Feather function and the evolution of birds

The ability of feathers to perform many functions either simultaneously or at different times throughout the year or life of a bird is integral to the evolutionary history of birds. Many studies focus on single functions of feathers, but any given feather performs many functions over its lifetime. These functions necessarily interact with each other throughout the evolution and development of birds, so our knowledge of avian evolution is incomplete without understanding the multifunctionality of feathers, and how different functions may act synergistically or antagonistically during natural selection. Here, we review how feather functions interact with avian evolution, with a focus on recent technological and discovery-based advances. By synthesising research into feather functions over hierarchical scales (pattern, arrangement, macrostructure, microstructure, nanostructure, molecules), we aim to provide a broad context for how the adaptability and multifunctionality of feathers have allowed birds to diversify into an astounding array of environments and life-history strategies. We suggest that future research into avian evolution involving feather function should consider multiple aspects of a feather, including multiple functions, seasonal wear and renewal, and ecological or mechanical interactions. With this more holistic view, processes such as the evolution of avian coloration and flight can be understood in a broader and more nuanced context.     

Defining structural homology between the mammalian and avian hippocampus through conserved gene expression patterns observed in the chick embryo

The mammalian hippocampus, a center of neurogenesis in the adult brain, is involved in critical functions such as learning and memory processing. Although there is an overall functional conservation between birds and mammals in the hippocampal region of the brain, there are several morphological differences. A few different models have been proposed for identifying regional and structural homology between the avian and mammalian hippocampus however a consensus is yet to be reached. In this study we have systematically and comprehensively characterized the developing chicken hippocampus at the molecular level. We have identified the time window of neurogenesis and apoptosis during hippocampal development as well as the likely origin and migration path of neurons of the ventral v-shaped region of chick hippocampus. In addition to this we have identified several genes with expression patterns that are conserved between the hippocampus of chicken and mice. Our study provides molecular data that partially supports one of the models reported in literature for structural homology between the avian and mammalian hippocampus. Functional characterization of the genes found in this study to be specifically expressed in the developing chicken hippocampus is likely to provide valuable information on the mechanisms regulating hippocampus development of birds and perhaps could be extrapolated to mammalian hippocampus development as well.     

北京市平原区受胁鸟类栖息地识别和评价

在北京分布的受胁鸟类主要分布在平原区,而平原区为城市发展的主要区域,因此,在城市管理中融入受胁鸟类保护的内容十分必要。以北京市平原区分布的24种受胁鸟类为研究对象,以鸟类对栖息地的需求为分类依据,结合国家土地利用分类标准,采用人工目视解译法,在北京市平原区的高清卫星影像图上识别出5类一级鸟类栖息地和17类二级鸟类栖息地,得到北京市平原区鸟类栖息地分布图。使用24种受胁鸟类的空间分布模型掩膜鸟类栖息地分布,得到24种受胁鸟类的预测空间分布,叠加之后获得受胁鸟类丰富度分布格局,结果显示,水域是受胁鸟类丰富度最高的栖息地。将受胁鸟类丰富度分布格局与北京市国家级和市级自然保护区分布叠加进行空缺分析,结果显示：1）北京市的自然保护区多分布在山区,不能有效保护受胁鸟类;2）受胁鸟类的保护与平原区的城市建设、绿地管理关系密切。采用分区统计方法,计算各类栖息地中分布的平均鸟类种类数,作为栖息地保护行动优先级指标,得出湖泊、水库、坑塘、滩地、沼泽地等湿地区域是具有最高保护优先级的栖息地类型,在保护实践资源充足的情况下,应对各类栖息地开展综合保护。该研究首次为北京城市区域受胁鸟类保护提出空间参考和管理建议。     

Temporal Limitations on Social Learning of Novel Predators by Indian Mynahs, Acridotheres tristis

