DNA markers reveal the complexity of livestock domestication

Salamini, F., Özkan, H., Brandolini, A., Schäfer-Pregl, R. & Martin, W. Genetics and geography of wild cereal domestication in the near east. Nature Rev. Genet. 3, 429–441 (2002).

MacHugh, D. E. & Bradley, D. G. Goats buck the trend. Proc. Natl Acad. Sci. USA 98, 5382–5384 (2001).

Goldstein, D. B. & Chikhi, L. Human migrations and population structure: what we know and why it matters. Annu. Rev. Genomics Hum. Genet. 3, 129–152 (2002).

Savolainen, P., Zhang, Y. P., Lu, J., Lundeberg, J. & Leitner, T. Genetic evidence for an East Asian origin of domestic dogs. Science 298, 1610–1613 (2002).

Rosenberg, N. A. et al. Empirical evaluation of genetic clustering methods using multilocus genotypes from 20 chicken breeds, Genetics 159, 699–713 (2001).

Food and Agriculture Organization of the United Nations. Secondary Guidelines for the Development of National Farm Animal Genetic Resources Management: Management of Small Populations at Risk. (Food and Agriculture Organization, Rome, 1998).

Froufe, E., Magyary, I., Lehoczky, I. & Weiss, S. MtDNA sequence data supports an Asian ancestry and single introduction of the common carp into the Danube basin. J. Fish Biol. 61, 301–304 (2002).

Blumler, M. A. Independent inventionism and recent genetic evidence on plant domestication. Econ. Bot. 46, 98–111 (1992).

Sherratt, A. Climatic cycles and behavioural revolutions: the emergence of modern humans and the beginning of farming. Antiquity 71, 271–287 (1997).

Kealhofer, L. Changing perceptions of risk: the development of agro-ecosystems in Southeast Asia. Am. Anthropol. 104, 178–194 (2002).

Diamond, J. Evolution, consequences and future of plant and animal domestication. Nature 418, 700–707 (2002). This review summarizes and synthesizes the different and complementary kinds of data (genetic, languistic, archaeozoological and so on) that are being used to infer the origins and spread of domestic agricultural plants and animals.

Richerson, P. J., Boyd, R. & Bettinger, R. L. Was agriculture impossible during the Pleistocene but mandatory during the Holocene? A climate change hypothesis. Am. Antiq. 66, 387–411 (2001).

Jansen, T. et al. Mitochondrial DNA and the origins of the domestic horse. Proc. Natl Acad. Sci. USA 99, 10905–10910 (2002).

Vila, C. et al. Widespread origins of domestic horse lineages. Science 291, 474–477 (2001).

Balasse, M., Bocherens, H., Tresset, A., Mariotti, A. & Vigne, J. D. Emergence of dairy production in the Neolithic? Contribution of isotopic analysis of cattle archaeological bones. Comptes Rendus Acad. Sci. Ser. II. 325, 1005–1010 (1997).

Alvard, M. S. & Kuznar, L. Deferred harvests: the transition from hunting to animal husbandry. Am. Anthropol. 103, 295–311 (2001).

Zeder, M. A. & Hesse, B. The initial domestication of goats (Capra hircus) in the Zagros mountains 10,000 years ago. Science 287, 2254–2257 (2000). This paper uses numerous precise carbon dates and a shift in demographic profiles (age and sex of harvested males) from goat fossil material to provide some of the oldest and best evidence for goat domestication along the border of Iraq and Iran.

Mannion, A. M. Domestication and the origins of agriculture: an appraisal. Phys. Geog. 23, 37–56 (1999).

Karp, A. et al. Molecular technologies for biodiversity evaluation: opportunities and challenges. Nature Biotech. 15, 625–628 (1997).

Sunnucks, P. Efficient genetic markers for population biology Trends Ecol. Evol. 15, 199–203 (2000).

Loftus, R. T., MacHugh, D. E., Bradley, D. G., Sharp, P. M. & Cunningham, P. Evidence for two independent domestications of cattle. Proc. Natl Acad. Sci. USA 91, 2757–2761 (1994). This paper was the first in a series of investigations of domestic animals that pointed towards numerous geographically separated domestications.

MacHugh, D. E., Loftus, R. T., Bradley, D. G., Sharp, P. M. & Cunningham, P. Microsatellite DNA variation within and among European cattle breeds. Proc. R. Soc. Lond. B 256, 25–31 (1994).

Handt, O., Meyer, S. & von Haeseler, A. Compilation of human mtDNA control region sequences. Nucleic Acids Res. 26, 126–129 (1998).

Luikart, G. et al. Multiple maternal origins and weak phylogeographic structure in domestic goats. Proc. Natl Acad. Sci. USA 98, 5927–5932 (2001). This study detected extremely high mtDNA diversity and surprisingly little intercontinental differentiation in goats as compared to cattle and sheep. It identified three potential origins (that is, three divergent mtDNA lineages), including one from south or east Asia, and suggested an emerging pattern of East–West dual domestications in farm animals.

