Evolution in a changing environment: a case study with great tit fledging mass

Heritable phenotypic traits under significant and consistent directional selection often fail to show the expected evolutionary response. A potential explanation for this contradiction is that because environmental conditions change constantly, environmental change can mask an evolutionary response to selection. We combined an "animal model" analysis with 36 years of data from a long-term study of great tits (Parus major) to explore selection on and evolution of a morphological trait: body mass at fledging. We found significant heritability of this trait, but despite consistent positive directional selection on both the phenotypic and the additive genetic component of body mass, the population mean phenotypic value declined rather than increased over time. However, the mean breeding value for body mass at fledging increased over time, presumably in response to selection. We show that the divergence between the response to selection observed at the levels of genotype and phenotype can be explained by a change in environmental conditions over time, that is, related both to increased spring temperature before breeding and elevated population density. Our results support the suggestion that measuring phenotypes may not always give a reliable impression of evolutionary trajectories and that understanding patterns of phenotypic evolution in nature requires an understanding of how the environment has itself changed.     

Latitudinal variation in blue tit and great tit nest characteristics indicates environmental adjustment

Aim The laying of eggs and the building of a nest structure to accommodate them are two of the defining characteristics of members of the class Aves. Nest structures vary considerably across avian taxa and for many species the structure of the completed nest can have important consequences both for parents and their offspring. While nest characteristics are expected to vary adaptively in response to environmental conditions, large‐scale spatial variation in nest characteristics has been largely overlooked. Here, we examine the effects of latitudinal variation in spring temperatures on nest characteristics, including insulatory properties, and reproductive success of blue tits, Cyanistes caeruleus, and great tits, Parus major. Location Great Britain. Methods Nests and reproductive data were collected from seven study sites, spread over 5° of latitude. The nest insulatory properties were then determined before the nests were separated into nest base material and cup lining material. Results As spring temperatures increased with decreasing latitude, the mass of the nest base material did not vary in either species, while the mass of the cup lining material and nest insulatory properties decreased in both species. This suggests that in response to increasing temperatures the breeding female reduces the mass of the cup lining material, thereby maintaining an appropriate microclimate for incubating and brooding. The mean first egg date of both species advanced with decreasing latitude and increasing spring temperatures, although clutch size and brood size at hatching and fledging did not vary. Main conclusions This is the first study to demonstrate that the nest‐construction behaviour of birds varies in response to large‐scale spatial variation in ambient temperatures. Therefore, nest composition reliably indicates environmental conditions and we suggest that studies of nest structure may be sentinels for the early signs of rapid climate change.     

Post‐fledging survival of altricial birds: ecological determinants and adaptation

For altricial young, fledging is an abrupt step into an unknown environment. Despite increasing numbers of studies addressing the post‐fledging period, our current knowledge of the causes and consequences of post‐fledging survival remains fragmentary. Here, we review the literature on post‐fledging survival of juvenile altricial birds, addressing the following main questions: Is low post‐fledging survival a bottleneck in the altricial reproductive cycle? What is known of proximate and ultimate causal factors such as trophic relations (food and predation), habitat conditions, or abiotic factors acting in the post‐fledging period? We analyzed weekly survival estimates from 123 data series based on studies of 65 species, covering weeks 1–13 post‐fledging. As a general pattern, survival of fledglings was low during the first week post‐fledging (median rate = 0.83), and improved rapidly with time post‐fledging (week 4 median rate = 0.96). For ground‐nesting species, survival immediately after leaving nests was similar to egg‐to‐fledging survival. For species breeding above‐ground, survival during the first week post‐fledging was substantially lower than during both the nestling period and later post‐fledging stages. Thus, the early post‐fledging period is a bottleneck of markedly elevated mortality for most altricial species. Predation was the main proximate cause of mortality. Various factors such as habitat, annual and seasonal variation in the environment, and the physical condition of fledglings have been found to affect post‐fledging survival. Individual survival depended strongly on physical traits such as mass and wing length, which likely influence the ability of fledglings to escape predation. Trophic relationships at various levels are the main ultimate driver of adaptation of traits relevant to survival during the pre‐ and post‐fledging periods. Spatiotemporal dynamics of food resources determine the physical development of juveniles and, in turn, their performance after fledging. However, predators can cause quick and efficient selection for fledgling traits and adult breeding decisions. Parental strategies related to clutch size and timing of breeding, and the age and developmental stage at which young fledge have substantial effects on post‐fledging survival. The intensity and duration of post‐fledging parental investment also influences fledgling survival. Post‐fledging mortality is therefore not a random and inevitable loss. Traits and strategies related to fledging and the post‐fledging stage create large fitness differentials and, therefore, are integral, yet poorly understood, parts of the altricial reproductive strategy.     

