Strong evidence for selection for larger brood size in a great tit population

We measured the selection pressure on brood size in a recentlyestablished population of great tits (Parus major L.) in thenorthern Netherlands by manipulating brood size in three years(1995: n = 51, 1997: n = 66, 1998: n = 51), and we estimatedfitness consequences in terms of local survival of both offspringand parents. Enlarged broods had highest fitness; the offspringfitness component was positively affected by manipulation andthe parental fitness component was unaffected. Parental survivaland the probability that parents produced a second clutch werenot affected by the treatment. However, parents that had raisedenlarged broods produced their second clutch later in the season.Clutch size, brood size, and laying date of birds recapturedin the next breeding season were largely independent of thetreatment. We conclude that there is strong evidence for selectionfor larger brood size and reject the individual optimizationhypothesis for this population because the number of young inthe nest predicts fitness independently of the manipulationhistory.     

Stability of genetic variance and covariance for reproductive characters in the face of climate change in a wild bird population

Global warming has had numerous effects on populations of animals and plants, with many species in temperate regions experiencing environmental change at unprecedented rates. Populations with low potential for adaptive evolutionary change and plasticity will have little chance of persistence in the face of environmental change. Assessment of the potential for adaptive evolution requires the estimation of quantitative genetic parameters, but it is as yet unclear what impact, if any, global warming will have on the expression of genetic variances and covariances. Here we assess the impact of a changing climate on the genetic architecture underlying three reproductive traits in a wild bird population. We use a large, long-term, data set collected on great tits (Parus major) in Wytham Woods, Oxford, and an 'animal model' approach to quantify the heritability of, and genetic correlations among, laying date, clutch size and egg mass during two periods with contrasting temperature conditions over a 40-year period (1965-1988 [cooler] vs. 1989-2004 [warmer]). We found significant additive genetic variance and heritability for all traits under both temperature regimes. We also found significant negative genetic covariances and correlations between clutch size and egg weight during both periods, and among laying date and clutch size in the colder years only. The overall G matrix comparison among periods, however, showed only a minor difference among periods, thus suggesting that genotype by environment interactions are negligible in this context. Our results therefore suggest that despite substantial changes in temperature and in mean laying date phenotype over the last decades, and despite the large sample sizes available, we are unable to detect any significant change in the genetic architecture of the reproductive traits studied.     

Climate change and breeding parameters of great and blue tits throughout the western Palaearctic

Increasing evidence suggests that climate change has consequences on avian breeding phenology. Here, variations in laying date and clutch size of great tit Parus major and blue tit Parus caeruleus within and between breeding populations through the western Palaearctic are examined in relation to climatic fluctuations, measured by the winter North Atlantic Oscillation (NAO) index. Within and across breeding sites, laying date was related to winter‐NAO index such that great and blue tit females lay earlier after warmer, moister winters (positive values of winter NAO‐index). The present study shows that for most populations there is an advancement of laying date, but the rate of change with respect to NAO significantly differed geographically across the western Palaearctic and did not differ between species. However, clutch size of great and blue tits was not affected by climatic fluctuations, presumably because the whole season is being shifted, but not in relation to food supplies. These combined analyses for the two species controlled for potentially confounding variables such as latitude, longitude, elevation and habitat of each study site.     

Natural selection on the genetical component of variance in body condition in a wild bird population

Although there is substantial evidence that skeletal measures of body size are heritable in wild animal populations, it is frequently assumed that the nonskeletal component of body weight (or ‘condition’) is determined primarily by environmental factors, in particular nutritional state. We tested this assumption by quantifying the genetic and environmental components of variance in fledgling body condition index (=relative body weight) in a natural population of collared flycatchers (Ficedula albicollis), and compared the strength of natural selection on individual breeding values with that on phenotypic values. A mixed model analysis of the components of variance, based on an ‘animal model’ and using 18 years of data on 17 717 nestlings, revealed a significant additive genetic component of variance in body condition, which corresponded to a narrow sense heritability (h²) of 0.30 (SE=0.03). Nongenetic contributions to variation in body condition were large, but there was no evidence of dominance variance nor of contributions from early maternal or common environment effects (pre‐manipulation environment) in condition at fledging. Comparison of pre‐ and post‐selection samples revealed virtually identical h² of body condition index, despite the fact that there was a significant decrease (35%) in the levels of additive genetic variance from fledging to breeding. The similar h² in the two samples occurred because the environmental component of variance was also reduced by selection, suggesting that natural selection was acting on both genotypic and environmental variation. The effects of selection on genetic variance were confirmed by calculation of the selection differentials for both phenotypic values and best linear unbiased predictor (BLUP) estimates of breeding values: there was positive directional selection on condition index both at the phenotypic and the genotypic level. The significant h² of body condition index is consistent with data from human and rodent populations showing significant additive genetic variance in relative body mass and adiposity, but contrasts with the common assumption in ecology that body condition reflects an individual’s nongenetic nutritional state. Furthermore, the substantial reduction in the additive genetic component of variance in body condition index suggests that selection on environmental deviations cannot alone explain the maintenance of additive genetic variation in heritable traits, but that other mechanisms are needed to explain the moderate to high heritabilities of traits under consistent and strong directional selection.     

