Abstract
Archaeological bone assemblages are almost always dominated by high proportions of fragmentary remains rendering them unidentifiable by morphological analysis. To overcome this, a number of alternative techniques of species identification have been proposed, with one of the most promising of these methods being the use of protein fingerprinting. Amongst the most abundant proteins in vertebrates, collagen is one of the most dominant biomolecules in the archaeological record due to its persistence in ancient bone. Despite its highly-conserved triple-helical structure, which is important for a range of functions, the collagen molecule possesses enough amino acid sequence variation to be able to discriminate between closely related and morphologically similar species, such as sheep and goat. Through the use of soft-ionization mass spectrometry, the collagen that survives for thousands, and in some cases millions, of years can be fingerprinted to yield taxonomic identifications of archaeological bone. The technique has been applied to a wide range of fragmentary and/or morphologically similar taxa from various archaeological and paleontological assemblages. In response to the most commonly asked question of ZooMS, this study investigates the taxonomic resolution achievable using collagen fingerprinting across a range of vertebrate groups in order to allow potential users a means to estimate the applicability of the technique to different archaeofaunal assemblages worldwide. Given the scope of this volume, it will also consider the practicalities of ZooMS protein fingerprint analyses, including sampling issues and amenability to high-throughput analyses of large assemblages and subsequent curation of such collections.
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References
Bakke, I., & Johansen, S. D. (2005). Molecular phylogenetics of Gadidae and related gadiformes based on mitochondrial DNA sequences. Marine Biotechnology, 7(1), 61–69.
Betancur-R, R., Broughton, R. E., Wiley, E. O., Carpenter, K., López, J. A., Li, C., et al. (2013). The tree of life and a new classification of bony fishes. PLOS Currents. http://dx.doi.org/10.1371/currents.tol.53ba26640df0ccaee75bb165c8c26288.
Bisbee, C. A., Baker, M. A., Wilson, A., Haji-Azimi, I., & Fischberg, M. (1977). Albumin phylogeny for clawed frogs (Xenopus). Science, 195(4280), 785–787.
Blaustein, A. R., Belden, L. K., Olson, D. H., Green, D. M., Root, T. L., & Kiesecker, J. M. (2001). Amphibian breeding and climate change. Conservation Biology, 15(6), 1804–1809.
Bossuyt, F., & Roelants, K. (2009). Frogs and toads (Anura). In S. B. Hedges & S. Kumar (Eds.), The timetree of life (pp. 357–364). New York: Oxford University Press.
Buckley, M., & Collins, M. J. (2011). Collagen survival and its use for species identification in Holocene-lower Pleistocene bone fragments from British archaeological and paleontological sites. Antiqua, 1(1), e1.
Buckley, M., & Kansa, S. W. (2011). Collagen fingerprinting of archaeological bone and teeth remains from Domuztepe, South Eastern Turkey. Archaeological and Anthropological Sciences, 3(3), 271–280.
Buckley, M., & Wadsworth, C. (2014). Proteome degradation in ancient bone: Diagenesis and phylogenetic potential. Palaeogeography, Palaeoclimatology, Palaeoecology, 416, 69–79.
Buckley, M., Collins, M., & Thomas-Oates, J. (2008). A method of isolating the collagen (I) alpha 2 chain carboxytelopeptide for species identification in bone fragments. Analytical Biochemistry, 374(2), 325–334.
Buckley, M., Collins, M., Thomas-Oates, J., & Wilson, J. C. (2009). Species identification by analysis of bone collagen using matrix-assisted laser desorption/ionisation time-of-flight mass spectrometry. Rapid Communications in Mass Spectrometry, 23(23), 3843–3854.
Buckley, M., Kansa, S. W., Howard, S., Campbell, S., Thomas-Oates, J., & Collins, M. (2010). Distinguishing between archaeological sheep and goat bones using a single collagen peptide. Journal of Archaeological Science, 37(1), 13–20.
Buckley, M., Larkin, N., & Collins, M. (2011). Mammoth and mastodon collagen sequences; survival and utility. Geochimica et Cosmochimica Acta, 75(7), 2007–2016.