Avise, J. C. Molecular Markers, Natural History and Evolution (Kluwer Academic, Boston, MA, 1993).

MacHugh, D. E., Shriver, M. D., Loftus, R. T., Cunningham, P. & Bradley, D. G. Microsatellite DNA variation and the evolution, domestication and phylogeography of taurine and zebu cattle (Bos taurus and Bos indicus). Genetics 146, 1071–1086 (1997). The novelty of this work was the uncoupling of paternal and maternal lineages in domestic population genetic history. African cattle populations show substantial Bos indicus ancestry in their Y chromosomes and autosomes, but lack any mtDNA variants from that taxon.

Buntjer, J. B., Otsen, M., Nijman, I. J., Kuiper, M. T. R. & Lenstra, J. A. Phylogeny of bovine species based on AFLP fingerprinting. Heredity 88, 46–51 (2002).

Ajmone Marsan, P. et al. Genetic distances within and across cattle breeds as indicated by biallelic AFLP markers. Anim. Genet. 33, 280–286 (2002).

Bruford, M. W. & Wayne, R. K. Microsatellites and their application to population genetics. Curr. Opin. Genet. Dev. 3, 939–943 (1993).

Diez-Tascón, C., Littlejohn, R. P., Almeida, P. A. R. & Crawford, A. M. Genetic variation within the Merino sheep breed: analysis of closely related populations using microsatellites. Anim. Genet. 31, 243–251 (2000).

Kadwell, M. et al. Genetic analysis reveals the wild ancestors of the llama and alpaca. Proc. R. Soc. Lond. B 268, 2575–2584 (2001). This study integrated mtDNA and microsatellite analyses to elucidate the origins of South American livestock despite their recurrent hybridization.

Matsuoka, Y. et al. A single domestication for maize shown by multilocus microsatellite genotyping. Proc. Natl Acad. Sci. USA 99, 6080–6084 (2002).

Cornuet, J. M., Piry, S., Luikart, G., Estoup, A. & Solignac, M. New methods employing multilocus genotypes to select or exclude populations as origins of individuals. Genetics 153, 1989–2000 (1999).

Maudet, C., Luikart, G. & Taberlet, P. Genetic diversity and assignment tests among seven French cattle breeds based on microsatellite DNA analysis. J. Anim. Sci. 80, 942–950 (2002).

Luikart, G. & Cornuet, J. -M. Empirical evaluation of a test for detecting recent historical population bottlenecks. Conserv. Biol. 12, 228–237 (1998).

Stanley, H. F., Kadwell, M. & Wheeler, J. C. Molecular evolution of the family Camelidae: a mitochondrial study. Proc. R. Soc. Lond. B 256, 1–6 (1994).

Wheeler, J. C. Evolution and present situation of the South American Camelidae. Biol. J. Linn. Soc. 54, 271–295 (1995).

Bradley, D. G., MacHugh, D. E., Cunningham, P. & Loftus, R. T. Mitochondrial diversity and the origins of African and European cattle. Proc. Natl Acad. Sci. USA 93, 5131–5135 (1996).

Loftus, R. T. et al. Mitochondrial genetic variation in European, African and Indian cattle populations. Anim. Genet. 25, 265–271 (1994).

Perkins, D., Jr. Fauna of Çatal Hüyük: evidence for early cattle domestication in Anatolia. Science 164, 177–178 (1969).

Vernesi, C. et al. Genetic characterization of the body attributed to the evangelist Luke. Proc. Natl Acad. Sci. USA 98, 13460–13463 (2001).

Troy, C. S. et al. Genetic evidence for Near-Eastern origins of European cattle. Nature 410, 1088–1091 (2001). Ancient and modern mtDNA phylogeography in European cattle indicates a derived origin from the Near East and supports a different history for African cattle.

Leonard, J. A. et al. Ancient DNA evidence for Old World origin of New World dogs. Science 298, 1613–1616 (2002).

Lister, A. M. et al. Ancient and modern DNA from a variety of sources in a study of horse domestication. Anc. Biomol. 2, 267–280 (1998).

Hiendleder, S., Mainz, K., Plante, Y. & Lewalski, H. Analysis of mitochondrial DNA indicates that domestic sheep are derived from two ancestral maternal sources: no evidence for contributions from urial and argali sheep. J. Hered. 89, 113–120 (1998).

Hiendleder, S., Kaupe, B., Wassmuth, R. & Janke, A. Molecular analysis of wild and domestic sheep questions current nomenclature and provides evidence for domestication from two different subspecies. Proc. R. Soc. Lond. B 269, 893–904 (2002).

Lau, C. H. et al. Genetic diversity of Asian water buffalo (Bubalus bubalis): mitochondrial D-loop and cytochrome b sequence variation. Anim. Genet. 29, 253–264 (1998).

Tanaka, K. et al. Phylogenetic relationship among all living species of the genus Bubalus based on DNA sequences of the cytochrome b gene. Biochem. Genet. 34, 443–452 (1996).

