Kara E. Yopak

Variation in brain organization and cerebellar foliation in chondrichthyans: Sharks and holocephalans

The widespread variation in brain size and complexity that is evident in sharks and holocephalans is related to both phylogeny and ecology. Relative brain size (expressed as encephalization quotients) and the relative development of the five major brain areas (the telencephalon, diencephalon, mesencephalon, cerebellum, and medulla) was assessed for over 40 species from 20 families that represent a range of different lifestyles and occupy a number of habitats. In addition, an index (1–5) quantifying structural complexity of the cerebellum was created based on length, number, and depth of folds. Although the variation in brain size, morphology, and complexity is due in part to phylogeny, as basal groups have smaller brains, less structural hypertrophy, and lower foliation indices, there is also substantial variation within and across clades that does not reflect phylogenetic relationships. Ecological correlations, with the relative development of different brain areas as well as the complexity of the cerebellar corpus, are supported by cluster analysis and are suggestive of a range of ‘cerebrotypes’. These correlations suggest that relative brain development reflects the dimensionality of the environment and/or agile prey capture in addition to phylogeny.

A conserved pattern of brain scaling from sharks to primates

Several patterns of brain allometry previously observed in mammals have been found to hold for sharks and related taxa (chondrichthyans) as well. In each clade, the relative size of brain parts, with the notable exception of the olfactory bulbs, is highly predictable from the total brain size. Compared with total brain mass, each part scales with a characteristic slope, which is highest for the telencephalon and cerebellum. In addition, cerebellar foliation reflects both absolute and relative cerebellar size, in a manner analogous to mammalian cortical gyrification. This conserved pattern of brain scaling suggests that the fundamental brain plan that evolved in early vertebrates permits appropriate scaling in response to a range of factors, including phylogeny and ecology, where neural mass may be added and subtracted without compromising basic function.

Brain organization and specialization in deep-sea chondrichthyans.

Chondrichthyans occupy a basal place in vertebrate evolution and offer a relatively unexplored opportunity to study the evolution of vertebrate brains. This study examines the brain morphology of 22 species of deep-sea sharks and holocephalans, in relation to both phylogeny and ecology. Both relative brain size (expressed as residuals) and the relative development of the five major brain areas (telencephalon, diencephalon, mesencephalon, cerebellum, and medulla) were assessed. The cerebellar-like structures, which receive projections from the electroreceptive and lateral line organs, were also examined as a discrete part of the medulla. Although the species examined spanned three major chondrichthyan groupings (Squalomorphii, Galeomorphii, Holocephali), brain size and the relative development of the major brain areas did not track phylogenetic groupings. Rather, a hierarchical cluster analysis performed on the deep-sea sharks and holocephalans shows that these species all share the common characteristics of a relatively reduced telencephalon and smooth cerebellar corpus, as well as extreme relative enlargement of the medulla, specifically the cerebellar-like lobes. Although this study was not a functional analysis, it provides evidence that brain variation in deep-sea chondichthyans shows adaptive patterns in addition to underlying phylogenetic patterns, and that particular brain patterns might be interpreted as ‘cerebrotypes’.

Neuroecology of cartilaginous fishes: the functional implications of brain scaling

