brood sizes. We speculate that proactive females might (i) take decisions based on biased perception of their environment, (ii) face energetic constraints in offspring production and/or (iii) be more willing to invest into current reproduction when given the option. Our findings provide experimental evidence for coping style-related differences in optimal reproductive decisions and life-history strategies.     

Determinants of distribution and prevalence of avian malaria in blue tit populations across Europe: separating host and parasite effects

Although avian malarial parasites are globally distributed, the factors that affect the geographical distribution and local prevalence of different parasite lineages across host populations or species are still poorly understood. Based on the intense screening of avian malarial parasites in nine European blue tit populations, we studied whether distribution ranges as well as local adaptation, host specialization and phylogenetic relationships can determine the observed prevalences within populations. We found that prevalence differed consistently between parasite lineages and host populations, indicating that the transmission success of parasites is lineage specific but is partly shaped by locality-specific effects. We also found that the lineage-specific estimate of prevalence was related to the distribution range of parasites: lineages found in more host populations were generally more prevalent within these populations. Additionally, parasites with high prevalence that were also widely distributed among blue tit populations were also found to infect more host species. These findings suggest that parasites reaching high local prevalence can also realize wide distribution at a global scale that can have further consequences for host specialization. Although phylogenetic relationships among parasites did not predict prevalence, we detected a close match between a tree based on the geographic distance of the host populations and the parasite phylogenetic tree, implying that neighbouring host populations shared a related parasite fauna.     

Olfactory conditioning experiments in a food-searching passerine bird in semi-natural conditions

Because passerine birds have a very small relative olfactory bulb size, they have been considered to have weak olfactory capacities for decades. Recent investigations however suggest that breeding female blue tits (Parus caeruleus) are sensitive to lavender odour in the reproductive context of building and maintaining the nest. Here, we present results of an olfactory conditioning experiment in blue tits held in semi-natural conditions during the breeding season. We show that captive male blue tits, trained to associate lavender odour with a food reward, are more attracted to an empty feeder box emitting lavender odour than an odourless empty feeder box. Females did not distinguish significantly between empty feeders with and without lavender odour during the test phase, although they responded positively at the end of the training phase. These results suggest that male blue tits can use olfaction in a context not related to nest building. Additional experiments will be required to better understand the observed sex differences in response to the experimental set up, and in what context free-ranging individuals use olfaction.     

Sex and environmental sensitivity in blue tit nestlings

In birds and mammals with sexual size dimorphism (SSD), the larger sex is typically more sensitive to adverse environmental conditions, such as food shortage, during ontogeny. However, some recent studies of altricial birds have found that the larger sex is less sensitive, apparently because large size renders an advantage in sibling competition. Still, this effect is not an inevitable outcome of sibling competition, because several studies of other species of altricial birds have found the traditional pattern. We investigated if the sexes differ in environmental sensitivity during ontogeny in the blue tit, a small altricial bird with c. 6% SSD in body mass (males larger than females). We performed a cross-fostering and brood size manipulation experiment during 2 years to investigate if the sexes were differently affected as regards body size (body mass, tarsus and wing length on day 14 after hatching) and pre-fledging survival. We also investigated if the relationship between body size and post-fledging survival differed between the sexes. Pre-fledging mortality was higher in enlarged than in reduced broods, representing poor and good environments, respectively, but the brood size manipulation did not affect the mortality rate of males and females differently. In both years, both males and females were smaller on day 14 after hatching in enlarged as compared to reduced broods. In one of the years, we also found significant Sex × Experiment interactions for body size, such that females were more affected by poor environmental conditions than that of males. Body size was positively correlated with post-fledging survival, but we found no interactive effects of sex and morphological traits on survival. We conclude that in the blue tit, females (the smaller sex) are more sensitive to adverse environmental conditions which, in our study, was manifest in terms of fledgling size. A review of published studies of sex differences in environmental sensitivity in sexually size-dimorphic altricial birds suggests that the smaller sex is more sensitive than the larger sex in species with large brood size and vice versa.     