A species‐specific multigene family mediates differential sperm displacement in Drosophila melanogaster

Sperm competition is a postcopulatory sexual selection mechanism in species in which females mate with multiple males. Despite its evolutionary relevance in shaping male traits, the genetic mechanisms underlying sperm competition are poorly understood. A recently originated multigene family specific to Drosophila melanogaster, Sdic, is important for the outcome of sperm competition in doubly mated females, although the mechanistic nature of this phenotype remained unresolved. Here, we compared doubly mated females, second mated to either Sdic knockout or nonknockout males, and directly visualize sperm dynamics in the female reproductive tract. We found that a less effective removal of first‐to‐mate male's sperm within the female's sperm storage organs is consistent with a reduced sperm competitive ability of the Sdic knockout males. Our results highlight the role young genes can play in driving the evolution of sperm competition.     

Sex‐specific heritability of cell‐mediated immune response in the blue tit nestlings (Cyanistes caeruleus)

Here, we aimed at estimating sex‐specific heritabilities of cell‐mediated immune response (CMI) in the blue tit nestlings (Cyanistes caeruleus). To separate genetic and environmental components of the phenotypic variance in CMI (measured using phytohaemagglutinin assay), we performed a cross‐fostering experiment. Additionally, controlled environmental variation was introduced by enlarging some broods. Our analyses revealed a significant genetic component (as approximated by the nest‐of‐origin term) of the phenotypic variance in immune response. More importantly, these genetic effects differed between sexes and experimentally manipulated brood sizes, as indicated by significant genotype‐by‐sex and genotype‐by‐environment interactions. We discuss possible causes of such sexual dimorphism in gene expression and suggest that sex‐ and environment‐specific genetic interactions may contribute to the maintenance of genetic variability in traits related to immune functions.     

The extended Moran effect and large-scale synchronous fluctuations in the size of great tit and blue tit populations

1. Synchronous fluctuations of geographically separated populations are in general explained by the Moran effect, i.e. a common influence on the local population dynamics of environmental variables that are correlated in space. Empirical support for such a Moran effect has been difficult to provide, mainly due to problems separating out effects of local population dynamics, demographic stochasticity and dispersal that also influence the spatial scaling of population processes. Here we generalize the Moran effect by decomposing the spatial autocorrelation function for fluctuations in the size of great tit Parus major and blue tit Cyanistes caeruleus populations into components due to spatial correlations in the environmental noise, local differences in the strength of density regulation and the effects of demographic stochasticity. 2. Differences between localities in the strength of density dependence and nonlinearity in the density regulation had a small effect on population synchrony, whereas demographic stochasticity reduced the effects of the spatial correlation in environmental noise on the spatial correlations in population size by 21.7% and 23.3% in the great tit and blue tit, respectively. 3. Different environmental variables, such as beech mast and climate, induce a common environmental forcing on the dynamics of central European great and blue tit populations. This generates synchronous fluctuations in the size of populations located several hundred kilometres apart. 4. Although these environmental variables were autocorrelated over large areas, their contribution to the spatial synchrony in the population fluctuations differed, dependent on the spatial scaling of their effects on the local population dynamics. We also demonstrate that this effect can lead to the paradoxical result that a common environmental variable can induce spatial desynchronization of the population fluctuations. 5. This demonstrates that a proper understanding of the ecological consequences of environmental changes, especially those that occur simultaneously over large areas, will require information about the spatial scaling of their effects on local population dynamics.     

Environmental factors shape cloacal bacterial assemblages in great tit Parus major and blue tit P. caeruleus nestlings

Despite their potential ecological and evolutionary importance, factors shaping the composition of bacterial communities in wild vertebrate populations remain poorly understood. The goal of this study was to examine the relative contributions of environmental factors and genetic factors (e.g. species and common origin) to the variation of cloacal bacterial assemblages in wild bird nestlings. We conducted a partial cross-fostering experiment with two passerine species, the great tit Parus major and the blue tit P. caeruleus, sharing similar habitats and breeding biology. Nestlings of the two species were exchanged four days after hatching and cloacal bacteria were sampled nine days later. The structure of cloacal bacterial communities was determined by Ribosomal Intergenic Spacer Analysis. Our results showed that each nestling displayed a unique bacterial community. Furthermore, nestlings raised in the same nest shared significantly similar bacterial communities. The similarity of bacterial community was higher among heterospecific siblings raised within the same nest than between biological siblings raised in separate nests. Effects of common origin between species could not be detected and, if present, were dominated by nest-based short-term environmental effects. Our results show that growth conditions within nests and individually based endogenous factors have significant effects on cloacal bacteria assemblages and could affect post-fledging condition.     

