A Comparison of Telencephalon Composition among Chickens, Junglefowl, and Wild Galliforms.

INTRODUCTION: Domestication is the process of modifying animals for human benefit through selective breeding in captivity. One of the traits that often diverges is the size of the brain and its constituent regions; almost all domesticated species have relatively smaller brains and brain regions than their wild ancestors. Although the effects of domestication on the brain have been investigated across a range of both mammal and bird species, almost nothing is known about the neuroanatomical effects of domestication on the world's most common bird: the chicken (Gallus gallus). METHODS: We compared the quantitative neuroanatomy of the telencephalon of white leghorn chickens with red junglefowl, their wild counterpart, and several wild galliform species. We focused specifically on the telencephalon because telencephalic regions typically exhibit the biggest differences in size in domesticate-wild comparisons. RESULTS: Relative telencephalon size was larger in chickens than in junglefowl and ruffed grouse (Bonasa umbellus). The relative size of telencephalic regions did not differ between chickens and junglefowl, but did differ in comparison with ruffed grouse. Ruffed grouse had larger hyperpallia and smaller entopallial, nidopallial, and striatal volumes than chickens and junglefowl. Multivariate analyses that included an additional three wild grouse species corroborated these findings: chicken and junglefowl have relatively larger nidopallial and striatal volumes than grouse. Conversely, the mesopallial and hyperpallial volumes tended to be relatively smaller in chickens and junglefowl. CONCLUSION: From this suite of comparisons, we conclude that chickens do not follow a pattern of widespread decreases in telencephalic region sizes that is often viewed as typical of domestication. Instead, chickens have undergone a mosaic of changes with some regions increasing and others decreasing in size, and there are few differences between chickens and junglefowl.

Quality not quantity: Deficient juvenile play experiences lead to altered medial prefrontal cortex neurons and sociocognitive skill deficits.

Reduced play experience over the juvenile period leads to adults with impoverished social skills and to anatomical and physiological aberrations of the neurons found in the medial prefrontal cortex (mPFC). Even rearing rats from high-playing strains with low-playing strains show these developmental consequences. In the present study, we evaluated whether low-playing rats benefit from being reared with higher playing peers. To test this, we reared male Fischer 344 rats (F344), typically thought to be a low-playing strain, with a Long-Evans (LE) peer, a relatively high-playing strain. As juveniles, F344 rats reared with LE rats experienced less play and lower quality play compared to those reared with another F344. As adults, the F344 rats reared with LE partners exhibited poorer social skills and the pyramidal neurons of their mPFC had larger dendritic arbors than F344 rats reared with same-strain peers. These findings show that being reared with a more playful partner does not improve developmental outcomes of F344 rats, rather the discordance in the play styles of F344 and LE rats leads to poorer outcomes.

Online repositories of photographs and videos provide insights into the evolution of skilled hindlimb movements in birds.

The ability to manipulate objects with limbs has evolved repeatedly among land tetrapods. Several selective forces have been proposed to explain the emergence of forelimb manipulation, however, work has been largely restricted to mammals, which prevents the testing of evolutionary hypotheses in a comprehensive evolutionary framework. In birds, forelimbs have gained the exclusive function of flight, with grasping transferred predominantly to the beak. In some birds, the feet are also used in manipulative tasks and appear to share some features with manual grasping and prehension in mammals, but this has not been systematically investigated. Here we use large online repositories of photographs and videos to quantify foot manipulative skills across a large sample of bird species (>1000 species). Our results show that a complex interaction between niche, diet and phylogeny drive the evolution of manipulative skills with the feet in birds. Furthermore, we provide strong support for the proposition that an arboreal niche is a key element in the evolution of manipulation in land vertebrates. Our systematic comparison of foot use in birds provides a solid base for understanding morphological and neural adaptations for foot use in birds, and for studying the convergent evolution of manipulative skills in birds and mammals.

Comparative Analysis of the Temporal Impacts of Corticosterone and Simulated Production Stressors on the Metabolome of Broiler Chickens.

