Scale-dependent phenological synchrony between songbirds and their caterpillar food source.

In seasonal environments, the timing of reproduction has important fitness consequences. Our current understanding of the determinants of reproductive phenology in natural systems is limited because studies often ignore the spatial scale on which animals interact with their environment. When animals use a restricted amount of space and the phenology of resources is spatially variable, selection may favor sensitivity to small-scale environmental variation. Population-level studies of how songbirds track the changing phenology of their food source have been influential in explaining how populations adjust to changing climates but have largely ignored the spatial scale at which phenology varies. We explored whether individual great tits (Parus major) synchronize their breeding with phenological events in their local environment and investigated the spatial scale at which this occurs. We demonstrate marked variation in the timing of food availability, at a spatial scale relevant to individual birds, and that such local variation predicts the breeding phenology of individuals. Using a 45-year data set, we show that measures of vegetation phenology at very local scales are the most important predictors of timing of breeding within years, suggesting that birds can fine-tune their phenology to that of other trophic levels. Knowledge of the determinants of variation in reproductive behavior at different spatial scales is likely to be critical in understanding how selection operates on breeding phenology in natural populations.

Molecular epidemiology of malaria prevalence and parasitaemia in a wild bird population.

Avian malaria (Plasmodium spp.) and other blood parasitic infections of birds constitute increasingly popular model systems in ecological and evolutionary host-parasite studies. Field studies of these parasites commonly use two traits in hypothesis testing: infection status (or prevalence at the population level) and parasitaemia, yet the causes of variation in these traits remain poorly understood. Here, we use quantitative PCR to investigate fine-scale environmental and host predictors of malaria infection status and parasitaemia in a large 4-year data set from a well-characterized population of blue tits (Cyanistes caeruleus). We also examine the temporal dynamics of both traits within individuals. Both infection status and parasitaemia showed marked temporal and spatial variation within this population. However, spatiotemporal patterns of prevalence and parasitaemia were non-parallel, suggesting that different biological processes underpin variation in these two traits at this scale. Infection probability and parasitaemia both increased with host age, and parasitaemia was higher in individuals investing more in reproduction (those with larger clutch sizes). Several local environmental characteristics predicted parasitaemia, including food availability, altitude, and distance from the woodland edge. Although infection status and parasitaemia were somewhat repeatable within individuals, infections were clearly dynamic: patent infections frequently disappeared from the bloodstream, with up to 26% being lost between years, and parasitaemia also fluctuated within individuals across years in a pattern that mirrored annual population-level changes. Overall, these findings highlight the ecological complexity of avian malaria infections in natural populations, while providing valuable insight into the fundamental biology of this system that will increase its utility as a model host-parasite system.

Evolution driven by differential dispersal within a wild bird population.

Evolutionary theory predicts that local population divergence will depend on the balance between the diversifying effect of selection and the homogenizing effect of gene flow. However, spatial variation in the expression of genetic variation will also generate differential evolutionary responses. Furthermore, if dispersal is non-random it may actually reinforce, rather than counteract, evolutionary differentiation. Here we document the evolution of differences in body mass within a population of great tits, Parus major, inhabiting a single continuous woodland, over a 36-year period. We show that genetic variance for nestling body mass is spatially variable, that this generates different potential responses to selection, and that this diversifying effect is reinforced by non-random dispersal. Matching the patterns of variation, selection and evolution with population ecological data, we argue that the small-scale differentiation is driven by density-related differences in habitat quality affecting settlement decisions. Our data show that when gene flow is not homogeneous, evolutionary differentiation can be rapid and can occur over surprisingly small spatial scales. Our findings have important implications for questions of the scale of adaptation and speciation, and challenge the usual treatment of dispersal as a force opposing evolutionary differentiation.

Heterogeneous selection on a heritable temperament trait in a variable environment.

1. Temperament traits increasingly provide a focus for investigating the evolutionary ecology of behavioural variation. Here, we examine the underlying causes and selective consequences of individual variation in the temperament trait 'exploration behaviour in a novel environment' (EB, based on an 8-min assay) in a free-ranging population of a passerine bird, the great tit Parus major. 2. First, we conducted a quantitative genetic analysis on EB using a restricted maximum likelihood-based animal model with a long-term pedigree. Although repeatability was relatively high, EB was only moderately heritable and permanent environment (V(PE)) effects contributed as much to phenotypic variance as additive genetic effects. 3. We then asked whether heterogeneous selection acted on EB at various temporal and spatial scales. Using estimates of lifetime reproductive success, we found evidence of weak negative directional selection acting on EB amongst females which was driven by selection through recruitment, but not fecundity, in one of the four breeding years. There was no evidence of any selection on EB through survival. 4. Heterogeneous selection on EB within seasons was also observed amongst males through fecundity along two fine-scale environmental gradients--local breeding density and habitat quality; we are unaware of any previous equivalent demonstrations. 5. All of these analyses were repeated on a second measure of exploration behaviour (EB(2), measured during a 2-min assay) to facilitate comparison with other studies. EB and EB(2) were strongly correlated to one another at the genetic level, but were only moderately correlated at the phenotypic level and V(PE) was undetected in EB(2). Selection on EB(2) was similar to that on EB; we conclude that both traits are broadly equivalent from an evolutionary perspective. 6. Our analyses suggest that to the extent that the temperament trait 'exploration behaviour' is subject to natural selection in this population, this selection is highly context dependent and most evident along two environmental gradients. Furthermore, the strong V(PE) effect detected suggests that understanding the causes and consequences of variation in this trait will require studies firmly embedded in an environmental context.

Edge effects in the great tit: analyses of long-term data with GIS techniques.

