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.     

Ultraviolet reflectance of plumage for parent-offspring communication in the great tit (Parus major)

Ultraviolet (UV) reflectance has been implicated in mate selection.Yet, in some bird species the plumage of young varies in UVreflectance already in the nest and long before mate choiceand sexual selection come into play. Most birds molt the juvenilebody plumage before reaching sexual maturity, and thus, someconspicuous traits of the juvenile body plumage may rather haveevolved by natural selection, possibly via predation or parentalpreference. This second hypothesis is largely untested and predictsa differential allocation of food between fledging and totalindependence, which is a time period of 2–3 weeks whereoffspring mortality is also highest. Here, we test the predictionthat parents use the individual variation in UV reflectanceamong fledglings for differential food allocation. We manipulatedUV reflectance of the plumage of fledgling great tits Parusmajor by treating chest and cheek feathers with a lotion thateither did or did not contain UV blockers and then recordedfood allocation by parents in an outdoor design simulating postfledgingconditions. The visible spectrum was minimally affected by thistreatment. Females were found to feed UV-reflecting offspringpreferentially, whereas males had no preference. It is the firstevidence showing that the UV reflectance of the feathers ofyoung birds has a signaling function in parent–offspringcommunication and suggests that the UV traits evolved via parentalpreference.     

Effects of common origin and common environment on nestling plumage coloration in the great tit (Parus major)

Abstract.— Carotenoids cannot be synthesized by birds and thus have to be ingested with food, suggesting that ca-rotenoid-based plumage coloration is environmentally determined. However signaling functions ascribed to plumage imply that plumage coloration is the outcome of an evolutionary process based on genetic variation. By means of a cross-fostering design we show significant effects of both a common rearing environment and the brood from which a nestling originally came from (common origin) on the plumage coloration of nestling great tits ( Parus major ). This demonstration of origin-related variation in carotenoid-based plumage coloration suggests that the observed variation of the trait has a partial genetic basis. Consistent with environmental determination of this trait, we also found a significant positive correlation between the color saturation of nestlings and their foster-father's plumage. There was no significant correlation between nestling plumage coloration and the food quantity provided to the nestlings by the male, the female, or both parents. This suggests that the nestling-foster father correlation arises by the carotenoid quantity ingested rather than the food quantity per se. No significant nestling-true father correlation was found, which suggests that nestling plumage coloration did not indirectly evolve due to sexual selection. Consistent with this result there was no significant correlation between the nestling's plumage color and its coloration as a breeding adult the following year, suggesting that nestling plumage color is a different trait than the first year plumage.     

Habitat structure and prey composition generate contrasting effects on carotenoid‐based coloration of great tit Parus major nestlings

Carotenoid‐based coloration of nestling plumage is generally considered a reliable signal of quality and has consistently been related to habitat structure. The main hypothesis proposed to explain this correlation is that high quality habitats contain high quality food, which in return affects the expression of carotenoid‐based plumage. It therefore assumes that, at the population level, the link between habitat structure and food composition is consistent and more relevant than inter‐individual differences in foraging ability or parental investment. In addition, it is assumed by default that food and habitat produce concordant effects on nestling coloration. In this work we evaluated habitat structure and prey composition in addition to several measures of parental investment. We investigated their relative effect on carotenoid‐based plumage coloration (lightness, chroma and hue) of great tit Parus major nestlings. We found a low correlation between carotenoid‐based coloration of nestlings and that of their parents. Nestling coloration, especially lightness and chroma, increased with the intake of more spiders. The time of breeding was positively correlated with lightness and chroma and negatively correlated with hue. Finally, the maturity of oak trees surrounding nest‐boxes correlated negatively with lightness, and the size of all tree species surrounding nest‐boxes correlated positively with hue of chick plumage. Our findings support the view that habitat structure and prey composition may produce divergent effects on feather pigmentation, and that prey proportions and variables related to parental investment should be assessed when considering carotenoid‐based coloration of chicks. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 547–555.     

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

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

Genetic variability in mitochondrial DNA in a regional population of the great tit (Parus major)

Genetic variation of mitochondrial DNA (mtDNA) in 18 great tits (Parus major) from three neighboring localities in Sweden was investigated with eight tetranucleotide restriction endonucleases. The 18 individuals could be separated into 13 different maternal lineages. The high number of female lineages present in this regional population contrasts with a low level of sequence divergence between the different mtDNA clones, with a mean of 0.19% sequence divergence between all individuals. There was no obvious spatial structuring of mtDNA clones among the three localities. The presence of a high number of different clones with a low degree of sequence divergence could be explained by the effects of a large long-term effective population size, with the mtDNA clones having diverged about 25,000–200,000 years ago.This study was supported by the Swedish Natural Science Research Council, the Erik Philip-Sörensen Foundation, and the Nilsson-Ehle Foundation.     

