Natural selection and inheritance of breeding time and clutch size in the collared flycatcher

Many characteristics of organisms in free-living populations appear to be under directional selection, possess additive genetic variance, and yet show no evolutionary response to selection. Avian breeding time and clutch size are often-cited examples of such characters. We report analyses of inheritance of, and selection on, these traits in a long-term study of a wild population of the collared flycatcher Ficedula albicollis. We used mixed model analysis with REML estimation ("animal models") to make full use of the information in complex multigenerational pedigrees. Heritability of laying date, but not clutch size, was lower than that estimated previously using parent-offspring regressions, although for both traits there was evidence of substantial additive genetic variance (h2 = 0.19 and 0.29, respectively). Laying date and clutch size were negatively genetically correlated (rA = -0.41 +/- 0.09), implying that selection on one of the traits would cause a correlated response in the other, but there was little evidence to suggest that evolution of either trait would be constrained by correlations with other phenotypic characters. Analysis of selection on these traits in females revealed consistent strong directional fecundity selection for earlier breeding at the level of the phenotype (beta = -0.28 +/- 0.03), but little evidence for stabilising selection on breeding time. We found no evidence that clutch size was independently under selection. Analysis of fecundity selection on breeding values for laying date, estimated from an animal model, indicated that selection acts directly on additive genetic variance underlying breeding time (beta = -0.20 +/- 0.04), but not on clutch size (beta = 0.03 +/- 0.05). In contrast, selection on laying date via adult female survival fluctuated in sign between years, and was opposite in sign for selection on phenotypes (negative) and breeding values (positive). Our data thus suggest that any evolutionary response to selection on laying date is partially constrained by underlying life-history trade-offs, and illustrate the difficulties in using purely phenotypic measures and incomplete fitness estimates to assess evolution of life-history trade-offs. We discuss some of the difficulties associated with understanding the evolution of laying date and clutch size in natural populations.     

An analysis of continent-wide patterns of sexual selection in a passerine bird

Patterns of selection are widely believed to differ geographically, causing adaptation to local environmental conditions. However, few studies have investigated patterns of phenotypic selection across large spatial scales. We quantified the intensity of selection on morphology in a monogamous passerine bird, the barn swallow Hirundo rustica, using 6495 adults from 22 populations distributed across Europe and North Africa. According to the classical Darwin-Fisher mechanism of sexual selection in monogamous species, two important components of fitness due to sexual selection are the advantages that the most attractive males acquire by starting to breed early and their high annual fecundity. We estimated directional selection differentials on tail length (a secondary sexual character) and directional selection gradients after controlling for correlated selection on wing length and tarsus length with respect to these two fitness components. Phenotype and fitness components differed significantly among populations for which estimates were available for more than a single year. Likewise, selection differentials and selection gradients differed significantly among populations for tail length, but not for the other two characters. Sexual selection differentials differed significantly from zero across populations for tail length, particularly in males. Controlling statistically for the effects of age reduced the intensity of selection by 60 to 81%, although corrected and uncorrected estimates were strongly positively correlated. Selection differentials and gradients for tail length were positively correlated between the sexes among populations for selection acting on breeding date, but not for fecundity selection. The intensity of selection with respect to breeding date and fecundity were significantly correlated for tail length across populations. Sexual size dimorphism in tail length was significantly correlated with selection differentials with respect to breeding date for tail length in male barn swallows across populations. These findings suggest that patterns of sexual selection are consistent across large geographical scales, but also that they vary among populations. In addition, geographical patterns of phenotypic selection predict current patterns of phenotypic variation among populations, suggesting that consistent patterns of selection have been present for considerable amounts of time.     