Paternal genetic effects on offspring fitness are context dependent within the extrapair mating system of a socially monogamous passerine

Avian extrapair mating systems provide an interesting model to assess the role of genetic benefits in the evolution of female multiple mating behavior, as potentially confounding nongenetic benefits of extrapair mate choice are seen to be of minor importance. Genetic benefit models of extrapair mating behavior predict that females engage in extrapair copulations with males of higher genetic quality compared to their social mates, thereby improving offspring reproductive value. The most straightforward test of such good genes models of extrapair mating implies pairwise comparisons of maternal half-siblings raised in the same environment, which permits direct assessment of paternal genetic effects on offspring traits. But genetic benefits of mate choice may be difficult to detect. Furthermore, the extent of genetic benefits (in terms of increased offspring viability or fecundity) may depend on the environmental context such that the proposed differences between extrapair offspring (EPO) and within-pair offspring (WPO) only appear under comparatively poor environmental conditions. We tested the hypothesis that genetic benefits of female extrapair mate choice are context dependent by analyzing offspring fitness-related traits in the coal tit (Parus ater) in relation to seasonal variation in environmental conditions. Paternal genetic effects on offspring fitness were context dependent, as shown by a significant interaction effect of differential paternal genetic contribution and offspring hatching date. EPO showed a higher local recruitment probability than their maternal half-siblings if born comparatively late in the season (i.e., when overall performance had significantly declined), while WPO performed better early in the season. The same general pattern of context dependence was evident when using the number of grandchildren born to a cuckolding female via her female WPO or EPO progeny as the respective fitness measure. However, we were unable to demonstrate that cuckolding females obtained a general genetic fitness benefit from extrapair fertilizations in terms of offspring viability or fecundity. Thus, another type of benefit could be responsible for maintaining female extrapair mating preferences in the study population. Our results suggest that more than a single selective pressure may have shaped the evolution of female extrapair mating behavior in socially monogamous passerines.     

Heritable circadian period length in a wild bird population

Timing is essential, but circadian clocks, which play a crucial role in timekeeping, are almost unaddressed in evolutionary ecology. A key property of circadian clocks is their free-running period length (τ), i.e. the time taken for a full cycle under constant conditions. Under laboratory conditions, concordance of τ with the ambient light–dark cycle confers major fitness benefits, but little is known about period length and its implications in natural populations. We therefore studied natural variation of circadian traits in a songbird, the great tit (Parus major), by recording locomotor activity of 98 hand-raised, wild-derived individuals. We found, unexpectedly, that the free-running period of this diurnal species was significantly shorter than 24 h in constant dim light. We furthermore demonstrate, to our knowledge for the first time in a wild vertebrate, ample genetic variation and high heritability (h² = 0.86 ± 0.24), implying that period length is potentially malleable by micro-evolutionary change. The observed, short period length may be a consequence of sexual selection, as offspring from extra-pair matings had significantly shorter free-running periods than their half-siblings from within-pair matings. These findings position circadian clocks in the ‘real world’ and underscore the value of using chronobiological approaches in evolutionary ecology. Evolutionary ecologists study variation and its fitness consequences, but often have difficulties relating behavioural variation to physiological mechanisms. The findings presented here open the possibility that properties of internal, circadian clocks affect performance in traits that are relevant to fitness and sexual selection.     

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.     

Long-term familiarity promotes joining in neighbour nest defence

Familiarity plays an important role in the evolution of sociality and cooperation. Familiar individuals may gain a reputation for participating in, or defecting from, cooperative tasks. Previous research suggests that long-term familiarity with territorial neighbours benefits breeders. We tested the hypothesis that great tits (Parus major) are more likely to join in neighbours' nest defence if those neighbours are familiar from the previous year. We show that neighbours that shared a territory boundary the previous year are more likely to join their neighbours' nest defence than neighbours that did not share a boundary before. Closer neighbours did not differ from distant neighbours in their latency to join. For familiar neighbours that joined, there was no difference in call rate in relation to whether one or both members of the focal pair were familiar. First-time breeders (by definition unfamiliar) did not join each other's nest defence. This is the first evidence of a relationship between familiarity and joining in nest defence. Such direct benefits of familiarity may have important implications in the evolution of sociality.