Decoding the Evolution of Melanin in Vertebrates

Melanins are widespread pigments in vertebrates, with important roles in visual signaling, UV protection, and homeostasis. Fossil evidence of melanin and melanin-bearing organelles – melanosomes – in ancient vertebrates may illuminate the evolution of melanin and its functions, but macroevolutionary trends are poorly resolved. Here, we integrate fossil data with current understanding of melanin function, biochemistry, and genetics. Mapping key genes onto phenotypic attributes of fossil vertebrates identifies potential genomic controls on melanin evolution. Taxonomic trends in the anatomical location, geometry, and chemistry of vertebrate melanosomes are linked to the evolution of endothermy. These shifts in melanin biology suggest fundamental links between melanization and vertebrate ecology. Tissue-specific and taxonomic trends in melanin chemistry support evidence for evolutionary tradeoffs between function and cytotoxicity. In extant vertebrates melanin fulfils diverse roles including visual communication, photoprotection, antioxidation, and mechanical strengthening of tissues, but the evolution of these functions is debated.The discovery that melanosomes in fossil and modern vertebrates are associated with tissue-specific suites of trace metals supports hypotheses that melanin has ancient functions in metal homeostasis and antioxidant regulation.Shifts in melanosome biology across the dinosaur–bird transition reveal intimate links between adaptive and pleiotropic processes relating to the evolution of endothermy, metal homeostasis, photoprotection and the lymphatic system.Key genes can be mapped onto color pattern phenotypes in fossil vertebrates.Melanin-based coloration in vertebrates is dominated by melanin forms associated with low cytotoxicity, possibly reflecting selective adaptation against forms linked with greater oxidative stress or co-option of melanin forms with specific metal binding behavior for coloration.