The impact of physiological stress on the metabolome of breast muscle, liver, kidney, and hippocampus was investigated in Ross 308 broiler chicks. Simulated on-farm stressors were compared to a corticosterone model of physiological stress. The three different stressors investigated were: (i) corticosterone at a dose of 15 mg/kg of feed; (ii) heat treatment of 36 °C and 40% RH for 8 h per day; and (iii) isolation for 1 h per day. Liver, kidney, breast muscle, and hippocampus samples were taken after 2, 4, 6, and 8 days of stress treatment, and subjected to untargeted 1H-nuclear magnetic resonance (NMR) spectroscopy-based metabolomic analysis to provide insights on how stress can modulate metabolite profiles and biomarker discovery. Many of the metabolites that were significantly altered in tissues were amino acids, with glycine and alanine showing promise as candidate biomarkers of stress. Corticosterone was shown to significantly alter alanine, aspartate, and glutamate metabolism in the liver, breast, and hippocampus, while isolation altered the same pathways, but only in the kidneys and hippocampus. Isolation also significantly altered the glycine, serine, and threonine metabolism pathway in the liver and breast, while the same pathway was significantly altered by heat in the liver, kidneys, and hippocampus. The study's findings support corticosterone as a model of stress. Moreover, a number of potential metabolite biomarkers were identified in chicken tissues, which may allow producers to effectively monitor stress and to objectively develop and evaluate on-farm mitigations, including practices that reduce stress and enhance bird health.

The relative sizes of nuclei in the oculomotor complex vary by order and behaviour in birds.

Eye movements are a critical component of visually guided behaviours, allowing organisms to scan the environment and bring stimuli of interest to regions of acuity in the retina. Although the control and modulation of eye movements by cranial nerve nuclei are highly conserved across vertebrates, species variation in visually guided behaviour and eye morphology could lead to variation in the size of oculomotor nuclei. Here, we test for differences in the size and neuron numbers of the oculomotor nuclei among birds that vary in behaviour and eye morphology. Using unbiased stereology, we measured the volumes and numbers of neurons of the oculomotor (nIII), trochlear (nIV), abducens (nVI), and Edinger-Westphal (EW) nuclei across 71 bird species and analysed these with phylogeny-informed statistics. Owls had relatively smaller nIII, nIV, nVI and EW nuclei than other birds, which reflects their limited degrees of eye movements. In contrast, nVI was relatively larger in falcons and hawks, likely reflecting how these predatory species must shift focus between the central and temporal foveae during foraging and prey capture. Unexpectedly, songbirds had an enlarged EW and relatively more nVI neurons, which might reflect accommodation and horizontal eye movements. Finally, the one merganser we measured also has an enlarged EW, which is associated with the high accommodative power needed for pursuit diving. Overall, these differences reflect species and clade level variation in behaviour, but more data are needed on eye movements in birds across species to better understand the relationships among behaviour, retinal anatomy, and brain anatomy.

Not like night and day: the nocturnal letter-winged kite does not differ from diurnal congeners in orbit or endocast morphology.

Nocturnal birds display diverse adaptations of the visual system to low-light conditions. The skulls of birds reflect many of these and are used increasingly to infer nocturnality in extinct species. However, it is unclear how reliable such assessments are, particularly in cases of recent evolutionary transitions to nocturnality. Here, we investigate a case of recently evolved nocturnality in the world's only nocturnal hawk, the letter-winged kite Elanus scriptus. We employed phylogenetically informed analyses of orbit, optic foramen and endocast measurements from three-dimensional reconstructions of micro-computed tomography scanned skulls of the letter-winged kite, two congeners, and 13 other accipitrid and falconid raptors. Contrary to earlier suggestions, the letter-winged kite was not unique in any of our metrics. However, all species of Elanus have significantly higher ratios of orbit versus optic foramen diameter, suggesting high visual sensitivity at the expense of acuity. In addition, visual system morphology varies greatly across accipitrid species, likely reflecting hunting styles. Overall, our results suggest that the transition to nocturnality can occur rapidly and without changes to key hard-tissue indicators of vision, but also that hard-tissue anatomy of the visual system may provide a means of inferring a range of raptor behaviours, well beyond nocturnality.

