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.
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.T he allometric relationship of brain parts to overall brain size has been studied and debated extensively (1-7). At the core of the debate lies the question of whether the brain is best characterized as a collection of independently varying structures/devices evolved for particular behavioral requirements or niches or as a single coordinated processing structure/device in which adaptation for species-specific behavioral capacities occurs without the production of delineable modules (8, 9). Many methodological issues have arisen as well, including what about a brain should be quantified [cells or volumes (10)], what should be compared and how, and how to take into account the statistical dependence of both structural and species relationships (11).Until recently, a single data corpus comprising primates, bats, and insectivorous mammals was the sole source for comparison (2), leaving the question of whether these mammals represented all vertebrates, or even all other mammals, unresolved. The addition of carnivorous mammals (including marine mammals), ungulates, xenarthrans, and the manatee demonstrated that the original conclusions drawn from primates, bats, and insectivores could be extended to this larger data set (8, 12). These studies revealed that mammalian brain structure exhibits a pattern of variation containing two principal components. The first component, accounting for ≈96% of the total variance of related brain parts to total brain size, loads most highly on neocortex and cerebellum. The second component loads most highly on the olfactory bulb and associated limbic structures and accounts for ≈3% of the original variance. Each brain part also has a characteristic slope with respect to absolute brain size, such that every large mammalian brain is composed disproportionately of neocortex and cerebellum. The remaining 1% of the variance must subsume all remaining sources, including niche, sex and individual differences, and measurement error. This 1% contribution is large in one sense: In two species with the same brain size, a single structure might differ by a factor of 2.5. The total range of structure sizes may differ by a factor of 100,000 or more b...
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.
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.
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’.
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.
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.
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