Ancient DNA of Guinea Pigs (Cavia spp.) Indicates a Probable New Center of Domestication and Pathways of Global Distribution.

Publisher: Nature Publishing Group Country of Publication: England NLM ID: 101563288 Publication Model: Electronic Cited Medium: Internet ISSN: 2045-2322 (Electronic) Linking ISSN: 20452322 NLM ISO Abbreviation: Sci Rep Subsets: MEDLINE

Original Publication: London : Nature Publishing Group, copyright 2011-

DNA, Ancient/*analysis ; DNA, Mitochondrial/*analysis ; Guinea Pigs/*classification ; Mitochondria/*genetics ; Sequence Analysis, DNA/*veterinary; Animals ; Belgium ; Bolivia ; Colombia ; Domestication ; Evolution, Molecular ; Guinea Pigs/genetics ; Peru ; Phylogeny ; Phylogeography ; Population Dynamics ; Puerto Rico ; United States

Guinea pigs (Cavia spp.) have a long association with humans. From as early as 10,000 years ago they were a wild food source. Later, domesticated Cavia porcellus were dispersed well beyond their native range through pre-Columbian exchange networks and, more recently, widely across the globe. Here we present 46 complete mitogenomes of archaeological guinea pigs from sites in Peru, Bolivia, Colombia, the Caribbean, Belgium and the United States to elucidate their evolutionary history, origins and paths of dispersal. Our results indicate an independent centre of domestication of Cavia in the eastern Colombian Highlands. We identify a Peruvian origin for the initial introduction of domesticated guinea pigs (Cavia porcellus) beyond South America into the Caribbean. We also demonstrate that Peru was the probable source of the earliest known guinea pigs transported, as part of the exotic pet trade, to both Europe and the southeastern United States. Finally, we identify a modern reintroduction of guinea pigs to Puerto Rico, where local inhabitants use them for food. This research demonstrates that the natural and cultural history of guinea pigs is more complex than previously known and has implications for other studies regarding regional to global-scale studies of mammal domestication, translocation, and distribution.

Erratum in: Sci Rep. 2020 Sep 1;10(1):14783. (PMID: 32879432)

