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Seaborne Spread of Domestic Pigs in Southern Italy and Sardinia During the Bronze and Iron Ages

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Seaborne Spread of Domestic Pigs in Southern Italy and Sardinia During the Bronze and Iron Ages Heredity (2017) 118, 154–159 & 2017 Macmillan Publishers Limited, part of Springer Nature. All rights reserved 0018-067X/17 www.nature.com/hdy ORIGINAL ARTICLE Like a pig out of water: seaborne spread of domestic pigs in Southern Italy and Sardinia during the Bronze and Iron Ages C Lega1,2, D Fulgione2, A Genovese2, L Rook3, M Masseti4, M Meiri5,6, A Cinzia Marra7, F Carotenuto8 and P Raia8 Southern Italy has a long history of human occupation and passage of different cultures since the Early Holocene. Repeated, ancient introductions of pigs in several geographic areas in Europe make it difficult to understand pig translocation and domestication in Italy. The archeozoological record may provide fundamental information on this, hence shedding light on peopling and on trading among different ancient cultures in the Mediterranean. Yet, because of the scanty nature of the fossil record, ancient remains from human-associated animals are somewhat rare. Fortunately, ancient DNA analysis as applied to domestic species proved to be a powerful tool in revealing human migrations. Herein, we analyzed 80-bp fragment of mitochondrial DNA control region from 27 Sus scrofa ancient samples retrieved from Southern Italian and Sardinian archeological sites, spanning in age from the Mesolithic to the Roman period. Our results surprisingly indicate the presence of the Near Eastern haplotype Y1 on both Italy’s major islands (Sardinia and Sicily) during the Bronze Age, suggesting the seaborne transportation of domestic pigs by humans at least during 1600–1300 BC. The presence of the Italian E2 clade in domestic contexts shows that the indigenous wild boar was effectively domesticated or incorporated into domestic stocks in Southern Italy during the Bronze Age, although the E2 haplotype has never been found in modern domestic breeds. Pigs belonging to the endemic E2 clade were thus traded between the Peninsula and Sardinia by the end of the second millennium BC and this genetic signature is still detected in Sardinian feral pigs. Heredity (2017) 118, 154–159; doi:10.1038/hdy.2016.74; published online 21 September 2016 INTRODUCTION clade is traditionally characterized by the Y1 haplotype, endemic to During the Neolithic Revolution, the combination of herding and Anatolia, and by the Y2 haplotype, whose geographical origin is agriculture induced one of the most important socioeconomic currently uncertain (Evin et al., 2015; Vai et al.,2015). transitions in human history. Domestication techniques spread into During the Neolithic Revolution, humans translocated pigs into Europe some 10 000 years ago, about 1000 years later than the first several regions across Eurasia, greatly complicating S. scrofa phylogeo- appearance of domestic species in the Fertile Crescent (Gronenborn graphy. Genetic analysis of human-associated animals can be used to 1999; Kuijt and Goring-Morris 2002; Colledge et al., 2004; Larson and infer human movements and migrations. However, massive transloca- Fuller, 2014). As part of the so-called Neolithic ‘package,’ S. scrofa tions, selective breeding and hybridization (Larson et al., 2007; represented an important prey assemblage to hunter–gatherers across Vigne et al., 2009) confuse patterns ascertained by using modern wide areas of Eurasia and until the Early Holocene (Pushkina and DNA only. Consequently, the analysis of ancient DNA (aDNA) must Raia, 2008), and, once domesticated, it became economically impor- be relied on, in order to get direct evidence on location and timing of tant to farmers. domestication events. The sequencing of a short mitochondrial D-loop The living wild boar shows strong phylogeographic structuring in region (80 bp) from ancient pig remains allowed, revealing that early Eurasia. In Western Eurasia, S. scrofa occurs in three divergent Neolithic farmers introduced domestic pigs into Northern Europe mitochondrial DNA (mtDNA) lineages geographically segregated in from the Near East by the sixth millennium BC, through the so-called continental Europe (E1), Italy (E2) and in the Near East. The Danubian route. By the Bronze Age (3900 BC), European domestic European clade (E1) further shows a geographical partition in two pigs had replaced the Near Eastern mitochondrial haplotype (more haplogroups: A-side haplotypes are common in Central Europe and likely through a reciprocal gene flow between local wild populations Italy, whereas C-side haplotypes are mostly found in Iberia and and introduced domestic stocks) and eventually spread into the Fertile Eastern Europe (Giuffra et al., 2000; Larson et al., 2005; Scandura Crescent (Larson et al.,2007;Evinet al., 2015; Vai et al., 2015). et