From brain development to reproductive axis: an integrated study of the nervous system in cartilaginous fish

Cartilaginous fishes (Class Chondrichthyes), including sharks, rays, and chimaeras, represent one of the oldest extant vertebrate lineages, with origins exceeding 400 million years. Despite their ecological importance and key phylogenetic position, major gaps persist in our understanding of their neurobiology, particularly regarding postnatal brain development, habitat-related brain organization, and the neuroendocrine control of reproduction. A critical review of the literature identified three main knowledge gaps: (i) the scarcity of allometric data on postnatal brain development in Mediterranean chondrichthyans; (ii) the limited availability of comparative neuroecological analyses testing habitat-related brain organization within the Mediterranean Sea; and (iii) the poor understanding of interactions between dopaminergic and gonadotropin-releasing hormone (GnRH) systems in regulating reproduction. Within this framework, the small-spotted catshark Scyliorhinus canicula emerged as a particularly informative model species. These gaps shaped the aims of this doctoral research, articulated into two main thematic lines and an integrative objective: (i) to investigate postnatal brain growth and its modulation by ecology, sex, and life-history stage; (ii) to test whether Mediterranean chondrichthyans exhibit habitat-related brain organization consistent with established cerebrotypes; and (iii) to assess whether dopaminergic and GnRH1 systems interact within the brain–pituitary–gonadal (BPG) axis of S. canicula and how this interaction relates to sexual maturity. Using extensive sampling, morphometric analyses, immunohistochemistry, and comparative approaches, several novel insights emerged. First, postnatal brain growth was characterized in two model species: the speckled skate Raja polystigma and the deep-sea blackmouth catshark Galeus melastomus. Both species exhibited rapid early brain growth followed by negative allometry, with region-specific trajectories reflecting ecological specialization and life-stage transitions. In G. melastomus, some traits were consistent with bathyal cerebrotypes, extending current knowledge of deep-sea shark neuroecology. Second, a comparative analysis of brain organization across 14 central-western Mediterranean species revealed clear habitat-related patterns. Bathyal taxa showed a relative expansion of the medulla oblongata and reduced telencephalon, whereas epipelagic species exhibited enlarged telencephala and cerebella, with coastal species occupying intermediate positions. These results demonstrate that cerebrotypes identified at global scales are also recovered at a regional Mediterranean scale. Finally, the dopaminergic system of female S. canicula was investigated in relation to the BPG axis. Tyrosine hydroxylase–immunoreactive neurons in the preoptic region varied across sexual maturity stages, supporting a potential inhibitory role of dopamine in reproduction. Complementary analyses of the GnRH1 system, including double-label immunofluorescence, revealed anatomical relationships and receptor distributions consistent with functional dopaminergic–GnRH1 interactions. In conclusion, this thesis integrates postnatal brain development, habitat-driven neuroecological specialization, and reproductive neuroendocrine regulation in chondrichthyans, highlighting their value as key models for understanding the evolution of vertebrate brain organization and endocrine control.