Zooarchaeology and Ancient DNA

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Zooarchaeology and Ancient DNA ROSS BARNETT Durham University, UK

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In the seminal 1984 paper by Higuchi et al. (1984) that first showed the post-mortem survival of ancient DNA and initiated the entire field of ancient DNA studies, the authors used small scraps of muscle tissue found while remounting a specimen of the extinct quagga. Using primitive bacterial cloning methods they showed that recognizably equine DNA sequences were still to be found within. From there, the field split into two main branches: those concerned with getting ancient DNA from human remains and those concerned with getting DNA from other sources. While the study of ancient DNA from human remains requires incredibly stringent laboratory protocols to prevent contamination, working on zooarchaeological material happily circumvents many of these issues due to lower risks associated with working on extinct species, rare specimens, and domesticates. In the first decade of ancient DNA research, the analysis of zooarchaeological remains followed a clear pattern. When bacterial cloning methods were supplanted with the infinitely more powerful polymerase chain reaction (PCR), many groups identified species with poor taxonomic resolution and used phylogenetic methods to definitively place them within recognized lineages. During this phase, recently extinct species such as the Tasmanian tiger (Thylacinus cynocephalus) and woolly mammoth (Mammuthus primigenius) were analyzed from preserved remnants of tissue. Museums were suddenly reimagined as vast repositories of genetic information, and studies of extinct populations of living species or phylogenetic analyses of species so rare that field studies were impossible became a reality. Initial publications were conservative in nature, mostly confirming pre-existing hypotheses about relationships. The power of PCR allowed researchers

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to experiment with alternative sources of DNA. In particular, the ability to extract high-quality DNA from subfossil bone, which is found in enormous quantities in permafrost regions, was a breakthrough that both massively expanded the age of the material that DNA could be recovered from and opened up the Late Pleistocene as a period that could be studied through genetics. This expansion brought with it an avalanche of new questions related to population dynamics, ecological regime changes, and the nature of the megafaunal extinction. However, at the same time, trouble was brewing. While some researchers were expanding the scope of questions that could be asked with ancient DNA within a short chronological time frame, others were simply trying to push back the age of putatively recovered DNA. Starting in the early 1990s and reaching a crisis point during the mid-decade, this singular agenda led to reports of DNA from Miocene fossils, Oligocene amber, and Cretaceous dinosaur bone. When these studies could not be reliably replicated, and further study suggested they violated the kinetics of DNA breakdown, the field lurched into a self-inflicted crisis of confidence. Trust was only recovered when a comprehensive set of guidelines were voluntarily adopted, with an emphasis on internal and external replication of results (see dna: next generation sequencing and dna: mitochondrial). Since then, the use of ancient DNA in zooarchaeological studies has expanded considerably. Study of the phylogenetics of extinct species has become a useful tool to place unusual taxa within a standard taxonomy. Recovery of longer fragments from mitochondrial and nuclear DNA has shown definitively that traditional morphometric methods can be by turns too conservative or too radical. Good examples of this can be found in the study of New Zealand’s recently extinct flightless moa (Aves: Dinornithiformes). Early work looking at variation in bones of this family vastly overestimated the number of species. Ancient DNA from well-preserved remains showed that species limits were quite clear genetically and the species contained appreciable morphological variation (Bunce et al. 2009). Similarly, the

The SAS Encyclopedia of Archaeological Sciences. Edited by Sandra L. López Varela. © 2019 John Wiley & Sons, Inc. Published 2019 by John Wiley & Sons, Inc.

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Z O O A R CH A E O L O G Y A N D A N CI E N T D N A

effects of sexual dimorphism had not been fully appreciated and it was only through recovery of sex-linked genetic loci that what had previously been classified as two morphologically distinct species could be correctly assigned as males and females of a single species (Bunce et al. 2003). In New Zealand the abundant remains of moa have also been used to explore traditional zooarchaeological questions about diet.Moa coprolites (see coprolites) have been used to reconstruct browsing and grazing niches in various extinct members of this family (Wood et al. 2012). DNA extracted from coprolites has the advantage of identifying both defecator and dietary remains that are too small or too degraded to be identified at the macroscopic level. Questions of species abundance and demography have also been addressed in moa using a combination of radiocarbon dating and microsatellite data to show that populations were not in decline before human settlement of New Zealand (Allentoft et al. 2014). This approach was first pioneered in Pleistocene Beringian steppe bison (Bison priscus). The region known as Beringia (modern-day Siberia, Alaska, the Yukon, and the submerged landscape of the Bering Strait) has been the focus of huge research interest. As a crossroads between the Old and New Worlds, Pleistocene Beringia was a dry steppe grassland subcontinent with a fauna of woolly mammoths, woolly rhinos (Coelodonta antiquitatis), cave lions (Panthera spelaea), hyenas (Crocuta crocuta), bison, horses (Equus ferus), and other species. The remaining areas within the permafrost zone provide a paleoenvironmental archive of vertebrate remains that allow the exploration of the transition from the Pleistocene to the Holocene. The permafrost conditions ensure that DNA is well preserved and remains of bison and other megafauna are abundant. Using combinations of radiocarbon dating and mitochondrial data, and employing coalescent theory (which states that genetic diversity varies in proportion to effective population size), it has been possible to graph effective population size (Ne ) for a number of extinct and extant Beringian megafauna. Paradoxically, the data have shown that while some species (mammoth, rhino, horse) did not appear to go through a population bottleneck at the end of the Pleistocene, bison went through a sharp decline at the beginning of the Holocene,