Post‐dispersal seed predation and its relations with seed traits: a thirty‐species‐comparative study

Post‐dispersal seed predation is a key process determining the variability in seed survival in forests, where most seeds are handled by rodents. Seed predation is thought to affect seedling regeneration, colonization ability and spatial distribution of plants. Basic seed traits are the essential factors affecting rodent foraging preferences and thus seed survival and seedling recruitment. Many studies have discussed several seed traits and their effects upon seed predation by rodents. However, the results of those previous studies are usually equivocal, likely because few seed traits and/or plant species tend to be incorporated into these studies. In order to elucidate the relationships between seed predation and seed traits, we surveyed the predation of 48 600 seeds in a natural pine forest, belonging to 30 species, for three consecutive years. The results demonstrated that: (i) seed size and seed coat hardness did not significantly affect seed predation; (ii) total phenolics had a negative effect upon seed predation; (iii) positive effects of nitrogen content upon seed predation were found. From our study, it seems that the better strategy to prevent heavy predation is for plants to produce seeds with higher total phenolics content rather than physical defenses (i.e. hard seed coat) or larger seeds. Additionally, rodent foraging preference may depend more on Nitrogen content than other nutrient content of seeds.     

Effects of habitat fragmentation on provisioning rates, diet and breeding success in two species of tit (great tit and blue tit)

The aim of this study was to examine the effects of forest fragmentation on the ability of parent birds to provide their young with an adequate food supply. To examine whether prey population densities of the great tit (Parus major L.) and the blue tit (P. caeruleus L.) vary between study areas in different forest size classes we compared provisioning rates and chick diet and related these parameters to breeding success. We filmed 217 nests over two breeding seasons and collected data on frass fall as a general estimate of caterpillar availability. Nests which were attended by none or one parent only during filming (n = 46) were excluded from the analyses. In both years and for both species feeding rates were highest in the smallest fragments and lowest in the large forest. There was also a suggestion that differences in feeding rates between areas vary between years. We found no consistent tendency for prey size to change with forest size, although both species brought slightly smaller prey items to the nest in the smallest forest fragments and feeding rates correlated negatively with prey size. Caterpillars were the main item fed to nestlings, in both species. We found no evidence to suggest that either frass fall or the proportion of caterpillars in the diet varied with forest size. There was also no correlation between mean frass fall and the total number of caterpillars brought to the nests, in either species. Breeding success, as measured by clutch size, brood size, fledging weight and fledging success, did not differ between the small fragments and the large forest, in either species. There was also no relationship between provisioning rate (as concerns volume of prey fed to nestlings and the quality of chick diet) and breeding success parameters. In conclusion, this study does not suggest suboptimal foraging or breeding conditions in small fragments compared to a nearby large forest, for either species. Received: 23 June 1997 / Accepted: 29 December 1997     

Post‐fledging survival of Little Owls Athene noctua in relation to nestling food supply

Among the range of determinants of post‐fledging survival in altricial birds, the energy supply to the growing juveniles is likely to play a central role. However, the exact mechanisms shaping post‐fledging survival are poorly understood. Using a food supplementation experiment, we determined the effect of variation in food supply on the survival of juvenile Little Owls Athene noctua from hatching to 2 months post‐fledging. Experimental broods were food‐supplemented for 36 days during the nestling and the early post‐fledging period. The fate of 307 juveniles (95 of them provided with extra food) was determined by nest monitoring and radiotelemetry. In unsupplemented birds, the rates of survival measured at 5‐day intervals were lowest during the nestling stage, remained low during the early post‐fledging stage and steadily increased after about 2 weeks post‐fledging. Food supplementation substantially increased nestling survival, but we detected no direct treatment effect on post‐fledging survival. Instead, we found a strong indirect effect of food supplementation, in that fledglings of good physical condition had markedly higher chances of surviving the post‐fledging period compared with those in poor condition. Experimental food supplementation increased survival over the first 3 months from 45% to 64.6%. This suggests that energy reserves built up during the nestling stage influence post‐fledging survival and ultimately parental reproductive output. The low nestling and post‐fledging survival shows that the early life‐history stages constitute a crucial bottleneck of reproductive ecology in Little Owls. The strong treatment effects on the number of independent offspring indicate that natural variation in food supply is an important determinant of spatio‐temporal patterns in Little Owl demography.     

