Neuroecology of cartilaginous fishes: the functional implications of brain scaling

Abstract

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.

The Cerebellum and Cerebellum-Like Structures of Cartilaginous Fishes

“…Output neurons from both the MON and the DON project to the contralateral midbrain. Interestingly, cartilaginous fishes with purported greater reliance on these non-visual octavolateralis senses have relatively enlarged MON and DON in comparison to other chondrichthyan species [Yopak et al, 2007;Yopak and Montgomery, 2008;Kajiura et al, 2010;Yopak, 2012], as described in later sections. …”

“…Currently, the primary literature contains brain-body data on approximately 16% of all known chondrichthyan species, and even fewer data on the development of major brain regions [reviewed by Yopak, 2012]. Analyses of brain-body scaling have demonstrated that chondrichthyans have relative brain sizes that are comparable to birds and mammals [Northcutt, 1977;Myagkov, 1991;Striedter, 2005;Yopak et al, 2007Yopak et al, , 2010a and that cartilaginous fishes possess larger brains than teleosts of similar body size [Striedter, 2005].…”

“…9 ). This neuromorphological pattern has been attributed to a number of factors, including specialization of the octavolateralis senses , somatotopic mapping of subdermal electroreceptors Kajiura et al, 2010], which extend down the elongated rostrum of deep sea sharks and holocephalans, and an increased selection pressure for sensitivity to novel stimuli via sensory adaptive filtering in prey-poor and conspecific-poor deep sea environments [for review, see Yopak, 2012].…”

“…We will also review the recent progress that has been made describing and analyzing the variation in the cerebellum and cerebellum-like structures across the cartilaginous fishes [Northcutt, 1978;Yopak et al, 2007;Yopak, 2012]. How does the evolution of these structures within the clade relate to phylogenetic and ecological patterns?…”

The Neuroecology of Cartilaginous Fishes: Sensory Strategies for Survival

“…Recent reviews on the sensory biology of cartilaginous fishes [Hueter et al, 2004;Gardiner et al, 2012], including vision [Hart et al, 2006;Lisney et al, 2012], electroreception Collin, 2010;Kempster et al, 2012], gustation [Tester, 1963;Atkinson and Collin, 2010], hearing [Myrberg, 2001;Hueter et al, 2004;Gardiner et al, 2012], and the central nervous system [Yopak, 2012] are also excellent resources for more detailed information about technical aspects of studying sensory systems in cartilaginous fishes.…”