It is a widely accepted view that neural development can reflect morphological adaptations and sensory specializations. The aim of this review is to give a broad overview of the current status of brain data available for cartilaginous fishes and examine how perspectives on allometric scaling of brain size across this group of fishes has changed within the last 50 years with the addition of new data and more rigorous statistical analyses. The current knowledge of neuroanatomy in cartilaginous fishes is reviewed and data on brain size (encephalization, n = 151) and interspecific variation in brain organization (n = 84) has been explored to ascertain scaling relationships across this clade. It is determined whether similar patterns of brain organization, termed cerebrotypes, exist in species that share certain lifestyle characteristics. Clear patterns of brain organization exist across cartilaginous fishes, irrespective of phylogenetic grouping and, although this study was not a functional analysis, it provides further evidence that chondrichthyan brain structures might have developed in conjunction with specific behaviours or enhanced cognitive capabilities. Larger brains, with well-developed telencephala and large, highly foliated cerebella are reported in species that occupy complex reef or oceanic habitats, potentially identifying a reef-associated cerebrotype. In contrast, benthic and benthopelagic demersal species comprise the group with the smallest brains, with a relatively reduced telencephalon and a smooth cerebellar corpus. There is also evidence herein of a bathyal cerebrotype; deep-sea benthopelagic sharks possess relatively small brains and show a clear relative hypertrophy of the medulla oblongata. Despite the patterns observed and documented, significant gaps in the literature have been highlighted. Brain mass data are only currently available on c. 16% of all chondrichthyan species, and only 8% of species have data available on their brain organization, with far less on subsections of major brain areas that receive distinct sensory input. The interspecific variability in brain organization further stresses the importance of performing functional studies on a greater range of species. Only an expansive data set, comprised of species that span a variety of habitats and taxonomic groups, with widely disparate behavioural repertoires, combined with further functional analyses, will help shed light on the extent to which chondrichthyan brains have evolved as a consequence of behaviour, habitat and lifestyle in addition to phylogeny.

Variation in brain organization and cerebellar foliation in chondrichthyans: batoids.

Interspecific variation in relative brain size (encephalization), the relative size of the five major brain areas (the telencephalon, diencephalon, mesencephalon, cerebellum, and medulla) and the level of cerebellar foliation was assessed in over 20 representative species of batoid (skates and rays), from eight families. Using species as independent data points and phylogenetically independent contrasts, relationships among each of the neuroanatomical variables and two ecological variables, habitat and lifestyle, were assessed. Variation in relative brain size and brain organization appears to be strongly correlated with phylogeny. Members of the basal orders Rajiformes and Torpediniformes tend to have relatively small brains, with relatively small telencephalons, large medullas, and smooth, unfoliated cerebellums. More advanced Myliobatiformes possess relatively large brains, with relatively large telencephalons, small medullas, and complex, heavily foliated cerebellums. Increased brain size, telencephalon size, and cerebellar foliation also correlate with living in a complex habitat (such as in association with coral reefs) and an active, benthopelagic lifestyle, but as primary habitat and lifestyle also closely match phylogenetic relationships in batoids, it is difficult to separate the influence of phylogeny and ecological factors on brain organization in these animals. However, the results of two forms of multivariate analysis (principal component analysis and cluster analysis) reveal that certain species are clustered with others that share ecological traits, rather than with more closely related species from the same order. This suggests that ecological factors do play a role in defining patterns of brain organization and there is some evidence for ‘cerebrotypes’ in batoids.

