The great tit HapMap project: A continental-scale analysis of genomic variation in a songbird.

A major aim of evolutionary biology is to understand why patterns of genomic diversity vary within taxa and space. Large-scale genomic studies of widespread species are useful for studying how environment and demography shape patterns of genomic divergence. Here, we describe one of the most geographically comprehensive surveys of genomic variation in a wild vertebrate to date; the great tit (Parus major) HapMap project. We screened ca 500,000 SNP markers across 647 individuals from 29 populations, spanning ~30 degrees of latitude and 40 degrees of longitude - almost the entire geographical range of the European subspecies. Genome-wide variation was consistent with a recent colonisation across Europe from a South-East European refugium, with bottlenecks and reduced genetic diversity in island populations. Differentiation across the genome was highly heterogeneous, with clear 'islands of differentiation', even among populations with very low levels of genome-wide differentiation. Low local recombination rates were a strong predictor of high local genomic differentiation (FST), especially in island and peripheral mainland populations, suggesting that the interplay between genetic drift and recombination causes highly heterogeneous differentiation landscapes. We also detected genomic outlier regions that were confined to one or more peripheral great tit populations, probably as a result of recent directional selection at the species' range edges. Haplotype-based measures of selection were related to recombination rate, albeit less strongly, and highlighted population-specific sweeps that likely resulted from positive selection. Our study highlights how comprehensive screens of genomic variation in wild organisms can provide unique insights into spatio-temporal evolutionary dynamics.

Nest building in titmice Paridae: Selectivity in bryophyte use.

In many bird species, reproductive success is dependent on nest quality. However, detailed data on nest composition are scarce, and quantitative analyses have generally used only rough categories, without species identification. Bryophytes dominate the nests of many passerine bird species, but little is known about whether birds have preferences for certain species. In this study, we determined the bryophyte species composition in nests of blue tits Cyanistes caeruleus and great tits Parus major in a forest near Oslo, Norway. We also sampled the abundance of the bryophyte species in plots on the forest floor surrounding a subset of the great tit nests. Blue tits and great tits both used 15 bryophyte species as nest materials, mainly the same pleurocarpous species but in different proportions. The tits preferred highly branched bryophyte species, i.e., Pleurozium schreberi, Rhytidiadelphus squarrosus, and Sanionia uncinata but avoided common forest floor bryophyte species that are sparsely branched. Great tits clearly collected bryophyte species selectively. We also found that bryophyte species content in great tit nests in the same nest box in different years was very similar. Our results also indicated that the great tits collected bryophyte nest materials close to their nests, mostly within 5 m, supporting the view that collecting nest materials is costly. We review several hypotheses to explain why the tits prefer certain species of bryophytes as nest materials. These include handling costs and their suitability as structural materials. We recommend field experiments to test specific hypotheses and to study whether preferences are heritable.

Long-term annual and spatial variation of polygyny in the white-throated dipper (Cinclus cinclus).

Mating strategies are key components in the fitness of organisms, and notably in birds the occurrence of monogamy versus polygyny has attracted wide interest. We address this by a very comprehensive dataset (2899 breeding events spanning the years 1978-2019) of the white-throated dipper Cinclus cinclus. Though the mating system of this species has been regarded as generally monogamous, we find that 7% of all breeding events were performed by polygynous males (approximately 15% of all pairs). The fraction of polygyny has been stable over the entire study period irrespective of population size. The assumption that polygyny is most common at low population density was not supported. Surprisingly, there was no difference between polygynous and monogamous males with regard to the quality of the territories they inhabited, ranked according to their overall frequency of use. The most common age group, first-year breeders, dominated among monogamous males, while among polygynous males second-year breeders were most common, followed by third and first-year breeders. The primary females were in general older than females mated to monogamous males, also when controlled for their general frequency in the population. The majority of the two females mated to a polygynous male, bred in the vicinity of each other. The probability for a male to be involved in polygyny more than once, was significantly higher than by chance, suggesting phenotypic quality differences among males.

