Patterns of shape diversification
Because we set boundaries for each brain region on the basis of appearance of the endocast (Fig. 1), our definition of brain regions does not completely coincide with that of external histological boundaries of the brain. Therefore, notably, the observed changing patterns in these regions observed in this study are an ‘apparent’ pattern. Although the boundaries used in this study did not completely coincide with the histological boundaries, it is considered that the definition of brain regions adopted here is adequate to explore the external shape variation in the avian brain.
Our results indicate that a considerable amount of shape diversity found in the brains of modern Aves can be described by a small number of dimensions using PCA (Figs 2,3 and 5). Two main trends of concerted changes were observed both in unadjusted and size-adjusted PCA: (i) expansion or shrinking of the telencephalon; and (ii) elongation or shortening of the brain base and brain stem. Accordingly, expansion of the telencephalon and shortening of the brain base and brain stem led to a rounder and more upward brain orientation (posture), while shrinking the telencephalon and elongation of the brain base and brain stem led to a more elongated and anteriorly inclined brain. Duijm (1951) and Marugán-Lobón & Buscalioni (2006, 2009) reported that the angle of the brain base correlated with the orientation of the plane of the foramen magnum in the avian skull. These trends in shape change revealed by previous studies are generally consistent with our results. The anterior part of the telencephalon extends anteroventrally with decreasing PC1 and PC2 scores in unadjusted and size-adjusted PCA. Stingelin (1957) recognized two directions of telencephalic development: (i) basal–frontal development; and (ii) dorsal–frontal development. With dorsal–frontal development, the eminentia sagittalis (Wulst) extends to the rostral part of the telencephalon, while with basal–frontal development, the position of the eminentia sagittalis is largely unaltered and it remains in the rostral part of the telencephalon. Anteroventral extension of the telencephalon (i.e. Phalacrocorax, Gallus, Anseriformes, Ciconiiformes and many water birds), which was recognized by PCA, coincides with dorsal–frontal development. On the other hand, rounded telencephalons (−PC1 and −PC2; i.e. Corvus, Falco, Strix and Columbiformes) match basal–frontal development. Thus, the mode of telencephalon development is an important factor determining the variation in avian brain shape. The developmental mode of the eminentia sagittalis is consistent within avian orders (Stingelin, 1957), suggesting that the avian brain shape and the developing mode of telencephalon have been coevolved. It seems that the rounded upwardly tilted brain of taxa such as Passeriformes, Falconiformes and Strigiformes has been evolved with the basal–frontal development, while Psittaciformes closely related with Passeriformes and Falconiformes shows a different shape of brain – upward tilted flat brain. It would appear that the brain shape of Psittaciformes has had a unique experience of evolution as compared with passeriform and falconiform birds.
Multivariate regression analysis suggested that expansion of the telencephalon and caudodorsal rotation of the posterior part of the brain correlates strongly with increasing brain size (Fig. 4). Allometric changes in brain shape were related to the slenderness of the brain and the degree of rotation. The rotation of brain causes a dramatic change of the relative position between the brain and lateral semicircular canal. In general, allometric shape changes appeared to generally correspond with positive changes in unadjusted PC1 and PC2, and negative changes in PC3. The roundness or slenderness of the avian brain is related to skull shape (Duijm, 1951; Dullemeijer, 1960; Marugán-Lobón & Buscalioni, 2006); therefore, the allometric shape changes also relate to skull shape. In fact, skull shape is also subject to change with increased size (Kulemeyer et al. 2009; Marugán-Lobón & Buscalioni, 2009).
Because some proportion of the variation in brain shape (8.81%) was explained by the brain size in unadjusted PCA, the effects of size on brain shape must be removed to understand the shape changes in the avian brain.
