Variation in Brain Organization and Cerebellar Foliation in Chondrichthyans: Batoids

Abstract

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.

Does more maternal investment mean a larger brain? Evolutionary relationships between reproductive mode and brain size in chondrichthyans

“…Data on brain weight and bodyweight for 85 chondrichthyan species were obtained from previously published studies (Northcutt 1977(Northcutt , 1978Kruska 1988;Ito et al 1999;Yopak et al 2007;Lisney et al 2008;Yopak and Montgomery 2008;Yopak and Frank 2009). Data on reproductive mode were collected from published literature (Dulvy and Reynolds 1997;Last and Stevens 2009) and each species was categorised into one of two reproductive modes, namely lecithotrophic or matrotrophic ( Fig.…”

“…litter size, gestation or incubation length). In chondrichthyans, the relative size of most major brain areas, including the telencephalon and cerebellum, are highly predictable from the overall brain size (Yopak et al 2007(Yopak et al , 2010Lisney et al 2008;Yopak and Montgomery 2008), potentially owing to a conserved order of neurogenesis (Yopak et al 2010), as documented in other vertebrates (Finlay and Darlington 1995;Finlay et al 1998Finlay et al , 2001). The telencephalon and cerebellum, in particular, enlarge disproportionately as the absolute brain size increases in chondrichthyans and scale similarly to the neocortex and cerebellum of mammals (Yopak et al 2010), brain areas that have been shown to continue neurogenesis longest through early development in mammals (Finlay and Darlington 1995;Yopak et al 2010).…”

“…Relative brain size and the relative development of major brain areas have been correlated with ecology (i.e. habitat type, feeding mode), and these patterns do not necessarily follow phylogenetic groupings (Yopak et al 2007;Lisney et al 2008;Yopak and Montgomery 2008;Yopak and Frank 2009), similar to patterns seen in other vertebrates, such as teleosts, birds and mammals (Huber et al 1997;Kotrschal et al 1998;de Winter and Oxnard 2001). There is some evidence that reproductive mode may be correlated with variation in brain size and organisation; the sharks with placental viviparity, such as the Carcharhinidae and Sphyrnidae, have among the largest relative brain sizes within chondrichthyans (Yopak et al 2007), although this has not as yet been statistically tested.…”

A conserved pattern of brain scaling from sharks to primates

“…These data are visualized as a regression against either total brain mass or the medulla, which allows the easiest visual comprehension of the data structure (not identical to the inferential statistical analysis, as detailed in SI Materials and Methods). SI Materials and Methods also provides details of the brain divisions, explanations of how data were collected from original reports (16)(17)(18)(19)(20) and how new data on the mass of the olfactory bulbs were collected in a subset of these species, and the phylogenetic relationships of the chondrichthyans used for independent contrast analyses.Here we present five major analyses. First, we explore covariation in the volume of brain parts by factor analysis.…”

“…As a group, these species sit closer to the first divergence of vertebrates, where multiple solutions to fundamental adaptive problems might have emerged and been stabilized, with mammals representing only one branch of this early tree. Chondrichthyans occupy a wide range of aquatic niches (14), have an extremely wide range of body size (15), and exhibit substantial variations in brain size and brain organization (16)(17)(18)(19)(20)(21). Because neurons are generated widely within the fish brain throughout life (22,23), engagement of neurogenesis in some aspect of later life history, which is not a major factor in mammals, also might alter numerical relationships established in early development (24).…”