Dorsal and Ventral Plumage Coloration Evolve as Distinct Modules with Different Environmental Correlations.

AbstractMany animals exhibit contrast between their dorsal coloration and their ventral coloration. If selection acts differently on dorsal versus ventral coloration, ancestral covariance between these traits should break down, eventually leading to independent modules of trait evolution. Here, we compare the evolution of feather color across body regions for a clade of Australasian songbirds (Meliphagoidea). We find evidence for three modules of covarying color regions. Among these modules, ventral feathers evolve with high lability, evolving at three times the rate of dorsal plumage and 20 times the rate of flight feathers. While both dorsal plumage and ventral plumage are darker in areas with more precipitation and vegetation, we find that dorsal plumage is twice as similar to colors in satellite photos of background substrates. Overall, differential selection on ventral and dorsal colors likely maintains these as distinct modules over evolutionary timescales-a novel explanation for dorsoventral contrast in pigmentation.

The Evolution of Local Co-occurrence in Birds in Relation to Latitude, Degree of Sympatry, and Range Symmetry.

AbstractRecent speciation rates and the degree of range-wide sympatry are usually higher farther from the equator. Is there also a higher degree of secondary syntopy (coexistence in local assemblages in sympatry) at higher latitudes and, subsequently, an increase in local species richness? We studied the evolution of syntopy in passerine birds using worldwide species distribution data. We chose recently diverged species pairs from subclades not older than 5 or 7 million years, range-wide degree of sympatry not lower than 5% or 25%, and three definitions of the breeding season. We related their syntopy to latitude, the degree of sympatry (breeding range overlap), range symmetry, and the age of split. Syntopy was positively related to latitude, but it did not differ between tropical and temperate regions, instead increasing from the Southern to the Northern Hemisphere. Syntopy was also higher in species pairs with a higher degree of sympatry and more symmetric ranges, but it did not predict local species richness. Following speciation, species in the Northern Hemisphere presumably achieve positive local co-occurrence faster than elsewhere, which could facilitate their higher speciation rates. However, this does not seem to be linked to local species richness, which is probably governed by other processes.

A late burst of colour evolution in a radiation of songbirds (Passeriformes: Parulidae) suggests secondary contact drives signal divergence.

Evolutionary radiations provide important insights into species diversification, which is especially true of adaptive radiations. New World wood warblers (Parulidae) are a family of small, insectivorous, forest-dwelling passerine birds, often considered an exemplar of adaptive radiation due to their rapid diversification followed by a slowdown. However, they deviate from the expectations of an adaptive radiation scenario due to the lack of conspicuous morphological and ecological differentiation. We fitted several macroevolutionary models to trait data in 105 species of wood warblers. We tested whether morphological traits underwent an early burst of evolution (suggesting adaptation to new ecological niches in adaptive radiations) and whether song and colour underwent a diversity-dependent acceleration of trait evolutionary rate (consistent with reproductive interference driving signal evolution). Morphology and song evolved gradually under stabilizing selection, suggesting niche conservatism, with morphology possibly acting as a constraint on song evolution. In contrast, many feather colour traits underwent a diversity-dependent burst of evolution occurring late in the clade's history. We suggest that a two-step process has led to the remarkable diversification of wood warblers. First, their early diversification probably proceeded by allopatric speciation. Second, feather colour divergence likely occurred during secondary contact after range expansion. This diversification of signalling traits might have facilitated species coexistence, in combination with behavioural niche partitioning. Wood warblers seem to present characteristics of both adaptive and non-adaptive radiations.

AVONET: morphological, ecological and geographical data for all birds.

Functional traits offer a rich quantitative framework for developing and testing theories in evolutionary biology, ecology and ecosystem science. However, the potential of functional traits to drive theoretical advances and refine models of global change can only be fully realised when species-level information is complete. Here we present the AVONET dataset containing comprehensive functional trait data for all birds, including six ecological variables, 11 continuous morphological traits, and information on range size and location. Raw morphological measurements are presented from 90,020 individuals of 11,009 extant bird species sampled from 181 countries. These data are also summarised as species averages in three taxonomic formats, allowing integration with a global phylogeny, geographical range maps, IUCN Red List data and the eBird citizen science database. The AVONET dataset provides the most detailed picture of continuous trait variation for any major radiation of organisms, offering a global template for testing hypotheses and exploring the evolutionary origins, structure and functioning of biodiversity.