The cerebellar anatomy of red junglefowl and white leghorn chickens: insights into the effects of domestication on the cerebellum.

Domestication is the process by which wild organisms become adapted for human use. Many phenotypic changes are associated with animal domestication, including decreases in brain and brain region sizes. In contrast with this general pattern, the chicken has a larger cerebellum compared with the wild red junglefowl, but what neuroanatomical changes are responsible for this difference have yet to be investigated. Here, we quantified cell layer volumes, neuron numbers and neuron sizes in the cerebella of chickens and junglefowl. Chickens have larger, more folded cerebella with more and larger granule cells than junglefowl, but neuron numbers and cerebellar folding were proportional to cerebellum size. However, chickens do have relatively larger granule cell layer volumes and relatively larger granule cells than junglefowl. Thus, the chicken cerebellum can be considered a scaled-up version of the junglefowl cerebellum, but with enlarged granule cells. The combination of scaling neuron number and disproportionate enlargement of cell bodies partially supports a recent theory that domestication does not affect neuronal density within brain regions. Whether the neuroanatomical changes we observed are typical of domestication or not requires similar quantitative analyses in other domesticated species and across multiple brain regions.

A quantitative analysis of cerebellar anatomy in birds.

The cerebellum is largely conserved in its circuitry, but varies greatly in size and shape across species. The extent to which differences in cerebellar morphology is driven by changes in neuron numbers, neuron sizes or both, remains largely unknown. To determine how species variation in cerebellum size and shape is reflective of neuron sizes and numbers requires the development of a suitable comparative data set and one that can effectively separate different neuronal populations. Here, we generated the largest comparative dataset to date on neuron numbers, sizes, and volumes of cortical layers and surface area of the cerebellum across 54 bird species. Across different cerebellar sizes, the cortical layers maintained relatively constant proportions to one another and variation in cerebellum size was largely due to neuron numbers rather than neuron sizes. However, the rate at which neuron numbers increased with cerebellum size varied across Purkinje cells, granule cells, and cerebellar nuclei neurons. We also examined the relationship among neuron numbers, cerebellar surface area and cerebellar folding. Our estimate of cerebellar folding, the midsagittal foliation index, was a poor predictor of surface area and number of Purkinje cells, but surface area was the best predictor of Purkinje cell numbers. Overall, this represents the first comprehensive, quantitative analysis of cerebellar anatomy in a comparative context of any vertebrate. The extent to which these relationships occur in other vertebrates requires a similar approach and would determine whether the same scaling principles apply throughout the evolution of the cerebellum.

Endocast structures are reliable proxies for the sizes of corresponding regions of the brain in extant birds.

Endocasts are increasingly relied upon to examine avian brain evolution because they can be used across extant and extinct species. The endocasts of birds appear to be relatively faithful representatives of the external morphology of their brains, but it is unclear how well the size of a surface feature visible on endocasts reflects the volume of the underlying brain region. The optic lobe and the Wulst are two endocast structures that are clearly visible on the external surface of avian endocasts. As they overlie two major visual regions of the brain, the optic tectum and hyperpallium, the surface areas of the optic lobe and Wulst, respectively, are often used to infer visual abilities. To determine whether the surface area of these features reflects the volume of the underlying brain regions, we compared the surface areas of the optic lobes and Wulsts from digital endocasts with the volumes of the optic tecta and hyperpallia from the literature or measured from histological series of brains of the same species. Regression analyses revealed strong, statistically significant correlations between the volumes of the brain regions and the surface areas of the overlying endocast structures. In other words, the size of the hyperpallium and optic tectum can be reliably inferred from the surface areas of the Wulst and optic lobe, respectively. This validation opens the possibility of estimating brain-region volumes for extinct species in order to gain better insights in their visual ecology. It also emphasizes the importance of adopting a quantitative approach to the analysis of endocasts in the study of brain evolution.

Selection for Divergent Reproductive Investment Affects Neuron Size and Foliation in the Cerebellum.

