Molecular development of fibular reduction in birds and its evolution from dinosaurs

Birds have a distally reduced, splinter‐like fibula that is shorter than the tibia. In embryonic development, both skeletal elements start out with similar lengths. We examined molecular markers of cartilage differentiation in chicken embryos. We found that the distal end of the fibula expresses Indian hedgehog (IHH), undergoing terminal cartilage differentiation, and almost no Parathyroid‐related protein (PTHrP), which is required to develop a proliferative growth plate (epiphysis). Reduction of the distal fibula may be influenced earlier by its close contact with the nearby fibulare, which strongly expresses PTHrP. The epiphysis‐like fibulare however then separates from the fibula, which fails to maintain a distal growth plate, and fibular reduction ensues. Experimental downregulation of IHH signaling at a postmorphogenetic stage led to a tibia and fibula of equal length: The fibula is longer than in controls and fused to the fibulare, whereas the tibia is shorter and bent. We propose that the presence of a distal fibular epiphysis may constrain greater growth in the tibia. Accordingly, many Mesozoic birds show a fibula that has lost its distal epiphysis, but remains almost as long as the tibia, suggesting that loss of the fibulare preceded and allowed subsequent evolution of great fibulo–tibial disparity.     

Mutual ornamentation and the parental behaviour of male and female Collared Flycatchers Ficedula albicollis during incubation

One of the benefits of mate choice based on sexually selected traits is the greater investment of more ornamented individuals in parental care. The choosy individual can also adjust its parental investment to the sexual signals of its partner. Incubation is an important stage of avian reproduction, but the relationship between behaviour during incubation and mutual ornamentation is unclear. Studying a population of Collared Flycatchers Ficedula albicollis, we monitored the behaviour of both sexes during incubation in relation to their own and their partner's plumage traits, including plumage‐level reflectance attributes and white patch sizes. There was a marginally positive relationship between male feeding rate during incubation and female incubation rate. Female but not male behavioural traits were associated with the laying date of the first egg and clutch size. The behaviour of the two sexes jointly determined the relative hatching speed of clutches and the hatching success of eggs. Females with larger white wing patches spent less time incubating eggs and left the nestbox more frequently. Males with larger white wing patches fed females less frequently, whereas males with brighter white plumage areas visited the nestbox more regularly without feeding. Females tended to leave the nest less often when mated to males with larger wing patches, and females spent less time incubating when males had more UV chromatic plumage. The behaviour of both partners during incubation therefore predicted hatching patterns and was correlated with their own and sometimes with their partner's plumage ornamentation. These results call for further studies of mutual ornamentation and reproductive effort during incubation.     

Evolution of olfaction in non-avian theropod dinosaurs and birds

Little is known about the olfactory capabilities of extinct basal (non-neornithine) birds or the evolutionary changes in olfaction that occurred from non-avian theropods through modern birds. Although modern birds are known to have diverse olfactory capabilities, olfaction is generally considered to have declined during avian evolution as visual and vestibular sensory enhancements occurred in association with flight. To test the hypothesis that olfaction diminished through avian evolution, we assessed relative olfactory bulb size, here used as a neuroanatomical proxy for olfactory capabilities, in 157 species of non-avian theropods, fossil birds and living birds. We show that relative olfactory bulb size increased during non-avian maniraptoriform evolution, remained stable across the non-avian theropod/bird transition, and increased during basal bird and early neornithine evolution. From early neornithines through a major part of neornithine evolution, the relative size of the olfactory bulbs remained stable before decreasing in derived neoavian clades. Our results show that, rather than decreasing, the importance of olfaction actually increased during early bird evolution, representing a previously unrecognized sensory enhancement. The relatively larger olfactory bulbs of earliest neornithines, compared with those of basal birds, may have endowed neornithines with improved olfaction for more effective foraging or navigation skills, which in turn may have been a factor allowing them to survive the end-Cretaceous mass extinction.     

Nest attendance by tropical and temperate passerine birds: Same constancy,different strategy

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Allometry of egg mass, clutch size and total clutch mass in dinosaurs: comparison with modern reptiles and birds

The author presents for the first time empirical allometrical equations corresponding the mass of dinosaurs with the mass of their eggs, clutch size and its total mass. Comparison of these equations with those that were proposed for modern taxa of reptiles and birds shows that dinosaurs can be characterized by intermediate value of allometry index.     