Gender and viability selection on morphology in fledgling pied flycatchers

Until recently, analyses of gender-dependent differences in viability selection and the ontogeny of sexual size dimorphism have been plagued by difficulties in determining the sex of nestling birds on the basis of morphology. Recently, this problem was overcome using molecular sex identification to report for the first time body-size-mediated antagonistic selection on the viability of male and female collared flycatchers. We used molecular sex identification to analyse natural selection on fledgling viability, sexual size dimorphism and effects of parasites in relation to gender in a Mediterranean population of the related pied flycatcher Ficedula hypoleuca. There was directional positive selection on fledgling weight but no selection on tarsus length. Fledgling weight was the most important determinant of fledgling survival, with heavier fledglings having increased viability. Although selective trends were of the same sign for both sexes, only among female fledglings were selection differentials and gradients statistically significant. Therefore, similar trends in selection were revealed in analyses of a data set where sex was ignored and in separate analyses using same-sex sibship trait means. Mite nest ectoparasites negatively affected fledgling weight, and the effects were stronger in female than male fledglings. There was no effect of parasitism on the tarsus length in males, as previously reported in retrospective analyses performed without knowledge of sex until recruitment. Overall, selection on fledgling viability on the basis of morphological traits and hatching date was not confounded by an individual's gender.     

Testing for biases in selection on avian reproductive traits and partitioning direct and indirect selection using quantitative genetic models

Key life history traits such as breeding time and clutch size are frequently both heritable and under directional selection, yet many studies fail to document microevolutionary responses. One general explanation is that selection estimates are biased by the omission of correlated traits that have causal effects on fitness, but few valid tests of this exist. Here, we show, using a quantitative genetic framework and six decades of life‐history data on two free‐living populations of great tits Parus major, that selection estimates for egg‐laying date and clutch size are relatively unbiased. Predicted responses to selection based on the Robertson–Price Identity were similar to those based on the multivariate breeder's equation (MVBE), indicating that unmeasured covarying traits were not missing from the analysis. Changing patterns of phenotypic selection on these traits (for laying date, linked to climate change) therefore reflect changing selection on breeding values, and genetic constraints appear not to limit their independent evolution. Quantitative genetic analysis of correlational data from pedigreed populations can be a valuable complement to experimental approaches to help identify whether apparent associations between traits and fitness are biased by missing traits, and to parse the roles of direct versus indirect selection across a range of environments.     

EXAMINING HYPOTHESES GENERATED BY FIELD MEASURES OF SEXUAL SELECTION ON MALE LIZARDS,UTA PALMERI

I examined sexual selection in the iguanid lizard Uta palmeri by measuring phenotypic selection in a cohort of males. Relative fitness was estimated by copulation rate from one breeding season, and I analyzed selection on five morphological traits (snout–vent length, mass, jaw length, head width, and head depth) and on male territory quality. Only territory quality and head depth were identified as direct targets of selection in a linear selection gradient analysis. Head depth was suggested to also be subject to quadratic selection. All traits exhibited significant directional selection differentials, suggesting indirect selection also was present because of the correlation of these traits with direct targets of selection. I used these results to generate hypotheses about the mechanisms of selection. For traits not identified as direct targets of selection (snout–vent length, mass, head width, jaw length), I could accept the null hypothesis of no female preference for the analyzed male traits; if these morphological traits were preferred by females in mate choice, they would have been identified as direct targets of selection. Exploring possible functional relationships within the cohort, I found that all five morphological traits contributed to explaining variation in territorial status. And in staged aggressive interactions between males that were similar in snout–vent length and mass, winning was associated only with greater head depth and not with head width or jaw length. Several possible interpretations of these results are presented. This study suggests that differential mating success arising from variation in territory quality gives rise to indirect selection on morphology. The possible mechanisms giving rise to the proposed direct selection on head depth require further study.     