Antipredator vocalizations of social companions are important for facilitating long-term changes in the responses of prey to novel predator stimuli. However, dynamic variation in the time course of acoustic communication has important implications for learning of predator cues associated with auditory signals. While animals often experience acoustic signals simultaneously with predator cues, they may also at times experience signals and predator stimuli in succession. The ability to learn about stimuli that are perceived not only together, but also after, acoustic signals has the potential to expand the range of opportunities for learning about novel events. Earlier work in Indian mynahs ( Acridotheres tristis ) has revealed that subjects acquire a visual exploratory response to a novel avian mount after they have experienced it together with conspecific distress vocalizations, a call produced in response to seizure by a predator. The present study explored to what extent such learning occurred if the avian mount was experienced after, rather than simultaneously with, distress calls, such as might happen if call production is interrupted by prey death. Results showed that mynahs that experienced a novel avian mount simultaneously with the sound of distress calls exhibited a sustained exploratory response to the mount after training relative to before that was not apparent in birds that received distress calls and mount in succession. This finding suggests that vocal antipredator signals may only trigger learning of environmental stimuli with which they share some temporal overlap. Recipients may need to access complementary non-vocal cues from the prey victim to learn about predator stimuli that are perceived after vocal behaviour.     

Hippocampal memory consolidation during sleep: a comparison of mammals and birds

The transition from wakefulness to sleep is marked by pronounced changes in brain activity. The brain rhythms that characterize the two main types of mammalian sleep, slow‐wave sleep (SWS) and rapid eye movement (REM) sleep, are thought to be involved in the functions of sleep. In particular, recent theories suggest that the synchronous slow‐oscillation of neocortical neuronal membrane potentials, the defining feature of SWS, is involved in processing information acquired during wakefulness. According to the Standard Model of memory consolidation, during wakefulness the hippocampus receives input from neocortical regions involved in the initial encoding of an experience and binds this information into a coherent memory trace that is then transferred to the neocortex during SWS where it is stored and integrated within preexisting memory traces. Evidence suggests that this process selectively involves direct connections from the hippocampus to the prefrontal cortex (PFC), a multimodal, high‐order association region implicated in coordinating the storage and recall of remote memories in the neocortex. The slow‐oscillation is thought to orchestrate the transfer of information from the hippocampus by temporally coupling hippocampal sharp‐wave/ripples (SWRs) and thalamocortical spindles. SWRs are synchronous bursts of hippocampal activity, during which waking neuronal firing patterns are reactivated in the hippocampus and neocortex in a coordinated manner. Thalamocortical spindles are brief 7–14 Hz oscillations that may facilitate the encoding of information reactivated during SWRs. By temporally coupling the readout of information from the hippocampus with conditions conducive to encoding in the neocortex, the slow‐oscillation is thought to mediate the transfer of information from the hippocampus to the neocortex. Although several lines of evidence are consistent with this function for mammalian SWS, it is unclear whether SWS serves a similar function in birds, the only taxonomic group other than mammals to exhibit SWS and REM sleep. Based on our review of research on avian sleep, neuroanatomy, and memory, although involved in some forms of memory consolidation, avian sleep does not appear to be involved in transferring hippocampal memories to other brain regions. Despite exhibiting the slow‐oscillation, SWRs and spindles have not been found in birds. Moreover, although birds independently evolved a brain region—the caudolateral nidopallium (NCL)—involved in performing high‐order cognitive functions similar to those performed by the PFC, direct connections between the NCL and hippocampus have not been found in birds, and evidence for the transfer of information from the hippocampus to the NCL or other extra‐hippocampal regions is lacking. Although based on the absence of evidence for various traits, collectively, these findings suggest that unlike mammalian SWS, avian SWS may not be involved in transferring memories from the hippocampus. Furthermore, it suggests that the slow‐oscillation, the defining feature of mammalian and avian SWS, may serve a more general function independent of that related to coordinating the transfer of information from the hippocampus to the PFC in mammals. Given that SWS is homeostatically regulated (a process intimately related to the slow‐oscillation) in mammals and birds, functional hypotheses linked to this process may apply to both taxonomic groups.     

Spina cortica and Tapetum spinosus, two new microstructures of flight feathers: description, function and distribution in modern birds

The importance of feathers for the avian group has made them one of the most studied epidermal structures both from the morphological and evolutionary point of view. Surprisingly, our observations by Scanning Electron Microscopy detected the presence of two structures widely distributed within different avian groups and not yet described. In this paper we describe these two new structures (Spina cortica and Tapetum spinosus) and map their distribution within modern birds. The S. cortica is a thorn-like microstructure that grows on the barb cortex and the T. spinosus is the assemblage of these thorns. The distribution of these new structures among birds and their morphological diversity could be of great interest to taxonomists and evolutionary biologists interested in the origin of bird flight.     

