Andrew N. Iwaniuk

On the origin of skilled forelimb movements

Homologizing behaviour was once considered unreliable, but the application of modern comparative methods has been shown to provide strong evidence of behavioural homologies. Skilled forelimb movements were thought to originate in the primate lineage but in fact are common among tetrapod taxa and probably share a common origin in early tetrapods. Furthermore, skilled movements are likely to have been derived from, and elaborated through, food-handling behaviour. In addition, it is now thought that the role played by the lateral and medial descending pathways of the spinal cord in the execution of skilled forelimb movements could be synergistic, rather than the exclusive responsibility of an individual pathway.

The Evolution of Cerebrotypes in Birds

Multivariate analyses of brain composition in mammals, amphibians and fish have revealed the evolution of ‘cerebrotypes’ that reflect specific niches and/or clades. Here, we present the first demonstration of similar cerebrotypes in birds. Using principal component analysis and hierarchical clustering methods to analyze a data set of 67 species, we demonstrate that five main cerebrotypes can be recognized. One type is dominated by galliforms and pigeons, among other species, that all share relatively large brainstems, but can be further differentiated by the proportional size of the cerebellum and telencephalic regions. The second cerebrotype contains a range of species that all share relatively large cerebellar and small nidopallial volumes. A third type is composed of two species, the tawny frogmouth (Podargus strigoides) and an owl, both of which share extremely large Wulst volumes. Parrots and passerines, the principal members of the fourth group, possess much larger nidopallial, mesopallial and striatopallidal proportions than the other groups. The fifth cerebrotype contains species such as raptors and waterfowl that are not found at the extremes for any of the brain regions and could therefore be classified as ‘generalist’ brains. Overall, the clustering of species does not directly reflect the phylogenetic relationships among species, but there is a tendency for species within an order to clump together. There may also be a weak relationship between cerebrotype and developmental differences, but two of the main clusters contained species with both altricial and precocial developmental patterns. As a whole, the groupings do agree with behavioral and ecological similarities among species. Most notably, species that share similarities in locomotor behavior, mode of prey capture or cognitive ability are clustered together. The relationship between cerebrotype and behavior/ecology in birds suggests that future comparative studies of brain-behavior relationships will benefit from adopting a multivariate approach.

Relative Wulst volume is correlated with orbit orientation and binocular visual field in birds

In mammals, species with more frontally oriented orbits have broader binocular visual fields and relatively larger visual regions in the brain. Here, we test whether a similar pattern of correlated evolution is present in birds. Using both conventional statistics and modern comparative methods, we tested whether the relative size of the Wulst and optic tectum (TeO) were significantly correlated with orbit orientation, binocular visual field width and eye size in birds using a large, multi-species data set. In addition, we tested whether relative Wulst and TeO volumes were correlated with axial length of the eye. The relative size of the Wulst was significantly correlated with orbit orientation and the width of the binocular field such that species with more frontal orbits and broader binocular fields have relatively large Wulst volumes. Relative TeO volume, however, was not significant correlated with either variable. In addition, both relative Wulst and TeO volume were weakly correlated with relative axial length of the eye, but these were not corroborated by independent contrasts. Overall, our results indicate that relative Wulst volume reflects orbit orientation and possibly binocular visual field, but not eye size.

Neural specialization for hovering in hummingbirds: hypertrophy of the pretectal nucleus Lentiformis mesencephali.

Hummingbirds possess an array of morphological and physiological specializations that allow them hover such that they maintain a stable position in space for extended periods. Among birds, this sustained hovering is unique to hummingbirds, but possible neural specializations underlying this behavior have not been investigated. The optokinetic response (OKR) is one of several behaviors that facilitates stabilization. In birds, the OKR is generated by the nucleus of the basal optic root (nBOR) and pretectal nucleus lentiformis mesencephali (LM). Because stabilization during hovering is dependent on the OKR, we predicted that nBOR and LM would be significantly enlarged in hummingbirds. We examined the relative size of nBOR, LM, and other visual nuclei of 37 species of birds from 13 orders, including nine hummingbird species. Also included were three species that hover for short periods of time (transient hoverers; a kingfisher, a kestrel, and a nectarivorous songbird). Our results demonstrate that, relative to brain volume, LM is significantly hypertrophied in hummingbirds compared with other birds. In the transient hoverers, there is a moderate enlargement of the LM, but not to the extent found in the hummingbirds. The same degree of hypertrophy is not, however, present in nBOR or the other visual nuclei measured: nucleus geniculatus lateralis, pars ventralis, and optic tectum. This selective hypertrophy of LM and not other visual nuclei suggests that the direction‐selective optokinetic neurons in LM are critical for sustained hovering flight because of their prominent role in the OKR and gaze stabilization. J. Comp. Neurol. 500:211–221, 2007.

Purkinje Cell Compartmentation as Revealed by Zebrin II Expression in the Cerebellar Cortex of Pigeons (Columba livia)

Purkinje cells in the cerebellum express the antigen zebrin II (aldolase C) in many vertebrates. In mammals, zebrin is expressed in a parasagittal fashion, with alternating immunopositive and immunonegative stripes. Whether a similar pattern is expressed in birds is unknown. Here we present the first investigation into zebrin II expression in a bird: the adult pigeon (Columba livia). Western blotting of pigeon cerebellar homogenates reveals a single polypeptide with an apparent molecular weight of 36 kDa that is indistinguishable from zebrin II in the mouse. Zebrin II expression in the pigeon cerebellum is prominent in Purkinje cells, including their dendrites, somata, axons, and axon terminals. Parasagittal stripes were apparent with bands of Purkinje cells that strongly expressed zebrin II (+ve) alternating with bands that expressed zebrin II weakly or not at all (−ve). The stripes were most prominent in folium IXcd, where there were seven +ve/−ve stripes, bilaterally. In folia VI–IXab, several thin stripes were observed spanning the mediolateral extent of the folia, including three pairs of +ve/−ve stripes that extended across the lateral surface of the cerebellum. In folium VI the zebrin II expression in Purkinje cells was stronger overall, resulting in less apparent stripes. In folia II–V, four distinct +ve/−ve stripes were apparent. Finally, in folia I (lingula) and X (nodulus) all Purkinje cells strongly expressed zebrin II. These data are compared with studies of zebrin II expression in other species, as well as physiological and neuroanatomical studies that address the parasagittal organization of the pigeon cerebellum. J. Comp. Neurol. 501:619–630, 2007.