No evidence that nest site choice in Pied Flycatchers is mediated by assessing the clutch size of a heterospecific, the Great Tit.

Among species that use similar resources, an individual may benefit by observing and copying the behavioural decision of a heterospecific. We tested the hypothesis of heterospecific social learning in passerine birds, namely that a migrant species, the Pied Flycatcher Ficedula hypoleuca, uses external markings on the nest cavities of a resident species, the Great Tit Parus major, as cues when choosing a nest site. Others have suggested that prospecting flycatchers assess the clutch size of tit "demonstrators" by entering their nest boxes and, assuming that a large clutch indicates a high-quality individual, will copy the nest appearance of tits with large, but not small clutches. During a 4-year period in Norway, we designed a similar study but did not find that flycatchers based their nest choice on the clutch size of tits. Neither were there any relationships between clutch size of the tit and its laying date, incubation behaviour, or the number of eggs visible through nest material during egg-laying so Pied Flycatchers did not use these indirect cues to assess quality of the tutor. Filming of tit nests showed that prospecting flycatchers did not enter tit nest boxes to assess the content. Indeed, incubating female tits only left their nest boxes for short bouts of unpredictable duration so there was little opportunity for flycatchers to inspect the nest contents unnoticed. Our study calls into question the mechanism of using the content of tit nests as public information for choosing traits of nest sites based on external characteristics. We suggest that similar studies of nest site choice in relation to possible social information transfer be replicated more widely.

Egg covering in cavity nesting birds may prevent nest usurpation by other species.

ABSTRACT: Some birds cover their eggs with nest material when they leave to forage. It has been suggested that such egg-covering aids thermoregulation or prevents predation but here we present a new hypothesis, that secondary cavity-nesting species cover their eggs to prevent nest usurpation by other birds. When the bottom of the cavity is dark, as when eggs are covered by nest material, it may be difficult for a prospecting competitor to see whether a defending nest owner or a predator is hiding inside the cavity. Competitors may therefore hesitate to enter dark cavities. We filmed 21 great tit (Parus major) nests during the egg-laying period and found that the female spent bouts of highly variable length outside the nest box (range 0.3-250 min, n = 51), so prospecting small passerines would have difficulty predicting whether an aggressive tit owner was in the box or would soon return. We presented prospecting male pied flycatchers (Ficedula hypoleuca) with a dyad of boxes (n = 93), each containing a great tit nest but only one with visible eggs. Flycatchers hesitated more to enter a nest box with no visible tit eggs than a box with exposed eggs. This was most evident for nest boxes with dark versus light interior paint, supporting the idea that better interior illumination makes prospecting birds more confident about entering an unfamiliar cavity. The usurpation and predation hypotheses are not mutually exclusive because both competitors and small predators may hesitate to enter dark, enclosed spaces if visibility is low. SIGNIFICANCE STATEMENT: Some birds deposit a layer of material on top of the eggs when they leave the nest. Several hypotheses have been proposed for such egg covering, for example that it may insulate the eggs and reduce the risk of nest predation. We propose a new hypothesis, namely that secondary hole-nesting birds cover their eggs when they leave the nest to prevent usurpation of the cavity by other birds. Great tits that we filmed at the nest during the egg-laying period could be absent for long periods. To test the hypothesis, we presented male pied flycatchers, potential nest competitors, with a dyad of nest boxes, each containing a great tit nest but only one with visible tit eggs. In support of the prediction, prospecting flycatchers hesitated to enter dark cavities with dark floors relative to boxes with exposed, reflective eggs.

Nest decoration: birds exploit a fear of feathers to guard their nest from usurpation.

