Cumulative route improvements spontaneously emerge in artificial navigators even in the absence of sophisticated communication or thought.

Homing pigeons (Columba livia) navigate by solar and magnetic compass, and fly home in idiosyncratic but stable routes when repeatedly released from the same location. However, when experienced pigeons fly alongside naive counterparts, their path is altered. Over several generations of turnover (pairs in which the most experienced individual is replaced with a naive one), pigeons show cumulative improvements in efficiency. Here, I show that such cumulative route improvements can occur in a much simpler system by using agent-based simulation. Artificial agents are in silico entities that navigate with a minimal cognitive architecture of goal-direction (they know roughly where the goal is), social proximity (they seek proximity to others and align headings), route memory (they recall landmarks with increasing precision), and continuity (they avoid erratic turns). Agents' behaviour qualitatively matched that of pigeons, and quantitatively fitted to pigeon data. My results indicate that naive agents benefitted from being paired with experienced agents by following their previously established route. Importantly, experienced agents also benefitted from being paired with naive agents due to regression to the goal: naive agents were more likely to err towards the goal from the perspective of experienced agents' memorised paths. This subtly biased pairs in the goal direction, resulting in intergenerational improvements of route efficiency. No cumulative improvements were evident in control studies in which agents' goal-direction, social proximity, or memory were lesioned. These 3 factors are thus necessary and sufficient for cumulative route improvements to emerge, even in the absence of sophisticated communication or thought.

Magnetic sensitivity of cryptochrome 4 from a migratory songbird.

Night-migratory songbirds are remarkably proficient navigators1. Flying alone and often over great distances, they use various directional cues including, crucially, a light-dependent magnetic compass2,3. The mechanism of this compass has been suggested to rely on the quantum spin dynamics of photoinduced radical pairs in cryptochrome flavoproteins located in the retinas of the birds4-7. Here we show that the photochemistry of cryptochrome 4 (CRY4) from the night-migratory European robin (Erithacus rubecula) is magnetically sensitive in vitro, and more so than CRY4 from two non-migratory bird species, chicken (Gallus gallus) and pigeon (Columba livia). Site-specific mutations of ErCRY4 reveal the roles of four successive flavin-tryptophan radical pairs in generating magnetic field effects and in stabilizing potential signalling states in a way that could enable sensing and signalling functions to be independently optimized in night-migratory birds.

Species coexistence by wide constant size spacing.

We consider the distribution of fruit pigeons of the genera Ptilinopus and Ducula on the island of New Guinea. Of the 21 species, between six and eight coexist inside humid lowland forests. We conducted or analyzed 31 surveys at 16 different sites, resurveying some sites in different years. The species coexisting at any single site in a single year are a highly nonrandom selection of the species to which that site is geographically accessible. Their sizes are both much more widely spread and more uniformly spaced than in random sets of species drawn from the locally available species pool. We also present a detailed case study of a highly mobile species that has been recorded on every ornithologically explored island in the West Papuan island group west of New Guinea. That species' rareness on just three well-surveyed islands within the group cannot be due to an inability to reach them. Instead, its local status decreases from abundant resident to rare vagrant in parallel with increasing weight proximity of the other resident species.

An allelic series at the EDNRB2 locus controls diverse piebalding patterns in the domestic pigeon.

Variation in pigment patterns within and among vertebrate species reflects underlying changes in cell migration and function that can impact health, reproductive success, and survival. The domestic pigeon (Columba livia) is an exceptional model for understanding the genetic changes that give rise to diverse pigment patterns, as selective breeding has given rise to hundreds of breeds with extensive variation in plumage color and pattern. Here, we map the genetic architecture of a suite of pigmentation phenotypes known as piebalding. Piebalding is characterized by patches of pigmented and non-pigmented feathers, and these plumage patterns are often breed-specific and stable across generations. Using a combination of quantitative trait locus mapping in F2 laboratory crosses and genome-wide association analysis, we identify a locus associated with piebalding across many pigeon breeds. This shared locus harbors a candidate gene, EDNRB2, that is a known regulator of pigment cell migration, proliferation, and survival. We discover multiple distinct haplotypes at the EDNRB2 locus in piebald pigeons, which include a mix of protein-coding, noncoding, and structural variants that are associated with depigmentation in specific plumage regions. These results identify a role for EDNRB2 in pigment patterning in the domestic pigeon, and highlight how repeated selection at a single locus can generate a diverse array of stable and heritable pigment patterns.