Orlando, L. Ancient Genomes Reveal Unexpected Horse Domestication and Management Dynamics. BioEssays 42, 1900164 (2020). (PMID: 10.1002/bies.201900164)
Irving-Pease, E. K. et al. Paleogenomics of Animal Domestication. in 225–272, https://doi.org/10.1007/13836_2018_55 (2018).
Verdugo, M. P. et al. Ancient cattle genomics, origins, and rapid turnover in the Fertile Crescent. Science (80-.). 365, 173–176 (2019).
Frantz, L. A. F. et al. Genomic and archaeological evidence suggest a dual origin of domestic dogs. Science (80-.). 352, 1228–1231 (2016). (PMID: 10.1126/science.aaf3161)
Frantz, L. A. F. et al. Ancient pigs reveal a near-complete genomic turnover following their introduction to Europe. Proc. Natl. Acad. Sci. USA 116, 17231–17238 (2019). (PMID: 10.1073/pnas.1901169116)
Storey, A. A. et al. Investigating the Global Dispersal of Chickens in Prehistory Using Ancient Mitochondrial DNA Signatures. PLoS One 7, e39171 (2012). (PMID: 10.1371/journal.pone.0039171)
Bruford, M. W., Bradley, D. G. & Luikart, G. DNA markers reveal the complexity of livestock domestication. Nature Reviews Genetics 4, 900–910 (2003). (PMID: 10.1038/nrg1203)
Thornton, E. K. et al. Earliest Mexican Turkeys (Meleagris gallopavo) in the Maya Region: Implications for Pre-Hispanic Animal Trade and the Timing of Turkey Domestication. PLoS One 7, e42630 (2012). (PMID: 10.1371/journal.pone.0042630)
Wing, E. S. Animal domestication in the Andes. in Advances in Andean archaeology (ed. Browman, D. L.) 167–188 (Mouton Publishers, 1978).
Sandweiss, D. H. & Wing, E. S. Ritual Rodents: The Guinea Pigs of Chincha, Peru. J. F. Archaeol. 24, 47 (1997).
Correal, G. & der Hammen, T. Investigaciones arqueológicas en los abrigos rocosos del Tequendama: 11.000 años de prehistoria en la Sabana de Bogotá. Bogotá (Biblioteca Banco Popular, 1977).
Stahl, P. W. Animal Domestication in South America. in The Handbook of South American Archaeology (eds. Silverman, H. & Isbell, W. H.) 121–130 (Springer New York, 2008), https://doi.org/10.1007/978-0-387-74907-5_8 .
Hesse, B. Archaic exploitation of small mammals and birds in Northern Chile. Estud. Atacameños 51, 37–51 (1984). (PMID: 10.22199/S07181043.1984.0007.00005)
Ijzereef, G. Faunal remains from the El Abra rock shelters (Colombia). Palaeogeogr. Palaeoclimatol. Palaeoecol. 25, 163–177 (1978). (PMID: 10.1016/0031-0182(78)90076-7)
Dunnum, J. L. & Salazar-Bravo, J. Molecular systematics, taxonomy and biogeography of the genus Cavia (Rodentia: Caviidae). J. Zool. Syst. Evol. Res. 48, 376–388 (2010). (PMID: 10.1111/j.1439-0469.2009.00561.x)
Spotorno, A. E. et al. Ancient and modern steps during the domestication of guinea pigs (Cavia porcellus L.). J. Zool. 270, 57–62 (2006).
Pinto, M., Zúñiga, H. & Torres, O. Estudio Sistemático Del Género Cavia Pallas, 1766 (Rodentia:Caviidae) En Colombia. (Academia de Ciencias Exactas, Físicas y Naturales, 2002).
Delgado, M. E. Stable isotope evidence for dietary and cultural change over the Holocene at the Sabana de Bogotá region, Northern South America. Archaeol. Anthropol. Sci. 10, 817–832 (2018). (PMID: 10.1007/s12520-016-0403-3)
Delgado, M. E. Holocene population history of the Sabana de Bogotá region, Northern South America: An assessment of the craniofacial shape variation. Am. J. Phys. Anthropol. 162, 350–369 (2017). (PMID: 10.1002/ajpa.23124)
Delgado, M. E. Mid and late Holocene populations changes at the Sabana de Bogotá (Northern South America) inferred from skeletal morphology and radiocarbon chronology. Quat. Int. 256, 2–11 (2015). (PMID: 10.1016/j.quaint.2011.10.035)
Martínez-Polanco, M. F. Beyond white-tailed deer hunting in Aguazuque: Archaeofaunal data from an archaic site at Sabana de Bogotá, Colombia. Int. J. Osteoarchaeol. 29, 108–116 (2019). (PMID: 10.1002/oa.2722)
Zeder, M. A. Core questions in domestication research. Proc. Natl. Acad. Sci. USA 112, 3191–8 (2015). (PMID: 10.1073/pnas.1501711112)
Martínez-Polanco, M. F. El Cuy (Cavia sp.), Un Recurso Alimenticio Clave en Aguazuque, Un Sitio Arqueológico de la Sabana de Bogotá, Colombia. Lat. Am. Antiq. 27, 512–526 (2016).