The evolution of egg shape in birds: selection during the incubation period

A recent broad comparative study suggested that factors during egg formation – in particular ‘flight efficiency’, which explained only 4% of the interspecific variation – are the main forces of selection on the evolution of egg shape in birds. As an alternative, we tested whether selection during the incubation period might also influence egg shape in two taxa with a wide range of egg shapes, the alcids (Alcidae) and the penguins (Spheniscidae). To do this, we analysed data from 30 species of these two distantly related but ecologically similar bird families with egg shapes ranging from nearly spherical to the most pyriform eggs found in birds. The shape of pyriform eggs, in particular, has previously proven difficult to quantify. Using three egg‐shape indices – pointedness, polar‐asymmetry and elongation – that accurately describe the shapes of all birds’ eggs, we examined the effects of egg size, chick developmental mode, clutch size and incubation site on egg shape. Linear models that include only these factors explained 70–85% of the variation in these egg‐shape indices, with incubation site consistently explaining > 60% of the variation in shape. The five species of alcids and penguins that produce the most pyriform eggs all incubate in an upright posture on flat or sloping substrates, whereas species that incubate in a cup nest have more spherical eggs. We suggest that breeding sites and incubation posture influence the ability of parents to manipulate egg position, and thus selection acting during incubation may influence egg‐shape variation across birds as a whole.     

Avian eggshell thickness: scaling and maximum body mass in birds

The avian eggshell represents a highly evolved structure adapted to the physiological requirements of the embryo and the potential fracturing forces it is exposed to during incubation. Given its many roles, it is not surprising that the eggshell is also central to the current hypothesis about maximum avian body mass. Eggshell thickness ( L ) and strength has historically been scaled as a function of initial egg mass (IEM). However, maximum incubator mass (IM) is likely a better indicator of the forces the shell must be selected to withstand during incubation. We compare the results of analyses of L ² (an indicator of shell strength) as a function of IEM and IM. We conclude from IM scaling that megapode and kiwi eggshells are not thin but rather are thicker than expected and in general birds with a clutch size of 1 have thicker shells, and further, that reversed sexual dimorphism in the large, particularly extinct birds may be a strategy to avoid shell breakage during incubation of the largest eggs without creating a shell so thick as to inhibit hatching.     

Successive clutches and parental roles in waders: the importance of timing in multiple clutch systems

Production of successive clutches within the same breeding season has received less attention than many other aspects of avian reproduction. Waders are of particular interest because in these birds, multiple clutches are associated with at least three different breeding systems: double-clutching (uniparental care), monogamous double-brooding (biparental care) and polyandry (uni- or biparental care). Data from eight species and twelve breeding populations suggest that early second clutches, and thus brood overlap, are associated with parental role division and uniparental care, whereas species or populations with biparental care tend to have long intervals between successive clutches. We suggest that ecological factors influencing the relative timing of the second clutch will have consequences for the parental care system. In particular, conditions that favour early laying of the second clutch (large brood overlap) are likely to lead to parental role division, as found in double-clutching species. Factors determining the timing of second clutches are discussed, as are possibilities for testing these ideas.     

Free‐moving artificial eggs containing temperature loggers reveal remarkable within‐clutch variance in incubation temperature

Incubation is a crucial aspect of avian parental care and measuring incubation temperature in the wild can improve our understanding of life history tradeoffs and inform conservation efforts. However, there are challenges associated with measuring the temperature of eggs in natural nests. Most studies to date have measured incubation temperature by using a single, stationary logger in each nest. However, real eggs are rotated and moved throughout the nest by the parent during the incubation period, and thus, a stationary logger may not accurately represent the temperature experienced by individual eggs within the entire clutch. We recorded incubation temperature in nests by using multiple, mobile artificial egg temperature loggers. We installed six mobile loggers and one stationary logger in wood duck Aix sponsa nests to compare the two logger types in the field. We found that at a given ambient temperature, mobile loggers recorded lower average and more variable temperatures than stationary loggers. Further, temperatures recorded by stationary loggers showed no relationship with clutch size, while mobile loggers captured temperatures that were lower and more variable as clutch size increased. Also, the multiple mobile loggers revealed that eggs within a nest experienced a substantial range of temperatures throughout the incubation period. We discuss potential limitations of this method, but believe that it is a promising way to collect biologically‐relevant incubation temperature data and provides an opportunity to advance our understanding of incubation temperature as a parental effect.     

Division of labour during incubation in a woodpecker Colaptes auratus with reversed sex roles and facultative polyandry

The contribution of males to incubation has rarely been studied in altricial birds because the pursuit of extra mating opportunities is believed to conflict with incubation. Woodpeckers show reversed sex roles in parental care with males doing most of the nest construction, incubating and brooding of the young while females may be polyandrous. I investigated incubation by each sex at 71 monogamous and four polyandrous nests of the Northern Flicker Colaptes auratus , predicting that males would contribute to incubation according to their energy reserves (body condition) whereas females would contribute based on alternate reproductive opportunities. Nest attendance was 99% with males contributing a mean of 66% of the total incubation including nocturnal incubation. The length of daytime bouts averaged about 2 h and did not differ between the sexes. Consistent with predictions of investment strategies, structurally larger males and those in poorer body condition incubated less than smaller males, perhaps because they required more recess time to forage or to conserve energy. Older females contributed less incubation than young females and polyandrous females contributed less incubation at their secondary nests than monogamous females. Incubation period, nest depredation rate and hatching success were not influenced by bout length, number of bouts or relative contribution of the sexes. Hatching success was 86% at nests of both monogamous and polyandrous females because males compensated for reduced female participation. Because incubation of the sexes is compensatory and not additive, incubation pattern did not influence short-term reproductive success. I conclude that males invest in incubation according to their energy needs, and females may adjust their contributions based on alternate reproductive tactics.     