Spatio-temporal transcriptome dynamics coordinate rapid transition of core crop functions in 'lactating' pigeon.

Pigeons (Columba livia) are among a select few avian species that have developed a specialized reproductive mode wherein the parents produce a 'milk' in their crop to feed newborn squabs. Nonetheless, the transcriptomic dynamics and role in the rapid transition of core crop functions during 'lactation' remain largely unexplored. Here, we generated a de novo pigeon genome assembly to construct a high resolution spatio-temporal transcriptomic landscape of the crop epithelium across the entire breeding stage. This multi-omics analysis identified a set of 'lactation'-related genes involved in lipid and protein metabolism, which contribute to the rapid functional transitions in the crop. Analysis of in situ high-throughput chromatin conformation capture (Hi-C) sequencing revealed extensive reorganization of promoter-enhancer interactions linked to the dynamic expression of these 'lactation'-related genes between stages. Moreover, their expression is spatially localized in specific epithelial layers, and can be correlated with phenotypic changes in the crop. These results illustrate the preferential de novo synthesis of 'milk' lipids and proteins in the crop, and provides candidate enhancer loci for further investigation of the regulatory elements controlling pigeon 'lactation'.

Increased neuron density in the midbrain of a foveate bird, pigeon, results from profound change in tissue morphogenesis.

The increase of brain neuron number in relation with brain size is currently considered to be the major evolutionary path to high cognitive power in amniotes. However, how changes in neuron density did contribute to the evolution of the information-processing capacity of the brain remains unanswered. High neuron densities are seen as the main reason why the fovea located at the visual center of the retina is responsible for sharp vision in birds and primates. The emergence of foveal vision is considered as a breakthrough innovation in visual system evolution. We found that neuron densities in the largest visual center of the midbrain - i.e., the optic tectum - are two to four times higher in modern birds with one or two foveae compared to birds deprived of this specialty. Interspecies comparisons enabled us to identify elements of a hitherto unknown developmental process set up by foveate birds for increasing neuron density in the upper layers of their optic tectum. The late progenitor cells that generate these neurons proliferate in a ventricular zone that can expand only radially. In this particular context, the number of cells in ontogenetic columns increases, thereby setting the conditions for higher cell densities in the upper layers once neurons did migrate.

Investigating pigeon circovirus infection in a pigeon farm: molecular detection, phylogenetic analysis and complete genome analysis.

BACKGROUND: Pigeon circovirus infections in pigeons (Columba livia domestica) have been reported worldwide. Pigeons should be PiCV-free when utilized as qualified experimental animals. However, pigeons can be freely purchased as experimental animals without any clear guidelines to follow. Herein, we investigated the status quo of PiCV infections on a pigeon farm in Beijing, China, which provides pigeons for experimental use. RESULTS: PiCV infection was verified in at least three types of tissues in all forty pigeons tested. A total of 29 full-length genomes were obtained and deposited in GenBank. The whole genome sequence comparison among the 29 identified PiCV strains revealed nucleotide homologies of 85.8-100%, and these sequences exhibited nucleotide homologies of 82.7-98.9% as compared with those of the reference sequences. The cap gene displayed genetic diversity, with a wide range of amino acid homologies ranging from 64.5% to 100%. Phylogenetic analysis of the 29 full-genome sequences revealed that the PiCV strains in this study could be further divided into four clades: A (17.2%), B (10.4%), C (37.9%) and D (34.5%). Thirteen recombination events were also detected in 18 out of the 29 PiCV genomes obtained in this study. Phylogenetic research using the rep and cap genes verified the recombination events, which occurred between clades A/F, A/B, C/D, and B/D among the 18 PiCV strains studied. CONCLUSIONS: In conclusion, PiCV infection, which is highly genetically varied, is extremely widespread on pigeon farms in Beijing. These findings indicate that if pigeons are to be used as experimental animals, it is necessary to evaluate the impact of PiCV infection on the results.