Early arrival is not associated with more extra‐pair fertilizations in a long‐distance migratory bird

When assessing the benefits of early arrival date of migratory birds, a hidden and often ignored component of males’ fitness is the higher chance of early‐arriving birds to obtain extra‐pair fertilizations. Here we investigated how extra‐pair paternity might affect the relationship between male arrival date and number of fertilizations in a model study system, the European pied flycatcher Ficedula hypoleuca. For this purpose, we sampled and genotyped breeding pairs, unpaired males and offspring (including embryos from unhatched eggs when possible) of a Dutch pied flycatcher population. Detailed information on arrival date of males, egg laying date of their social mates and nest success was also recorded. Early‐arriving males had early‐laying females and males with early‐laying females had a higher probability of siring extra‐pair eggs and obtain more fertilizations. However, male arrival date alone did not correlate with the probability to gain extra‐pair paternity and neither to the amount of fertilized eggs. Both early‐ and late‐arriving males had a higher probability of losing paternity in their own nest compared to birds with an intermediate arrival date. Finally, late‐arriving males were more likely to remain unpaired but, interestingly, a few of these birds obtained paternity via extra‐pair copulations. Because earlier arrival date did not lead to more extra‐pair fertilizations and because such relationship seems to be driven mainly by the female's laying date, we conclude that the contribution of extra‐pair paternity to the overall fitness benefits of early male arrival date is relatively small.     

Relaxed selection when you least expect it: why declining bird populations might fail to respond to phenological mismatches

Ongoing climate change threatens to cause mismatches between the phenology of many organisms and their resources. Populations of migratory birds may need to undergo ‘evolutionary rescue’ if resource availability moves to earlier dates in the year, as shifted arrival dates at the breeding grounds may be required for persistence under new environmental schedules. Here we show a counterintuitive process that can reduce the strength of selection for early arrival when the resource peaks earlier. This happens when two processes combine to determine selection for early arrival: breeding success is higher if a bird does not miss the resource peak, but this occurs together with a ‘zero‐sum game’ where birds acquire good territories ahead of their competitors if they arrive early. The latter process can relax if the population has experienced a recent decline. Therefore, climate change can have two opposing effects: its direct effect on breeding success strengthens selection for early arrival, but this combines with an indirect effect of relaxed selection due to population declines, if territoriality is a significant determinant of population dynamics and fitness. We show that the latter process can predominate, and this can cause a failure for a population to adapt to a new schedule under changing environmental conditions.     

Giving offspring a head start in life: field and experimental evidence for selection on maternal basking behaviour in lizards

The timing of birth is often correlated with offspring fitness in animals, but experimental studies that disentangle direct effects of parturition date and indirect effects mediated via variation in female traits are rare. In viviparous ectotherms, parturition date is largely driven by female thermal conditions, particularly maternal basking strategies. Our field and laboratory studies of a viviparous lizard (Niveoscincus ocellatus) show that earlier‐born offspring are more likely to survive through their first winter and are larger following that winter, than are later‐born conspecifics. Thus, the association between parturition date and offspring fitness is causal, rather than reflecting an underlying correlation between parturition date and maternal attributes. Survival selection on offspring confers a significant advantage for increased maternal basking in this species, mediated through fitness advantages of earlier parturition. We discuss the roles of environmentally imposed constraints and parent–offspring conflict in the evolution of maternal effects on parturition date.     

No evidence for pre-copulatory sexual selection on sperm length in a passerine bird

There is growing evidence that post-copulatory sexual selection, mediated by sperm competition, influences the evolution of sperm phenotypes. Evidence for pre-copulatory sexual selection effects on sperm traits, on the other hand, is rather scarce. A recent paper on the pied flycatcher, Ficedula hypoleuca, reported phenotypic associations between sperm length and two sexually selected male traits, i.e. plumage colour and arrival date, thus invoking pre-copulatory sexual selection for longer sperm. We were unable to replicate these associations with a larger data set from the same and two additional study populations; sperm length was not significantly related to either male plumage colour or arrival date. Furthermore, there was no significant difference in sperm length between populations despite marked differences in male plumage colour. We also found some evidence against the previously held assumption of longer sperm being qualitatively superior; longer sperm swam at the same speed as shorter sperm, but were less able to maintain speed over time. We argue that both empirical evidence and theoretical considerations suggest that the evolution of sperm morphology is not primarily associated with pre-copulatory sexual selection on male secondary sexual traits in this or other passerine bird species. The relatively large between-male variation in sperm length in this species is probably due to relaxed post-copulatory sexual selection.     

Phenotypic selection in natural populations: what limits directional selection?