In contemporary fragmented landscapes, edges are commonplace, and understanding the effects of edge environments is thus essential for the conservation of forest communities. The reproductive output of forest passerines is often reduced close to forest edges. Possible explanations include overcrowding by conspecifics, elevated rates of predation, and the occurrence of lower-quality habitat and/or individuals at forest edges. We attempted to separate these processes by examining edge effects in the absence of nest predation and by effectively controlling for differences in breeding density and the quality of habitats and individuals. We used an edge distance index (EDI), which accounts for the number and distribution of edges in close proximity to a breeding location, to help explain variation in breeding density, nesting success, and reproductive traits of 8308 pairs of Great Tits (Parus major) breeding between 1965 and 2005, in Wytham, near Oxford, United Kingdom. Results from linear mixed modeling confirmed higher breeding density and a higher proportion of immigrant individuals at forest edges. Nevertheless, independently of these effects, we also found that birds laying later, with smaller clutches but larger eggs, were typical of edge environments. The number of offspring recruited to the breeding offspring per breeding attempt was also reduced at edges, both directly and mediated through changes in clutch size and laying date. Edge effects on life histories were detectable within individual females and up to 500 m from the woodland edge. Woodland edges are increasingly common in contemporary fragmented landscapes. Therefore these results, which suggest a pervasive effect of edges on reproduction, are of considerable importance to the management and conservation of forest communities.

Sex differences in the persistence of natal environmental effects on life histories.

"Silver spoon" effects of early environments on adult characteristics and life-history trajectories are thought to be widespread among vertebrates and are important because they imply that environments can have cascading transgenerational effects. Here we test for such effects by using a sample of 5425 great tits (Parus major) for which both natal and breeding environments were known in detail. Female life histories were strongly coupled with breeding conditions, but we found little evidence for any persistent effects of the natal environment. In contrast, life span and breeding success in males were influenced by the quality of the environment in which they were raised. Potential explanations for persistent environmental effects in males, but not females, include differential sex allocation benefiting males from high-quality environments and phenotypic plasticity allowing females to optimize reproductive decisions to current conditions, hence masking any residual natal effects. Thus, in contrast to findings of much recent work, persistent effects of the early environment are not all-pervasive and may differ between the sexes within a single species, potentially leading to sex-differential selection. Further work should attempt to understand the conditions under which these transgenerational environmental effects are likely to occur.

Within-population variation in prevalence and lineage distribution of avian malaria in blue tits, Cyanistes caeruleus.

The development of molecular genetic screening techniques for avian blood parasites has revealed many novel aspects of their ecology, including greatly elevated diversity and complex host-parasite relationships. Many previous studies of malaria in birds have treated single study populations as spatially homogeneous with respect to the likelihood of transmission of malaria to hosts, and we have very little idea whether any spatial heterogeneity influences different malaria lineages similarly. Here, we report an analysis of variation in the prevalence and cytochrome b lineage distribution of avian malaria infection with respect to environmental and host factors, and their interactions, in a single blue tit (Cyanistes caeruleus) population. Of 11 Plasmodium and Haemoproteus cytochrome b lineages found in 997 breeding individuals, the three most numerous (pSGS1, pTURDUS1 and pBT7) were considered separately, in addition to analyses of all avian malaria lineages pooled. Our analyses revealed marked spatial differences in the prevalence and distribution of these lineages, with local prevalence of malaria within the population ranging from over 60% to less than 10%. In addition, we found several more complex patterns of prevalence with respect to local landscape features, host state, parasite genotype, and their interactions. We discuss the implications of such heterogeneity in parasite infection at a local scale for the study of the ecology and evolution of infectious diseases in natural populations. The increased resolution afforded by the combination of molecular genetic and geographical information systems (GIS) tools has the potential to provide many insights into the epidemiology, evolution and ecology of these parasites in the future.

Density effects on life-history traits in a wild population of the great tit Parus major: analyses of long-term data with GIS techniques.

1. Population density often has strong effects on the population dynamics and reproductive processes of territorial animals. However, most estimates of density-dependent effects use the number of breeding pairs per unit area in a given season and look for correlations across seasons, a technique that assigns the same density score to each breeding pair, irrespective of local spatial variation. 2. In this study, we employed GIS techniques to estimate individual breeding densities for great tits breeding in Wytham Woods UK, between 1965 and 1996. We then used linear mixed modelling to analyse the effect of density on reproductive processes. 3. The areas of Thiessen polygons formed around occupied nestboxes were used to approximate territory size (necessarily inverse of breeding density). There were significant, independent and positive relationships between clutch size, fledging mass and the number of offspring recruited to the population, and territory size (all P < 0.001), but no effect of territory size on lay-date or egg mass. 4. Thiessen polygons are contiguous and cover all of the available area. Therefore, at low nest densities territory polygons were excessively oversized. Using a novel procedure to address this limitation, territory sizes were systematically capped through a range of maxima, with the greatest effect in the models when territories were capped at 0.9-2.3 ha. This figure approximates to the maximum effective territory size in our population and is in close agreement with several field-based studies. This capping refinement also revealed a significant negative relationship between lay-date and territory size capped at 0.9 ha (P < 0.001). 5. These density-dependent effects were also detected when analyses were restricted to changes within individual females, suggesting that density effects do not merely result from either increased proportions of low-quality individuals, or increased occupation of poor sites, when population density is high. 6. Overall, these results suggest that, in the current population, great tits with territories smaller than c. 2 ha independently lay smaller and later clutches, have lighter fledglings, and recruit fewer offspring to the breeding population. These analyses thus suggest a pervasive and causal role of local population density in explaining individual reproductive processes.