Synchrotron X-ray absorption spectroscopy of melanosomes in vertebrates and cephalopods: implications for the affinity of Tullimonstrum

Abstract

Screening pigments are essential for vision in animals. Vertebrates use melanins bound in melanosomes as screening pigments, whereas cephalopods are assumed to use ommochromes. Preserved eye melanosomes in the controversial fossil Tullimonstrum (Mazon Creek, IL, USA) are partitioned by size and/or shape into distinct layers. These layers resemble tissue-specific melanosome populations considered unique to the vertebrate eye. Here, we show that extant cephalopod eyes also show tissue-specific size- and/or shape-specific partitioning of melanosomes; these differ from vertebrate melanosomes in the relative abundance of trace metals and in the binding environment of copper. Chemical signatures of melanosomes in the eyes of Tullimonstrum more closely resemble those of modern cephalopods than those of vertebrates, suggesting that an invertebrate affinity for Tullimonstrum is plausible. Melanosome chemistry may thus provide insights into the phylogenetic affinities of enigmatic fossils where melanosome size and/or shape are equivocal.

Decoding the Evolution of Melanin in Vertebrates

“…Melanin is an essential screening pigment in vertebrate eyes [38]. Dark-toned fossil eyespots preserve melanosomes in fossil fish [19,39,40], an unidentified bird [41], the mosasaur Platecarpus [42], and in the enigmatic fossil Tullimonstrum [43]. Size-specific layering of melanosomes in the eye of a fossil is diagnostic of (a) melanic tissue layer(s); for example, the vertebrate retinal pigmented epithelium (RPE) that protects the retina from photooxidative damage.…”

“…Size-specific layering of melanosomes in the eye of a fossil is diagnostic of (a) melanic tissue layer(s); for example, the vertebrate retinal pigmented epithelium (RPE) that protects the retina from photooxidative damage. The chemistry of fossil eye melanosomes may carry taxonomic information and has been used to suggest an invertebrate affinity for Tullimonstrum [40].…”

“…This reflects, in part, an incomplete understanding of the phylogenetic distribution of pheomelanin. Our recent research shows that pheomelanin is not restricted to mammals, birds, and reptiles [6] but also occurs in amphibians and fish (and cephalopods) [7,40,80]. It is thus unlikely that pheomelanin has multiple independent origins in vertebrates [81]; a single deep origin (for vertebrates and potentially for Metazoa) is more parsimonious.…”

Synchrotron x‐ray fluorescence analysis reveals diagenetic alteration of fossil melanosome trace metal chemistry

“…Preserved associations between these metals and melanosomes can be tissue and taxon‐specific (Rogers et al . 2019; Rossi et al . 2019), thus offering the potential to inform on the internal anatomy (Rossi et al .…”

“…The metal inventory of fossil melanin, however, differs from that of modern analogues, even in closely related taxa (Rogers et al . 2019; Rossi et al . 2019).…”