The Cerebellum and Cerebellum-Like Structures of Cartilaginous Fishes

The cerebellum is well developed in cartilaginous fishes, with the same cell types (barring basket cells) and organizational features found in other vertebrate groups, including mammals. In particular, the lattice-like organization of cerebellar cortex (with a molecular layer of parallel fibers, interneurons, spiny Purkinje cell dendrites, and climbing fibers) is a defining characteristic. In addition to the cerebellum, cartilaginous fishes have cerebellum-like structures in the dorsolateral wall of the hindbrain. These structures are adjacent to and, in part, contiguous with the cerebellum. They are cerebellum-like in that they have a molecular layer of parallel fibers and inhibitory interneurons that has striking organizational similarities to the molecular layer of the cerebellar cortex. However, these structures also have characteristics that differ from the cerebellum. For example, cerebellum-like structures do not have climbing fibers and are clearly sensory. They receive direct afferent input from peripheral sensory receptors and relay their outputs to midbrain sensory areas. As a consequence of this close sensory association and the ability of researchers to characterize signal processing in these structures in a behaviorally relevant context, good progress has been made in determining the fundamental processing algorithm of the cerebellum-like structures. This algorithm enables the molecular layer to act as an adaptive filter that cancels self-generated noise in electrosensory and lateral line systems. Given the fundamental similarities of the molecular layer across these structures and the phylogeny of these structures across basal vertebrates, it is clear that these structures share a common genetic-developmental program. Syngeny is a term that has been used to describe similarity of structure due to a shared genetic-developmental program, whether the structures are phylogenetically homologous or not. Given that the cerebellum and cerebellum-like structures are physically adjacent, we propose that cerebellum-like structures were the evolutionary antecedent of the cerebellum and that the cerebellum arose through a change in the genetic-developmental program, amounting to a duplication of existing structure. Such duplication to form adjacent structures can be considered a special case of syngeny. On this view, the cerebellum is an evolutionary innovation in gnathostomes that is literally superimposed on pre-existing underlying brain structures and pathways. From this perspective, the cerebellum can be considered an example of ‘subsumption architecture’, a term that describes the addition of modules that add computational power while maintaining existing fundamental functionality. This addition is reflected in the finding that in elasmobranchs with relatively large brains, the size of the telencephalon and cerebellum enlarge disproportionately, while those parts of the brain that contain more direct sensory and motor connections do not. Added ‘computational’ power in the chondrichthyan brain and the comparative function and evolution of the cerebellum and cerebellum-like structures across the cartilaginous fishes supports the idea of the cerebellum as an example of subsumption architecture.

Brain Size and Brain Organization of the Whale Shark, Rhincodon typus, Using Magnetic Resonance Imaging

Very little is known about the brain organization of the suction filter feeder, Rhincodon typus, and how it compares to other orectolobiforms in light of its specialization as a plankton-feeder. Brain size and overall brain organization was assessed in two specimens of R. typus in relation to both phylogeny and ecology, using magnetic resonance imaging (MRI). In comparison to over 60 other chondrichthyan species, R. typus demonstrated a relatively small brain for its body size (expressed in terms of encephalization quotients and residuals), similar to the lamniforms Carcharodon carcharias, Cetorhinus maximus, and Carcharias taurus. R. typus possessed a relatively small telencephalon with some development of the dorsal pallium, which was suggestive of moderate social behavior, in addition to a relatively large diencephalon and a relatively reduced mesencephalon. The most notable characteristic of the brain of Rhincodon was a large and highly foliated cerebellum, one of the largest cerebellums within the chondrichthyan clade. Early development of the brain was qualitatively assessed using an in situ MRI scan of the brain and chondrocranium of a neonate specimen of R. typus. There was evidence that folding of the cerebellar corpus appeared in early development, although the depth and number of folds might vary ontogenetically in this species. Hierarchical cluster analysis and multidimensional scaling ordinations showed evidence of convergent evolution with the basking shark, Cetorhinus maximus, another large-bodied filter feeding elasmobranch, supporting the claim that organization of the brain is more similar in species with analogous but independently evolved lifestyles than those that share taxonomic classification.

Not all sharks are “swimming noses”: variation in olfactory bulb size in cartilaginous fishes

Olfaction is a universal modality by which all animals sample chemical stimuli from their environment. In cartilaginous fishes, olfaction is critical for various survival tasks including localizing prey, avoiding predators, and chemosensory communication with conspecifics. Little is known, however, about interspecific variation in olfactory capability in these fishes, or whether the relative importance of olfaction in relation to other sensory systems varies with regard to ecological factors, such as habitat and lifestyle. In this study, we have addressed these questions by directly examining interspecific variation in the size of the olfactory bulbs (OB), the region of the brain that receives the primary sensory projections from the olfactory nerve, in 58 species of cartilaginous fishes. Relative OB size was compared among species occupying different ecological niches. Our results show that the OBs maintain a substantial level of allometric independence from the rest of the brain across cartilaginous fishes and that OB size is highly variable among species. These findings are supported by phylogenetic generalized least-squares models, which show that this variability is correlated with ecological niche, particularly habitat. The relatively largest OBs were found in pelagic-coastal/oceanic sharks, especially migratory species such as Carcharodon carcharias and Galeocerdo cuvier. Deep-sea species also possess large OBs, suggesting a greater reliance on olfaction in habitats where vision may be compromised. In contrast, the smallest OBs were found in the majority of reef-associated species, including sharks from the families Carcharhinidae and Hemiscyllidae and dasyatid batoids. These results suggest that there is great variability in the degree to which these fishes rely on olfactory cues. The OBs have been widely used as a neuroanatomical proxy for olfactory capability in vertebrates, and we speculate that differences in olfactory capabilities may be the result of functional rather than phylogenetic adaptations.

