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

Area of Science:

• Developmental Biology
• Evolutionary Biology
• Comparative Neuroscience

Background:

• Ray-finned fishes, comprising ~50% of vertebrate species, display unique telencephalon development (eversion) unlike other vertebrates (evagination).
• The evolutionary and developmental reasons for this difference remain unexplained.

Purpose of the Study:

• To propose and provide evidence for the hypothesis that telencephalic eversion in ray-finned fishes is an adaptation to small embryonic size.
• To explain the morphogenetic basis of telencephalic eversion in ray-finned fish embryos.

Main Methods:

• Cladistic analyses to infer evolutionary history of body size and reproduction in early ray-finned fishes.
• Comparative analysis of serially sectioned embryonic heads from ray-finned and cartilaginous fishes.
• Three-dimensional reconstructions of embryonic ray-finned fish brains.

Main Results:

• Phylogenetic reduction in body size in early ray-finned fishes correlates with increased brain:body ratio.
• Embryonic ray-finned fish brains occupy a significantly larger portion (36-46%) of the cranial cavity compared to embryonic sharks (<20%).
• Telencephalon morphology in ray-finned fish embryos demonstrates a lack of space for evagination, leading to spreading into adjacent cranial spaces, resulting in eversion.

Conclusions:

• Telencephalic eversion in ray-finned fishes is a consequence of their small embryonic size and the resulting spatial constraints.
• This eversion is facilitated by specific morphogenetic movements, including spreading into nasal and ocular-adjacent spaces and forebrain roof thinning.
• The findings link evolutionary pressures on body size to fundamental differences in vertebrate brain development.