Redefining the Evolutionary History of the Rock Dove, Columba livia, Using Whole Genome Sequences.

The domestic pigeon's exceptional phenotypic diversity was key in developing Darwin's Theory of Evolution and establishing the concept of artificial selection. However, unlike its domestic counterpart, its wild progenitor, the rock dove Columba livia has received considerably less attention. Therefore, questions regarding its domestication, evolution, taxonomy, and conservation status remain unresolved. We generated whole-genome sequencing data from 65 historical rock doves that represent all currently recognized subspecies and span the species' original geographic distribution. Our dataset includes 3 specimens from Darwin's collection, and the type specimens of 5 different taxa. We characterized their population structure, genomic diversity, and gene-flow patterns. Our results show the West African subspecies C. l. gymnocyclus is basal to rock doves and domestic pigeons, and suggests gene-flow between the rock dove's sister species C. rupestris, and the ancestor of rock doves after its split from West African populations. These genomes allowed us to propose a model for the evolution of the rock dove in light of the refugia theory. We propose that rock dove genetic diversity and introgression patterns derive from a history of allopatric cycles and dispersion waves during the Quaternary glacial and interglacial periods. To explore the rock dove domestication history, we combined our new dataset with available genomes from domestic pigeons. Our results point to at least 1 domestication event in the Levant that gave rise to all domestic breeds analysed in this study. Finally, we propose a species-level taxonomic arrangement to reflect the evolutionary history of the West African rock dove populations.

Quantitative functional imaging of the pigeon brain: implications for the evolution of avian powered flight.

The evolution of flight is a rare event in vertebrate history, and one that demands functional integration across multiple anatomical/physiological systems. The neuroanatomical basis for such integration and the role that brain evolution assumes in behavioural transformations remain poorly understood. We make progress by (i) generating a positron emission tomography (PET)-based map of brain activity for pigeons during rest and flight, (ii) using these maps in a functional analysis of the brain during flight, and (iii) interpreting these data within a macroevolutionary context shaped by non-avian dinosaurs. Although neural activity is generally conserved from rest to flight, we found significant increases in the cerebellum as a whole and optic flow pathways. Conserved activity suggests processing of self-movement and image stabilization are critical when a bird takes to the air, while increased visual and cerebellar activity reflects the importance of integrating multimodal sensory information for flight-related movements. A derived cerebellar capability likely arose at the base of maniraptoran dinosaurs, where volumetric expansion and possible folding directly preceded paravian flight. These data represent an important step toward establishing how the brain of modern birds supports their unique behavioural repertoire and provide novel insights into the neurobiology of the bird-like dinosaurs that first achieved powered flight.

Segmented spin-echo echo-planar imaging improves whole-brain BOLD functional MRI in awake pigeon brains.

Functional magnetic resonance imaging (fMRI) in awake small animals such as pigeons or songbirds opens a new window into the neural fundaments of cognitive behavior. However, high-field fMRI in the avian brain is challenging due to strong local magnetic field inhomogeneities caused by air cavities in the skull. A spoiled gradient-echo fMRI sequence has already been used to map the auditory network in songbirds, but due to susceptibility artifacts only 50% of the whole brain could be recorded. Since whole-brain fMRI coverage is vital to reveal whole-brain networks, an MRI sequence that is less susceptible to these artifacts was required. This was recently achieved in various bird species by using a rapid acquisition with relaxation enhancement (RARE) sequence. Weak blood oxygen level-dependent (BOLD) sensitivity, low temporal resolution, and heat caused by the long train of RF refocusing pulses are the main limits of RARE fMRI at high magnetic fields. To go beyond some of these limitations, we here describe the implementation of a two-segmented spin-echo echo-planar imaging (SE-EPI). The proposed sequence covers the whole brain of awake pigeons. The sequence was applied to investigate the auditory network in awake pigeons and assessed the relative merits of this method in comparison with the single-shot RARE sequence. At the same imaging resolution but with a volume acquisition of 3 s versus 4 s for RARE, the two-segmented SE-EPI provided twice the strength of BOLD activity compared with the single-shot RARE sequence, while the image signal-to-noise ratio (SNR) and in particular the temporal SNR were very similar for the two sequences. In addition, the activation patterns in two-segmented SE-EPI data are more symmetric and larger than single-shot RARE results. Two-segmented SE-EPI represents a valid alternative to the RARE sequence in avian fMRI research since it yields more than twice the BOLD sensitivity per unit of time with much less energy deposition and better temporal resolution, particularly for event-related experiments.