Functional diversity of avian communities increases with canopy height: From individual behavior to continental-scale patterns.

Vegetation complexity is an important predictor of animal species diversity. Specifically, taller vegetation should provide more potential ecological niches and thus harbor communities with higher species richness and functional diversity (FD). Resource use behavior is an especially important functional trait because it links species to their resource base with direct relevance to niche partitioning. However, it is unclear how exactly the diversity of resource use behavior changes with vegetation complexity. To address this question, we studied avian FD in relation to vegetation complexity along a continental-scale vegetation gradient. We quantified foraging behavior of passerine birds in terms of foraging method and substrate use at 21 sites (63 transects) spanning 3,000 km of woodlands and forests in Australia. We also quantified vegetation structure on 630 sampling points at the same sites. Additionally, we measured morphological traits for all 111 observed species in museum collections. We calculated individual-based, abundance-weighted FD in morphology and foraging behavior and related it to species richness and vegetation complexity (indexed by canopy height) using structural equation modeling, rarefaction analyses, and distance-based metrics. FD of morphology and foraging methods was best predicted by species richness. However, FD of substrate use was best predicted by canopy height (ranging 10-30 m), but only when substrates were categorized with fine resolution (17 categories), not when categorized coarsely (8 categories). These results suggest that, first, FD might increase with vegetation complexity independently of species richness, but whether it does so depends on the studied functional trait. Second, patterns found might be shaped by how finely we categorize functional traits. More complex vegetation provided larger "ecological space" with more resources, allowing the coexistence of more species with disproportionately more diverse foraging substrate use. We suggest that the latter pattern was driven by nonrandom accumulation of functionally distinct species with increasing canopy height.

Adaptation and constraint shape the evolution of growth patterns in passerine birds across the globe.

BACKGROUND: Growth trajectories should be adapted to selective factors of each species' environment. However, major shaping forces of growth and development are unclear, especially when studying several traits at once. Birds provide an ideal opportunity to analyze growth patterns across species due to there being enough available data. We tested the relative importance of nest predation risk, the number of care-givers, nest height, foraging substrate, clutch size, and latitude on growth patterns of passerine birds (Passeriformes) using phylogenetic comparative methods. Specifically, we studied the evolution of fledging time, average and peak growth rates, and relative development at fledging of body mass and tarsus, wing, and tail length. RESULTS: Using a comprehensive literature search and data quality control, we obtained data on growth in 231 species based on 295 populations. Species with long development in the nest grew slowly and had well-developed traits at fledging. Species breeding under high nest predation risk, building their nests close to the ground, and those living in northern temperate regions fledged early and grew fast, sometimes fledging with less developed body mass and traits critical for locomotion (tarsus, wing, and tail). On the other hand, the number of caring adults, clutch size, and species' foraging substrate had very limited predictive value for growth patterns across passerine species. CONCLUSIONS: Shortening of the nestling period was a primary means of accelerating development (in relation to nest predation, nest height, and latitude), sometimes supplemented by higher peak growth rates of body mass, tarsus, and wing (especially in relation to latitude). Overall growth patterns of passerines were adaptively tuned to nest predation risk and nest height, with northern temperate species having especially short nestling periods and fast growth rates of body mass, tarsus, and wing.

Evolution of a multifunctional trait: shared effects of foraging ecology and thermoregulation on beak morphology, with consequences for song evolution.

While morphological traits are often associated with multiple functions, it remains unclear how evolution balances the selective effects of different functions. Birds' beaks function not only in foraging but also in thermoregulating and singing, among other behaviours. Studies of beak evolution abound, however, most focus on a single function. Hence, we quantified relative contributions of different functions over an evolutionary timescale. We measured beak shape using geometric morphometrics and compared this trait with foraging behaviour, climatic variables and song characteristics in a phylogenetic comparative study of an Australasian radiation of songbirds (Meliphagidae). We found that both climate and foraging behaviour were significantly correlated with the beak shape and size. However, foraging ecology had a greater effect on shape, and climate had a nearly equal effect on size. We also found that evolutionary changes in beak morphology had significant consequences for vocal performance: species with elongate-shaped beaks sang at higher frequencies, while species with large beaks sang at a slower pace. The evolution of the avian beak exemplifies how morphological traits can be an evolutionary compromise among functions, and suggests that specialization along any functional axis may increase ecological divergence or reproductive isolation along others.