Garcia, J. L. The Foods and Crops of the Muisca: A Dietary Reconstruction of the Intermediate Chiefdoms of Bogotá (Bacatá) and Tunja (Hunza), Colombia. (Citeseer, 2012).
Stahl, P. W. Pre-Columbian Andean animal domesticates at the edge of empire. World Archaeol. 34, 470–483 (2003). (PMID: 10.1080/0043824021000026459)
Stahl, P. W. & Norton, P. Precolumbian Animal Domesticates from Salango, Ecuador. Am. Antiq. 52, 382 (1987). (PMID: 10.2307/281791)
LeFebvre, M. J. & deFrance, S. D. Guinea Pigs in the Pre-Columbian West Indies. J. Isl. Coast. Archaeol. 9, 16–44 (2014). (PMID: 10.1080/15564894.2013.861545)
LeFebvre, M. J. & deFrance, S. D. Animal management and domestication in the realm of Ceramic Age farming. in The Archaeology of Caribbean and Circum-Caribbean Farmers (600 BC- AD 1500) (ed. Reid, B. A.) (Routledge, 2018).
Wing, E. Guinea pig (Cavia porcellus) remains from Finca Valencia (NCS-1), Northwest Puerto Rico, contribution to Phase II Zooarchaeology at the Finca Valencia (NCS-1) and NCS-4 Site, Northwest Puerto Rico. Final Phase II Archaeological Evaluation for the Finca Valencia Site North Coast Superaqueduct Project Municipality of Arecibo, Puerto Rico. (2000).
Kimura, B. K. et al. Origin of pre-Columbian guinea pigs from Caribbean archeological sites revealed through genetic analysis. J. Archaeol. Sci. Reports 5, 442–452 (2016). (PMID: 10.1016/j.jasrep.2015.12.012)
Pagán-Jiménez, J. R., Rodríguez-Ramos, R., Reid, B. A., van den Bel, M. & Hofman, C. L. Early dispersals of maize and other food plants into the Southern Caribbean and Northeastern South America. Quat. Sci. Rev. 123, 231–246 (2015). (PMID: 10.1016/j.quascirev.2015.07.005)
Lord, E., Collins, C., deFrance, S. D., LeFebvre, M. J. & Matisoo-Smith, E. Complete mitogenomes of ancient Caribbean Guinea pigs (Cavia porcellus). J. Archaeol. Sci. Reports 17, 678–688 (2018). (PMID: 10.1016/j.jasrep.2017.12.004)
Endersby, J. A guinea pig’s history of biology: the plants and animals who taught us the facts of life. (Random House, 2012).
Wagner, J. E. Chapter 1 - Introduction and Taxonomy. in The Biology of the Guinea Pig (eds. Wagner, J. E. & Manning, P. J.) 1–4 (Academic Press, 1976).
Pigière, F., Van Neer, W., Ansieau, C. & Denis, M. New archaeozoological evidence for the introduction of the guinea pig to Europe. J. Archaeol. Sci. 39, 1020–1024 (2012). (PMID: 10.1016/j.jas.2011.11.021)
Hamilton-Dyer, S. Animal Bones. in Hill Hall: A Singular House Devised by a Tudor Intellectual. (eds. Dury, P. & Simpson, R.) 345–351 (Society of Antiquities/EH Monograph, 2009).
Zierden, M. A. & Reitz, E. J. Animal use and the urban landscape in colonial Charleston, South Carolina, USA. Int. J. Hist. Archaeol. 13, 327–365 (2009). (PMID: 10.1007/s10761-009-0084-z)
Lalueza-Fox, C., Calderon, F. L., Calafell, F., Morera, B. & Bertranpetit, J. MtDNA from extinct Tainos and the peopling of the Caribbean. Ann Hum Genet 65, 137–151 (2001). (PMID: 10.1046/j.1469-1809.2001.6520137.x)
Lalueza-Fox, C. et al. Mitochondrial DNA from pre-Columbian Ciboneys from Cuba and the prehistoric colonization of the Caribbean. Am J Phys Anthr. 121, 97–108 (2003). (PMID: 10.1002/ajpa.10236)
Mendisco, F. et al. Where are the Caribs? Ancient DNA from ceramic period human remains in the Lesser Antilles. Philos Trans R Soc L. B Biol Sci 370, 20130388 (2015). (PMID: 10.1098/rstb.2013.0388)
Schroeder, H. et al. Origins and genetic legacies of the Caribbean Taino. Proc. Natl. Acad. Sci. 201716839, https://doi.org/10.1073/PNAS.1716839115 (2018).
Greig, K. et al. Complete mitochondrial genomes of New Zealand’s first dogs. PLoS One 10, e0138536 (2015). (PMID: 10.1371/journal.pone.0138536)
Knapp, M. et al. Complete mitochondrial DNA genome sequences from the first New Zealanders. Proc. Natl. Acad. Sci. 109, 18350–18354 (2012). (PMID: 10.1073/pnas.1209896109)
West, K. et al. The Pacific Rat Race to Easter Island: Tracking the Prehistoric Dispersal of Rattus exulans Using Ancient Mitochondrial Genomes. Front. Ecol. Evol. 5, 52 (2017). (PMID: 10.3389/fevo.2017.00052)