Many species of birds incorporate feathers into their nest as structural support and to insulate the eggs or offspring. Here, we investigated the novel idea that birds reduce the risk of nest usurpation by decorating it with feathers to trigger a fear response in their rivals. We let prospecting birds choose between a dyad of nest-boxes in the wild, both containing some nest materials, but where one had a few white feathers and the other had none. All three species of cavity-nesting birds studied, the pied flycatcher Ficedula hypoleuca, the blue tit Cyanistes caeruleus, and the tree swallow Tachycineta bicolor, hesitated to enter boxes with white feathers. A similar avoidance of white feathers was found when the alternative nest-box of a dyad held black feathers. However, the birds readily collected white feathers that we placed in front of their nest-box, showing the fear of such feathers was context-dependent. We suggest that naive prospecting birds may perceive feathers in nests as the result of a predation event, and that owners decorate nests with bright feathers that can be seen from the opening to deter others from entering.

Hydrology influences breeding time in the white-throated dipper.

BACKGROUND: Earlier breeding is one of the strongest responses to global change in birds and is a key factor determining reproductive success. In most studies of climate effects, the focus has been on large-scale environmental indices or temperature averaged over large geographical areas, neglecting that animals are affected by the local conditions in their home ranges. In riverine ecosystems, climate change is altering the flow regime, in addition to changes resulting from the increasing demand for renewable and clean hydropower. Together with increasing temperatures, this can lead to shifts in the time window available for successful breeding of birds associated with the riverine habitat. Here, we investigated specifically how the environmental conditions at the territory level influence timing of breeding in a passerine bird with an aquatic lifestyle, the white-throated dipper Cinclus cinclus. We relate daily river discharge and other important hydrological parameters, to a long-term dataset of breeding phenology (1978-2015) in a natural river system. RESULTS: Dippers bred earlier when winter river discharge and groundwater levels in the weeks prior to breeding were high, and when there was little snow in the catchment area. Breeding was also earlier at lower altitudes, although the effect dramatically declined over the period. This suggests that territories at higher altitudes had more open water in winter later in the study period, which permitted early breeding also here. Unexpectedly, the largest effect inducing earlier breeding time was territory river discharge during the winter months and not immediately prior to breeding. The territory river discharge also increased during the study period. CONCLUSIONS: The observed earlier breeding can thus be interpreted as a response to climate change. Measuring environmental variation at the scale of the territory thus provides detailed information about the interactions between organisms and the abiotic environment.

Advancement of spring arrival in a long-term study of a passerine bird: sex, age and environmental effects.

In migratory birds, mistimed arrival might have negative consequences for individual fitness, causing population declines. This may happen if arrival time is not synchronized with breeding time, especially when earlier springs favour earlier reproduction. We studied spring arrival time to the breeding areas in a pied flycatcher Ficedula hypoleuca population in southern Norway during a 30-year period (1985-2014). We investigated trends in arrival both for the entire population and for different population fractions (e.g. early vs. late arrivals). We also studied sex and age class differences, along with repeatability of arrival. Finally, we explored how arrival is influenced by environmental conditions at the areas birds use throughout the year, using mixed-effects models and quantile regressions with individual-based data. Spring arrival advanced over five days, at a similar rate through the entire population. Males and adult birds arrived earlier than females and yearlings. Arrival was significantly repeatable for males and females. Birds arrived earlier in years with high temperature and rainfall at the breeding grounds, and low NDVI both on the Iberian Peninsula and in central Europe. Later fractions of the population showed a steeper response to these environmental variables. This intra-population heterogeneity in the responses to the environment probably stems from a combination between the different selection pressures individuals are subject to and their age-related experience. Our results highlight the importance of studying how migration phenology is affected by the environment not only on the breeding grounds but also on the other areas birds use throughout the year.

Interactions between demography and environmental effects are important determinants of population dynamics.

Climate change will affect the population dynamics of many species, yet the consequences for the long-term persistence of populations are poorly understood. A major reason for this is that density-dependent feedback effects caused by fluctuations in population size are considered independent of stochastic variation in the environment. We show that an interplay between winter temperature and population density can influence the persistence of a small passerine population under global warming. Although warmer winters favor an increased mean population size, density-dependent feedback can cause the local population to be less buffered against occasional poor environmental conditions (cold winters). This shows that it is essential to go beyond the population size and explore climate effects on the full dynamics to elaborate targeted management actions.