Studies of phenotypic selection document directional selection in many natural populations. What factors reduce total directional selection and the cumulative evolutionary responses to selection? We combine two data sets for phenotypic selection, representing more than 4,600 distinct estimates of selection from 143 studies, to evaluate the potential roles of fitness trade-offs, indirect (correlated) selection, temporally varying selection, and stabilizing selection for reducing net directional selection and cumulative responses to selection. We detected little evidence that trade-offs among different fitness components reduced total directional selection in most study systems. Comparisons of selection gradients and selection differentials suggest that correlated selection frequently reduced total selection on size but not on other types of traits. The direction of selection on a trait often changes over time in many temporally replicated studies, but these fluctuations have limited impact in reducing cumulative directional selection in most study systems. Analyses of quadratic selection gradients indicated stabilizing selection on body size in at least some studies but provided little evidence that stabilizing selection is more common than disruptive selection for most traits or study systems. Our analyses provide little evidence that fitness trade-offs, correlated selection, or stabilizing selection strongly constrains the directional selection reported for most quantitative traits.     

Fitness Consequences of Timing of Migration and Breeding in Cormorants

In most bird species timing of breeding affects reproductive success whereby early breeding is favoured. In migratory species migration time, especially arrival at the breeding grounds, and breeding time are expected to be correlated. Consequently, migration time should also have fitness consequences. However, in contrast to breeding time, evidence for fitness consequences of migration time is much more limited. Climate change has been shown to negatively affect the synchrony between trophic levels thereby leading to directional selection on timing but again direct evidence in avian migration time is scarce. We here analysed fitness consequences of migration and breeding time in great cormorants and tested whether climate change has led to increased selection on timing using a long-term data set from a breeding colony on the island of Vorsø (Denmark). Reproductive success, measured as number of fledglings, correlated with breeding time and arrival time at the colony and declined during the season. This seasonal decline became steeper during the study period for both migration and breeding time and was positively correlated to winter/spring climate, i.e. selection was stronger after warmer winters/springs. However, the increasing selection pressure on timing seems to be unrelated to climate change as the climatic variables that were related to selection strength did not increase during the study period. There is indirect evidence that phenology or abundances of preferred prey species have changed which could have altered selection on timing of migration and breeding.     

Age-related change in breeding performance in early life is associated with an increase in competence in the migratory barn swallow Hirundo rustica

1. We investigated age-related changes in two reproductive traits (laying date and annual fecundity) in barn swallows Hirundo rustica L. using a mixed model approach to di-stinguish among between- and within-individual changes in breeding performance with age. 2. We tested predictions of age-related improvements of competence (i.e. constraint hypothesis) and age-related progressive disappearance of poor-quality breeders (i.e. selection hypothesis) to explain age-related increase in breeding performance in early life. 3. Reproductive success increased in early life, reaching a plateau at middle age (e.g. at 3 years of age) and decreasing at older age (> 4 years). Age-related changes in breeding success were due mainly to an effect of female age. 4. Age of both female and male affected timing of reproduction. Final linear mixed effect models (LME) for laying date included main and quadratic terms for female and male age, suggesting a deterioration in reproductive performance at older age for both males and females. 5. We found evidence supporting the constraints hypothesis that increases in competence within individuals, with ageing being the most probable cause of the observed increase in breeding performance with age in early life. Two mechanisms were implicated: (1) advance in male arrival date with age provided middle-aged males with better access to mates. Yearling males arrived later to the breeding grounds and therefore had limited access to high-quality mates. (2) Breeding pairs maintaining bonds for 2 consecutive years (experienced pairs) had higher fecundity than newly formed inexperienced breeding pairs. 6. There was no support for the selection hypothesis because breeding performance was not correlated with life span. 7. We found a within-individual deterioration in breeding and migratory performance (arrival date) in the oldest age-classes consistent with senescence in these reproductive and migratory traits.     