Trans‐generational effects on ageing in a wild bird population

Ageing, long thought to be too infrequent to study effectively in natural populations, has recently been shown to be ubiquitous, even in the wild. A major challenge now is to explain variation in the rates of ageing within populations. Here, using 49 years of data from a population of great tits (Parus major), we show that offspring life‐history trajectories vary with maternal age. Offspring hatched from older mothers perform better early in life, but suffer from an earlier onset, and stronger rate, of reproductive senescence later in life. Offspring reproductive lifespan is, however, unaffected by maternal age, and the different life‐history trajectories result in a similar fitness payoff, measured as lifetime reproductive success. This study therefore identifies maternal age as a new factor underlying variation in rates of ageing, and, given the delayed trans‐generational nature of this effect, poses the question as to proximate mechanisms linking age‐effects across generations.     

Why breeding time has not responded to selection for earlier breeding in a songbird population

A crucial assumption underlying the breeders' equation is that selection acts directly on the trait of interest, and not on an unmeasured environmental factor which affects both fitness and the trait. Such an environmentally induced covariance between a trait and fitness has been repeatedly proposed as an explanation for the lack of response to selection on avian breeding time. We tested this hypothesis using a long-term dataset from a Dutch great tit (Parus major) population. Although there was strong selection for earlier breeding in this population, egg-laying dates have changed only marginally over the last decades. Using a so-called animal model, we quantified the additive genetic variance in breeding time and predicted breeding values for females. Subsequently, we compared selection at the phenotypic and genetic levels for two fitness components, fecundity and adult survival. We found no evidence for an environmentally caused covariance between breeding time and fitness or counteracting selection on the different fitness components. Consequently, breeding time should respond to selection but the expected response to selection was too small to be detected.     

The effects of environmental heterogeneity on multivariate selection on reproductive traits in female great tits

Describing natural selection on phenotypic traits under varying environmental conditions is essential for a quantitative assessment of the scale at which adaptation might occur and of the impact of environmental variability on evolution. Here we analyzed patterns of multivariate selection via fecundity and viability on three reproductive traits (laying date, clutch size, and egg weight) in a population of great tits (Parus major). We quantified selection under different environmental conditions using (1) local variation in breeding density and (2) distinct areas of the population's habitat. We found that selection gradients were generally stronger for fecundity than for viability selection. We also found correlational selection acting on the combination of laying date and clutch size; this is the first documented evidence of such selection acting on these two traits in a passerine bird. Our analyses showed that both local breeding density and habitat significantly influenced selection patterns, hence favoring different patterns of reproductive investment at a small-scale relative to typical dispersal distances in this species. Canonical rotation of the nonlinear selection matrices yielded similar conclusions as traditional nonlinear selection analyses, and also showed that the main axes of selection and fitness surfaces varied over space within the population. Our results emphasize the importance of quantifying different forms of selection, and of including variation in environmental conditions at small scales to gain a better understanding of potential evolutionary dynamics in wild populations. This study suggests that the fitness landscape for this species is relatively rugged at scales relevant to the life histories of individual birds and their close relatives.     

Female variation in allocation of steroid hormones,antioxidants and fatty acids: a multilevel analysis in a wild passerine bird

The environment where an embryo develops can be influenced by components of maternal origin, which can shape offspring phenotypes and therefore maternal fitness. In birds that produce more than one egg per clutch, females differ in the concentration of components they allocate into the yolk along the laying sequence. However, identification of processes that shape female yolk allocation and thus offspring phenotype still remains a major challenge within evolutionary ecology. A way to increase our understanding is by acknowledging that allocation patterns can differ depending on the level of analysis, such as the population versus the among‐female (within‐population) level. We employed mixed models to analyze at both levels the variation in allocation along the laying sequence of four steroid hormones, three antioxidants, and four groups of fatty acids present in the egg yolks of wild great tits Parus major. We also quantified repeatabilities for each component to study female consistency. At a population level, the concentrations/proportions of five yolk components varied along the laying sequence, implying that the developmental environment is different for offspring developing in first versus last eggs. Females varied substantially in the mean allocation of components and in their plasticity along the laying sequence. For most components, these two parameters were negatively correlated. Females were also remarkably repeatable in their allocation. Overall, our data emphasize the need to account for female variation in yolk allocation along the laying sequence at multiple levels, as variation at a population level is underpinned by different individual patterns. Our findings also highlight the importance of considering both levels of analysis in future studies investigating the causes and fitness consequences of yolk compounds. Finally, our results on female repeatability confirm that analyzing one egg per nest is a suitable way to address the consequences of yolk resource deposition for the offspring.     