The cerebellum has a highly conserved internal circuitry, but varies greatly in size and morphology within and across species. Despite this variation, the underlying volumetric changes among the layers of the cerebellar cortex or their association with Purkinje cell numbers and sizes is poorly understood. Here, we examine intraspecific scaling relationships and variation in the quantitative neuroanatomy of the cerebellum in Japanese quail (Coturnix japonica) selected for high or low reproductive investment. As predicted by the circuitry of the cerebellum, the volumes of the constituent layers of the cerebellar cortex were strongly and positively correlated with one another and with total cerebellar volume. The number of Purkinje cells also significantly and positively co-varied with total cerebellar volume and the molecular layer, but not the granule cell layer or white matter volumes. Purkinje cell size and cerebellar foliation did not significantly covary with any cerebellar measures, but differed significantly between the selection lines. Males and females from the high-investment lines had smaller Purkinje cells than males and females from the low-investment lines and males from the high-investment lines had less folded cerebella than quail from the low-investment lines. These results suggest that within species, the layers of the cerebellum increase in a coordinated fashion, but Purkinje cell size and cerebellar foliation do not increase proportionally with overall cerebellum size. In contrast, selection for differential reproductive investment affects Purkinje cell size and cerebellar foliation, but not other quantitative measures of cerebellar anatomy.

Allometric Scaling Rules of the Cerebellum in Galliform Birds.

Although the internal circuitry of the cerebellum is highly conserved across vertebrate species, the size and shape of the cerebellum varies considerably. Recent comparative studies have examined the allometric rules between cerebellar mass and number of neurons, but data are lacking on the numbers and sizes of Purkinje and granule cells or scaling of cerebellar foliation. Here, we investigate the allometric rules that govern variation in the volumes of the layers of the cerebellum, the numbers and sizes of Purkinje cells and granule cells and the degree of the cerebellar foliation across 7 species of galliform birds. We selected Galliformes because they vary greatly in body and brain sizes. Our results show that the molecular, granule and white matter layers all increase in volume at the same rate relative to total cerebellum volume. Both numbers and sizes of Purkinje cells increased with cerebellar volume, but numbers of Purkinje cells increased at a much faster rate than size. Granule cell numbers increased with cerebellar volume, but size did not. Sizes and numbers of Purkinje cells as well as numbers of granule cells were positively correlated with the degree of cerebellar foliation, but granule cell size decreased with higher degrees of foliation. The concerted changes among the volumes of cerebellar layers likely reflects the conserved neural circuitry of the cerebellum. Also, our data indicate that the scaling of cell sizes can vary markedly across neuronal populations, suggesting that evolutionary changes in cell sizes might be more complex than what is often assumed.

Author Correction: The endocast of the Night Parrot (Pezoporus occidentalis) reveals insights into its sensory ecology and the evolution of nocturnality in birds.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

The endocast of the Night Parrot (Pezoporus occidentalis) reveals insights into its sensory ecology and the evolution of nocturnality in birds.

The Night Parrot (Pezoporus occidentalis) is a rare, nocturnal parrot species that has largely escaped scientific investigation due to its behaviour and habitat preferences. Recent field studies have revealed some insights into Night Parrot behaviour, but nothing is known of its sensory abilities. Here, we used µCT scans of an intact Night Parrot specimen to determine if its visual system shares similarities with other nocturnal species. The endocast of the Night Parrot revealed relatively small optic lobes and optic foramina, especially compared with closely related grass parakeets, but no apparent differences in orbit dimensions. Our data suggests that the Night Parrot likely has lower visual acuity than most other parrots, including its congener, the Eastern Ground Parrot (P. wallicus). We propose that the visual system of the Night Parrot might represent a compromise between the need to see under low light conditions and the visual acuity required to detect predators, forage, and fly. Based on the endocast and optic foramen measurements, the Night Parrot fits into a common pattern of decreased retinal input to the optic lobes in birds that should be explored more thoroughly in extant and extinct species.

Sensory systems in birds: What we have learned from studying sensory specialists.