Buckley, M., Fraser, S., Herman, J., Melton, N., Mulville, J., & Pálsdóttir, A. (2014). Species identification of archaeological marine mammals using collagen fingerprinting. Journal of Archaeological Science, 41, 631–641.
Buckley, M., Gu, M., Shameer, S., Patel, S., & Chamberlain, A. T. (2016). High-throughput collagen fingerprinting of intact microfaunal remains; a low-cost method for distinguishing between murine rodent bones. Rapid Communications in Mass Spectrometry, 30(7), 805–812.
Buckley, M., Harvey, V. L., & Chamberlain, A. T. (2017). Species identification and decay assessment of Late Pleistocene fragmentary vertebrate remains from Pin Hole Cave (Creswell Crags, UK) using collagen fingerprinting. Boreas. doi:10.1111/bor.12225.
Burger, J., Hummel, S., & Herrmann, B. (2000). Palaeogenetics and cultural heritage. Species determination and STR-genotyping from ancient DNA in art and artefacts. Thermochimica Acta, 365(1), 141–146.
Campana, M. G., Robinson, T., Campos, P. F., & Tuross, N. (2013). Independent confirmation of a diagnostic sheep/goat peptide sequence through DNA analysis and further exploration of its taxonomic utility within the Bovidae. Journal of Archaeological Science, 40(2), 1421–1424.
Cornish, T. J., Cotter, R. J., & Todd, P. J. (1994). A curved field reflectron time-of-flight mass spectrometer for the simultaneous focusing of metastable product ions. Rapid Communications in Mass Spectrometry, 8(9), 781–785.
Evans, B. J., Kelley, D. B., Tinsley, R. C., Melnick, D. J., & Cannatella, D. C. (2004). A mitochondrial DNA phylogeny of African clawed frogs: Phylogeography and implications for polyploid evolution. Molecular Phylogenetics and Evolution, 33(1), 197–213.
Fenn, J. B., Mann, M., Meng, C., Wong, S. F., & Whitehouse, C. M. (1989). Electrospray ionization for mass spectrometry of large biomolecules. Science, 246(4926), 64–71.
Fernández, M. H., & Vrba, E. S. (2005). A complete estimate of the phylogenetic relationships in Ruminantia: A dated species-level supertree of the extant ruminants. Biological Reviews, 80(2), 269–302.
Fiore, I., Gala, M., & Tagliacozzo, A. (2004). Ecology and subsistence strategies in the Eastern Italian Alps during the Middle Palaeolithic. International Journal of Osteoarchaeology, 14(34), 273–286.
Gómez-Guillén, M. C., Turnay, J., Fernández-Dıaz, M. D., Ulmo, N., Lizarbe, M. A., & Montero, P. (2002). Structural and physical properties of gelatin extracted from different marine species: A comparative study. Food Hydrocolloids, 16(1), 25–34.
Götherström, A., Collins, M., Angerbjörn, A., & Lidén, K. (2002). Bone preservation and DNA amplification. Archaeometry, 44(3), 395–404.
Gu, X., & Li, W.-H. (1992). Higher rates of amino acid substitution in rodents than in humans. Molecular Phylogenetics and Evolution, 1(3), 211–214.
Hall, D., & Reed, R. (1957). Hydroxyproline and thermal stability of collagen. Nature, 180, 243.
Hardy, B. L., & Moncel, M.-H. (2011). Neanderthal use of fish, mammals, birds, starchy plants and wood 125–250,000 years ago. PLOS ONE, 6(8), e23768.
Helm-Bychowski, K. M., & Wilson, A. C. (1986). Rates of nuclear DNA evolution in pheasant-like birds: Evidence from restriction maps. Proceedings of the National Academy of Sciences, 83(3), 688–692.
Horsburgh, K. A. (2008). Wild or domesticated? An ancient DNA approach to canid species identification in South Africa’s Western Cape Province. Journal of Archaeological Science, 35(6), 1474–1480.