Using size-adjusted data sets, which were also adjusted for phylogeny, the consistent shape change correlations were found between three region pairs, the telencephalon and cerebellum, the diencephalon and optic tectum, and the cerebellum and myelencephalon (Fig. 2). Although the telencephalon and diencephalon might also show a weak shape correlation, this was not detected by our analysis. Iwaniuk et al. (2004) reported that the volumes of the following region pairs were consistently correlated in the avian brain: telencephalon and diencephalon; diencephalon and optic tectum; mesencephalon and optic tectum; and cerebellum and myelencephalon (‘mosaic brain evolution’: Iwaniuk et al. 2004; Striedter, 2005; Charvet & Striedter, 2009a,b). Their volumetric results are generally consistent with our shape analysis results. Specifically, both volumetric and shape analyses suggest mosaic brain evolution in birds. That is, it may be said that brain regions that share connections as part of the same functional pathway tend to covary in shape, while regions that differ in function change shape independently. However, there is a correlation in shape changes between the telencephalon, cerebellum and brain stem. Although they share few substantial neuronal connections (Iwaniuk et al. 2004), expansion of the telencephalon pushed the cerebellum posteriorly, causing the brain stem to rotate ventrorostrally in all PCs. This concerted shape change among the telencephalon, cerebellum and brain stem was caused mainly by the structural restriction than the strength of the neuronal connection. The strength of the neuronal connection is a dominant regulator of the brain shape, but location or structural constraints among each brain region also play a major role in determining the brain shape in Aves. However, it must be noted that geometric morphometrics pictures only the shape (not size) change of brains. Hence, it requires a much more detailed theoretical development of the method using geometric morphometrics to discuss mosaic brain evolution more clearly and precisely.
The brain with an expanded telencephalon (size-adjusted negative PC1, PC2, positive PC3, and non-size-adjusted negative PC1) had a relatively small optic tectum, cerebellum and myelencephalon in proportion to the whole brain. Hence, it is known that the brain with a larger telencephalon is highly encephalized (Iwaniuk et al. 2005), a large telencephalon correlates with an increase in relative brain volume. Iwaniuk et al. (2005) reported that psittaciforms and passerines whose telencephalon is significantly larger than that of other birds have a relatively smaller mesencephalon, optic tectum, cerebellum and myelencephalon than non-passerines. We clarified that the apparent size of the brain regions changes according to the degree of encephalization, and this finding corroborates the volumetric result of Iwaniuk et al. (2005). That is, encephalization is reflected in the brain shape of birds.
In addition, as described above, the brain with a large telencephalon (size-adjusted negative PC1, PC2, positive PC3 and non-size-adjusted negative PC1) tends to have a short cranial base (brain base), and this makes the brain ventrally flexed, which means that the anterior cranial base largely flexes ventrally. In other words, there is a correlation observed between cranial base angulation and encephalization in birds. This phenomenon has been previously reported in birds (Marugán-Lobón, 2010). A more ventrally flexed cranial base helps to accommodate a large brain volume in mammals (Biegert, 1963; Gould, 1977; Ross & Ravosa, 1993; Lieberman et al. 2008), and the flexion of the cranial base is a phenomenon common to both mammals and birds.
Covariation between brain shape and orbital shape
Only a small proportion of the variation in brain shape was explained by brain size, leaving approximately 90% of variance unexplained. Subsequent 2B-PLS analysis indicated that orbital shape can explain a significant proportion of the remaining variation in brain shape. Indeed, brain shape strongly correlated with orbital shape (Fig. 6). Thus, birds with a negative brain shape (narrower brains) have relatively elongated orbits, while birds with a positive brain shape (rounder, ventrally flexed) have relatively round orbits (Fig. 6). In addition, elongated orbits are more anterior in the skull while rounder orbits are posterolateral. Because the vertebrate retina is ontogenetically a part of the brain, the optic nerve is regarded as a central tract and the tectum as a coordinating or distributing center between other brain centers (Johnston, 1902). Thus, the anteroposterior elongation and contraction of the orbit is considered to be related to the change in length of the optic nerve or the relative position of the eyeball. This indicates that in rounder brains, the center of gravity lies above and nearer to the neck, while in narrower brains, the center of gravity is more anterior. Birds with narrow brains and elongated, anterior orbits (concentrated in the lower left in Fig. 6a) belong to ‘the straight skull type’ (Duijm, 1951), with relatively longer bills and a medulla that extends in the posterior direction. Duijm (1951) suggested that the skull and bill of birds of the straight skull type lie in line with the neck. The large shape change in the orbits stems largely from the major shift in the lacrimal bone, and this shift changes the direction of the viscerocranium and/or skull. The rounded orbits accompany the short and more ventrally tilted bill, whereas the bill with elongated orbits extends in a horizontal direction. Thus, brain shape may also be affected by head posture. In addition, Kulemeyer et al. (2009) noted a possible link between the position of foramen magnum and head posture, and suggested a correlation between head posture and the ability for sustained flight. Thus, brain shape may be affected by brain size, orbital shape and flight behavior.
