Hierarchical biota-level and taxonomic controls on the chemistry of fossil melanosomes revealed using synchrotron X-ray fluorescence

Abstract

Fossil melanosomes, micron-sized granules rich in melanin in vivo, provide key information for investigations of the original coloration, taxonomy and internal anatomy of fossil vertebrates. Such studies rely, in part, on analysis of the inorganic chemistry of preserved melanosomes and an understanding of melanosome chemical taphonomy. The extent to which the preserved chemistry of fossil melanosomes is biased by biotic and abiotic factors is, however, unknown. Here we report the discovery of hierarchical controls on the inorganic chemistry of melanosomes from fossil vertebrates from nine biotas. The chemical data are dominated by a strong biota-level signal, indicating that the primary taphonomic control is the diagenetic history of the host sediment. This extrinsic control is superimposed by a biological, tissue-level control; tissue-specific chemical variation is most likely to survive in fossils where the inorganic chemistry of preserved melanosomes is distinct from that of the host sediment. Comparative analysis of our data for fossil and modern amphibians reveals that most fossil specimens show tissue-specific melanosome chemistries that differ from those of extant analogues, strongly suggesting alteration of original melanosome chemistry. Collectively, these findings form a predictive tool for the identification of fossil deposits with well-preserved melanosomes amenable to studies of fossil colour and anatomy.

Figure 1

Fossil vertebrates and preserved melanosomes. (a,d,g,j) Fossil specimens presenting dark organic rich films. Scale bars 10 mm. (a) P. diluvianus (NHML-30271); (d) B. amplystomus (NHMD-155208); (g) M. credneri (NHMB-MB-Am.-1187); (j) Amphibia indet. (CNU-SAL-NN2013002P). White triangles denote sampling points. (b,c,e,f,h,i,k,l) Scanning electron micrographs of preserved melanosomes in soft tissue samples. Scale bars: b,c,e,f,g,i, 5 µm;  k and l, 2 µm.

Figure 2

Linear Discriminant Analysis (LDA) of inorganic chemistry data for fossil melanosomes and sedimentary matrices. (a) Scatterplot of the LDA chemospace for the entire dataset with biplot (grey circle). Biplots show the most discriminating variables, i.e. those that contribute most to the separation among groups. (b–e) Panels highlighting the data for the Messel (b), Orsberg (c), Yanliao (d) and Jehol (e) biotas in the LDA plot in (a).

Figure 3

SRS-XRF and LDA analysis of individual fossil specimens. (a–d) P. diluvianus (NHML-30271); (e–h) B. amplystomus (NHMD-155208); (i–l) M. credneri (NHMB-MB-Am.-1187). (m–p); Amphibia indet. (CNU-SAL-NN2013002P); (b,f,j,n) SRS-XRF tricolor maps of each specimen; maps created using SMAK 1.50 https://www.sams-xrays.com/smak. Asterisks (*) denote internal tissues. (c,g,k,o) LDA plot for each specimen; colours and numbers denote different regions of interest; S, sediment. (d,h,l,p) biplots showing the most discriminating variables, i.e. those that contribute most to the separation among groups.

Figure 4

Multivariate analysis of the inorganic chemistry of modern and fossil melanosomes from amphibian tissues. (a) Linear Discriminant Analysis (LDA) of extant and fossil species. (b) Principal Component Analysis (PCA) of the inorganic chemistry of melanosomes from skin and liver. Grey circles are biplots. Note extensive overlap of the data for these two tissues in fossil amphibians only.