Specialization and niche overlap across spatial scales: Revealing ecological factors shaping species richness and coexistence in Australian songbirds.

Ecological specialization enables the partitioning of resources and thus can facilitate the coexistence of species and promote higher species richness. Specialization and niche partitioning are expected to exert a decisive influence on local spatial scales, while species richness at regional scales should be shaped mostly by historical factors and abiotic conditions. Moreover, specialization is expected to be particularly important in communities that are exceptionally species rich for their environmental conditions. Concurrently, niche overlap in these communities should be minimized to enable species coexistence. We tested these hypotheses by studying specialization-richness relationship and niche overlap in assemblages of 298 species of songbirds (Passeriformes) across Australia. We used local (2-6 ha) to regional (bioregions) spatial scales and detailed data on habitat, diet and foraging behaviour (method, substrate and stratum). We expected the richness-specialization relationship to be particularly strong (a) on local spatial scales and (b) in communities exceptionally species rich for given environmental conditions (approximated by moisture and vegetation complexity). We also expected (c) low niche overlap in assemblages with specialized species. Only the third prediction was partly supported. First, while the specialization and species richness were often positively related, the strength and the direction of the relationship changed between traits and across spatial scales. The strength of the specialization-richness relationship was consistently positive only in foraging stratum, and it increased towards smaller spatial scales only in case of habitat and diet. Simultaneously, species in local communities demonstrated high overlap in habitat and diet. Second, we did not find particularly strong specialization-richness relationships in exceptionally species-rich communities. Third, we found the expected negative relationship between specialization and overlap in foraging stratum and substrate (in local communities), suggesting that species partition ecological space locally in terms of where they find food. Our expectations were only weakly supported. Specialization on foraging stratum was probably important in facilitating species coexistence. Conversely, although species were often specialized on habitat and diet, high overlap in these traits did not preclude their local coexistence. Overall, specialization and overlap in foraging traits were more important for species coexistence than habitat or diet.

A Morphological Integration Perspective on the Evolution of Dimorphism among Sexes and Social Insect Castes.

Many species have evolved alternate phenotypes, thus enabling individuals to conditionally produce phenotypes that are favorable for reproductive success. Examples of this phenomenon include sexual dimorphism, alternative reproductive strategies, and social insect castes. While the evolutionary functions and developmental mechanisms of dimorphic phenotypes have been studied extensively, little attention has focused on the evolutionary covariance between each phenotype. We extend the conceptual framework and methods of morphological integration to hypothesize that dimorphic traits tend to be less integrated between sexes or social castes. In the case of social insects, we describe results from our recent study of an ant genus in which workers have major and minor worker castes that perform different behavioral repertoires in and around the nest. In the case of birds, we describe a new analysis of a family of songbirds that exhibits plumage coloration that can differ greatly between males and females, with apparently independent changes in each sex. Ant head shape, which is highly specialized in each worker caste, was weakly integrated between worker castes, whereas thorax shape, which is more monomorphic, was tightly integrated. Similarly, in birds, we found a negative association between dimorphism and the degree of integration between sexes. We also found that integration decreased in fairy wrens (Malurus) for many feather patches that evolved greater dichromatism. Together, this suggests that the process of evolving increased dimorphism results in a decrease in integration between sexes and social castes. We speculate that once a mechanism for dimorphism evolves, that mechanism can create independent variation in one sex or caste upon which selection may act.

Disentangling direct and indirect effects of water availability, vegetation, and topography on avian diversity.

Climate is a major driver of species diversity. However, its effect can be either direct due to species physiological tolerances or indirect, whereby wetter climates facilitate more complex vegetation and consequently higher diversity due to greater resource availability. Yet, studies quantifying both direct and indirect effects of climate on multiple dimensions of diversity are rare. We used extensive data on species distributions, morphological and ecological traits, and vegetation across Australia to quantify both direct (water availability) and indirect (habitat diversity and canopy height) effects of climate on the species richness (SR), phylogenetic diversity (PD), and functional diversity (FD) of 536 species of birds. Path analyses revealed that SR increased with wetter climates through both direct and indirect effects, lending support for the influence of both physiological tolerance and vegetation complexity. However, residual PD and residual FD (adjusted for SR by null models) were poorly predicted by environmental conditions. Thus, the FD and PD of Australian birds mostly evolved in concert with SR, with the possible exception of the higher-than-expected accumulation of avian lineages in wetter and more productive areas in northern and eastern Australia (with high residual PD), permitted probably by older biome age.