Orientation and navigation of migrating birds

The question of how migrating birds find their way to winter quarters and back has fascinated humans since the beginning of scientific research into avian biology. Migrating birds have been shown to possess compass systems that allow them to select and maintain certain compass directions. Three such systems are known, solar, stellar and magnetic. Their details are not quite clear and need further research. Hierarchy and interaction of compass systems of migrating birds are poorly studied; different species may vary in this respect. During migration, birds learn to use maps that make true navigation possible, i.e. to detect their position relatively to the goal of movement. The physical nature of navigational maps is an object of intensive research; currently the most promising concepts are the geomagnetic and possibly olfactory maps. A significant contribution to the study of formation of navigational maps was made by Soviet/Russian researchers, whose work was published in Zoologicheskii Zhurnal (Sokolov et al., 1984). Migrating birds have no innate map, and first-autumn individuals reach their species-specific wintering areas by using compass sense and counting time that should be spent moving in certain genetically fixed directions. However, in recent years more and more data surface that suggest that juveniles (maybe not of all species) do have some mechanism of controlling their position on the migratory route that allows them to compensate for errors of the spatio-temporal programme of migration.     

Light matters: testing the “Light Environment Hypothesis” under intra‐ and interspecific contexts

The “Light Environment Hypothesis” (LEH) proposes that evolution of interspecific variation in plumage color is driven by variation in light environments across habitats. If ambient light has the potential to drive interspecific variation, a similar influence should be expected for intraspecific recognition, as color signals are an adaptive response to the change in ambient light levels in different habitats. Using spectrometry, avian‐appropriate models of vision, and phylogenetic comparative methods, I quantified dichromatism and tested the LEH in both intra‐ and interspecific contexts in 33 Amazonian species from the infraorder Furnariides living in environments with different light levels. Although these birds are sexually monochromatic to humans, 81.8% of the species had at least one dichromatic patch in their plumage, mostly from dorsal areas, which provides evidence for a role for dichromatism in sex recognition. Furthermore, birds from habitats with high levels of ambient light had higher dichromatism levels, as well as brighter, more saturated, and more diverse plumages, suggesting that visual communication is less constrained in these habitats. Overall, my results provide support for the LEH and suggest that ambient light plays a major role in the evolution of color signals in this group of birds in both intra‐ and interspecific contexts. Additionally, plumage variation across light environments for these drab birds highlights the importance of considering ambient light and avian‐appropriate models of vision when studying the evolution of color signals in birds.     

Altered auditory BOLD response to conspecific birdsong in zebra finches with stuttered syllables

How well a songbird learns a song appears to depend on the formation of a robust auditory template of its tutor's song. Using functional magnetic resonance neuroimaging we examine auditory responses in two groups of zebra finches that differ in the type of song they sing after being tutored by birds producing stuttering-like syllable repetitions in their songs. We find that birds that learn to produce the stuttered syntax show attenuated blood oxygenation level-dependent (BOLD) responses to tutor's song, and more pronounced responses to conspecific song primarily in the auditory area field L of the avian forebrain, when compared to birds that produce normal song. These findings are consistent with the presence of a sensory song template critical for song learning in auditory areas of the zebra finch forebrain. In addition, they suggest a relationship between an altered response related to familiarity and/or saliency of song stimuli and the production of variant songs with stuttered syllables.     

Frequency-dependent taste-rejection by avian predation may select for defence chemical polymorphisms in aposematic prey

Chemically defended insects advertise their unpalatability to avian predators using conspicuous aposematic coloration that predators learn to avoid. Insects utilize a wide variety of different compounds in their defences, and intraspecific variation in defence chemistry is common. We propose that polymorphisms in insect defence chemicals may be beneficial to insects by increasing survival from avian predators. Birds learn to avoid a colour signal faster when individual prey possesses one of two unpalatable chemicals rather than all prey having the same defence chemical. However, for chemical polymorphisms to evolve within a species, there must be benefits that allow rare chemical morphs to increase in frequency. Using domestic chicks as predators and coloured crumbs for prey, we provide evidence that birds taste and reject proportionally more of the individuals with rare defence chemicals than those with common defence chemicals. This indicates that the way in which birds attack and reject prey could enhance the survival of rare chemical morphs and select for chemical polymorphism in aposematic species. This is the first experiment to demonstrate that predators can directly influence the form taken by prey's chemical defences.     