Early gonadogenesis in Columba livia (birds: Columbiformes): Migration, colonization, and differentiation of germ cells.

In birds, primordial germ cells (PGCs) use the bloodstream to travel to a specific region, where the cells undergo extravasation followed by intrastromal migration to the gonadal crest for further colonization. Currently, DDX4, SSEA1, and Oct4 are used to identify germ cells. Other germline cell-associated molecules are N-cadherin, GnRHR, and 3ß hydroxysteroid dehydrogenase (3ßHSD), which have been used in mice and birds during gonadal development; however, its role in early gonadogenesis in birds is poorly described. This study aimed to evaluate the differential immunodetection of N-cadherin binding molecule, Oct4 pluripotency protein, GnRHR receptor, and 3ßHSD enzyme in Columba livia embryos during migration colonization of PGCs in the gonadal crest and early gonadogenesis. These markers were revealed by immunohistochemistry in histological preparations of C. livia corresponding to stages (S)15 to S40. Immunodetection of N-cadherin, Oct4, GnRHR, and 3ßHSD in the germ line of C. livia allowed the identification of PGCs in the yolk sac membrane at the level of the splanchnic mesoderm during migration to the genital crest and its colonization. In the same way, it was possible to characterize and localize PGCs during early gonadogenesis. This study in C. livia demonstrates that Oct4, N-cadherin, GNRHR, and 3ßHSD are immunodetected in PGCs and could be used as potential germline cell markers during cell migration out of blood vessels, colonization in the genital crest, and early gonadogenesis. Furthermore, this study could be used as a novel general model to understand the early gonadogenesis in altricial species.

On the value of advanced information about delayed rewards.

In a variety of laboratory preparations, several animal species prefer signaled over unsignaled outcomes. Here we examine whether pigeons prefer options that signal the delay to reward over options that do not and how this preference changes with the ratio of the delays. We offered pigeons repeated choices between two alternatives leading to a short or a long delay to reward. For one alternative (informative), the short and long delays were reliably signaled by different stimuli (e.g., SS for short delays, SL for long delays). For the other (non-informative), the delays were not reliably signaled by the stimuli presented (S1 and S2). Across conditions, we varied the durations of the short and long delays, hence their ratio, while keeping the average delay to reward constant. Pigeons preferred the informative over the non-informative option and this preference became stronger as the ratio of the long to the short delay increased. A modified version of the Δ-Σ hypothesis (González et al., J Exp Anal Behav 113(3):591-608. https://doi.org/10.1002/jeab.595 , 2020a) incorporating a contrast-like process between the immediacies to reward signaled by each stimulus accounted well for our findings. Functionally, we argue that a preference for signaled delays hinges on the potential instrumental advantage typically conveyed by information.

Identification of pigeon mitochondrial antiviral signaling protein (MAVS) and its role in antiviral innate immunity.

Pigeons can be infected with various RNA viruses, and their innate immune system responds to viral infection to establish an antiviral response. Mitochondrial antiviral signaling protein (MAVS), an important adaptor protein in signal transduction, plays a pivotal role in amplifying the innate immune response. In this study, we successfully cloned pigeon MAVS (piMAVS) and performed a bioinformatics analysis. The results showed that the caspase recruitment domain (CARD) and transmembrane (TM) domain are highly conserved in poultry and mammals but poorly conserved in other species. Furthermore, we observed that MAVS expression is upregulated both in pigeons and pigeon embryonic fibroblasts (PEFs) upon RNA virus infection. Overexpression of MAVS resulted in increased levels of ß-interferon (IFN-ß), IFN-stimulated genes (ISGs), and interleukin (ILs) mRNA and inhibited Newcastle disease virus (NDV) replication. We also found that piMAVS and human MAVS (huMAVS) induced stronger expression of IFN-ß and ISGs when compared to chicken MAVS (chMAVS), and this phenomenon was also reflected in the degree of inhibition of NDV replication. Our findings demonstrate that piMAVS plays an important role in repressing viral replication by regulating the activation of the IFN signal pathway in pigeons. This study not only sheds light on the function of piMAVS in innate immunity but also contributes to a more comprehensive understanding of the innate immunity system in poultry. Our data also provide unique insights into the differences in innate immunity between poultry and mammal.