Egg mass and incubation period allometry in birds and reptiles: effects of phylogeny

Here we test the hypothesis that the relationship between egg mass at oviposition (IEM) and incubation period ( I _p) is a function of the taxonomic relatedness of bird and reptile species. Allometric relationships between IEM and I _p were examined for 1525 bird species and 201 reptilian species. Treating species as independent data revealed the allometric exponent linking I _p to IEM to be 0.234 for birds and 0.138 for reptiles. However, ANCOVA revealed that within both birds and reptiles the elevation and slope of the regression lines were dependent on the taxonomic order studied, indicating that the exponents were confounded by the phylogenetic relatedness of species. Thus, allometric exponents were recalculated based on the method of comparative analysis using independent contrasts. This technique revealed that the allometric exponent in both birds and reptiles was confounded by phylogeny. In birds the allometric relationship between I _p and IEM was almost halved to 0.122, whereas in reptiles the exponent increased to 0.185. Importantly, the results demonstrate that some results of allometric analyses can be artefacts of the method of analysis of the dataset. That for bird eggs I _p is not determined in large part by egg mass allows new questions to be posed regarding the ecological and physiological factors affecting the length of incubation, and hence rates of embryonic growth, for different taxa and habitats.     

Red coloration and male parental behaviour in the threespine stickleback

In an anadromous population of the threespine stickleback, male red coloration was correlated with agonistic and egg care behaviour of parental males, but not with hatching success. When one male took over a neighbour's territory, the dominant male had more intense red coloration.     

Evolution of reproductive life histories in island birds worldwide

Island environments typically share characteristics such as impoverished biotas and less-seasonal climates, which should be conducive to specific adaptations by organisms. However, with the exception of morphological studies, broad-scale tests of patterns of adaptation on islands are rare. Here, I examine reproductive patterns in island birds worldwide. Reproductive life histories are influenced by latitude, which could affect the response to insularity; therefore, I additionally test this hypothesis. Island colonizers showed mostly bi-parental care, but there was a significant increase in cooperative breeding on islands. Additionally, I found support for previous suggestions of reduced fecundity, longer developmental periods and increased investment in young on islands. However, clutch size increased with latitude at a rate nearly five times faster on the mainland than on the islands revealing a substantially stronger effect of insularity at higher latitudes. Latitude and insularity may also interact to determine egg volume and incubation periods, but these effects were less clear. Analyses of reproductive success did not support an effect of reduced nest predation as a driver of reproductive change, but this requires further study. The effect of latitude detected here suggests that the evolutionary changes associated with insularity relate to environmental stability and improved adult survival.     

Parental conflict in birds: comparative analyses of offspring development, ecology and mating opportunities

Parents often conflict over how much care to provide to their offspring. This conflict is expected to produce a negative relationship between male and female parental care, the strength of which may be mediated by both ecological and life-history variables. Previous studies have observed such trade-offs, but it is not known how generally they occur. Traditional views of sexual conflict place great importance on ecological factors in determining levels of parental care, whereas alternative views propose that the key determinant is mating opportunity. We carried out a broad-scale comparative study of parental conflict using 193 species from 41 families of birds. Using phylogenetic comparative analysis, we establish the generality of intersexual parental care conflict. We also show that parental conflict, as indicated by the disparity in care between the male and the female, depends on offspring development and mating opportunities, since in precocial species both males and females responded to increased mating opportunities. Altricial birds, however, failed to show these relationships. We also found little influence of breeding climate on parental conflict. Taken together, our results suggest that sexual conflict is a key element in the evolution of parental care systems. They also support the view that the major correlates of the intersexual conflict are mating opportunities for both sexes, rather than the breeding environment.     

Strategic female reproductive investment in response to male attractiveness in birds

Life-history theory predicts that individuals should adjust their reproductive effort according to the expected fitness returns on investment. Because sexually selected male traits should provide honest information about male genetic or phenotypic quality, females may invest more when paired with attractive males. However, there is substantial disagreement in the literature whether such differential allocation is a general pattern. Using a comparative meta-regression approach, we show that female birds generally invest more into reproduction when paired with attractive males, both in terms of egg size and number as well as food provisioning. However, whereas females of species with bi-parental care tend to primarily increase the number of eggs when paired with attractive males, females of species with female-only care produce larger, but not more, eggs. These patterns may reflect adaptive differences in female allocation strategies arising from variation in the signal content of sexually selected male traits between systems of parental care. In contrast to reproductive effort, female allocation of immune-stimulants, anti-oxidants and androgens to the egg yolk was not consistently increased when mated to attractive males, which probably reflects the context-dependent costs and benefits of those yolk compounds to females and offspring.     