Jenkins, C. L., Bretscher, L. E., Guzei, I. A., & Raines, R. T. (2003). Effect of 3-hydroxyproline residues on collagen stability. Journal of the American Chemical Society, 125(21), 6422–6427.
Ji, R., Cui, P., Ding, F., Geng, J., Gao, H., Zhang, H., et al. (2009). Monophyletic origin of domestic bactrian camel (Camelus bactrianus) and its evolutionary relationship with the extant wild camel (Camelus bactrianus ferus). Animal Genetics, 40(4), 377–382.
Kahila Bar-Gal, G., Khalaily, H., Mader, O., Ducos, P., & Horwitz, L. K. (2002). Ancient DNA evidence for the transition from wild to domestic status in Neolithic goats: A case study from the site of Abu Gosh, Israel. Ancient Biomolecules, 4(1), 9–17.
Kan, X. Z., Yang, J. K., Li, X. F., Chen, L., Lei, Z. P., Wang, M., et al. (2010). Phylogeny of major lineages of galliform birds (Aves: Galliformes) based on complete mitochondrial genomes. Genetics and Molecular Research, 9(3), 1625–1633.
Karas, M., & Krüger, R. (2003). Ion formation in MALDI: The cluster ionization mechanism. Chemical Reviews, 103(2), 427–440.
Kimura, S., & Ohno, Y. (1987). Fish type I collagen: Tissue-specific existence of two molecular forms,(α1) 2α2 and α1α2α3, in Alaska pollack. Comparative Biochemistry and Physiology. B, 88(2), 409–413.
Kimura, S., Miyauchi, Y., & Uchida, N. (1991). Scale and bone type I collagens of carp (Cyprinus carpio). Comparative Biochemistry and Physiology. B, 99(2), 473–476.
Langergraber, K. E., Prüfer, K., Rowney, C., Boesch, C., Crockford, C., Fawcett, K., et al. (2012). Generation times in wild chimpanzees and gorillas suggest earlier divergence times in great ape and human evolution. Proceedings of the National Academy of Sciences, 109(39), 15716–15721.
Larson, G., Albarella, U., Dobney, K., Rowley-Conwy, P., Schibler, J., Tresset, A., et al. (2007). Ancient DNA, pig domestication, and the spread of the Neolithic into Europe. Proceedings of the National Academy of Sciences, 104(39), 15276–15281.
Leikina, E., Mertts, M., Kuznetsova, N., & Leikin, S. (2002). Type I collagen is thermally unstable at body temperature. Proceedings of the National Academy of Sciences, 99(3), 1314–1318.
Lyman, R. L. (1994). Vertebrate taphonomy. Cambridge: Cambridge University Press.
Martof, B. (1953). Home range and movements of the green frog Rana clamitans. Ecology, 34(3), 529–543.
Miyauchi, Y., & Kimura, S. (1990). Characterization of an alpha3 chain from carp skin type I collagen. Bulletin of the Japan Society for the Science of Fish, 35(5), 456–459.
Morvan-Dubois, G., Le Guellec, D., Garrone, R., Zylberberg, L., & Bonnaud, L. (2003). Phylogenetic analysis of vertebrate fibrillar collagen locates the position of zebrafish α3 (I) and suggests an evolutionary link between collagen α chains and Hox clusters. Journal of Molecular Evolution, 57(5), 501–514.
O’Connor, S., Ono, R., & Clarkson, C. (2011). Pelagic fishing at 42,000 years before the present and the maritime skills of modern humans. Science, 334(6059), 1117–1121.
Pereiraa, S. L., & Bakera, A. J. (2009). Waterfowl and gamefowl (Galloanserae). In S. B. Hedges & S. Kumar (Eds.), The timetree of life (pp. 415–418). New York: Oxford University Press.
Poinar, H. N., Höss, M., Bada, J. L., & Pääbo, S. (1996). Amino acid racemization and the preservation of ancient DNA. Science, 272(5263), 864–866.
Ricard-Blum, S. (2011). The collagen family. Cold Spring Harbor Perspectives in Biology, 3(1), a004978.