yet recovered to become the most abundant large mammal in North America by the Late Holocene (Lorenzen et al. 2011). Large-scale studies of population change necessarily rely on huge datasets consisting of hundreds of well-dated sequences with accurate provenance. The number of taxa for which this is possible is few, but even with smaller-scale datasets, vital information on population movement can be gleaned. Carnivores tend to be found at low density in ecosystems and are correspondingly rare in the fossil record. Nonetheless, they are often of major conservation concern and have been intensively studied using modern genetic analyses. A classic case is that of North American brown bears (Ursus arctos) and polar bears (Ursus maritimus). Until recently, brown bears were classified into static phylogenetic lineages, with an implied long history of separation and with polar bears nestling within the diversity presented by brown bears. Analyses of ancient bear remains have exploded this view of phylogeography, showing that various intraspecific lineages have been highly dynamic and wide ranging, sometimes retreating to refugia, other times expanding outwards and even hybridizing with related species (Barnes et al. 2002). Despite the place that large-scale studies now hold within ancient DNA there is still scope for singular, well-preserved specimens to contribute. In these cases, deep sequencing (i.e., high-coverage nuclear genomes) of one or a few specimens can give as much information as shallower sequencing (i.e., mitochondrial DNA, or single locus) from scores of specimens. A good example of this has come to the fore with the development of next generation sequencing technologies that allow in-depth recovery of ancient genomes with high coverage. First pioneered in cave bears, the high-throughput systems allow access to nuclear genomes, including protein-coding genes that influence the phenotype and autosomal markers that give information on population history (Noonan et al. 2005). Since each gene in a diploid genome can contain two alleles it is possible to estimate how long ago those alleles diverged from each other. By comparing the alleles of many hundreds of genes from a single genome, it is possible to reconstruct in a timeline where alleles converge, which corresponds to periods of low effective

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population size. This approach has been used in studies of Pleistocene horses, confirming that climate acted as a major driver of population change in the horse (Orlando et al. 2013). Alternatively, the effects of single genes can be analyzed. One of the first to be investigated, MC1R, is involved with coat color and has been sequenced from extinct mammoths, horses, and other taxa (Römpler et al. 2006). MC1R codes for a cell membrane receptor that when stimulated switches between production of red-yellow pheomelanin and brown-black eumelanin. Loss-of-function mutations are well known in modern species and lead to a pale/red phenotype in living animals. This ideal one gene>one protein>phenotypic effect cascade is perfect for studying ancient and extinct remains, allowing us to say something definite about the appearance of animals that is not preserved in the fossil record. Typing of MC1R in fossil mammoths has shown that there was coat-color variation: Some mammoths were dark-colored and some were perhaps blonde (Römpler et al. 2006). The intersection of zooarchaeology (see zooarchaeology) and ancient DNA has given us great insight into the process of domestication (see domestication). Using ancient DNA it has been possible to test hypotheses about relationships between wild ancestors and domesticates. Going further, work has also used phylogeography to look at domestication at the population level: identifying regions where domestication may have taken place based on the genetic signatures of wild ancestors compared to modern domesticates and commensals. As human groups often took domesticates with them as they moved, signals of that movement can be found in the genetics of ancient remains. While humans are in general genetically uniform, their commensals and domesticates tend to contain a strong signal of regional origin, reflecting histories of expansion and contraction (Dobney and Larson 2006). These signals can be used to identify focal origins for human migrations, routes taken, and even timescales. A good use of this has been with domestic pigs (see pigs), where multiple centers of domestication have been identified, including in the Near East, and it has been possible to track the introgression of Near-Eastern domestic pigs into Neolithic Europe and hybridization with autochthonous wild boars (Larson et al. 2007).