Evolution of parental activity at the nest is shaped by the risk of nest predation and ambient temperature across bird species.

Incubation is an important component of parental care in birds, and species differ widely in their incubation rhythm. In this comparative study, we focused on factors responsible for those differences. As hypothesized by A. Skutch, increased parental activity at the nest increases the probability of nest depredation. High risk of nest predation should therefore lead to the evolution of lower frequency of parental activity at the nest. We thus expected to find a negative relationship between frequency of nest visits and the risk of nest depredation. Using a large dataset of 256 species of passerines breeding worldwide, we found that the frequency of nest visits decreased as the risk of nest depredation increased and that this effect was strongest in tropical species. Further, foraging bouts were longer in species experiencing warmer ambient temperatures during incubation and those with domed nests. Incubation bouts were longer and frequency of nest visits was lower in species with higher body mass. Our results support the view that natural selection favors lower frequency of nests visits in species under higher risk of nest predation and demonstrate the importance of other factors (temperature, geographic space, nest type, and body mass) in shaping the evolution of incubation rhythm.

Effects of interspecific coexistence on laying date and clutch size in two closely related species of hole-nesting birds.

Coexistence between great tits Parus major and blue tits Cyanistes caeruleus, but also other hole-nesting taxa, constitutes a classic example of species co-occurrence resulting in potential interference and exploitation competition for food and for breeding and roosting sites. However, the spatial and temporal variations in coexistence and its consequences for competition remain poorly understood. We used an extensive database on reproduction in nest boxes by great and blue tits based on 87 study plots across Europe and Northern Africa during 1957-2012 for a total of 19,075 great tit and 16,729 blue tit clutches to assess correlative evidence for a relationship between laying date and clutch size, respectively, and density consistent with effects of intraspecific and interspecific competition. In an initial set of analyses, we statistically controlled for a suite of site-specific variables. We found evidence for an effect of intraspecific competition on blue tit laying date (later laying at higher density) and clutch size (smaller clutch size at higher density), but no evidence of significant effects of intraspecific competition in great tits, nor effects of interspecific competition for either species. To further control for site-specific variation caused by a range of potentially confounding variables, we compared means and variances in laying date and clutch size of great and blue tits among three categories of difference in density between the two species. We exploited the fact that means and variances are generally positively correlated. If interspecific competition occurs, we predicted a reduction in mean and an increase in variance in clutch size in great tit and blue tit when density of heterospecifics is higher than the density of conspecifics, and for intraspecific competition, this reduction would occur when density of conspecifics is higher than the density of heterospecifics. Such comparisons of temporal patterns of means and variances revealed evidence, for both species, consistent with intraspecific competition and to a smaller extent with interspecific competition. These findings suggest that competition associated with reproductive behaviour between blue and great tits is widespread, but also varies across large spatial and temporal scales.

Smaller beaks for colder winters: Thermoregulation drives beak size evolution in Australasian songbirds.

Birds' beaks play a key role in foraging, and most research on their size and shape has focused on this function. Recent findings suggest that beaks may also be important for thermoregulation, and this may drive morphological evolution as predicted by Allen's rule. However, the role of thermoregulation in the evolution of beak size across species remains largely unexplored. In particular, it remains unclear whether the need for retaining heat in the winter or dissipating heat in the summer plays the greater role in selection for beak size. Comparative studies are needed to evaluate the relative importance of these functions in beak size evolution. We addressed this question in a clade of birds exhibiting wide variation in their climatic niche: the Australasian honeyeaters and allies (Meliphagoidea). Across 158 species, we compared species' climatic conditions extracted from their ranges to beak size measurements in a combined spatial-phylogenetic framework. We found that winter minimum temperature was positively correlated with beak size, while summer maximum temperature was not. This suggests that while diet and foraging behavior may drive evolutionary changes in beak shape, changes in beak size can also be explained by the beak's role in thermoregulation, and winter heat retention in particular.

