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Animal coloration through deep time: evolutionary novelty, homology and taphonomy

Periodic Reporting for period 4 - ANICOLEVO (Animal coloration through deep time: evolutionary novelty, homology and taphonomy)

Reporting period: 2020-07-01 to 2021-04-30

Evidence of colour in fossils can inform on the visual signalling strategies used by ancient animals, but previous research is narrow in focus, lacks a broad phylogenetic and temporal context, and rarely incorporates information on taphonomy. This proposal represents a bold new holistic approach to the study of fossil colour. It couples powerful imaging- and chemical analytical techniques with a rigorous programme of fossilisation experiments simulating decay, burial, and transport, and analysis of fossils and their sedimentary context, to construct the first robust models for the evolution of colour in animals through deep time.

The project’s societal importance lies in its position at the interface of several scientific disciplines and rooting in palaeontology. As such, the project naturally lends itself to inspiring the public in the wonders of the natural world and encouraging prospective future scientists via the provision of high-profile role models and cutting-edge research discoveries.

The overall objectives of the research relate to the evolution of coloration in fossil vertebrates and insects. Regarding vertebrates, the key objectives centre around resolution of the biological distribution, geometry, chemistry, function and evolution of melanin. Regarding insects, the key objectives relate to the origins, chemistry and evolution of colour patterns and 3D photonic crystals. All objectives are underpinned by taphonomic insights in order to maximise the credibility of the data.

Several important conclusions have already been published. Broad phylogenetic analysis of the biology of melanin across vertebrates reveals tissue-specific and taxonomic trends in melanin abundance, location and chemistry that supports evidence for evolutionary tradeoffs between function and cytotoxicity. Melanosome chemistry, however, is not preserved in fossils intact, and instead the metal chemistry of melanosomes from different tissues can converge during thermal maturation, potentially masking real original differences in chemistry and related anatomical and taxonomic interpretations. Fossil skin can preserve evidence of the full colour gamut via diverse chromatophores in authigenically mineralized tissue and can preserve evidence of a deep co-evolutionary history with feathers. Preservation of branched feathers in pterosaurs confirms feathers originated in the avemetatarsalian ancestor of pterosaurs and dinosaurs in the Early Triassic. Finally, 3D photonic crystals preserved in weevils from the Swiss Pleistocene likely functioned in substrate matching.
We analysed over 400 tissue samples and regions from over 100 extant species and over 50 fossil taxa. Work on vertebrate melanosomes leaned heavily on analytical approaches such as tissue histology, Warthin-Starry staining, SEM, synchrotron-XRF and -XANES, HPLC-AHPO and taphonomic experiments at elevated pressures and temperatures. Work on insect cuticular pigments and photonic crystals used SEM, morphometrics and spectrophotometry, bandgap modelling, plus taphonomic experiments.

The results have been disseminated primarily in 24 publications (with an additional 30 papers in preparation or in review), including high-profile publications in Nature Communications (n=2), Nature Ecology & Evolution (n=2), Trends in Ecology and Evolution (n=2), Science Advances (n=1), Current Biology (n=1), Proceedings B (n=1), PNAS (n=1) and Journal of the Royal Society Interface (n=2). The results have also been disseminated to the scientific community via 63 conference presentations (50 of these oral presentations) across 44 international meetings, plus 16 invited keynotes and lectures (by the PI). The project results have been disseminated to the public via 67 public engagement activities, including exhibits, lectures, a website and blog, news articles, TV and radio interviews and documentaries.

The main results of the project include several important discoveries that have already been published. These include internal melanosomes in fossil and extant vertebrates, a new tool for interpreting fossil soft part anatomy, preservation of diverse colour-producing cells and keratinocytes in fossils, preservation of branched feathers in pterosaurs, the controls on the chemistry of fossil melanosomes, single diamond 3D photonic crystals in fossil weevils, and new models for the functional evolution of melanin in vertebrates.
This project represents a major advance in our understanding of the evolutionary history of animal colour. Aside from the key discoveries outlined above, the project revealed several important findings relating to melanin biology and evolution. The results demonstrate that the fossil record can preserve evidence of the true original colours of fossil animals, with the proviso that the fossil tissues are replicated in authigenic minerals. The project has greatly enhanced our understanding of melanin biology through a “big data” approach spanning almost the entire vertebrate phylogeny and systematic analysis of tissues. Our results show that internal and ocular (eye) melanosomes are abundant, phylogenetically widespread, have tissue-specific signatures and are informative for both taxonomy and anatomy. Further, we have used a comprehensive suite of taphonomic experiments to better understand the chemical mechanisms and other diagenetic factors that control the preservation of melanin and melanosomes in vertebrates, and to assess the preservation potential of colour-producing structures and pigments in fossil insects.

This project also represents a major advance in research approach. We tackled various issues relating to colour evolution in animals using a very grounded, systematic, and comprehensive analytical approach. Many of the techniques we employed are rarely used in palaeobiology, e.g. tissue histology, microspectrophotometry, fourier transform infrared radiation spectroscopy, Raman spectroscopy, and synchrotron-X-ray absorption spectroscopy, but this project has played an important role in embedding these approaches in the palaeobiology mainstream. In particular, we have now published a substantial body of work using synchrotron-XAS approaches on both fossil and extant animals; this, combined with our critical taphonomy-based narrative, has enhanced the credibility of XAS data from fossils.

This project highlights the need for future palaeobiological studies on fossil soft tissues to use a broad phylogenetic approach. In doing so, our work has enabled robust interrogation of evolutionary trends relating to keratinous tissues, melanin biology and chemistry for the first time. Critically, this approach even allows integration of fossil and genomic data, highlighting the potential for new future research avenues.
This project is also unique in its strong foundation in taphonomy – both experimental and theoretical. This is essential to accurate interpretation of fossils and application of fossil data to diverse evolutionary questions. Our publications have established a new standard for reporting experimental taphonomic data by including a dedicated section justifying our experimental approach, to facilitate progress beyond the “black box” model and to cement the credibility of experimental taphonomy in the scientific community.
The project team in the field in NE China
PhD student Valentina Rossi at the Stanford Synchrotron Radiation Lightsource
PhD student Tiffany Slater and her award for Top Project from her BSc
Postdoc Dr James Jepson examining fossil insects
Postdoc Dr Luke McDonald and volunteers doing public outreach
PhD student Valentina Rossi and postdoc Dr Chris Rogers doing melanin extractions in the lab
Postdoc Dr Giliane Odin analysing insects using microspectrophotometry
Postdoc Dr Thomas Clements using the synchrotron to analyse fossil insect chemistry
PI Maria McNamara during her keynote at GeoBonn in 2018