Sperm performance in conspecific and heterospecific female fluid.

Divergent sexual selection within allopatric populations may result in divergent sexual phenotypes, which can act as reproductive barriers between populations upon secondary contact. This hypothesis has been most tested on traits involved in precopulatory sexual selection, with less work focusing on traits that act after copulation and before fertilization (i.e., postcopulatory prezygotic traits), particularly in internally fertilizing vertebrates. However, postcopulatory sexual selection within species can also drive trait divergence, resulting in reduced performance of heterospecific sperm within the female reproductive tract. Such incompatibilities, arising as a by-product of divergent postcopulatory sexual selection in allopatry, can represent reproductive barriers, analogous to species-assortative mating preferences. Here, we tested for postcopulatory prezygotic reproductive barriers between three pairs of taxa with diverged sperm phenotypes and moderate-to-high opportunity for postcopulatory sexual selection (barn swallows Hirundo rustica versus sand martins Riparia riparia, two subspecies of bluethroats, Luscinia svecica svecica versus L. s. namnetum, and great tits Parus major versus blue tits Cyanistes caeruleus). We tested sperm swimming performance in fluid from the outer reproductive tract of females, because the greatest reduction in sperm number in birds occurs as sperm swim across the vagina. Contrary to our expectations, sperm swam equally well in fluid from conspecific and heterospecific females, suggesting that postcopulatory prezygotic barriers do not act between these taxon pairs, at this stage between copulation and fertilization. We therefore suggest that divergence in sperm phenotypes in allopatry is insufficient to cause widespread postcopulatory prezygotic barriers in the form of impaired sperm swimming performance in passerine birds.

Assessing the effects of climate on host-parasite interactions: a comparative study of European birds and their parasites.

BACKGROUND: Climate change potentially has important effects on distribution, abundance, transmission and virulence of parasites in wild populations of animals. METHODOLOGY/PRINCIPAL FINDING: Here we analyzed paired information on 89 parasite populations for 24 species of bird hosts some years ago and again in 2010 with an average interval of 10 years. The parasite taxa included protozoa, feather parasites, diptera, ticks, mites and fleas. We investigated whether change in abundance and prevalence of parasites was related to change in body condition, reproduction and population size of hosts. We conducted analyses based on the entire dataset, but also on a restricted dataset with intervals between study years being 5-15 years. Parasite abundance increased over time when restricting the analyses to datasets with an interval of 5-15 years, with no significant effect of changes in temperature at the time of breeding among study sites. Changes in host body condition and clutch size were related to change in temperature between first and second study year. In addition, changes in clutch size, brood size and body condition of hosts were correlated with change in abundance of parasites. Finally, changes in population size of hosts were not significantly related to changes in abundance of parasites or their prevalence. CONCLUSIONS/SIGNIFICANCE: Climate change is associated with a general increase in parasite abundance. Variation in laying date depended on locality and was associated with latitude while body condition of hosts was associated with a change in temperature. Because clutch size, brood size and body condition were associated with change in parasitism, these results suggest that parasites, perhaps mediated through the indirect effects of temperature, may affect fecundity and condition of their hosts. The conclusions were particularly in accordance with predictions when the restricted dataset with intervals of 5-15 years was used, suggesting that short intervals may bias findings.

Size-biased allocation of prey from male to offspring via female: family conflicts, prey selection, and evolution of sexual size dimorphism in raptors.