How to use molecular marker data to measure evolutionary parameters in wild populations

Estimating the genetic basis of phenotypic traits and the selection pressures acting on them are central to our understanding of the evolution and conservation of wild populations. However, obtaining such evolutionary-related parameters is not an easy task as it requires accurate information on both relatedness among individuals and their breeding success. Polymorphic molecular markers are very useful in estimating relatedness between individuals and parentage analyses are now extensively used in most taxa. The next step in the application of molecular data to wild populations is to use them to derive estimates of evolutionary-related parameters for quantitative traits, such as quantitative genetic parameters (e.g. heritability, genetic correlations) and measures of selection (e.g. selection gradients). Despite their great appeal and potential, the optimal use of molecular tools is still debated and it remains unclear how they should best be used to obtain reliable estimates of evolutionary parameters in the wild. Here, we review the methods available for estimating quantitative genetic and selection parameters and discuss their merits and shortcomings, to provide a tool that summarizes the potential uses of molecular data to obtain such parameters in wild populations.     

NATURAL SELECTION ON AVIAN BREEDING TIME: CAUSALITY,FECUNDITY-DEPENDENT,AND FECUNDITY-INDEPENDENT SELECTION

Natural selection on breeding time through postfledgling survival was investigated in a population of blue tits, Parus caeruleus, between 1993 and 1996. In particular, selection acting through large brood sizes among early breeders (fecundity-dependent selection) was separated from selection acting through fitness benefits unrelated to the numerical benefits of large brood sizes (fecundity-independent selection). There was evidence that natural selection favored early breeding in 1993 and 1995 (significantly so in 1993), whereas in 1994 there was a tendency for selection to be stabilizing. Analyses of selection gradients further showed that there was direct selection for both early breeding and large brood sizes in 1993. Experimentally delayed pairs produced a lower proportion of surviving young among their fledglings compared to early pairs, indicating that the seasonal fitness trend is a causal one and not caused by differences between early and late breeders in territory or individual quality. There was no evidence for significant heritability for four reproductive traits (clutch sizes, laying dates, hatching dates, and brood size at fledging) although repeatability values ranged from 0.26 to 0.53. The importance of year-specific selective regimes in the evolution of avian breedings times are discussed and a role for population density in this context is proposed.     

Differential response by males and females to manipulation of partner contribution in the great tit (Parus major)

1.  In birds with bi-parental care, handicapping is often assumed to decrease the amount of parental care of the handicapped partner. We discuss how handicapping could alter the shape of the handicapped bird's survival–effort curve (theoretical curve relating the survival of a parent to its effort) and show that the optimal response could yield a decrease, no response or even an increase in effort of the handicapped bird.
2.  Male or female great tits Parus major (L.) were handicapped during the nestling period by clipping a number of feathers in order to study the effects on parental care and body condition.
3.  Handicapped males significantly decreased their feeding rates, while handicapped females did not. Condition of handicapped females significantly deteriorated, while condition of handicapped males did not change during the experiment. Females with a handicapped partner fully compensated for their partner's decrease in work rate, while males with a handicapped partner did not show any compensation and even tended to decrease their feeding rates.
4.  Using an inverse optimality approach, we reconstructed the theoretical curve relating the survival of a parent to its effort on the basis of the experimental effects. The handicapped male's survival–effort curve appeared to be slightly steeper than that of handicapped females. This suggests that handicapped males suffer more from an increase in effort than handicapped females.     

