Interpreting melanin-based coloration through deep time: a critical review

Abstract

Colour, derived primarily from melanin and/or carotenoid pigments, is integral to many aspects of behaviour in living vertebrates, including social signalling, sexual display and crypsis. Thus, identifying biochromes in extinct animals can shed light on the acquisition and evolution of these biological traits. Both eumelanin and melanin-containing cellular organelles (melanosomes) are preserved in fossils, but recognizing traces of ancient melanin-based coloration is fraught with interpretative ambiguity, especially when observations are based on morphological evidence alone. Assigning microbodies (or, more often reported, their 'mouldic impressions') as melanosome traces without adequately excluding a bacterial origin is also problematic because microbes are pervasive and intimately involved in organismal degradation. Additionally, some forms synthesize melanin. In this review, we survey both vertebrate and microbial melanization, and explore the conflicts influencing assessment of microbodies preserved in association with ancient animal soft tissues. We discuss the types of data used to interpret fossil melanosomes and evaluate whether these are sufficient for definitive diagnosis. Finally, we outline an integrated morphological and geochemical approach for detecting endogenous pigment remains and associated microstructures in multimillion-year-old fossils.

Keywords: bacteria; eumelanin; melanosome; pheomelanin; pyomelanin; vertebrate.

Figure 1.

(a) Articulated skull of FUM-N-2268A. (b) Enlargement showing organic matter within the orbital cavity. (c) FEG-SEM micrograph of massed microbodies revealing morphological variation consistent with retinal melanosomes found in extant vertebrate eyes. Inset details elongate microbodies with homogeneous interior structure. (d) Surface pits (arrows) and depressions (arrowheads) on densely packed sub-spherical microbodies, the latter probably produced by diagenetic compression. Laminar structures are infiltrating sedimentary matrix. Note distinct size difference between moulds formed by diagenetic minerals and microbodies (see also f). (e) TEM micrograph of sectioned, unstained microbodies exposing external nodules (arrows) and electron-dense interior. Corrugated internal texture might be diagenetic; darker coloration (arrowheads) may represent replacement by inorganic material, possibly (based on ToF-SIMS data) iron sulfate. (f) TEM micrograph indicating diagenetic shrinkage of microbodies within the enclosing matrix. Scale bars: (a) 2 mm; (b) 500 µm; (c) 2 µm; (d,e) 500 nm; (f) 200 nm.

Figure 2.

Negative ion ToF-SIMS spectra collected from fossil microbodies located within the ‘eye spot’ of FUM-N-2268 (‘fossil microbodies’) and synthetic eumelanin. Bars represent the integrated signal intensity at each nominal mass (the spectra are normalized to the sum intensity of the major eumelanin peaks). Peaks in the fossil spectrum that are not present in the eumelanin spectrum correspond to inorganic ions (as indicated), sulfur-containing organic ions (C₂HS⁻ at 57 u, CSN⁻ at 58 u and C₃SN⁻ at 82 u) and oxygen-containing organic ions (C₂H₃O₂⁻ at 59 u and C₃H₃O₂⁻ at 71 u), respectively.