Sex differences in parental care: Gametic investment, sexual selection, and social environment.

Male and female parents often provide different type and amount of care to their offspring. Three major drivers have been proposed to explain parental sex roles: (1) differential gametic investment by males and females that precipitates into sex difference in care, (2) different intensity of sexual selection acting on males and females, and (3) biased social environment that facilitates the more common sex to provide more care. Here, we provide the most comprehensive assessment of these hypotheses using detailed parental care data from 792 bird species covering 126 families. We found no evidence for the gametic investment hypothesis: neither gamete sizes nor gamete production by males relative to females was related to sex difference in parental care. However, sexual selection correlated with parental sex roles, because the male share in care relative to female decreased with both extra-pair paternity and frequency of male polygamy. Parental sex roles were also related to social environment, because male parental care increased with male-biased adult sex ratios (ASRs). Taken together, our results are consistent with recent theories suggesting that gametic investment is not tied to parental sex roles, and highlight the importance of both sexual selection and ASR in influencing parental sex roles.

The evolution of parental cooperation in birds.

Parental care is one of the most variable social behaviors and it is an excellent model system to understand cooperation between unrelated individuals. Three major hypotheses have been proposed to explain the extent of parental cooperation: sexual selection, social environment, and environmental harshness. Using the most comprehensive dataset on parental care that includes 659 bird species from 113 families covering both uniparental and biparental taxa, we show that the degree of parental cooperation is associated with both sexual selection and social environment. Consistent with recent theoretical models parental cooperation decreases with the intensity of sexual selection and with skewed adult sex ratios. These effects are additive and robust to the influence of life-history variables. However, parental cooperation is unrelated to environmental factors (measured at the scale of whole species ranges) as indicated by a lack of consistent relationship with ambient temperature, rainfall or their fluctuations within and between years. These results highlight the significance of social effects for parental cooperation and suggest that several parental strategies may coexist in a given set of ambient environment.

The importance of having a partner: male help releases females from time limitation during incubation in birds.

INTRODUCTION: Male contribution to parental care varies widely among avian species. Yet the reasons for this variation, as well as its consequences, are still unclear. Because the amount of care provided by one sex is ultimately constrained by the time available for energy acquisition, contribution by the other sex should increase when overall parental workload is high. We tested this prediction by analyzing male contribution to incubation in 528 populations of 320 species of passerines, where females usually devote more time to incubation than males. Our worldwide sample included species with female-only parental care (the male is not present), incubation feeding (the male feeds the incubating female), and shared incubation (both sexes incubate the eggs). RESULTS: Overall nest attentiveness was greatest in species with shared incubation followed by species with incubation feeding and lowest in species with female-only care. Nest attentiveness and the degree of male contribution to incubation in species with shared incubation were very strongly correlated, whereas this correlation was absent in females. Interestingly, female contribution decreased towards the equator while male contribution did not change significantly with latitude. Hence, relative male incubation effort increased towards the equator, whereas that of female decreased. In species with incubation feeding, female nest attentiveness increased with the frequency of male feeding. CONCLUSIONS: These findings support the hypothesis that male help is indispensable for increasing nest attentiveness in birds, either in the form of incubation feeding (supply of energy) or direct incubation of eggs. We conclude that energy acquisition constraints might be a potent force driving sex-specific contribution to parental care.

More ornamented females produce higher-quality offspring in a socially monogamous bird: an experimental study in the great tit (Parus major).

INTRODUCTION: Animals are often conspicuously colored and explanations range from aposematism and mimicry to sexual selection. Although sexual selection explains vivid coloration in males, functional significance of vivid coloration in females of socially monogamous species remains unclear. The hypothesis of mutual mate choice predicts that more ornamented females produce offspring of higher quality. We tested this prediction in the great tit (Parus major), a small, insectivorous, socially monogamous passerine. RESULTS: In both females and males we quantified three ornaments that have been hypothesized to have signaling role in this species (size of black breast stripe, carotenoid chroma of yellow breast feathers, immaculateness of the white cheek). We swapped broods between nests soon after hatching, thus separating genetic plus pre-hatching vs. post-hatching effects on offspring performance. Body mass of offspring at 14 days of age was positively related to the area of black breast stripe of genetic mothers. Immune response to a novel antigen (phytohaemagglutinin) at 14 days of age was positively related to the immaculateness of the white cheek patch of both genetic and foster mothers. CONCLUSIONS: We showed that females with more elaborate ornaments produced higher-quality offspring and we discuss potential proximate mechanisms of these relationships. We conclude that as more elaborate ornaments were reliable signals of offspring quality, direct selection by male mate choice might have been responsible for the evolution and/or maintenance of these signaling traits in females.