al., 2011; Vilaça et al., 2014; Lega et al., 2016). The Near Eastern Domestication and dispersal of pigs into Europe following the 1Department of Earth Sciences, University of Pisa, Pisa, Italy; 2Department of Biology, University of Naples ‘Federico II’, Naples, Italy; 3Department of Earth Sciences, University of Florence, Florence, Italy; 4Department of Biology, University of Florence, Florence,Italy; 5The Steinhardt Museum of Natural History and Israel National Center for Biodiversity Studies, Tel Aviv University, Tel Aviv, Israel; 6Institute of Archaeology, Tel Aviv University, Tel Aviv, Israel; 7Department of Mathematical and Computer Sciences, Physical Sciences and Earth Sciences, University of Messina, Messina, Italy and 8Department of Earth Sciences, Environment and Resources, University of Naples ‘Federico II’, Naples, Italy Correspondence: Professor P Raia, Department of Earth Sciences, Environment and Resources, University of Naples ‘Federico II’, Largo San Marcellino 10, Naples 80138, Italy. E-mail: [email protected] Received 6 May 2016; accepted 25 July 2016; published online 21 September 2016 Seaborne spread of pigs in ancient Italy CLegaet al 155 Northern (Danubian) route is thus well documented (Larson et al., processing (Cooper and Poinar, 2000). Contamination prevention included 2007; Krause-Kyora et al., 2013). In stark contrast, the identity of disposable coveralls, masks and gloves. All working areas and equipment were ancient domestic pigs in Southern Europe is still poorly known, decontaminated using bleach and/or UV irradiation. Only sterile RNA/DNA- especially so in Southern Italy, that is exactly where European free manufactured plastic and filter tips in small packaging units were used. All Neolithic farming started (Price, 2000; Zilhao, 2001). reagents were molecular biology grade and, when possible, were decontami- Southern Italy is located in a strategic geographical position in the nated using UV irradiation (Fulton, 2012). Post-PCR work was conducted in Mediterranean basin and had a long history of human occupation and facilities different from those where aDNA was processed. Negative controls were used in all experimental steps (grinding, DNA extraction, pre-PCR passage of different cultures since the Early Holocene. Wild boar was preparation, PCR and sequencing), to rule out the possibility of laboratory common and widespread in Italy in Mesolithic sites. During the Early contamination. Primers applied in this study were specific for the genus Sus and Neolithic in Italy, farmers mainly bred cattle and goats, but pig showed no amplification with DNA of human or other animals either. All et al. exploitation also started soon, playing a major role (Albarella , extractions were independently amplified and sequenced twice at least for each 2006a, b). According to the zooarcheological record (Albarella et al., fragment, to rule out no misincorporated bases (Champlot et al., 2010). 2006a), the first S. scrofa appeared in Sardinia (and in Corsica) during the Early Neolithic, associated to human settlements and to other DNA extraction and amplification domestic animals, such as sheep, goat and cattle. The importance of The surface of all samples was sanded down with a circular saw and bleached to pigs in human economy greatly increased during Iron and Roman remove contaminants. Samples were ground to fine-grained powder and DNA Ages, when its frequency in archeological sites was greater than other was extracted according a modified protocol from Yang et al., 1998. Fifty to domestic animal (MacKinnon, 2001). 100 mg of powder was incubated overnight in a water bath at 56 °C in a European Neolithic cultures were well distinct in terms of tradi- digestion solution of 0.5 M EDTA pH 8 (Invitrogen, Carlsbad, CA, USA), 0.5% − 1 tions, way of life and resource exploitation. These differences persisted SDS and 0.1 mg ml Proteinase K. DNA was extracted through silica-based spin columns (Minielute PCR Purification Kit, Qiagen, Inc., CA, USA) with a in the Bronze and Iron Ages, and were obviously still apparent during final elution volume of 50–100 μl. For each individual, a minimum of two the Roman period. Yet, there is scarce hint about farming and independent DNA extractions was performed. husbandry in Southern regions, in comparison with Northern sites. Following Larson et al., 2007, a 80 bp diagnostic fragment from the control The genetic history of Italian pigs through a very large span of time region of the S. scrofa mitochondrial genome was amplified using the primers would be telling in terms of trading, origin and traditions of peopling ANC1-F (5′-CTTTAAAACAAAAAAACCCATAAAAA-3′) and ANC1-R (5′-TT in the Italian Peninsula. AATGCACGACGTACATAGG-3′). This fragment is highly variable and can Herein, in order to clarify domestication and dispersal of S. scrofa in distinguish between European, Near Eastern and East Asian
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