Teddy A. Wilkin

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.

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.

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.

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.

An experimental test of the causes of small-scale phenotypic differentiation in a population of great tits

Phenotypic differentiation between populations is thought to occur mainly at spatial scales where gene‐flow is restricted and selection regimes differ. However, if gene flow is nonrandom, dispersal may reinforce, rather than counteract, evolutionary differentiation, meaning that differences occurring over small scales might have a genetic basis. The purpose of this study was to determine the cause of differences in mean phenotype between two parts of a population of great tits Parus major, separated by <3 km. We conducted a partial cross‐fostering experiment between two contrasting parts of this population to separate genetic and environmental sources of variation, and to test for gene–environment interaction. We found strong environmental effects on nestling size, mass and condition index, with nestlings reared in a low density part of the population being larger, heavier and in better condition, than those in a high density part, irrespective of their origin. In addition, we found smaller, but significant, differences in nestling condition and shape associated with the areas that birds originated from, suggesting the presence of genetic differences between parts of this population. There was no evidence of gene–environment interaction for any character. This experiment is thus consistent with previous analyses suggesting that differences between parts of this population had evolved recently, apparently due to phenotype‐dependent dispersal, and indicates that population differentiation can be maintained over small spatial scales despite extensive dispersal.

Fecundity selection on ornamental plumage colour differs between ages and sexes and varies over small spatial scales.

Avian plumage colours are some of the most conspicuous sexual ornaments, and yet standardized selection gradients for plumage colour have rarely been quantified. We examined patterns of fecundity selection on plumage colour in blue tits (Cyanistes caeruleus L.). When not accounting for environmental heterogeneity, we detected relatively few cases of selection. We found significant disruptive selection on adult male crown colour and yearling female chest colour and marginally nonsignificant positive linear selection on adult female crown colour. We discovered no new significant selection gradients with canonical rotation of the matrix of nonlinear selection. Next, using a long‐term data set, we identified territory‐level environmental variables that predicted fecundity to determine whether these variables influenced patterns of plumage selection. The first of these variables, the density of oaks within 50 m of the nest, influenced selection gradients only for yearling males. The second variable, an inverse function of nesting density, interacted with a subset of plumage selection gradients for yearling males and adult females, although the strength and direction of selection did not vary predictably with population density across these analyses. Overall, fecundity selection on plumage colour in blue tits appeared rare and inconsistent among sexes and age classes.

Eggshell speckling in a passerine bird reveals chronic long-term decline in soil calcium

ABSTRACT Capsule: Long-term changes in eggshell speckling correlated temporally and spatially with declining soil calcium in an English Great Tit Parus major population. Aims: Eggshell speckling in the Great Tit correlates with eggshell thickness and calcium availability. We investigated whether eggshell speckling changed in a Great Tit population during a period when soil calcium declined, and estimated changes in eggshell thickness. Methods: Eggshell pigmentation of 2313 Great Tit clutches was recorded in 1988–2007 across a geological gradient in Wytham Woods, UK. Soil surveys conducted in 1974 and 1991 were repeated in 2008. Temporal and spatial changes in eggshell speckling and soil calcium were examined using generalized linear mixed models. We also estimated the change in eggshell thickness over this period. Results: Soil-calcium availability declined 1974–2008 especially in calcium-rich limestone areas. A systematic change in eggshell speckling, approximating to a 6.5% reduction in eggshell thickness, occurred between 1988 and 2007. The change was greatest in parts of Wytham that experienced the greatest decline in soil calcium. Hatching success was unaffected. Conclusion: Soil-calcium availability has declined in Wytham Woods, affecting Great Tit eggshell characteristics. This is the first evidence that declining soil calcium affects birds nesting in calcium-rich areas. Practical applications of these findings are considered.