Because the eye is a part of the brain, the eye is also considered to be a module of the brain. Thus, understanding the relationship between the optic organ and brain components sheds light on the evolution of the brain shape in birds. Changes in brain shape expressed by covariance are almost identical to those expressed by unadjusted PC1. Because unadjusted PC1 explained the greatest proportion of the variation in avian brain shape, it can also be assumed that orbital shape considerably affects brain shape. There is also a possibility that the pattern of telencephalon development (Stingelin, 1957) correlates with the orbital shape, i.e. a brain with a relatively rostroventrally situated eminentia saggitalis (involved in integration and processing of the visual signal; Iwaniuk & Wylie, 2006) is associated with the more posterolaterally situated round orbit. In fact, the roofs of both hemispheres of the telencephalon showed the biggest change according to the PLS axis change (Fig. 6), and these parts corresponded to the position of the eminentia sagittalis. In other words, the shape or size of the eminentia sagittalis changes with the orbital shape. These orbital and telencephalic changes correlate with an integrated change in the brain shape, such as ventrodorsal rotation of the cerebellum and myelencephalon.
Compared with body and cranial sizes, birds have relatively large eyes because vision is the predominant sensory modality. Birds also have relatively large brains to process visual input. Several studies have shown a significant correlation between brain size and eye size (Garamszegi et al. 2002; Thomas et al. 2006; Burton, 2008), and one study has speculated a complex interdependence of eye size or shape, skull shape, and brain shape (Dubbeldam, 1989). Thus, the structure of the avian brain is strongly influenced by eye size and shape, and it is significant that this study shows a clear quantitative relationship between brain shape and orbital shape. In light of recent studies showing a correlation between eye size and behavior (Brooke et al. 1999; Garamszegi et al. 2002; Thomas et al. 2006; Hall, 2008; Hall & Heesy, 2011), the present study results may lead to a better understanding of brain shape evolution and the relationship between eye shape and behavior.
The cranial base angle covaried with the shape change of the orbits. Brains with a more ventrally flexed cranial base (positive PLS1; Fig. 5) had more anteroposteriorly shorter orbits than those with a more dorsally flexed cranial base. In the case of mammals, cranial base angulation is closely related to brain size and facial length (Moss & Young, 1960; Biegert, 1963; Ross & Ravosa, 1993; Ross & Henneberg, 1995; Lieberman, 1998; Lieberman et al. 2000a,b; McCarthy & Lieberman, 2001; Ross et al. 2004; Bastir & Rosas, 2006; Bastir et al. 2006). Architecturally, the cranial base provides growth space for the brain and face. Hence, cranial base angulation also results in variation in facial prognathism and orientation (Ashton, 1957; Biegert, 1963). The cranial base may help accommodate the spatial packing of the face in mammals. As is the case of the mammalian face, the avian orbit is also lengthened according to the angulation of the cranial base. The face is the prime component of the mammalian skull and influences the entire skull shape, whereas the eyes are the prime component of the avian skull. Considering that the mammalian face and avian orbit are the important components of the viscerocranium, the cranial base angulation may also play an important role in the spatial packing in the avian viscerocranium.