Molecular evolutionary genomics of birds

Insight into the molecular evolution of birds has been offered by the steady accumulation of avian DNA sequence data, recently culminating in the first draft sequence of an avian genome, that of chicken. By studying avian molecular evolution we can learn about adaptations and phenotypic evolution in birds, and also gain an understanding of the similarities and differences between mammalian and avian genomes. In both these lineages, there is pronounced isochore structure with highly variable GC content. However, while mammalian isochores are decaying, they are maintained in the chicken lineage, which is consistent with a biased gene conversion model where the high and variable recombination rate of birds reinforces heterogeneity in GC. In Galliformes, GC is positively correlated with the rate of nucleotide substitution; the mean neutral mutation rate is 0.12-0.15% at each site per million years but this estimate comes with significant local variation in the rate of mutation. Comparative genomics reveals lower d(N)/d(S) ratios on micro- compared to macrochromosomes, possibly due to population genetic effects or a non-random distribution of genes with respect to chromosome size. A non-random genomic distribution is shown by genes with sex-biased expression, with male-biased genes over-represented and female-biased genes under-represented on the Z chromosome. A strong effect of selection is evident on the non-recombining W chromosome with high d(N)/d(S) ratios and limited polymorphism. Nucleotide diversity in chicken is estimated at 4-5 x 10(-3) which might be seen as surprisingly high given presumed bottlenecks during domestication, but is lower than that recently observed in several natural populations of other species. Several important aspects of the molecular evolutionary process of birds remain to be understood and it can be anticipated that the upcoming genome sequence of a second bird species, the zebra finch, as well as the integration of data on gene expression, shall further advance our knowledge of avian evolution.     

The early history of modern birds inferred from DNA sequences of nuclear and mitochondrial ribosomal genes

The traditional view of avian evolution places ratites and tinamous at the base of the phylogenetic tree of modern birds (Neornithes). In contrast, most recent molecular studies suggest that neognathous perching birds (Passeriformes) compose the oldest lineage of modern birds. Here, we report significant molecular support for the traditional view of neognath monophyly based on sequence analyses of nuclear and mitochondrial DNA (4.4 kb) from every modern avian order. Phylogenetic analyses further show that the ducks and gallinaceous birds are each other's closest relatives and together form the basal lineage of neognathous birds. To investigate why other molecular studies sampling fewer orders have reached different conclusions regarding neognath monophyly, we performed jackknife analyses on our mitochondrial data. Those analyses indicated taxon-sampling effects when basal galloanserine birds were included in combination with sparse taxon sampling. Our phylogenetic results suggest that the earliest neornithines were heavy-bodied, ground-dwelling, nonmarine birds. This inference, coupled with a fossil bias toward marine environments, provides a possible explanation for the large gap in the early fossil record of birds.     

Cognitive ornithology: the evolution of avian intelligence

Comparative psychologists interested in the evolution of intelligence have focused their attention on social primates, whereas birds tend to be used as models of associative learning. However, corvids and parrots, which have forebrains relatively the same size as apes, live in complex social groups and have a long developmental period before becoming independent, have demonstrated ape-like intelligence. Although, ornithologists have documented thousands of hours observing birds in their natural habitat, they have focused their attention on avian behaviour and ecology, rather than intelligence. This review discusses recent studies of avian cognition contrasting two different approaches; the anthropocentric approach and the adaptive specialization approach. It is argued that the most productive method is to combine the two approaches. This is discussed with respects to recent investigations of two supposedly unique aspects of human cognition; episodic memory and theory of mind. In reviewing the evidence for avian intelligence, corvids and parrots appear to be cognitively superior to other birds and in many cases even apes. This suggests that complex cognition has evolved in species with very different brains through a process of convergent evolution rather than shared ancestry, although the notion that birds and mammals may share common neural connectivity patterns is discussed.     