"Diversity" is an apt descriptor of the research career of Jack Pettigrew as it ranged from the study of trees, to clinical conditions, to sensory neuroscience. Within sensory neuroscience, he was fascinated by the evolution of sensory systems across species. Here, we review some of his work on avian sensory specialists and research that he inspired in others. We begin with an overview of the importance of the Wulst in stereopsis and the need for further study of the Wulst in relation to binocularity across avian species. Next, we summarize recent anatomical, behavioral, and physiological studies on optic flow specializations in hummingbirds. Beyond vision, we discuss the first evidence of a tactile "fovea" in birds and how this led to detailed studies of tactile specializations in waterfowl and sensorimotor systems in parrots. We then describe preliminary studies by Pettigrew of two endemic Australian species, the plains-wanderer (Pedionomus torquatus) and letter-winged kite (Elanus scriptus), that suggest the evolution of some unique auditory and visual specializations in relation to their unique behavior and ecology. Finally, we conclude by emphasizing the importance of a comparative and integrative approach to understanding avian sensory systems and provide an example of one system that has yet to be properly examined: tactile facial bristles in birds. Through reviewing this research and offering future avenues for discovery, we hope that others also embrace the comparative approach to understanding sensory system evolution in birds and other vertebrates.

Zebrin Expression in the Cerebellum of Two Crocodilian Species.

While in birds and mammals the cerebellum is a highly convoluted structure that consists of numerous transverse lobules, in most amphibians and reptiles it consists of only a single unfolded sheet. Orthogonal to the lobules, the cerebellum is comprised of sagittal zones that are revealed in the pattern of afferent inputs, the projection patterns of Purkinje cells, and Purkinje cell response properties, among other features. The expression of several molecular markers, such as aldolase C, is also parasagittally organized. Aldolase C, also known as zebrin II (ZII), is a glycolytic enzyme expressed in the cerebellar Purkinje cells of the vertebrate cerebellum. In birds, mammals, and some lizards (Ctenophoresspp.), ZII is expressed in a heterogenous fashion of alternating sagittal bands of high (ZII+) and low (ZII-) expression Purkinje cells. In contrast, turtles and snakes express ZII homogenously (ZII+) in their cerebella, but the pattern in crocodilians is unknown. Here, we examined the expression of ZII in two crocodilian species (Crocodylus niloticus and Alligator mississippiensis) to help determine the evolutionary origin of striped ZII expression in vertebrates. We expected crocodilians to express ZII in a striped (ZII+/ZII-) manner because of their close phylogenetic relationship to birds and their larger and more folded cerebellum compared to that of snakes and turtles. Contrary to our prediction, all Purkinje cells in the crocodilian cerebellum had a generally homogenous expression of ZII (ZII+) rather than clear ZII+/- stripes. Our results suggest that either ZII stripes were lost in three groups (snakes, turtles, and crocodilians) or ZII stripes evolved independently three times (lizards, birds, and mammals).

Landscape effects on the contemporary genetic structure of Ruffed Grouse (Bonasa umbellus) populations.

The amount of dispersal that occurs among populations can be limited by landscape heterogeneity, which is often due to both natural processes and anthropogenic activity leading to habitat loss or fragmentation. Understanding how populations are structured and mapping existing dispersal corridors among populations is imperative to both determining contemporary forces mediating population connectivity, and informing proper management of species with fragmented populations. Furthermore, the contemporary processes mediating gene flow across heterogeneous landscapes on a large scale are understudied, particularly with respect to widespread species. This study focuses on a widespread game bird, the Ruffed Grouse (Bonasa umbellus), for which we analyzed samples from the western extent of the range. Using three types of genetic markers, we uncovered multiple factors acting in concert that are responsible for mediating contemporary population connectivity in this species. Multiple genetically distinct groups were detected; microsatellite markers revealed six groups, and a mitochondrial marker revealed four. Many populations of Ruffed Grouse are genetically isolated, likely by macrogeographic barriers. Furthermore, the addition of landscape genetic methods not only corroborated genetic structure results, but also uncovered compelling evidence that dispersal resistance created by areas of unsuitable habitat is the most important factor mediating population connectivity among the sampled populations. This research has important implications for both our study species and other inhabitants of the early successional forest habitat preferred by Ruffed Grouse. Moreover, it adds to a growing body of evidence that isolation by resistance is more prevalent in shaping population structure of widespread species than previously thought.

Breakdown of brain-body allometry and the encephalization of birds and mammals.

