Seasonal and lifetime reproductive consequences of inbreeding in the great tit Parus major

Inbreeding depression has been hypothesized to drive the evolutionof mating systems and dispersal. Some studies have shown thatinbreeding strongly affects survival and/or fecundity, but otherstudies suggest that fitness consequences of inbreeding areless detrimental or more complex. We studied consequences ofmating with a relative in a population of great tits (Parusmajor) with a high local recruitment rate. Genotypic informationfrom microsatellite markers was used to calculate coefficientsof kinship, and fitness was measured as seasonal and lifetimereproductive success. We show that mating with a relative affectsseasonal reproductive success, as was found in other studiesof the same species. However, these effects do not result ina lifetime fitness reduction, suggesting that individuals mayhave scope for avoidance of inbreeding after inbreeding depression.Several explanations are proposed as compensatory mechanisms.Although individuals are more likely to divorce after experiencinginbreeding depression, we show that divorce alone cannot explainthe compensation for inbreeding depression in subsequent breedingattempts in our study. We conclude that the costs of matingwith a relative in the short term do not necessarily imply lifetimefitness consequences.     

Endocrine phenotype,reproductive success and survival in the great tit,Parus major

A central goal in evolutionary ecology is to characterize and identify selection patterns on the optimal phenotype in different environments. Physiological traits, such as hormonal responses, provide important mechanisms by which individuals can adapt to fluctuating environmental conditions. It is therefore expected that selection shapes hormonal traits, but the strength and the direction of selection on plastic hormonal signals are still under investigation. Here, we determined whether, and in which way, selection is acting on the hormones corticosterone and prolactin by characterizing endocrine phenotypes and their relationship with fitness in free‐living great tits, Parus major. We quantified variation in circulating concentrations of baseline and stress‐induced corticosterone and in prolactin during the prebreeding (March) and the breeding season (May) for two consecutive years, and correlated these with reproductive success (yearly fledgling number) and overwinter survival in female and male individuals. In both years, individuals with high baseline corticosterone concentrations in March had the highest yearly fledgling numbers; while in May, individuals with low baseline corticosterone had the highest yearly reproductive success. Likewise, individuals that displayed strong seasonal plasticity in baseline corticosterone concentrations (high in March and low in May) had the highest reproductive success in each year. Prolactin concentrations were not related to reproductive success, but were positively correlated to the proximity to lay. Between‐year plasticity in stress‐induced corticosterone concentrations of males was related to yearly variation in food abundance, but not to overall reproductive success. These findings suggest that seasonally alternating directional selection is operating on baseline corticosterone concentrations in both sexes. The observed between‐year consistency in selection patterns indicates that a one‐time hormone sample in a given season can allow the prediction of individual fitness.     

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

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

Variation in plumage colour of the Great tit Parus major in relation to habitat, season and food

The plumage colour of nestling and adult Great tits Parus major major L. was studied at Trondheim (63 °N, 10 °E), Norway. Nestlings reared in deciduous woodland were yellower than those reared in coniferous woodland, those reared in 1983 were yellower than those in 1982, and the later in the breeding season they were reared the more yellow they were. Furthermore, adults were yellower than nestlings, and for both groups the males were yellower than the females. Experimental interchange of eggs between nests showed that the variation in plumage colour observed between broods was related primarily to the food and not to genetic differences. Sampling, by the neck-collar method, of the food brought by the parent birds showed that the yellower nestlings received a greater proportion of lepidopteran larvae, in particular greenish-coloured ones, than did the nestlings with a paler plumage. A speculation is whether or not the variation in plumage colour has some adaptive value (viz. background matching).
In avian systematics, plumage coloration has been used to distinguish and describe subspecies. The present study shows that such a classification should only be made with certain reservations, until possible variation in the food quality of the subspecies is known to have no influence on plumage coloration.     