First transcriptomic insight into the working muscles of racing pigeons during a competition flight.

BACKGROUND: The currently known homing pigeon is a result of a sharp one-sided selection for flight characteristics focused on speed, endurance, and spatial orientation. This has led to extremely well-adapted athletic phenotypes in racing birds. METHODS: Here, we identify genes and pathways contributing to exercise adaptation in sport pigeons by applying next-generation transcriptome sequencing of m.pectoralis muscle samples, collected before and after a 300 km competition flight. RESULTS: The analysis of differentially expressed genes pictured the central role of pathways involved in fuel selection and muscle maintenance during flight, with a set of genes, in which variations may therefore be exploited for genetic improvement of the racing pigeon population towards specific categories of competition flights. CONCLUSIONS: The presented results are a background to understanding the genetic processes in the muscles of birds during flight and also are the starting point of further selection of genetic markers associated with racing performance in carrier pigeons.

Geographic distribution and genetic diversity of Newcastle disease virus in pigeons from Pakistan.

RESEARCH HIGHLIGHTS: Virulent NDV genotypes were repeatedly isolated from pigeons.Evidence of epidemiological links among viruses isolated from various locations.Distinct phylogenetic branches suggest separate, simultaneous evolution of NDVs.Study information could be helpful in the development of an effective vaccine.

Tissue-specific distributions of organic ultraviolet absorbents in free-range chickens and domestic pigeons from Guangzhou, China.

The ecological risks of organic ultraviolet absorbents (UVAs) have been of increasing concern. Studies have found that these chemicals could be accumulated in terrestrial animals and pose toxicities. However, tissue distribution of UVAs in terrestrial species was far from well understood. In this study, free-range chickens and domestic pigeons were selected to investigate the occurrence and tissue distribution of UVAs. Total concentrations of eleven UVAs in muscles ranged from 778 to 2874 (mean 1413 ± 666) ng/g lipid weight, which were higher than those in aquatic species worldwide. Since low UVA concentrations in local environment were previously reported, the results implied the strong accumulation of UVAs in studied species. Brain, stomach and kidney were main target organs for studied UVAs, differentiating from the strong liver sequestration in aquatic species. The mean tissue-to-muscle ratios of 1.02-4.23 further indicated the preferential accumulation of target UVAs in these tissues. The tissue-to-blood ratios of benzophenone (BP), 2-ethylhexyl salicylate (EHS) and homosalate (HMS) in brain were 370, 1207 and 52.0, respectively, implying their preferential accumulation in brain. More research is needed to characterize the toxicokinetics and tissue distribution of UVAs in terrestrial wild species, in order to further understand their potential risks.

Blood lead increases and haemoglobin decreases in urban birds along a soil contamination gradient in a mining city.

Lead contaminated soil is a persistent global threat to the health of animal populations. Nevertheless, links between soil lead and its adverse effects on exposed wildlife remain poorly understood. Here, we explore local geographic patterns of exposure in urban birds along a gradient of lead contamination in Broken Hill, an Australian mining city. Soil lead concentrations are linked to co-located blood lead measurements in rock pigeons (Columba livia), house sparrows (Passer domesticus), crested pigeons (Ocyphaps lophotes) and white-plumed honeyeaters (Lichenostomus ornatus). Median blood lead levels were highest in crested pigeons (59.6 µg/dL), followed by house sparrows (35.2 µg/dL), rock pigeons (35.1 µg/dL), and white-plumed honeyeaters (27.4 µg/dL). Blood lead levels in all species declined away from mining areas, the primary source of lead contamination in Broken Hill. Blood lead increased significantly and at the greatest rate relative to soil lead in the three ground foraging species (crested pigeons, house sparrows, rock pigeons). For these species, soil lead concentrations below 200 mg/kg and 900 mg/kg were needed to maintain a median blood lead concentration under the lower threshold of the subtoxic (20-50 µg/dL) and toxic (≥50 µg/dL) effect ranges previously identified for some bird species. We also investigated the effects of lead exposure on blood haemoglobin levels as a general measure of physiological condition in birds exposed to different levels of soil lead contamination. Overall, for every 1 µg/dL increase in blood lead, haemoglobin decreased by 0.11 g/L. The rate of this decrease was not significantly different between species, which supports the measurement of haemoglobin as a consistent though insensitive measure of physiological condition in chronically lead exposed birds. Our findings reflect the importance of lead contaminated soil as a widespread source of elevated blood lead and supressed haemoglobin levels in birds inhabiting urbanised and mining impacted environments.