Evolutionary Divergence in Brain Size between Migratory and Resident Birds

Despite important recent progress in our understanding of brain evolution, controversy remains regarding the evolutionary forces that have driven its enormous diversification in size. Here, we report that in passerine birds, migratory species tend to have brains that are substantially smaller (relative to body size) than those of resident species, confirming and generalizing previous studies. Phylogenetic reconstructions based on Bayesian Markov chain methods suggest an evolutionary scenario in which some large brained tropical passerines that invaded more seasonal regions evolved migratory behavior and migration itself selected for smaller brain size. Selection for smaller brains in migratory birds may arise from the energetic and developmental costs associated with a highly mobile life cycle, a possibility that is supported by a path analysis. Nevertheless, an important fraction (over 68%) of the correlation between brain mass and migratory distance comes from a direct effect of migration on brain size, perhaps reflecting costs associated with cognitive functions that have become less necessary in migratory species. Overall, our results highlight the importance of retrospective analyses in identifying selective pressures that have shaped brain evolution, and indicate that when it comes to the brain, larger is not always better.

Do big-brained animals play more? Comparative analyses of play and relative brain size in mammals.

It has been hypothesized that play is more likely to be present in larger brained species. We tested this hypothesis in mammals using independent contrasts, a method that controls for phylogenetic relatedness. Comparisons across 15 orders revealed that the prevalence and complexity of play was significantly correlated with brain size, with larger brained orders having more playful species. Three orders, Rodentia, Marsupialia, and Primates, were used for within-order comparisons among species and, where possible, among families. The comparisons were not significant for rodents or primates, and those for marsupials yielded inconsistent results. Therefore, although a strong relationship is present at the highest taxonomic level of comparison, it diminishes or evaporates at lower level comparisons.

Is digital dexterity really related to corticospinal projections?: a re-analysis of the Heffner and Masterton data set using modern comparative statistics

Using a data set of 69 different mammalian species, Heffner and Masterton propose that the longer and deeper the fibres of the corticospinal tract, the greater an animals digital dexterity. Because of the effects that phylogeny may have upon the extant phenotype of a given species, however, data from a wide range of species can rarely be considered to represent fully independent data points. Using modern comparative statistics, which incorporate phylogenetic information, we reanalysed their data set such that the assumption of independence was not violated. If Heffner and Mastertons hypothesis is correct, then one would expect evidence of strong correlated evolution between corticospinal tract anatomy and digital dexterity once the effects of the phylogenetic relationships between the species in the data set have been removed. The results show that a distinct bias in the number of primate species sampled by Heffner and Masterton significantly affected their findings. Furthermore, once phylogeny has been taken into account, only the length of the corticospinal tract fibres showed a significant relationship with two out of the four behaviours analysed, digital dexterity and hand-eye coordination. Based upon our results we recommend the use of modern comparative statistics for synthesising neural structure and behaviour, rather than examining structure function relationships in an ahistorical context. It is also evident that there is a need for data on the length and depth of the corticospinal fibres for a greater range of species so that the relationship between the corticospinal tract structure and motor behaviour for mammals as a whole can be more readily interpreted.

Comparative analyses of the role of postnatal development on the expression of play fighting.

Whether it is that animals are young so that they can play, or whether it is that they play because they are young, play should be more prevalent in species that have a greater degree of postnatal development. This hypothesis is tested by comparative analyses within two mammalian orders (primates and muroid rodents) using independent contrasts. This technique can account for the relative degree of relatedness among the species. For both orders, the complexity or prevalence of play fighting is compared to the degree of prenatal development (neonatal weight/adult weight). In addition, the prevalence of play in primates is compared to prenatal brain development (neonatal brain weight/adult brain weight). Significant negative regressions show that 30% of the variance in the distribution of play in the rodents is accounted for by the degree of prenatal development of body size, and 60% of the variance in play in the primates is accounted for by prenatal brain growth. The findings are thus consistent with the prediction. Species with a greater proportion of their growth occurring postnatally play more and have more complex play than do species with more of their growth occurring prenatally.

The roles of phylogeny and sociality in the evolution of social play in muroid rodents

A composite index incorporating the frequency and structure (target, type of defence, etc.) of play fighting was used to compare the complexity of such play in 13 species of muroid rodents whose behaviour has been previously described. A phylogenetic comparison of the distribution of the complexity of play fighting revealed that relatedness did not predict complexity. The most likely pattern for the ancestral rodent was moderate levels of complexity, from which increases or decreases in complexity then appeared to have evolved independently, at the level of subfamily and genus. Given that phylogeny did not predict the distribution of the pattern of play fighting, an alternative hypothesis was tested. That is, that instead, the distribution was produced by species differences in sociality, as reflected by the degrees of male-female association amongst adults. The analysis revealed that play complexity was unrelated to species differences in sociality, with both highly social and relatively asocial species being equally likely to have high or low levels of play complexity. The implications of these results for the evolution of mammalian play are considered. Copyright 1999 The Association for the Study of Animal Behaviour.