Mortality costs of sexual selection and parental care in natural populations of birds

Abstract Is the cost of reproduction different between males and females? On the one hand, males typically compete intensely for mates, thus sexual selection theory predicts higher cost of reproduction for males in species with intense male‐male competition. On the other hand, care provisioning such as incubating the eggs and raising young may also be costly, thus parental care theory predicts higher mortality for the care‐giving sex, which is often the female. We tested both hypotheses of reproductive costs using phylogenetic comparative analyses of sex‐specific adult mortality rates of 194 bird species across 41 families. First, we show that evolutionary increases in male‐male competition were associated with male‐biased mortalities. This relationship is consistent between two measures of mating competition: social mating system and testis size. Second, as predicted by the parental cost hypothesis, females have significantly higher adult mortalities (mean ± SE, 0.364 ± 0.01) than males (0.328 ± 0.01). However, the mortality cost of parental care was only detectable in males, when the influence of mating competition was statistically controlled. Taken together, our results challenge the traditional explanation of female‐biased avian mortalities, because evolutionary changes in female care were unrelated to changes in mortality bias. The interspecific variation in avian mortality bias, as we show here, is driven by males, specifically via the costs of both mating competition and parental care. We also discuss alternative hypotheses for why most birds exhibit female‐biased mortalities, whereas in mammals male‐biased mortalities predominate.     

Geographic variation in avian incubation periods and parental influences on embryonic temperature

Theory predicts shorter embryonic periods in species with greater embryo mortality risk and smaller body size. Field studies of 80 passerine species on three continents yielded data that largely conflicted with theory; incubation (embryonic) periods were longer rather than shorter in smaller species, and egg (embryo) mortality risk explained some variation within regions, but did not explain larger differences in incubation periods among geographic regions. Incubation behavior of parents seems to explain these discrepancies. Bird embryos are effectively ectothermic and depend on warmth provided by parents sitting on the eggs to attain proper temperatures for development. Parents of smaller species, plus tropical and southern hemisphere species, commonly exhibited lower nest attentiveness (percent of time spent on the nest incubating) than larger and northern hemisphere species. Lower nest attentiveness produced cooler minimum and average embryonic temperatures that were correlated with longer incubation periods independent of nest predation risk or body size. We experimentally tested this correlation by swapping eggs of species with cool incubation temperatures with eggs of species with warm incubation temperatures and similar egg mass. Incubation periods changed (shortened or lengthened) as expected and verified the importance of egg temperature on development rate. Slower development resulting from cooler temperatures may simply be a cost imposed on embryos by parents and may not enhance offspring quality. At the same time, incubation periods of transferred eggs did not match host species and reflect intrinsic differences among species that may result from nest predation and other selection pressures. Thus, geographic variation in embryonic development may reflect more complex interactions than previously recognized.     

Strategies of mass change in breeding birds

Birds experience strikingly different patterns of mass change during breeding. In some species with uniparental incubation, the incubating parents (mostly females) lose mass and attain their lowest point when the chicks hatch (Incubatory mass loss strategy = IML). In species with shared incubation, or with intense incubation feeding, the incubating parents maintain or increase in body mass without reducing attentiveness levels (Incubatory mass constancy = IMC). In other species, uniparental incubation with IMC is associated with reduced levels of attentiveness. The mobilization of fat stores or its preservation are involved in the two strategies. IML leads to mass increases after hatching of the young, while the opposite is true for IMC. The non-incubating sex in uniparental species does not experience significant mass changes during breeding. Fasting endurance, predation risk and mode of development are proposed as the main selective factors determining strategy. Latitude, climate, diet and food availability interact with the main factors. From a revision of the literature we can deduce that IML is mainly found among large birds with precocial development, while IMC is typical of smaller species with altricial development. Proportional mass losses are positively correlated with body mass in IML-species, as well as in precocial species, where body mass explains more than 70% of the variation in proportional mass change. Incubation periods increase with body mass in uniparental IMC-species, but not in IML-species. IML is thus associated to fast embryonic growth in large species. Successful raising of highly-dependent young in altricial and semialtricial species apparently depends on one of the parents retaining reserves until hatching. Subsequent mass losses may be necessary to maintain the brooding parent through a period when nestlings require heat, insulation and food. Patterns of mass change are not mere consequences of reproductive stress but the outcome of adaptive compromises between different selective factors and constitute an important aspect of the breeding biology and life history of birds.