Guiffra, E. et al. The origin of the domestic pig: independent domestication and subsequent introgression. Genetics 154, 1785–1791 (2000). A clear illustration of the separation of the eastern and western clades of domestic pig, including comparisons of both mtDNA and nuclear gene sequences.

Kijas, J. M. H. & Andersson, L. A phylogenetic study of the origin of the domestic pig estimated from the near-complete mtDNA genome. J. Mol. Evol. 52, 302–308 (2001).

Watanobe, T. et al. Prehistoric introduction of domestic pigs onto the Okinawa islands: ancient mitochondrial DNA evidence. J. Mol. Evol. 55, 222–231 (2002).

Townsend, S. J. Genetic diversity and domestication in sheep (Ovis). Thesis, Univ. East Anglia (2000).

Kim, K. I., Lee, J. H., Lee, S. S. & Yang, Y. H. Phylogenetic relationships of northeast Asian cattle to other cattle populations determined using mitochondrial DNA D-loop sequence polymorphism. Biochem. Genet. 41, 91–98 (2003).

Kikkawa, Y. et al. Phylogenies using mtDNA and SRY provide evidence for male-mediated introgression in Asian domestic cattle. Anim. Genet. 34, 96–101 (2003).

Miretti, M. M., Pereira, H. A., Poli, M. A., Contel, E. P. B. & Ferro, J. A. African-derived mitochondria in South American native cattle breeds (Bos taurus): evidence of a new taurine mitochondrial lineage. J. Hered. 93, 323–330 (2002).

Hanotte, O. et al. African pastoralism: genetic imprints of origins and migrations. Science 296, 336–339 (2002). This applied the synthetic map approach of Cavalli-Sforza and colleagues to cattle diversity on a well-sampled continent and uncovered separate and interpretable levels of genetic variation.

Wood, N. J. & Phua, S. H. Variation in the control region sequence of the sheep mitochondrial genome. Anim. Genet. 27, 25–33 (1996).

Porter, V. Goats of the World (Farming Press, Ipswich, UK, 1996).

Yerxat, M. Y. Application of wild goats in cashmere breeding. Small Ruminant Res. 15, 287–291 (1995).

Moritz, C. Applications of mitochondrial DNA analysis in conservation — a critical review. Mol. Ecol. 3, 401–411 (1994).

Weitzman, S. 'On diversity'. Quart. J. Econ. 107, 363–405 (1992).

Hanotte, O. et al. Geographic distribution and frequency of a taurine Bos taurus and an indicine Bos indicus Y specific allele amongst sub-Saharan African cattle breeds. Mol. Ecol. 9, 387–396 (2000).

Heaton, M. P. et al. Selection and use of SNP markers for animal identification and paternity analysis in US beef cattle. Mamm. Genome 13, 272–281 (2002).

Irwin, D. M., Kocher, T. D. & Wilson, A. C. Evolution of the cytochrome-b gene of mammals. J. Mol. Evol. 32, 128–144 (1991).

Avise, J. C. Phylogeography: The History and Formation of Species (Harvard Univ. Press, Harvard, 2000).

Bandelt, H. J., Forster, P., Sykes, B. C. & Richards, M. B. Mitochondrial portraits of human populations using median networks. Genetics 141, 743–753 (1995).

Bandelt, H. J., Forster, P. & Röhl, A. Median joining networks for inferring intraspecific phylogenies. Mol. Biol. Evol. 16, 37–48 (1999).

Rogers, A. R. & Harpending, H. Population growth makes waves in the distribution of pairwise genetic differences. Mol. Biol. Evol. 9, 552–569 (1992).

Loftus, R. T. et al. A microsatellite survey of cattle from a centre of origin: the Near East. Mol. Ecol. 8, 2015–2022 (1999).

Steinborn, R. et al. Coexistence of Bos taurus and Bos indicus mitochondrial DNAs in nuclear transfer-derived somatic cattle clones. Genetics 162, 823–829 (2002).

Watanobe, T. et al. Genetic relationship and distribution of the Japanese wild boar (Sus scrofa leucomystax) and Ryukyu wild boar (Sus scrofa riukiuanus) analysed by mitochondrial DNA. Mol. Ecol. 8, 1509–1512 (1999).

Brown, W. M., George, M. and Wilson, A. C. Rapid evolution of animal mitochondrial DNA. Proc. Natl Acad. Sci. USA 76, 1967–1971 (1979).

Horai, S., Hayasaka, K., Kondo, R., Tsugane, K. & Takahata, N. Recent African origin of modern humans revealed by complete sequences of hominid mitochondrial DNAs. Proc. Natl Acad. Sci. USA 92, 532–536 (1995).

IUCN/SSC Caprinae Specialist Group. Wild Sheep and Goats and their Relatives (Shackleton, D. M., ed.) (Gland, Switzerland and Cambridge, UK, 1997).