Inheritance and variation in eggshell patterning in the great tit Parus major

The inheritance of patterns on avian eggshells is central to understanding the evolution of traits such as egg mimicry (e.g. in cuckoos). Yet little is known about the inheritance, or indeed function, of eggshell patterns. It has long been believed that the evolution of eggshell pattern mimicry required that patterns be determined by genes situated on the female-specific W chromosome. However, it has never been demonstrated for any bird that egg pattern traits (rather than ground colour) are female sex linked, or indeed that they are inherited. We studied the inheritance of three measures of egg-pigment patterns in a wild great tit population. Egg patterns were female specific but unrelated to female attributes such as age or condition and showed only weak environmental effects. Eggs of daughters resembled those of both their mothers and maternal grandmothers, but not of their paternal grandmothers. We conclude that this is the first demonstration of female sex-linked inheritance of avian eggshell patterning, so raising the probability that such a system operates in egg mimics and their hosts.     

Realized heritability of personalities in the great tit (Parus major)

Behaviour under conditions of mild stress shows consistent patterns in all vertebrates: exploratory behaviour, boldness, aggressiveness covary in the same way. The existence of highly consistent individual variation in these behavioural strategies, also referred to as personalities or coping styles, allows us to measure the behaviour under standardized conditions on birds bred in captivity, link the standardized measurements to the behaviour under natural conditions and measure natural selection in the field. We have bred the great tit (Parus major), a classical model species for the study of behaviour under natural conditions, in captivity. Here, we report a realized heritability of 54 +/- 5% for early exploratory behaviour, based on four generations of bi-directional artificial selection. In addition to this, we measured hand-reared juveniles and their wild-caught parents in the laboratory. The heritability found in the mid-offspring-mid-parent regression was significantly different from zero. We have thus established the presence of considerable amounts of genetic variation for personality types in a wild bird.     

Speckled eggs: water-loss and incubation behaviour in the great tit Parus major

Many small passerine birds worldwide lay white eggs speckled with red, brown and black protoporphyrin pigment spots (maculation). Unlike some patterns of avian eggshell pigmentation which clearly serve a crypsis or signalling function, the ubiquity of maculation among passerines suggests that its origins lie in another function, not specific to any particular ecological or behavioural group. Elsewhere, we have presented evidence that protoporphyrin pigments serve a structural function related to eggshell thickness and calcium availability: eggshell maculation in the great tit Parus major increases with decreasing soil calcium levels, pigments demarcate thinner areas of shell, and both the pigment intensity and distribution are related to shell thickness. Here we show that maculation also affects the rate of water loss from the egg during incubation (≈ Mass Loss per Day or MLD, which is critical to egg viability), but not that of unincubated eggs. We also demonstrate, both by observation and experiment, that the effect of female incubation behaviour on MLD compensates in some way for variation in egg characteristics, and that differences between females in the degree of such compensation are related to differences in clutch maculation. Our results suggest that, while a principal function of maculation in this species may be to strengthen the eggshell, it may also reduce eggshell permeability when large amounts of pigment are used, and that this necessitates a behavioural adjustment from the female during incubation. We discuss these findings and make further testable predictions from our model.     

Fat reserves and perceived predation risk in the great tit, Parus major

The fat reserves of small birds are built up daily as insurance against starvation. They are believed to reflect a trade-off between the risks of starvation and predation such that in situations of high predation risk birds are expected either to reduce their fat reserves in response to mass-dependent predation risk or to increase them in response to foraging interruptions. We assessed the effect on fat reserves of experimentally altering the perceived (but not the actual) risk of predation of wild great tits at a winter feeding site. The perceived predation risk was alternated between 'safe' and 'risky'. Increasing the perceived risk of predation involved 'swooping' a model sparrowhawk over the feeder at four unpredictable times each day using a remote mechanism We produce evidence that the experiment was suceessfull in altering the perceived risk of predation. As predicted from the hypothesis of mass-dependent predation risk, great tits (Parus major) carried significantly reduced fat reserves during the 'risky' treatment. Furthermore, dominant individuals were able to reduce their reserves more than subordinates. As birds returned to feeders within seconds after a predator 'attack', the reduction in fat reserves cannot be attributed to an interruption in feeding.     