Persistence and space preemption explain species‐specific founder effects on the organization of marine sessile communities

Community assembly may not follow predictable successional stages, with a large fraction of the species pool constituted by potential pioneering species and successful founders defined through lottery. In such systems, priority effects may be relevant in the determination of trajectories of developing communities and hence diversity and assemblage structure at later advanced states. In order to assess how different founder species may trigger variable community trajectories and structures, we conducted an experimental study using subtidal sessile assemblages as model. We manipulated the identity of functionally different founders and initial colony size (a proxy of the time lag before the arrival of later species), and followed trajectories. We did not observe any effects of colony size on response variables, suggesting that priority effects take place even when the time lag between the establishment of pioneering species and late colonizers is very short. Late community structure at experimental panels that started either with the colonial ascidian Botrylloides nigrum, or the arborescent bryozoan Bugula neritina, was similar to control panels allowed natural assembling. In spite of high potential for fast space domination, and hence negative priority effects, B. nigrum suffered high mortality and did not persist throughout succession. Bugula neritina provided complex physical microhabitats through conspecific clustering that have enhanced larval settlement of late species arrivals, but no apparent facilitation was observed. Differently, panels founded by the encrusting bryozoan Schizoporella errata led to different and less diverse communities compared to naturally assembled panels, evidencing strong negative priority effects through higher persistence and space preemption. Schizoporella errata founder colonies inhibited further conspecific settlement, which may greatly relax intraspecific competition, allowing resource allocation to colony growth and space domination, thus reducing the chances for the establishment of other species.     

Energetic cost of calling: general constraints and species‐specific differences

The energetic cost of acoustic signalling varies tremendously among species. Understanding factors responsible for this heterogeneity is important for understanding the costs and benefits of signalling. Here, we present a general model, based on well‐established principles of bioenergetics, which predicts the energetic cost of call production across species. We test model predictions using an extensive database of resting and calling metabolic rates of insects, amphibians and birds. Results are largely supportive of model predictions. Calling metabolic rates scale predictably with body mass and temperature such that calling and resting metabolic rates are directly proportional to each other. The cost of acoustic signalling is ～8 times higher than resting metabolic rate in ectotherms, and ～2 times higher in birds. Differences in the increase in metabolic rate during calling are explained by the relative size of species’ sound‐producing muscles. Combined with published work, we quantify call efficiency and discuss model implications.     

Malaria infection status predicts extra‐pair paternity in the blue tit

Extra‐pair matings comprise a common reproductive strategy among socially monogamous bird species. However, it remains unclear why females decide to mate with extra‐pair males. Indirect benefits in terms of improving offspring genetic quality are usually invoked to explain this phenomenon. Parasite resistance genes are often considered as a female target of seeking extra‐pair matings, but the direct test of this hypothesis is generally lacking. Here, we report on a relationship between the status of infection with malaria parasites (Plasmodium and Haemoproteus) and occurrence of extra‐pair paternity in a wild population of the blue tit Cyanistes caeruleus inhabiting Gotland (Sweden). We found that the probability of extra‐pair paternity is significantly related to the infection status of social parents. Infected males showed higher probability of being cuckolded than uninfected ones. However, this was observed only among males mated to uninfected females. Thus, avian malaria may potentially contribute to explanation of extra‐pair mating behaviour.     

Thermoregulation in gregarious dipteran larvae: evidence of species‐specific temperature selection