Caterpillar abundance in the territory affects the breeding performance of great tit Parus major minor

The effects of caterpillar food supply on the breeding performance of a population of the Japanese great tit Parus major minor were investigated. Since more than 90% of the food items in our study site were caterpillars living on trees, we estimated the food availability using 20 frass traps per hectare. The sampling error of this method was about 10% on average, which was accurate enough to detect differences between territories. Food abundance at laying in each territory affected the timing of egg laying. However, food amount after hatching was correlated with clutch size. No relationship was found between fledgling quality and food availability, probably because the effects of local variation in food abundance could be canceled out by parental effort such as extending the foraging area. There was a significant negative correlation between the length of the nestling period and food availability. We suggest that parent tits decide the timing of fledging at the point where two factors, predation risk before fledging and additional improvement of nestling quality, are balanced. Food availability just after fledging affected the length of post-fledging parental care; it seems that fledglings in “poor” territories would have had difficulty in finding food and hence needed to depend on their parents longer than those in “rich” territories. Received: 10 June 1997 / Accepted: 29 December 1997     

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.     

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.     

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.     

Energy expenditure, nestling age, and brood size: an experimental study of parental behavior in the great tit Parus major

A brood manipulation experiment on great tits Parus major was performedto study the effects of nestling age and brood size on parentalcare and offspring survival. Daily energy expenditure (DEE)of females feeding nestlings of 6 and 12 days of age was measuredusing the doubly-labeled water technique. Females adjusted theirbrooding behavior to the age of the young. The data are consistentwith the idea that brooding behavior was determined primarilyby the thermoregulatory requirements of the brood. Female DEEdid not differ with nestling age; when differences in body masswere controlled for, it was lower during the brooding periodthan later. In enlarged broods, both parents showed significantlyhigher rates of food provisioning to the brood. Female DEE wasaffected by brood size manipulation, and it did not level offwith brood size. There was no significant effect of nestlingage on the relation between DEE and manipulation. Birds wereable to raise a larger brood than the natural brood size, althoughlarger broods suffered from increased nestling mortality ratesduring the peak demand period of the nestlings. Offspring conditionat fledging was negatively affected by brood size manipulation,but recruitment rate per brood was positively related to broodsize, suggesting that the optimal brood size exceeds the naturalbrood size in this population.     

Effects of snow cover on the benthic fauna in a glacier-fed stream

1. Alpine streams above the tree line are covered by snow for 6–9 months a year. However, winter dynamics in these streams are poorly known. The annual patterns of macroinvertebrate assemblages were studied in a glacial stream in the Austrian Alps, providing information on conditions under the snow.
2. Snow cover influenced water temperature, the content of benthic organic matter and insect development. Taxa richness and abundance of macroinvertebrates did not show a pronounced seasonal pattern. The duration of the autumn period with stable stream beds was important in determining the abundance and composition of the winter fauna.
3. There were significant differences in species composition between summer and winter. Two potential strategies in larval survival were evident: adaptation to the extreme abiotic conditions in summer (e.g. Diamesa spp.) or avoidance of these conditions and development during winter (e.g. Ephemeroptera and Plecoptera).
4. A comparison of a stream reach with continuous snow cover and a stream reach that remained open throughout winter showed that conditions under snow are suboptimal. At the open stream site, with higher water temperatures and greater food supply (benthic organic matter content), abundance and taxa richness was higher and larval growth was faster. Several taxa were found exclusively at this site.
5. Winter conditions did not provide an entirely homogeneous environment, abiotic conditions changed rapidly, especially at the onset of snowfall and at snowmelt. Continuous monitoring is necessary to recognize spatial and temporal heterogeneity in winter environments and the fauna of alpine streams.     

Isolation and characterization of 16 microsatellite loci in the Great Tit Parus major

Six dinucleotide, three trinucleotide and seven tetranucleotide microsatellite loci developed for the great tit Parus major are presented. Thirty individual birds were screened at each locus. Loci were polymorphic (four to 19 alleles per locus). These markers provide a system to study paternity, genetic diversity in natural populations, gene flow, dispersal and inbreeding.     

Offspring sex ratio is related to male body size in the great tit (Parus major)

Sex allocation theory predicts that the allocation of resourcesto male and female function should depend on potential fitnessgain realized through investment in either sex. In the greattit (Parus major), a monogamous passerine bird, male resourceholdingpotential (RHP) and fertilization success both depend on malebody size (e.g., tarsus length) and plumage traits (e.g., breaststripe size). It is predicted that the proportion of sons ina brood should increase both with male body size and plumage traits,assuming that these traits show a father—offspring correlation. Thiswas confirmed in our study: the proportion of sons in the brood increasedsignificantly with male tarsus length and also, though not significantly,with the size of the breast stripe. A sex ratio bias in relationto male tarsus length was already present in the eggs because(1) the bias was similar among broods with and without mortalitybefore the nestlings' sex was determined, and (2) the bias remainedsignificant when the proportion of sons in the clutch was conservativelyestimated, assuming that differential mortality before sex determinationcaused the bias. The bias was still present among recruits.The assumption of a father—offspring correlation was confirmedfor tarsus length. Given that both RHP and fertilization successof male great tits depend on body size, and size of father andoffspring is correlated, the sex ratio bias may be adaptive.     

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.     

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.