Head size constrains forebrain development and evolution in ray‐finned fishes

Abstract

SUMMARY In ray‐finned fishes, which comprise nearly half of all vertebrate species, the telencephalon does not evaginate, as it does in other vertebrates, but instead everts. No detailed explanation for this species difference has ever been offered. Here we propose that telencephalic eversion evolved because ray‐finned fish embryos are so small that their telencephalon cannot evaginate but must, instead, squeeze into the space just dorsal to the developing nasal epithelia and rostral to the eyes—morphogenetic movements that amount to eversion. Evidence for this hypothesis derives from cladistic analyses, which show that early ray‐finned fishes reduced their adult body size and adopted a novel reproductive strategy, based on the production of myriad minute young. Because body size tends to be inversely proportional to brain:body ratio, this phylogenetic reduction in body size implies that embryonic ray‐finned fishes should have proportionately larger brains than embryos of species whose telencephalons evaginate. This prediction was confirmed by comparing serially sectioned heads of representative ray‐finned and cartilaginous fish embryos at several stages of development. The brain, excluding its ventricles, occupies 36–46% of the cranial cavity in embryonic ray‐finned fishes, but less than 20% in embryonic sharks. Moreover, three‐dimensional reconstructions show that in embryonic ray‐finned fishes the telencephalon has no room for a full‐fledged evagination; instead, it spreads into the spaces just dorsal and caudal to the developing nasal epithelia. These morphogenetic movements, in conjunction with a thinning of the forebrain roof, generate telencephalic eversion.