Due to the ephemeral nature of carcasses they grow on, necrophagous blowfly larvae should minimize the time spent on the cadaver. This could be achieved by moving to high‐temperature areas. On that basis, we theorized that larvae placed in a heterogeneous thermal environment would move to the higher temperature that speed up their development. This study was designed to (1) test the ability of necrophagous larvae to orientate in a heterogeneous thermal environment, and (2) compare the temperatures selected by the larvae of three common blowfly species: Lucilia sericata (Meigen), Calliphora vomitoria (L.) and Calliphora vicina (Robineau‐Desvoidy). For this purpose, we designed a setup we named Thermograde. It consists of a food‐supplied linear thermal gradient that allows larvae to move, feed, and grow in close‐to‐real conditions, and to choose to stay at a given temperature. For each species and replication, 80 young third instars were placed on the thermal gradient. The location of larvae was observed after 19 h, with fifteen replications per species. The larvae of each species formed aggregations that were always located at the same temperatures, which were highly species‐specific: 33.3 ± 1.52 °C for L. sericata, 29.6 ± 1.63 °C for C. vomitoria, and 22.4 ± 1.55 °C for C. vicina. According to the literature, these value allows a fast development of the larvae, but not to reach the maximum development rate. As control experiments clearly demonstrate that larval distribution was not due to differences in food quality, we hypothesized that the local temperature selection by larvae may result from a trade‐off between development quality and duration. Indeed, temperature controls not only the development rate of the larvae, but also the quality of their growth and survival rate. Finally, results raise questions regarding the way larvae moved on the gradient and located their preferential temperature.     

Male-biased sex ratio among unhatched eggs in great tit Parus major, blue tit P. caeruleus and collared flycatcher Ficedula albicollis

An increasing number of studies have demonstrated that brood sex ratios are frequently unequal, but the proximate mechanisms underlying this deviation are largely unknown. In the current study we analysed deviation from expected 1:1 sex ratio among dead embryos from unhatched eggs collected from partially unhatched clutches of three passerine bird species. We showed that male embryos were significantly overrepresented among unhatched eggs of great tit Parus major , blue tit P. caeruleus and collared flycatcher Ficedula albicollis . Moreover, the bias in sex ratio differed among species and tended to differ among study years. We discuss several hypotheses to explain the observed male bias among unhatched eggs. We conclude that sex specific embryo mortality may contribute to explain the observed variation in sex ratios in several species of wild birds and that sexing unhatched eggs is important in studies of sex ratio allocation.     

Sacoglossan sea slugs make routine use of photosynthesis by a variety of species‐specific adaptations

The phenomenon of the uptake, intracellular sequestration, and subsequent usage of algal chloroplasts by the digestive cells of many species of sacoglossan sea slugs, currently called kleptoplasty, has been of considerable interest since its discovery in the 1960s. While a large body of literature reported that captured chloroplasts were photosynthetically active inside slug cells and that plastid longevity in some species might be the result of the horizontal transfer of functional algal nuclear genes into the slug genome, a few recent studies have called the older results into question. Here, we have reviewed the literature and showed that while kleptoplasty occurs in many slug species and almost all derive benefit from kleptoplast photosynthesis, the slug adaptations to maintain the chloroplasts differ from species to species. These adaptations range from behavioral to molecular, including gene transfer, in a variety of combinations.     

Age,sex and beauty: methodological dependence of age‐ and sex‐dichromatism in the great tit Parus major

Carotenoid‐based colour expression is frequently involved in sexual dichromatism, particularly in bird plumage, suggesting a role in sexual selection. Despite much work on expression of the carotenoid‐based ventral plumage coloration of the great tit (Parus major), which represents a popular model in evolution and ecology, a consensus on even the most basic demographic patterns of variation (e.g. age and sex differences) is lacking. This may reflect the use of variable methods for analysing colour variation, although what is not clear, either in this case or in general, is the extent to which these alternative methods are equally effective at describing age‐ and sex‐related dichromatism. Using data obtained over 4 years from a large sample of free‐ranging great tits, we examined how colour‐scoring methodology influences estimates of age‐ and sex‐related dichromatism. We compare: (1) principal components analysis‐derived scores; (2) tristimulus colour variables; (3) a visual model‐independent, carotenoid‐focussed colour score; and (4) two colour scoring methods based on avian visual models, examining how they assess colour variation with respect to age and sex to determine how methodology may influence results. We demonstrate clear age‐ and sex‐dependent expression of this colour trait, both in our own data and in meta‐analyses of results from great tit populations across Europe, and discuss the merits of the various colour scores, which yield very different estimates of the extent of age‐ and sex‐dependent dichromatism. We show variation is likely to be visible to conspecifics and propose a novel, visual model‐derived scoring system for describing variation in carotenoid‐based colour patches, where the perceived signal is divided into independent chromatic and achromatic components, in line with current understanding of visual perception. The present study highlights the impact of colour‐scoring methodology and shows that, as novel measures continue to be developed, researchers should consider carefully how they quantify colour expression. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 101 , 777–796.