Phenotypic plasticity in the scaling of avian basal metabolic rate

Many birds exhibit short-term, reversible adjustments in basal metabolic rate (BMR), but the overall contribution of phenotypic plasticity to avian metabolic diversity remains unclear. The available BMR data include estimates from birds living in natural environments and captive-raised birds in more homogenous, artificial environments. All previous analyses of interspecific variation in BMR have pooled these data. We hypothesized that phenotypic plasticity is an important contributor to interspecific variation in avian BMR, and that captive-raised populations exhibit general differences in BMR compared to wild-caught populations. We tested this hypothesis by fitting general linear models to BMR data for 231 bird species, using the generalized least-squares approach to correct for phylogenetic relatedness when necessary. The scaling exponent relating BMR to body mass in captive-raised birds (0.670) was significantly shallower than in wild-caught birds (0.744). The differences in metabolic scaling between captive-raised and wild-caught birds persisted when migratory tendency and habitat aridity were controlled for. Our results reveal that phenotypic plasticity is a major contributor to avian interspecific metabolic variation. The finding that metabolic scaling in birds is partly determined by environmental factors provides further support for models that predict variation in scaling exponents, such as the allometric cascade model.     

Birds help plants: a meta-analysis of top-down trophic cascades caused by avian predators

The tritrophic interactions between plants, herbivores and avian predators are complex and prone to trophic cascades. We conducted a meta-analysis of original articles that have studied birds as predators of invertebrate herbivores, to compare top-down trophic cascades with different plant responses from different environments and climatic areas. Our search found 29 suitable articles, with a total of 81 separate experimental study set-ups. The meta-analysis revealed that plants benefited from the presence of birds. A significant reduction was observed in the level of leaf damage and plant mortality. The presence of birds also positively affected the amount of plant biomass, whereas effects on plant growth were negligible. There were no differences in the effects between agricultural and natural environments. Similarly, plants performed better in all climatic areas (tropical, temperate and boreal) when birds were present. Moreover, both mature plants and saplings gained benefits from the presence of birds. Our results show that birds cause top-down trophic cascades and thus they play an integral role in ecosystems.     

The avian 'prefrontal cortex' and cognition

Both mammals and birds can flexibly organize their behavior over time. In mammals, the mental operations generating this ability are called executive functions and are associated with the prefrontal cortex. The corresponding structure in birds is the nidopallium caudolaterale. Anatomical, neurochemical, electrophysiological and behavioral studies show these structures to be highly similar. The avian forebrain displays no lamination that corresponds to the mammalian neocortex, hence lamination does not seem to be a requirement for higher cognitive functions. Because all other aspects of the neural architecture of the mammalian and the avian prefrontal areas are extremely comparable, the freedom to create different neural architectures that generate prefrontal functions seems to be very limited.     

Ecological factors affect the level and scaling of avian BMR

The basal rate of metabolism (BMR) in 533 species of birds, when examined with ANCOVA, principally correlates with body mass, most of the residual variation correlating with food habits, climate, habitat, a volant or flightless condition, use or not of torpor, and a highland or lowland distribution. Avian BMR also correlates with migratory habits, if climate and a montane distribution is excluded from the analysis, and with an occurrence on small islands if a flightless condition and migration are excluded. Residual variation correlates with membership in avian orders and families principally because these groups are behaviorally and ecologically distinctive. However, the distinction between passerines and other birds remains a significant correlate of avian BMR, even after six ecological factors are included, with other birds having BMRs that averaged 74% of the passerine mean. This combination of factors accounts for 97.7% of the variation in avian BMR. Yet, migratory species that belong to Anseriformes, Charadriiformes, Pelecaniformes, and Procellariiformes and breed in temperate or polar environments have mass-independent basal rates equal to those found in passerines. In contrast, penguins belong to an order of polar, aquatic birds that have basal rates lower than passerines because their flightless condition depresses basal rate. Passerines dominate temperate, terrestrial environments and the four orders of aquatic birds dominate temperate and polar aquatic environments because their high BMRs facilitate reproduction and migration. The low BMRs of tropical passerines may reflect a sedentary lifestyle as much as a life in a tropical climate. Birds have BMRs that are 30-40% greater than mammals because of the commitment of birds to an expensive and expansive form of flight.     