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Ancient DNA therefore not only gives access to the progress of domestication but also provides insights into the process itself. At the forefront of ancient DNA are new laboratory techniques that allow researchers to circumvent many of the problems traditionally associated with ancient remains. Poor preservation, modern contaminants, and co-extraction of inhibitors have all stymied ancient DNA analyses of important specimens and sites. New methods using bait RNA molecules to fish out surviving endogenous sequence show great promise in greatly expanding both the range of materials that can be accessed and the maximum age of remains from which DNA can be recovered. Researchers are also experimenting with alternative sources of genetic information including eggshell, soil, hair, parchment, and many other zooarchaeological remains.

SEE ALSO: Sequencing DNA; Zooarchaeology and Human Diet Reconstruction; Zooarchaeology and Human Trade and Migration; Zooarchaeology and Stable Isotopes

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Noonan, James P., Michael Hofreiter, Doug Smith, James R. Priest, Nadin Rohland, Gernot Rabeder, Johannes Krause, J. Chris Detter, Svante Pääbo, and Edward M. Rubin. 2005. “Genomic Sequencing of Pleistocene Cave Bears.” Science 309: 597–600. Orlando, Ludovic, Aurelien Ginolhac, Guojie Zhang, Duane Froese, Anders Albrechtsen, Mathias Stiller, and Mikkel Schubert, Enrico Cappellini, Bent Petersen, Ida Moltke, Philip L. F. Johnson, Matteo Fumagalli, Julia T. Vilstrup, Maanasa Raghavan, Thorfinn Korneliussen, Anna-Sapfo Malaspinas, Josef Vogt, Damian Szklarczyk, Christian D. Kelstrup, Jakob Vinther, Andrei Dolocan, Jesper Stenderup, Amhed M. V. Velazquez, James Cahill, Morten Rasmussen, Xiaoli Wang, Jiumeng Min, Grant D. Zazula, Andaine Seguin-Orlando, Cecilie Mortensen, Kim Magnussen, John F. Thompson, Jacobo Weinstock, Kristian Gregersen, Knut H. Roed, Vera Eisenmann, Carl J. Rubin, Donald C. Miller, Douglas F. Antczak, Mads F. Bertelsen, Soren Brunak, Khaled A. S. Al-Rasheid, Oliver Ryder, Leif Andersson, John Mundy, Anders Krogh, M. Thomas P. Gilbert, Kurt Kjaer, Thomas Sicheritz-Ponten, Lars Juhl Jensen, Jesper V. Olsen, Michael Hofreiter, Rasmus Nielsen, Beth Shapiro, Jun Wang, and Eske Willerslev. 2013. “Recalibrating Equus Evolution Using the Genome Sequence of an Early Middle Pleistocene Horse.” Nature 499 (7456): 74–78. DOI:10.1038/nature12323. Römpler, Hölger, Nadin Rohland, Carlos Lalueza-Fox, Eske Willerslev, Tatyana V. Kuznetsova, Gernot Rabeder, Jaume Bertranpetit, Torsten Schöneberg, and Michael Hofreiter. 2006. “Nuclear Gene Indicates Coat-Color Polymorphism in Mammoths.” Science 313: 62. Wood, Jamie R., Janet M. Wilmshurst, Steven J. Wagstaff, Trevor H. Worthy, Nicolas J. Rawlence, and Alan Cooper. 2012. “High-Resolution Coproecology: Using Coprolites to Reconstruct the Habits and Habitats of New Zealand’s Extinct Upland Moa (Megalapteryx didinus).” PLoS ONE 7 (6): e40025. DOI:10.1371/journal.pone.0040025.

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Please note that the abstract and keywords will not be included in the printed book, but are required for the online presentation of this book which will be published on Wiley’s own online publishing platform. If the abstract and keywords are not present below, please take this opportunity to add them now. The abstract should be a short paragraph upto 200 words in length and keywords between 5 to 10 words.

ABSTRACT The study of ancient DNA is inextricably linked to zooarchaeology. From the first published paper on museum quagga (Equus quagga) material through to the first extinct genome of cave bear (Ursus spelaeus) and beyond, the ready availability of zooarchaeological specimens has been a boon to researchers. It is particularly important to note that, almost invariably, advances in ancient DNA research are pioneered using zooarchaeological material before being put to use in analyses of human archaeological and paleoanthropological remains. This entry provides a condensed history of the use of ancient DNA in zooarchaeology and some examples of the questions that can be addressed through these techniques. k

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KEYWORDS Ancient DNA; zooarchaeology; Pleistocene; megafauna; domestication; extinction; biogeography; Holocene

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