The course of Rotavirus A (RVA) infection in young racing pigeons during the racing season.

BACKGROUND: Pigeon Rotavirus A (RVA) infection has been confirmed in pigeons in the last decade as a cause of Young Pigeon Disease (YPD). Although YPD has been known for many years to date, no studies have been conducted to track the spread of RVA infection in pigeons during the racing season. The presented research aims to determine the course of RVA infection during the flights of young racing pigeons in the summer season, in one of the districts in the Mazovian Voivodeship in Poland. RESULTS: Faecal samples of pigeons collected from transport baskets in vehicles transporting pigeons to the starting point were tested. The quantitative RT-PCR (qRT-PCR) was used to detect the genetic material of RVA. Samples taken during 6 flights were analysed. The study showed a percentage increase in infections up to the fourth flight of pigeons, and then their decrease. With Cq values below 20, breeders did not participate in the next flight and/or reported disease in the flock. With positive Cq values of 20 to 30, clinical signs of disease were not reported. Of the 76 breeders participating in the races, at least one positive result was found in 46 (60.5%). Including the occurrence of the disease during the racing season was reported by 11 breeders (14.4%). The main clinical signs in sick pigeons were vomiting, diarrhea and stowed crop. The tested pigeons were not vaccinated against RVA. CONCLUSIONS: During training and racing of pigeons, it is not possible to avoid exposing them to pathogens, including RVA, regardless of whether pigeons from different breeders are placed in the same baskets or are in separate baskets. However, after four flights the number of new cases of the disease decreases which indicates the development of immunity. The qRT-PCR test is useful in the diagnosis and differentiation of clinical (Cq below 20) and subclinical RVA infections in racing pigeons.

Limits of flexibility and associative learning in pigeons.

In a recent study, Wasserman, Kain, and O'Donoghue (Current Biology, 33(6), 1112-1116, 2023) set out to resolve the associative learning paradox by showing that pigeons can solve a complex category learning task through associative learning. The present Outlook paper presents their findings, expands on this paradox, and discusses implications of their results.

Landmarks, beacons, or panoramic views: What do pigeons attend to for guidance in familiar environments?

Birds and social insects represent excellent systems for understanding visually guided navigation. Both animal groups use surrounding visual cues for homing and foraging. Ants extract sufficient spatial information from panoramic views, which naturally embed all near and far spatial information, for successful homing. Although egocentric panoramic views allow for parsimonious explanations of navigational behaviors, this potential source of spatial information has been mostly neglected during studies of vertebrates. Here we investigate how distinct landmarks, a beacon, and panoramic views influence the reorientation behavior in pigeons (Columba livia). Pigeons were trained to search for a location characterized by a beacon and several distinct landmarks. Transformation tests manipulated aspects of the landmark configuration, allowing for a dissociation among navigational strategies. Quantitative image and path analyses provided support that the panoramic view was used by the pigeons. Although the results from some individuals support the use of beaconing, overall the pigeons relied predominantly on the panoramic view when spatial cues provided conflicting information regarding the goal location. Reorientation based on vector and bearing information derived from distinct landmarks as well as environmental geometry failed to account fully for the results. Thus, the results of our study support that pigeons can use panoramic views for reorientation in familiar environments. Given that the current model for landmark use by pigeons posits the use of different vectors from an object, a global panorama-matching strategy suggests a fundamental change in the theory of how pigeons use surrounding visual cues for localization.