The allometric relationship between brain and body size among vertebrates is often considered a manifestation of evolutionary constraints. However, birds and mammals have undergone remarkable encephalization, in which brain size has increased without corresponding changes in body size. Here, we explore the hypothesis that a reduction of phenotypic integration between brain and body size has facilitated encephalization in birds and mammals. Using a large dataset comprising 20,213 specimens across 4,587 species of jawed vertebrates, we show that the among-species (evolutionary) brain-body allometries are remarkably constant, both across vertebrate classes and across taxonomic levels. Birds and mammals, however, are exceptional in that their within-species (static) allometries are shallower and more variable than in other vertebrates. These patterns are consistent with the idea that birds and mammals have reduced allometric constraints that are otherwise ubiquitous across jawed vertebrates. Further exploration of ontogenetic allometries in selected taxa of birds, fishes and mammals reveals that birds and mammals have extended the period of fetal brain growth compared to fishes. Based on these findings, we propose that avian and mammalian encephalization has been contingent on increased variability in brain growth patterns.

Predictable evolution towards larger brains in birds colonizing oceanic islands.

Theory and evidence suggest that some selective pressures are more common on islands than in adjacent mainland habitats, leading evolution to follow predictable trends. The existence of predictable evolutionary trends has nonetheless been difficult to demonstrate, mainly because of the challenge of separating in situ evolution from sorting processes derived from colonization events. Here we use brain size measurements of >1900 avian species to reveal the existence of one such trend: increased brain size in island dwellers. Based on sister-taxa comparisons and phylogenetic ancestral trait estimations, we show that species living on islands have relatively larger brains than their mainland relatives and that these differences mainly reflect in situ evolution rather than varying colonization success. Our findings reinforce the view that in some instances evolution may be predictable, and yield insight into why some animals evolve larger brains despite substantial energetic and developmental costs.

Parrots have evolved a primate-like telencephalic-midbrain-cerebellar circuit.

It is widely accepted that parrots show remarkable cognitive abilities. In mammals, the evolution of complex cognitive abilities is associated with increases in the size of the telencephalon and cerebellum as well as the pontine nuclei, which connect these two regions. Parrots have relatively large telencephalons that rival those of primates, but whether there are also evolutionary changes in their telencephalon-cerebellar relay nuclei is unknown. Like mammals, birds have two brainstem pontine nuclei that project to the cerebellum and receive projections from the telencephalon. Unlike mammals, birds also have a pretectal nucleus that connects the telencephalon with the cerebellum: the medial spiriform nucleus (SpM). We found that SpM, but not the pontine nuclei, is greatly enlarged in parrots and its relative size significantly correlated with the relative size of the telencephalon across all birds. This suggests that the telencephalon-SpM-cerebellar pathway of birds may play an analogous role to cortico-ponto-cerebellar pathways of mammals in controlling fine motor skills and complex cognitive processes. We conclude that SpM is key to understanding the role of telencephalon-cerebellar pathways in the evolution of complex cognitive abilities in birds.

Visual-Cerebellar Pathways and Their Roles in the Control of Avian Flight.

In this paper, we review the connections and physiology of visual pathways to the cerebellum in birds and consider their role in flight. We emphasize that there are two visual pathways to the cerebellum. One is to the vestibulocerebellum (folia IXcd and X) that originates from two retinal-recipient nuclei that process optic flow: the nucleus of the basal optic root (nBOR) and the pretectal nucleus lentiformis mesencephali (LM). The second is to the oculomotor cerebellum (folia VI-VIII), which receives optic flow information, mainly from LM, but also local visual motion information from the optic tectum, and other visual information from the ventral lateral geniculate nucleus (Glv). The tectum, LM and Glv are all intimately connected with the pontine nuclei, which also project to the oculomotor cerebellum. We believe this rich integration of visual information in the cerebellum is important for analyzing motion parallax that occurs during flight. Finally, we extend upon a suggestion by Ibbotson (2017) that the hypertrophy that is observed in LM in hummingbirds might be due to an increase in the processing demands associated with the pathway to the oculomotor cerebellum as they fly through a cluttered environment while feeding.