Influence of temperatures during the nestling period on post-fledging survival of great tit Parus major in a Mediterranean habitat

Survival during the first year is one of the most important factors determining fitness in birds. Birds have poor thermoregulatory abilities during the nestling period when the plumage is not fully developed, thus temperature during the nestling period is a serious candidate to affect post-fledging survival, although it has been usually ignored in previous studies. We analysed the relationship between temperatures and post-fledging survival in a great tit Parus major population in Sagunto (Spain) using capture-recapture data from 12 years. Hatching dates, mass at fledging and temperatures during the nestling period (maximum, minimum and mean ambient temperatures as an estimation of the mean and extreme weather conditions that chicks encountered at the nest) were used as individual covariates. Mean post-fledging survival was 0.13±0.01. Adult survival probability was 0.64±0.02. Multi-model inference suggested that post-fledging survival increased with fledging mass, and decreased as temperatures increased. Furthermore, the effect of mass on survival was less important as temperature was higher. We consider that high temperatures affect nestlings' health due to low thermoregulatory abilities of nestlings. Model selection did not support a relationship between hatching dates and survival once mass and temperatures were taken into account. The results suggest the possibility that the effect of date on post-fledging survival found in previous studies was, at least in part, a consequence of the seasonal pattern of temperature variation.     

Evolution and genetic structure of the great tit (Parus major) complex

The great tit complex is divided into four groups, each containing several subspecies. Even though the groups are known to differ markedly on morphological, vocal and behavioural characters, some hybridization occurs in the regions where they meet. The great tit has often been referred to as an example of a ring species, although this has later been questioned. Here, we have studied the genetic structure and phylogenetic relationships of the subspecies groups to clarify the evolutionary history of the complex using control region sequences of the mitochondrial DNA. The subspecies groups were found to be monophyletic and clearly distinct in mitochondrial haplotypes, and therefore must have had long-independent evolutionary histories. This conflicts with the ring species assignment and supports the formation of secondary contact zones of previously temporarily isolated groups. According to the phylogenetic species concept, all the subspecies groups could be considered as separate species, but if the definition of the biological species concept is followed, none of the subspecies groups is a true species because hybridization still occurs.     

Paternal leakage of mitochondrial DNA in the great tit (Parus major)

Animal mitochondrial DNA is normally inherited clonally from a mother to all her offspring. Mitochondrial heteroplasmy, the occurrence of more than one mitochondrial haplotype within an individual, can be generated by relatively common somatic mutations within an individual, by heteroplasmy of the oocytes, or by paternal leakage of mitochondria during fertilization of an egg. This biparental inheritance has so far been reported only in mice, mussels, Drosophila, and humans. Here we present evidence that paternal leakage occurs in a bird, the great tit Parus major. The major and minor subspecies groups of the great tit mix in the middle Amur Valley in far-eastern Siberia, where we found a bird that possessed the very distinct haplotypes of the two groups. To our knowledge this is the first report of paternal leakage in birds.     

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.     

Urbanisation lowers great tit Parus major breeding success at multiple spatial scales

While numerous studies have reported negative effects of urbanisation on birds, few have examined the role of urban scale in influencing breeding success. Furthermore, many studies have relied on qualitative rather than quantitative assessments of urbanisation. This study sought to address these issues by testing the effects of urbanisation, measured at two spatial scales, on the breeding success of great tits Parus major. A nested study design, incorporating over 400 nestboxes, was used in study sites across northern Belgium with a priori quantified degrees of urbanisation at both local and regional scales. All measured breeding parameters were found to vary at one or both spatial scales of urbanisation; in more urbanised areas great tits displayed advanced laying dates but lower breeding success compared to rural areas, with smaller clutch sizes, lower nestling masses and fewer fledglings per egg. Importantly, urbanisation effects were not limited to big cities as birds breeding in gardens or parks in small towns also had comparatively low success. We found that both regional‐ and local‐scale urbanisation had consistent significant effects on laying date, clutch size and nestling mass, while the number of fledglings per egg was negatively influenced by local‐scale urbanisation only. Results of this study therefore highlight the importance of utilising multiple spatial scales in analysing urbanisation effects, as well as the potential negative impact of local urbanisation on breeding success. This calls for further investigation into mechanisms driving urbanisation effects and how these may vary at different scales.     