A novel method for comparative analysis of retinal specialization traits from topographic maps

Vertebrates possess different types of retinal specializations that vary in number, size, shape, and position in the retina. This diversity in retinal configuration has been revealed through topographic maps, which show variations in neuron density across the retina. Although topographic maps of about 300 vertebrates are available, there is no method for characterizing retinal traits quantitatively. Our goal is to present a novel method to standardize information on the position of the retinal specializations and changes in retinal ganglion cell (RGC) density across the retina from published topographic maps. We measured the position of the retinal specialization using two Cartesian coordinates and the gradient in cell density by sampling ganglion cell density values along four axes (nasal, temporal, ventral, and dorsal). Using this information, along with the peak and lowest RGC densities, we conducted discriminant function analyses (DFAs) to establish if this method is sensitive to distinguish three common types of retinal specializations (fovea, area, and visual streak). The discrimination ability of the model was higher when considering terrestrial (78%-80% correct classification) and aquatic (77%-86% correct classification) species separately than together. Our method can be used in the future to test specific hypotheses on the differences in retinal morphology between retinal specializations and the association between retinal morphology and behavioral and ecological traits using comparative methods controlling for phylogenetic effects.

Allometric Scaling of the Optic Tectum in Cartilaginous Fishes

In cartilaginous fishes (Chondrichthyes; sharks, skates and rays (batoids), and holocephalans), the midbrain or mesencephalon can be divided into two parts, the dorsal tectum mesencephali or optic tectum (analogous to the superior colliculus of mammals) and the ventral tegmentum mesencephali. Very little is known about interspecific variation in the relative size and organization of the components of the mesencephalon in these fishes. This study examined the relative development of the optic tectum and the tegmentum in 75 chondrichthyan species representing 32 families. This study also provided a critical assessment of attempts to quantify the size of the optic tectum in these fishes volumetrically using an idealized half-ellipsoid approach (method E), by comparing this method to measurements of the tectum from coronal cross sections (method S). Using species as independent data points and phylogenetically independent contrasts, relationships between the two midbrain structures and both brain and mesencephalon volume were assessed and the relative volume of each brain area (expressed as phylogenetically corrected residuals) was compared among species with different ecological niches (as defined by primary habitat and lifestyle). The relatively largest tecta and tegmenta were found in pelagic coastal/oceanic and oceanic sharks, benthopelagic reef sharks, and benthopelagic coastal sharks. The smallest tecta were found in all benthic sharks and batoids and the majority of bathyal (deep-sea) species. These results were consistent regardless of which method of estimating tectum volume was used. We found a highly significant correlation between optic tectum volume estimates calculated using method E and method S. Taxon-specific variation in the difference between tectum volumes calculated using the two methods appears to reflect variation in both the shape of the optic tectum relative to an idealized half-ellipsoid and the volume of the ventricular cavity. Because the optic tectum is the principal termination site for retinofugal fibers arising from the retinal ganglion cells, the relative size of this brain region has been associated with an increased reliance on vision in other vertebrate groups, including bony fishes. The neuroecological relationships between the relative size of the optic tectum and primary habitat and lifestyle we present here for cartilaginous fishes mirror those established for bony fishes; we speculate that the relative size of the optic tectum and tegmentum similarly reflects the importance of vision and sensory processing in cartilaginous fishes.