In birds with bi-parental care, the provisioning link between prey capture and delivery to dependent offspring is regarded as often symmetric between the mates. However, in raptors, the larger female usually broods and feeds the nestlings, while the smaller male provides food for the family, assisted by the female in the latter part of the nestling period, if at all. Prey items are relatively large and often impossible for nestlings to handle without extended maternal assistance. We video-recorded prey delivery and handling in nests of a raptor with a wide diet, the Eurasian kestrel Falco tinnunculus, and simultaneously observed prey transfer from male to female outside the nest. The male selectively allocated larger items, in particular birds and larger mammals, to the female for further processing and feeding of nestlings, and smaller items, in particular lizards and smaller mammals, directly to the nestlings for unassisted feeding. Hence, from the video, the female appeared to have captured larger prey than the male, while in reality no difference existed. The female's size-biased interception of the male's prey provisioning line would maximize the male's foraging time, and maximize the female's control of the allocation of food between her own need and that of the offspring. The male would maximize his control of food allocation by capturing smaller prey. This conflict would select for larger dominant females and smaller energy-efficient males, and induce stronger selection the longer the female depends on the male for self-feeding, as a proportion of the offspring dependence period.

Year-round territorial aggression is independent of plasma DHEA in the European nuthatch Sitta europaea.

Plasma testosterone can play an important role in promoting aggressive behaviors relating to territory defense in breeding male birds. Some birds defend territories also during the non-breeding phase, when testosterone circulates at basal levels. In such species, plasma levels of the pro-hormone dehydroepiandrosterone (DHEA) may support non-breeding territoriality by acting as a local substrate for sex steroids. To test this possible role of plasma DHEA, we examined the seasonal DHEA profile of male (and female) European nuthatches Sitta europaea: a male and female nuthatch pair will defend an all-purpose territory throughout the year. We hypothesized that plasma DHEA would be detectable in wintering nuthatches with a territory. However, only ca. half of the territorial wintering males (and females) displayed detectable DHEA levels, suggesting that plasma DHEA is not a major sex steroid precursor during non-breeding. Further, among hatching-year birds, plasma DHEA was significantly lower in territorial birds than in "floaters", i.e., subordinate birds without a territory. To experimentally examine the role of DHEA in non-breeding territoriality, we treated adult wintering males with DHEA and measured effects on aggressive responses to conspecific challenge. DHEA treatment elevated plasma levels of DHEA (and testosterone), but did not enhance territorial behaviors or their persistence. Taken together, our data suggest that DHEA (and, indeed, sex steroids per se) do not regulate non-breeding territoriality in the nuthatch. Given that territorial aggression in nuthatches is expressed year-round, a hormone for its activation may be redundant.

Impact of nesting mortality on avian breeding phenology: a case study on the red-backed shrike (Lanius collurio).

The seasonal timing of avian reproduction is supposed primarily to coincide with favourable feeding conditions. Long-term changes in avian breeding phenology are thus mostly scrutinized in relation to climatic factors and matching of the food supplies, while the role of nesting mortality is largely unexplored. Here we show that higher seasonal mean daily mortality rate leads to a shift in the distribution of breeding times of the successful nests to later dates in an an open-nesting passerine bird, the red-backed shrike Lanius collurio. The effect appeared to be strong enough to enhance or counteract the influence of climatic factors and breeding density on the inter-annual variation in mean hatching dates. Moreover, the seasonal distribution of reproductive output was shifted to larger, or smaller, broods early in the season when the nesting mortality increased, or decreased, respectively, during the season. We suggest that population level changes in timing of breeding caused by a general advancement of spring and of the food supplies might be altered by the seasonality in nesting mortality. Hence, we argue that consideration of nesting mortality is of major importance for understanding long-term trends in avian phenology, particularly in species capable of renesting.

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.

Climate change, breeding date and nestling diet: how temperature differentially affects seasonal changes in pied flycatcher diet depending on habitat variation.

