Brain Organization and Specialization in Deep-Sea Chondrichthyans

Abstract

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’.

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).…”