Environmental and genetic effects on pigment-based vs. structural component of yellow feather colouration.

BACKGROUND: Carotenoid plumage is of widespread use in bird communication. Carotenoid-based feather colouration has recently been shown to be dependent on both pigment concentration and feather structure. If these two components are determined differently, one plumage patch may potentially convey different aspects of individual quality. METHODOLOGY/PRINCIPAL FINDINGS: We evaluated the effects of genetic and environmental factors on carotenoid-based yellow breast colouration of Great Tit (Parus major) nestlings. By partial cross-fostering, we separated the genetic and pre-natal vs. post-natal parental effects on both the structural and the pigment-based component of carotenoid-based plumage colouration. We also simultaneously manipulated the post-hatching environment by brood size manipulation. The structural component of nestling colouration reflected features of female colouration. On the other hand, the pigment-based component was more affected by rearing conditions presumably representing food quality. While the structural component was related to both origin- and environment-related factors, the pigment-based component seemed to be environment-dependent only. These results support the notion that pigment-based and structural components of feather colouration are determined differently. CONCLUSIONS/SIGNIFICANCE: Chromatic and achromatic components of carotenoid-based feather colouration reflected different aspects of individual quality and history, and thus may potentially form a multicomponent signal.

Explaining postnatal growth plasticity in a generalist brood parasite.

Selection of a particular host has clear consequences for the performance of avian brood parasites. Experimental studies showed that growth rate and fledging mass of brood parasites varied between host species independently of the original host species. Finding correlates of this phenotypic plasticity in growth is important for assessing adaptiveness and potential fitness consequences of host choice. Here, I analyzed the effects of several host characteristics on growth rate and fledging mass of the young of brown-headed cowbird (Molothrus ater), a generalist, non-evicting brood parasite. Cowbird chicks grew better in fast-developing host species and reached higher fledging mass in large hosts with fast postnatal development. A potential proximate mechanism linking fast growth and high fledging mass of cowbird with fast host development is superior food supply in fast-developing foster species. So far, we know very little about the consequences of the great plasticity in cowbird growth for later performance of the adult parasite. Thus, cowbird species could become interesting model systems for investigating the role of plasticity and optimization in the evolution of growth rate in birds.

Growth strategies of passerine birds are related to brood parasitism by the brown-headed cowbird (Molothrus ater).

Sibling competition was proposed as an important selective agent in the evolution of growth and development. Brood parasitism by the brown-headed cowbird (Molothrus ater) intensifies sibling competition in the nests of its hosts by increasing host chick mortality and exposing them to a genetically unrelated nestmate. Intranest sibling competition for resources supplied by parents is size dependent. Thus, it should select for high development rates and short nestling periods, which would alleviate negative impacts of brood parasitic chicks on host young. I tested these predictions on 134 North American passerines by comparative analyses. After controlling for covariates and phylogeny, I showed that high parasitism rate was associated with higher nestling growth rate, lower mass at fledging, and shorter nestling periods. These effects were most pronounced in species in which sibling competition is most intense (i.e., weighing over about 30 g). When species were categorized as nonhosts versus old hosts (parasitized for thousands of years) versus new hosts (parasitized the last 100-200 years), there was a clear effect of this parasitism category on growth strategies. Nestling growth rate was the most evolutionarily flexible trait, followed by mass at fledging and nestling period duration. Adjustments during incubation (incubation period length, egg volume) were less pronounced and generally disappeared after controlling for phylogeny. I show that sibling competition caused by brood parasites can have strong effects on the evolution of host growth strategies and that the evolution of developmental traits can take place very rapidly. Human alteration of habitats causing spread of brood parasites to new areas thus cascades into affecting the evolution of life-history traits in host species.