Richards, M. P., Pettitt, P. B., Stiner, M. C., & Trinkaus, E. (2001). Stable isotope evidence for increasing dietary breadth in the European mid-Upper Paleolithic. Proceedings of the National Academy of Sciences, 98(11), 6528–6532.
Richter, K. K., Wilson, J., Jones, A. K. G., Buckley, M., van Doorn, N., & Collins, M. J. (2011). Fish ‘n chips: ZooMS peptide mass fingerprinting in a 96 well plate format to identify fish bone fragments. Journal of Archaeological Science, 38(7), 1502–1510.
Rybczynski, N., Gosse, J. C., Harington, C. R., Wogelius, R. A., Hidy, A. J., & Buckley, M. (2013). Mid-Pliocene warm-period deposits in the high Arctic yield insight into camel evolution. Nature Communications, 4, 1550.
Shedlock, A. M., & Edwards, S. V. (2009). Amniotes (Amniota). In S. B. Hedges & S. Kumar (Eds.), The timetree of life (pp. 375–379). New York: Oxford University Press.
Shoulders, M. D., & Raines, R. T. (2009). Collagen structure and stability. Annual Review of Biochemistry, 78, 929.
Smith, R. D., Loo, J. A., Edmonds, C. G., Barinaga, C. J., & Udseth, H. R. (1990). New developments in biochemical mass spectrometry: Electrospray ionization. Analytical Chemistry, 62(9), 882–899.
Szpak, P. (2011). Fish bone chemistry and ultrastructure: Implications for taphonomy and stable isotope analysis. Journal of Archaeological Science, 38(12), 3358–3372.
Tuross, N. (1994). The biochemistry of ancient DNA in bone. Experientia, 50(6), 530–535.
Tuross, N., & Stathoplos, L. (1993). Ancient proteins in fossil bones. Methods in Enzymology, 224, 121–129.
van der Sluis, L., Hollund, H., Buckley, M., De Louw, P., Rijsdijk, K., & Kars, H. (2014). Combining histology, stable isotope analysis and ZooMS collagen fingerprinting to investigate the taphonomic history and dietary behaviour of extinct giant tortoises from the Mare aux Songes deposit on Mauritius. Palaeogeography, Palaeoclimatology, Palaeoecology, 416, 80–91.
van Niekerk, K. L. (2011). Marine fish exploitation during the Middle and Later Stone Age of South Africa. Azania: Archaeological Research in Africa, 46(3), 392–392.
von Holstein, I. C., Ashby, S. P., van Doorn, N. L., Sachs, S. M., Buckley, M., Meiri, M., et al. (2014). Searching for Scandinavians in pre-Viking Scotland: Molecular fingerprinting of Early Medieval combs. Journal of Archaeological Science, 41, 1–6.
Waugh, J. (2007). DNA barcoding in animal species: Progress, potential and pitfalls. BioEssays, 29(2), 188–197.
Zeder, M. A., & Lapham, H. A. (2010). Assessing the reliability of criteria used to identify postcranial bones in sheep, Ovis, and goats, Capra. Journal of Archaeological Science, 37(11), 2887–2905.
Zenobi, R., & Knochenmuss, R. (1998). Ion formation in MALDI mass spectrometry. Mass Spectrometry Reviews, 17(5), 337–366.
Acknowledgments
The author would like to thank the Royal Society for fellowship funding, the University of Manchester’s Faculty of Life Sciences Proteomics Core Facility for access to instrumentation, the University of Sheffield’s Department of Archaeology for access to samples and Prof. Andrew Chamberlain as well as the peer reviewers for reading and commenting on early drafts of this chapter.
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Buckley, M. (2018). Zooarchaeology by Mass Spectrometry (ZooMS) Collagen Fingerprinting for the Species Identification of Archaeological Bone Fragments. In: Giovas, C., LeFebvre, M. (eds) Zooarchaeology in Practice. Springer, Cham. https://doi.org/10.1007/978-3-319-64763-0_12
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