Sexual selection resulting from extrapair paternity in collared flycatchers

Extrapair paternity has been suggested to represent a potentially important source of sexual selection on male secondary sexual characters, particularly in birds with predominantly socially monogamous mating systems. However, relatively few studies have demonstrated sexual selection within single species by this mechanism, and there have been few attempts to assess the importance of extrapair paternity in relation to other mechanisms of sexual selection. We report estimates of sexual selection gradients on male secondary sexual plumage characters resulting from extrapair paternity in the collared flycatcher Ficedula albicollis, and compare the importance of this form of sexual selection with that resulting from variation in mate fecundity. Microsatellite genotyping revealed that 15% of nestlings, distributed nonrandomly among 33% of broods (N=79), were the result of extrapair copulations. Multivariate selection analyses revealed significant positive directional sexual selection on two uncorrelated secondary sexual characters in males (forehead and wing patch size) when fledgling number was used as the measure of fitness. When number of offspring recruiting to the breeding population was used as the measure of male fitness, selection on these traits appeared to be directional and stabilizing, respectively. Pairwise comparisons of cuckolded and cuckolding males revealed that males that sired young through extrapair copulations had wider forehead patches, and were paired to females that bred earlier, than the males that they cuckolded. Path analysis was used to partition selection on these traits into pathways via mate fecundity and sperm competition, and suggested that the sperm competition pathway accounted for between 64 and 90% of the total sexual selection via the two paths. The selection revealed in these analyses is relatively weak in comparison with many other measures of selection in natural populations. We offer some explanations for the relatively weak selection detected. Copyright 1999 The Association for the Study of Animal Behaviour.     

Phenotypic selection and response to selection in Lobularia maritima: importance of direct and correlational components of natural selection

By using selection differentials, gradients and structural equation modelling (SEM), I have quantified the phenotypic selection acting on Lobularia maritima (Cruciferae) flower size, display, colour and density, using data on lifetime female fitness. Furthermore, by analysing the resulting F₁ generation in field and greenhouse conditions, I estimated the actual intergenerational change in the value of these traits. Both pollinators preferred plants with many and large flowers. Strong directional selection for increased flower display was found in all years of the study, regardless of the technique used. Indirect selection due to a high significant correlation with flower display occurred on flower colour and size. SEM showed that pollinators played only a minor role in this observed phenotypic selection. The analysis of the phenotypes of F₁ plants showed that flower display actually increased across generations. In addition, white flowers were significantly more frequent in the offspring population than in the parental one, mostly due to the association between flower display and white coloured flowers. This suggests that both direct and indirect selection can play a role in the evolution of correlated traits in this crucifer.     

SEASONAL VARIATION IN SEXUAL SELECTION IN THE MOTTLED SCULPIN

Seasonal variation in sexual and natural selection in male mottled sculpins (Cottus bairdi) can be evaluated by calculating selection differentials, which measure the magnitude of phenotypic change resulting from selection, and by calculating indices of the opportunity for selection, which indicate the potential for phenotypic selection in a given interval. Selection differentials are high at the beginning of the breeding season and decline throughout the breeding season. The magnitude and direction of selection differentials depend on when spawning occurs and are independent of the size or age of the females that spawn. Annual selection differentials due to differences in mating success (female choice) are nearly constant between years. Annual selection differentials associated with hatching success are variable. Opportunities for selection (I = fitness variance/[mean fitness]²) show clear seasonal patterns. They are highest at the beginning and at the end of the spawning season. However, this variation is dependent on the mean used to calculate I, and hence variation in I values does not indicate a significant change in the variance of male fitness.     

Statistical Genetics of an Annual Plant, Impatiens Capensis. II. Natural Selection

Measurement of natural selection on correlated characters provides valuable information on fitness surfaces, patterns of directional, stabilizing, or disruptive selection, mechanisms of fitness variation operating in nature, and possible spatial variation in selective pressures. We examined effects of seed weight, germination date, plant size, early growth, and late growth on individual fitness. Path analysis showed that most characters had direct or indirect effects on individual fitness, indicating directional selection. For most early life-cycle characters, indirect effects via later characters exceed the direct causal effect on fitness. Selection gradients were uniform across the experimental site. There was no evidence for stabilizing or disruptive selection. We discuss several definitions of stabilizing and disruptive selection. Although early events in the life of an individual have important causal effects on subsequent characters and fitness, there is no detectable genetic variance for most of these characters, so little or no genetic response to natural selection is expected.     