1. Climate warming has led to shifts in the seasonal timing of species. These shifts can differ across trophic levels, and as a result, predator phenology can get out of synchrony with prey phenology. This can have major consequences for predators such as population declines owing to low reproductive success. However, such trophic interactions are likely to differ between habitats, resulting in differential susceptibility of populations to increases in spring temperatures. A mismatch between breeding phenology and food abundance might be mitigated by dietary changes, but few studies have investigated this phenomenon. Here, we present data on nestling diets of nine different populations of pied flycatchers Ficedula hypoleuca, across their breeding range. This species has been shown to adjust its breeding phenology to local climate change, but sometimes insufficiently relative to the phenology of their presumed major prey: Lepidoptera larvae. In spring, such larvae have a pronounced peak in oak habitats, but to a much lesser extent in coniferous and other deciduous habitats. 2. We found strong seasonal declines in the proportions of caterpillars in the diet only for oak habitats, and not for the other forest types. The seasonal decline in oak habitats was most strongly observed in warmer years, indicating that potential mismatches were stronger in warmer years. However, in coniferous and other habitats, no such effect of spring temperature was found. 3. Chicks reached somewhat higher weights in broods provided with higher proportions of caterpillars, supporting the notion that caterpillars are an important food source and that the temporal match with the caterpillar peak may represent an important component of reproductive success. 4. We suggest that pied flycatchers breeding in oak habitats have greater need to adjust timing of breeding to rising spring temperatures, because of the strong seasonality in their food. Such between-habitat differences can have important consequences for population dynamics and should be taken into account in studies on phenotypic plasticity and adaptation to climate change.

Rearing conditions have long-term consequences for stress responsiveness in free-living great tits.

In captivity, the adrenocortical stress response can be permanently altered by events that occur during early life. Free-living animals have rarely been examined in this regard. To examine whether early-life events impact the hypothalamo-pituitary-adrenal (HPA) axis in the natural setting, we evaluated the stress response of free-living interspecifically cross-fostered great tits (Parus major). Cross-fostered birds may show a long-term potentiation of the adrenocortical stress response because species-specific nutritional requirements may not be met in the nest and/or cross-fostered birds may experience psychosocial stress while being raised by heterospecifics. Nevertheless, we hypothesized that in the natural setting, programmed changes in HPA function would be eclipsed by reactive responses to the immediate environment. Thus, we predicted that adult cross-fostered great tits and controls would show no differences in their adrenocortical stress response. Contrary to predictions, we found that stress responsiveness (i.e., the rate of the corticosterone increase associated with capture and handling) was significantly higher in cross-fostered great tits than in controls. Further, stress responsiveness was not significantly different between mature adults and first-year juveniles. Thus, data indicate significant effects of early rearing conditions on adrenocortical reactivity in the natural setting and also suggest that effects of rearing conditions in free-living animals can last into adulthood.

To make the most of what we have: extracting phenological data from nestling measurements.

To study the ecological and evolutionary effects of climate change on timing of annual events, scientists need access to data that have been collected over long time periods. High-quality long-term phenology data are rare and costly to obtain and there is therefore a need to extract this information from other available data sets. Many long-term studies on breeding birds include detailed information on individually marked parents and offspring, but do not include information on timing of breeding. Here, we demonstrate how a study of repeated standard measurements of white-throated dipper Cinclus cinclus nestlings in our study system in southernmost Norway can be used for modeling nestling growth, and how this statistical model can be used to estimate timing of breeding for birds with sparser data. We also evaluate how the accuracies of nestling growth models based on different morphological traits (mass and feather length) differ depending on the nestling age, present user guidelines and demonstrate how they can be applied to an independent data set. In conclusion, the approach presented is likely to be useful for a wide variety of species, even if the preferred measurement may differ between species.

Evolution and possible storage of information in a magnetite system of significance for brain development.

The initial evolutionary electromagnetic steps in the history of brain development are still unknown, although such knowledge might be of high relevance in understanding human degenerative diseases. All prokaryote organisms, one-celled or multicellular, must have an inherited system to process and store information activating instincts and reflexes, in order to give a quick response to external stimuli. We argue that magnetite is an obvious compound to be evaluated as an initial precursor from prebiotic Earth history in the evolution of such a system. Magnetite is a stable ferrimagnetic compound, present in organisms ranging from bacteria to humans. It occurred naturally in the early Earth environment and was later synthesized de novo in biotic organisms. We suggest that the use of magnetite has evolved to represent the main storage system for learned memory in all organisms living today.