Robins, J. H. et al. Dating of divergences within the Rattus genus phylogeny using whole mitochondrial genomes. Mol. Phylogenet. Evol. 49, 460–466 (2008). (PMID: 10.1016/j.ympev.2008.08.001)
Allen, J. A. List of mammals collected in Colombia by the American Museum of Natural History expeditions, 1910-1915. Bull. Am. Museum Nat. Hist. XXXVI, 191–238 (1916).
Zúñiga, H., Pinto-Nolla, M., Hernández-Camacho, J. I. & María Torres-Martínez, O. Revisión taxonómica de las especies del genero Cavia (Rodentia: Caviidae) en Colombia. Acta Zool. Mex 87, 111–123 (2002).
Campos, H. A. & Ruiz-García, M. Genética poblacional de cobayas de Colombia, Cavia spp.(Rodentia: Caviidae) con marcadores moleculares RAPD. Rev. Biol. Trop. 56, 1481–1501 (2008).
Chanlatte Baik, L. Huecoid Culture and the Antillean Agroalfarero (Farmer-Potter) Period. in The Oxford Handbook of Caribbean Archaeology (eds. Keegan, W. F., Hofman, C. L. & Rodriguez Ramos, R.) 171–183 (Oxford University Press, 2013).
Rodríquez Ramos, R. What is the Caribbean? An archaeological perspective. J. Caribb. Archaeol. 3, 19–51 (2010).
Giovas, C. M. The Beasts at Large – Perennial Questions and New Paradigms for Caribbean Translocation Research. Part I: Ethnozoogeography of Mammals. Environ. Archaeol. 1–17, https://doi.org/10.1080/14614103.2017.1315208 (2017).
Eeckhout, P. Change and permanency on the coast of ancient Peru: the religious site of Pachacamac. World Archaeol. 45, 119–142 (2013). (PMID: 10.1080/00438243.2012.759516)
Hofman, C. L. The Post-Saladoid in the Lesser Antilles (AD 600/800-1492). Oxford Handb. Caribb. Archaeol. Oxford Univ. Press. Oxford 205–220 (2013).
Hofman, C. L., Bright, A. J. & Rodríquez Ramos, R. Crossing the Caribbean Sea: towards a holistic view of pre-colonial mobility and exchange. J. Caribb. Archaeol. 10, 1–18 (2010).
Laffoon, J. E. et al. Long-distance exchange in the precolonial Circum-Caribbean: A multi-isotope study of animal tooth pendants from Puerto Rico. J. Anthropol. Archaeol. 35, 220–233 (2014). (PMID: 10.1016/j.jaa.2014.06.004)
Garson, A. Prehistory, Settlement, and Food Production in the Savanna Region of La Calzada de Paez, Venezuela. Department of Anthropology PhD, (Yale University, 1980).
Sýkora, A. Manejo de Recursos Faunísticos por los Pobladores del Sitio Prehispánico en Palmasola, Estado Carabobo, Venezuela. (Universidad Central de Venezuela, 2006).
Rodríquez Ramos, R. Isthmo–Antillean Engagements. Oxford Handb. Caribb. Archaeol. 155 (2013).
Garcia-Casco, A. et al. Pre-Columbian jadeitite artifacts from the Golden Rock Site, St. Eustatius, Lesser Antilles, with special reference to jadeitite artifacts from Elliot’s, Antigua: implications for potential source regions and long-distance exchange networks in the Greater Caribbean. J. Archaeol. Sci. 40, 3153–3169 (2013).
Curet, A. L., Newsom, L. A. & DeFrance, S. D. Cultural continuity and discontinuity in the social history of ancient Puerto Rico: The case of the Ceremonial Center of Tibes. J. F. Archaeol. 31, 23–39 (2006). (PMID: 10.1179/009346906791072115)
LeFebvre, M. J. Animals, Food, and Social Life Among the Pre-Columbian Taíno of En Bas Saline, Hispaniola. (University of Florida, Gainesville, 2015).
Reitz, E. J. & McEwan, B. G. Animals, environment, and the Spanish diet at Puerto Real. Puerto Real Archaeol. a Sixt. Spanish T. Hisp. 287–334 (1995).
Zierden, M. A., Reitz, E. J., Pavao-Zuckerman, B., Reitsema, L. J. & Manzano, B. L. What is this bird? The quest to identify parrot remains from the Heyward-Washington House, Charleston, South Carolina. Southeast. Archaeol. 1–11, https://doi.org/10.1080/0734578X.2018.1555407 (2018).
Knapp, M., Clarke, A. C., Horsburgh, K. A. & Matisoo-Smith, E. A. Setting the stage–building and working in an ancient DNA laboratory. Ann. Anatomy-Anatomischer Anzeiger 194, 3–6 (2012). (PMID: 10.1016/j.aanat.2011.03.008)

0 (DNA, Ancient)
0 (DNA, Mitochondrial)

Date Created: 20200603 Date Completed: 20201204 Latest Revision: 20210601

20240104

PMC7264122

10.1038/s41598-020-65784-6

32483316