Sometimes slower is better: slow-exploring birds are more sensitive to changes in a vocal discrimination task

Animal personality, defined as consistent individual differences across context and time, has attracted much recent research interest in the study of animal behaviour. More recently, this field has begun to examine how such variation arose and is maintained within populations. The habitat-dependent selection hypothesis, which posits that animals with differing personality types may fare better (i.e. have a fitness advantage) in different habitats, suggests one possible mechanism. In the current experiment, we tested whether slow- and fast-exploring black-capped chickadees (Poecile atricapillus), determined by performance in a novel environment exploration task, perform differentially when the demands of an acoustic operant discrimination (cognitive) task were altered following successful task acquisition. We found that slow-exploring birds learn to reverse previously learned natural category rules more quickly than faster exploring conspecifics. In accordance with the habitat-dependent selection hypothesis, and previous work with great tits (Parus major), a close relative of the black-capped chickadee, our results suggest that fast-exploring birds may perform better in stable, predictable environments where forming a routine is advantageous, while slow-exploring birds are favoured in unstable, unpredictable environments, where task demands often change. Our results also support a hypothesis derived from previous work with great tits; slow-exploring birds may be generally more flexible (i.e. able to modify their behaviour in accordance with changes in environmental stimuli) in some learning tasks.     

Avian navigation and geographic positioning

Site fidelity to breeding and wintering grounds, and even stopover sites, suggests that passerines are capable of accurate navigation during their annual migrations. Geolocator‐based studies are beginning to demonstrate precise population‐specific migratory routes and even some interannual consistency in individual routes. Displacement studies of birds have shown that at least adult birds are capable of goal‐oriented movements, likely involving some type of map or geographic position system. In contrast, juveniles on their first migration use a clock‐and‐compass orientation strategy, with limited knowledge about locations along their migratory routes. Positioning information could come from a variety of cues including visual, olfactory, acoustic, and geomagnetic sources. How information from these systems is integrated and used for avian navigation has yet to be fully articulated. In this review, we (1) define geographic positioning and distinguish the types of navigational strategies that birds could use for orientation, (2) describe sensory cues available to birds for geographic positioning, (3) review the evidence for geographic positioning in birds and methods used to collect that evidence, and (4) discuss ways ornithologists, particularly field ornithologists, can contribute to and advance our knowledge of the navigational abilities of birds. Few studies of avian orientation and navigation mechanisms have been conducted in the Western Hemisphere. To fully understand migratory systems in the Western Hemisphere and develop better conservation policies, information about the orientation and navigation mechanisms used by specific species needs to be integrated with other aspects of their migration ecology and biology.     

Review. Meiotic drive and sex determination: molecular and cytological mechanisms of sex ratio adjustment in birds

Differences in relative fitness of male and female offspring across ecological and social environments should favour the evolution of sex-determining mechanisms that enable adjustment of brood sex ratio to the context of breeding. Despite the expectation that genetic sex determination should not produce consistent bias in primary sex ratios, extensive and adaptive modifications of offspring sex ratio in relation to social and physiological conditions during reproduction are often documented. Such discordance emphasizes the need for empirical investigation of the proximate mechanisms for modifying primary sex ratios, and suggests epigenetic effects on sex-determining mechanisms as the most likely candidates. Birds, in particular, are thought to have an unusually direct opportunity to modify offspring sex ratio because avian females are heterogametic and because the sex-determining division in avian meiosis occurs prior to ovulation and fertilization. However, despite evidence of strong epigenetic effects on sex determination in pre-ovulatory avian oocytes, the mechanisms behind such effects remain elusive. Our review of molecular and cytological mechanisms of avian meiosis uncovers a multitude of potential targets for selection on biased segregation of sex chromosomes, which may reflect the diversity of mechanisms and levels on which such selection operates in birds. Our findings indicate that pronounced differences between sex chromosomes in size, shape, size of protein bodies, alignment at the meiotic plate, microtubule attachment and epigenetic markings should commonly produce biased segregation of sex chromosomes as the default state, with secondary evolution of compensatory mechanisms necessary to maintain unbiased meiosis. We suggest that it is the epigenetic effects that modify such compensatory mechanisms that enable context-dependent and precise adjustment of primary sex ratio in birds. Furthermore, we highlight the features of avian meiosis that can be influenced by maternal hormones in response to environmental stimuli and may account for the precise and adaptive patterns of offspring sex ratio adjustment observed in some species.