Melanosome evolution shaped sensory biology and terrestrial adaptations in early aquatic vertebrates

The photic environment is a key driver of fish ecology that shapes adaptations to aquatic habitats. The evolutionary history of these adaptations, however, is difficult to trace. Melanosomes, melanin-rich organelles, offer unique insights into physiology and ecology and often fossilise. Here, we present a comparative analysis of melanosomes from extant and fossil fishes to trace the evolution of ecological and physiological adaptations through deep time. Melanosomes from internal tissues of extant fishes exhibit highly conserved geometries in all major taxonomic groups examined, indicating persistent functional constraints during evolution. Larger, more abundant melanosomes in lungfish likely reflect adaptations that underpin the vertebrate water-to-land transition. In contrast, eye melanosomes exhibit lineage-specific patterns. Bony fishes possess cylindrical eye melanosomes associated with retinomotor movements, photoreceptor protection, and improved visual acuity, whereas jawless and cartilaginous fishes possess only spheroidal melanosomes, consistent with visual sensitivity and alternative light-regulation strategies including pupillary modulation. These taxonomic differences are preserved in fossils from the late Carboniferous Mazon Creek biota, indicating that links between melanosome morphology and function were established during the early evolutionary history of these lineages in the Ordovician, approximately 445 million years ago. Early innovations in melanin biology uniquely facilitated vertebrate sensory evolution and ecological diversification.