Reproductive competition promotes the evolution of female weaponry

Secondary sexual traits in females are a relatively rare phenomenon. Empirical studies have focused on the role of male mate choice in their evolution; however, recently it has been suggested that secondary sexual traits in females are more likely to be under selection via reproductive competition. We investigated female competition and the influence of female phenotype on fitness in Onthophagus sagittarius, a species of dung beetle that exhibits female-specific horns. We compared reproductive fitness when females were breeding in competition versus breeding alone and found that competition for breeding resources reduced fitness for all females, but that smaller individuals suffered a greater fitness reduction than larger individuals. When females were matched for body size, those with the longest horns gained higher reproductive fitness. The fitness function was positive and linear, favouring increased horn expression. Thus, we present evidence that female body size and horn size in O. sagittarius are under directional selection via competition for reproductive resources. Our study is a rare example of female contest competition selecting for female weaponry.     

Fecundity selection does not vary along a large geographical cline of trait means in a passerine bird

Local environmental and ecological conditions are commonly expected to result in local adaptation, although there are few examples of variation in phenotypic selection across continent‐wide spatial scales. We collected standardized data on selection with respect to the highly variable plumage coloration of pied flycatcher (Ficedula hypoleuca Pall.) males from 17 populations across the species' breeding range. The observed selection on multiple male coloration traits via the annual number of fledged young was generally relatively weak. The main aim of the present study, however, was to examine whether the current directional selection estimates are associated with distance to the sympatric area with the collared flycatcher (Ficedula albicollis Temminck), a sister species with which the pied flycatcher is showing character displacement. This pattern was expected because plumage traits in male pied flycatchers are changing with the distance to these areas of sympatry. However, we did not find such a pattern in current selection on coloration. There were no associations between current directional selection on ornamentation and latitude or longitude either. Interestingly, current selection on coloration traits was not associated with the observed mean plumage traits of the populations. Thus, there do not appear to be geographical gradients in current directional fecundity selection on male plumage ornamentation. The results of the present study do not support the idea that constant patterns in directional fecundity selection would play a major role in the maintenance of coloration among populations in this species. By contrast, the tendency for relatively weak mosaic‐like variation in selection among populations could reflect just a snapshot of temporally variable, potentially environment‐dependent, selection, as suggested by other studies in this system. Such fine‐grained variable selection coupled with gene flow could maintain extensive phenotypic variation across populations. © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 114 , 808–827.     

Selection and evolutionary potential of spring arrival phenology in males and females of a migratory songbird

The timing of annual life‐history events affects survival and reproduction of all organisms. A changing environment can perturb phenological adaptations and an important question is if populations can evolve fast enough to track the environmental changes. Yet, little is known about selection and evolutionary potential of traits determining the timing of crucial annual events. Migratory species, which travel between different climatic regions, are particularly affected by global environmental changes. To increase our understanding of evolutionary potential and selection of timing traits, we investigated the quantitative genetics of arrival date at the breeding ground using a multigenerational pedigree of a natural great reed warbler (Acrocephalus arundinaceus) population. We found significant heritability of 16.4% for arrival date and directional selection for earlier arrival in both sexes acting through reproductive success, but not through lifespan. Mean arrival date advanced with 6 days over 20 years, which is in exact accordance with our predicted evolutionary response based on the breeder's equation. However, this phenotypic change is unlikely to be caused by microevolution, because selection seems mainly to act on the nongenetic component of the trait. Furthermore, demographical changes could also not account for the advancing arrival date. Instead, a strong correlation between spring temperatures and population mean arrival date suggests that phenotypic plasticity best explains the advancement of arrival date in our study population. Our study dissects the evolutionary and environmental forces that shape timing traits and thereby increases knowledge of how populations cope with rapidly changing environments.