Intensity of nest defence is related to offspring sex ratio in the great tit Parus major

Nest-defence behaviour of passerines is a form of parental investment. Parents are selected, therefore, to vary the intensity of their nest defence with respect to the value of their offspring. Great tit, Parus major, males were tested for their defence response to both a nest predator and playback of a great tit chick distress call. The results from the two trials were similar; males gave more alarm calls and made more perch changes if they had larger broods and if they had a greater proportion of sons in their brood. This is the first evidence for a relationship between nest-defence intensity and offspring sex ratio. Paternal quality, size, age and condition, lay date and chick condition did not significantly influence any of the measured nest-defence parameters.     

Variation in personality and behavioural plasticity across four populations of the great tit Parus major

1. Interest in the evolutionary origin and maintenance of individual behavioural variation and behavioural plasticity has increased in recent years. 2. Consistent individual behavioural differences imply limited behavioural plasticity, but the proximate causes and wider consequences of this potential constraint remain poorly understood. To date, few attempts have been made to explore whether individual variation in behavioural plasticity exists, either within or between populations. 3. We assayed 'exploration behaviour' among wild-caught individual great tits Parus major when exposed to a novel environment room in four populations across Europe. We quantified levels of individual variation within and between populations in average behaviour, and in behavioural plasticity with respect to (i) repeated exposure to the room (test sequence), (ii) the time of year in which the assays were conducted and (iii) the interval between successive tests, all of which indicate habituation to novelty and are therefore of functional significance. 4. Consistent individual differences ('I') in behaviour were present in all populations; repeatability (range: 0.34-0.42) did not vary between populations. Exploration behaviour was also plastic, increasing with test sequence - but less so when the interval between subsequent tests was relatively large - and time of year; populations differed in the magnitude of plasticity with respect to time of year and test interval. Finally, the between-individual variance in exploration behaviour increased significantly from first to repeat tests in all populations. Individuals with high initial scores showed greater increases in exploration score than individuals with low initial scores; individual by environment interaction ('I × E') with respect to test sequence did not vary between populations. 5. Our findings imply that individual variation in both average level of behaviour and behavioural plasticity may generally characterize wild great tit populations and may largely be shaped by mechanisms acting within populations. Experimental approaches are now needed to confirm that individual differences in behavioural plasticity (habituation) - not other hidden biological factors - caused the observed patterns of I × E. Establishing the evolutionary causes and consequences of this variation in habituation to novelty constitutes an exciting future challenge.     

Isolation of polymorphic microsatellite markers in the great tit (Parus major minor)

Six microsatellite loci were developed for a passerine bird, the great tit (Parus major), using two methods. These loci were polymorphic (3–8 alleles per locus) and exhibited expected heterozygosities from 0.45 to 0.77. At one locus the genotypic frequencies deviated significantly from Hardy–Weinberg expectations.     

Is variation in brood sex ratios adaptive in the great tit (Parus major)?

Life-history theory predicts skewed offspring sex ratios ina range of situations in which the costs and benefits of producingthe two sexes differ. In recent years, many studies have demonstratedbiased sex ratios in a variety of bird species. However, manyof these investigations have been based on small sample sizes,on data from a single year, or both. Using a recently developedpolymerase chain reaction-based molecular DNA technique, 912great tit (Parus major) nestlings from 118 broods in 5 differentyears were sexed. As found in a number of previous studieson the same species, there were significant predictors of offspringsex ratio in individual years. However, there were no consistenttrends across years, and none of the measured variables significantlypredicted sex ratio over all years combined. Furthermore, broodsex ratio of the population did not depart from the expectedbinomial distribution. Although there are theoretical advantagesto manipulating the sex ratio in this and other species, thephysiological mechanism by which it is achieved in birds remainsobscure. We argue that data from several years are needed toconfirm whether facultative sex ratio manipulation is a consistentbreeding strategy used by birds.