Heritability of gonad size varies across season in a wild songbird

Many organisms advance their seasonal reproduction in response to global warming. In birds, which regress their gonads to a nonfunctional state each winter, these shifts are ultimately constrained by the time required for gonadal development in spring. Gonadal development is photoperiodically controlled and shows limited phenotypic plasticity in relation to environmental factors, such as temperature. Heritable variation in the time required for full gonadal maturation to be completed, based on both onset and speed of development and resulting in seasonally different gonad sizes among individuals, is thus a crucial prerequisite for an adaptive advancement of seasonal reproduction in response to changing temperatures. We measured seasonal gonadal development in climate‐controlled aviaries for 144 great tit (Parus major) pairs, which consisted of siblings obtained as whole broods from the wild. We show that the extent of ovarian follicle development (follicle size) in early spring is highly heritable (h² = 0.73) in females, but found no heritability of the extent of testis development in males. However, heritability in females decreased as spring advanced, caused by an increase in environmental variance and a decrease in additive genetic variation. This low heritability of the variation in a physiological mechanism underlying reproductive timing at the time of selection may hamper genetic adaptation to climate change, a key insight as this great tit population is currently under directional selection for advanced egg‐laying.     

Effect of an ectoparasite on lay date, nest-site choice, desertion, and hatching success in the great tit (Pants major)

Ectoparasites are common in most bird species, but experimentalevidence of their effects on life-history traits is scarce.We investigated experimentally the effects of the hematophagoushen flea (Ceratophyllus gallinae) on timing of reproduction,nest-site choice, nest desertion, clutch size, and hatchingsuccess in the great tit (Parus major). When great tits wereoffered a choice on their territory between an infested anda parasite-free nest-box, they chose the one without parasites.When there was no choice, the great tits in a territory containingan infested nest-box delayed laying the clutch by 11 days ascompared with the birds that were offered a parasite-free nestingopportunity. The finding that there was no difference in phenotypictraits related to dominance between the birds nesting in infestedboxes and birds nesting in parasite-free boxes suggests thatthe delay is not imposed by social dominance. Nest desertionbetween laying and shortly after hatching was significandy higherin infested nests. There was no difference between infestedand parasite-free nests in clutch size, but hatching successand hence brood size at hatching were significantly smallerin infested nests. Nest-box studies of great tits have beenseminal in the development of evolutionary, ecological, andbehavioral theory, but recently a polemic has arisen in theliterature about the validity of the conclusions drawn fromnest-box studies where the naturally occurring, detrimentalectoparasites are eliminated by the routine removal of old nestsbetween breeding seasons. Our study suggests that this criticismis valid and that the evaluation of the effects of ectoparasitesmay improve our understanding of behavioral traits, life-historytraits, or population dynamics     

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.     

Sexual size dimorphism in the great tit (Parus major) in relation to history and current selection

We investigated the possible causes of the evolution of sexual size and shape dimorphism in the great tit (Parus major) by using two different approaches. First, we used the equilibrium approach, i.e. analysing current selection to see whether it was possible to find directional selection in the direction of the dimorphism, or stabilising selection maintaining dimorphism at its current level. Second, we used the historical approach, i.e. putting the degree of dimorphism in a phylogenetic perspective to analyse what kind of changes (if any) have occurred. This was carried out in the following way: (i) we described the level of sexual dimorphism in a population of Swedish great tits by means of path model. (ii) We used the path model design to analyse survival and reproductive selection in this population. (iii) We compared the level of dimorphism in relation to size in the great tit with that of the closest congener, the blue tit P. caeruleus. (iv) We compared the amount of interspecific morphological variation with that which would be expected under a drift model. We found no evidence of either stabilising or directional survival or reproductive selection. Size and shape variation in the great tit seemed unrelated to fitness in adults. Dimorphism was somewhat greater in the great tit compared to the blue tit, but only with an amount predictable by its larger size. In terms of phenotypic standard deviations, the great tit was not more dimorphic than the blue tit, although it was larger. The amount of interspecific variance with regard to size was lower or equal to that expected by the drift model, showing that long-term directional selection for an increase in size and dimorphism is improbable. These results agree with recent theoretical findings that size and dimorphism should be related and that strong conservatism with regard to dimorphism is to be expected. They also agree with the view that in equilibrium populations, fitness components (if there are many of them) should appear neutral with regard to total fitness.     

Implications of the difference between true and predicted breeding values for the study of natural selection and micro-evolution

The ability to predict individual breeding values in natural populations with known pedigrees has provided a powerful tool to separate phenotypic values into their genetic and environmental components in a nonexperimental setting. This has allowed sophisticated analyses of selection, as well as powerful tests of evolutionary change and differentiation. To date, there has, however, been no evaluation of the reliability or potential limitations of the approach. In this article, I address these gaps. In particular, I emphasize the differences between true and predicted breeding values (PBVs), which as yet have largely been ignored. These differences do, however, have important implications for the interpretation of, firstly, the relationship between PBVs and fitness, and secondly, patterns in PBVs over time. I subsequently present guidelines I believe to be essential in the formulation of the questions addressed in studies using PBVs, and I discuss possibilities for future research.