Am.J.Hnm. Genet.65:1718-1724,1999 Y-Chromosome Evidence for a northward migration of Modern Humans into Eastern Asia during the Last Ice Age Bing Su, Junhua Xiao, Peter Underhill, Ranjan Deka, Weiling Zhang Joshua Akey, Wei Huang,, 4 Di Shen, Daru Lu, 2 Jingchun Luo, Jiayou Chu, Jiazhen Tan, 2 Peidong Shen, 5 Ron Davis, ,b Luca Cavalli-Sforza, Ranajit Chakraborty Momiao Xiong, Ruofu Du, Peter Oefner, b Zhu Chen , and Li jin Human Genetics Center, University of Texas-Houston, Houston nter for Life Sciences and Institute of genetics Fudan University, io pie ai Second Medical University, Shangha Department of Genetics, Stanford University, and Stanford DNA Center, Palo Alto;Department of Environmental Health, University of Cincinnati, Cincinnati; Insti cal Biology, The Chinese Academy of Medical Sciences, Kunming, Yunnan, China; and Institute of Genetics, The Chinese Sciences, Beijing Summary arrival there(Brooks and Wood 1990; Li and Etler 1992 Wu and Poirier 1995; Etler 1996; Wolpoff 1996), which The timing and nature of the arrival and the subsequent has been claimed to be a challenge to the well-known expansion of modern humans into eastern Asia remains "out-of-Africa"hypothesis of modern human evolution controversial. Using Y-chromosome biallelic markers, (Cann et al. 1987; Vigilant et al. 1991). However,not we investigated the ancient human-migration patterns in all paleoanthropologists agree that the Asian fossil rec eastern Asia. Our data indicate that southern popula- ord shows a clear continuity from Homo erectus to H tions in eastern Asia are much more polymorphic than sapiens sapiens(Stringer and Andrew 1988; Wilson and northern populations, which have only a subset of the Cann 1992), thereby casting doubt on the in situ Asian- southern haplotypes. This pattern indicates that the first origin hypothesis settlement of modern humans in eastern Asia occurred A recent study of Asian populations, which used mi in mainland Southeast Asia during the last Ice Age, co- crosatellite markers, questioned the validity of the in situ inciding with the absence of human fossils in eastern Asian-origin hypothesis and suggested that modern hu Asia, 50,000-100,000 years ago. After the initial peo- mans in eastern Asia originated from Africa( Chu et al. pling, a great northward migration extended into north- 1998). It also confirmed the previous observation of the ern China and Siberia substantial genetic and morphological differences be- tween northern and southern Mongoloids(Zhao et al 1986; Weng et al. 1989)and suggested that such dif- ferences could be attributed to a northward migration n eastern Asia(Chu et al. 1998). However, the stud Introduction fell short of providing unequivocal evidence in support of this hypothesis, because of the high mutation rates Although the expansions of modern humans into Eu- associated with the microsatellite markers used(Chu et rope, the Americas, and Oceania are now relatively well al. 1998). Therefore, a systematic study based on stable characterized, little is known of the earliest migratory and informative biallelic markers would shed more light routes by which modern humans spread from western on the prehistoric migrations in eastern Asia to eastern Asia( Cavalli-Sforza et al. 1994). Eastern Asia Recently, researchers have recognized the power of Y- is one of the few regions with relatively abundant hom- chromosome markers in resolving the migratory patterns inid fossils that span the last several hundreds of of modern humans Jobling and Tyler-Smith 1995).The thousands of years. Such evidence suggests the possi- introduction of denaturing high-performance liquid bility of continuous in situ evolution of Homo since its chromatography, a powerful mutation-detection tech nique, has made it possible to efficiently identify biallelic Received August 6, 1999, accepted for publication September 8, markers on Y chromosomes(Oefner and Underhill 1999; electronically published November 2, 1999 1995, 1998; Underhill et al. 1996, 1997b). The biallelic Address for correspondence and reprints: Dr. Li Jin, Human Genet Center, University of Texas-Houston, 6901 Bertmer, Hous ston, Tx markers are single-base changes or small indels that usu- 7030. E-mail: Ijin @utsph. sph uth. tmc.edu ally have occurred only once during the evolution of e 1999 by The American Society of Human Genetics. All rights reserve human y chromosomes and that are therefore m 00029297/9996506-002802.00 ble than microsatellite loci. The markers on the nonre.Am. J. Hum. Genet. 65:1718–1724, 1999 1718 Y-Chromosome Evidence for a Northward Migration of Modern Humans into Eastern Asia during the Last Ice Age Bing Su,1 Junhua Xiao,2 Peter Underhill,5 Ranjan Deka,7 Weiling Zhang,2 Joshua Akey,1 Wei Huang,3,4 Di Shen,1 Daru Lu,2 Jingchun Luo,2 Jiayou Chu,8 Jiazhen Tan,2 Peidong Shen,5 Ron Davis,5,6 Luca Cavalli-Sforza,5 Ranajit Chakraborty,1 Momiao Xiong,1 Ruofu Du,9 Peter Oefner,5,6 Zhu Chen,3,4 and Li Jin1,2,3 1 Human Genetics Center, University of Texas-Houston, Houston; 2 Morgan-Tan International Center for Life Sciences and Institute of Genetics, Fudan University, 3 National Human Genome Center at Shanghai, and 4 Rui-Jin Hospital, Shanghai Second Medical University, Shanghai; 5 Department of Genetics, Stanford University, and 6 Stanford DNA Sequencing and Technology Center, Palo Alto; 7 Department of Environmental Health, University of Cincinnati, Cincinnati; 8 Institute of Medical Biology, The Chinese Academy of Medical Sciences, Kunming, Yunnan, China; and 9 Institute of Genetics, The Chinese Academy of Sciences, Beijing Summary The timing and nature of the arrival and the subsequent expansion of modern humans into eastern Asia remains controversial. Using Y-chromosome biallelic markers, we investigated the ancient human-migration patterns in eastern Asia. Our data indicate that southern popula￾tions in eastern Asia are much more polymorphic than northern populations, which have only a subset of the southern haplotypes. This pattern indicates that the first settlement of modern humans in eastern Asia occurred in mainland Southeast Asia during the last Ice Age, co￾inciding with the absence of human fossils in eastern Asia, 50,000–100,000 years ago. After the initial peo￾pling, a great northward migration extended into north￾ern China and Siberia. Introduction Although the expansions of modern humans into Eu￾rope, the Americas, and Oceania are now relatively well characterized, little is known of the earliest migratory routes by which modern humans spread from western to eastern Asia (Cavalli-Sforza et al. 1994). Eastern Asia is one of the few regions with relatively abundant hom￾inid fossils that span the last several hundreds of thousands of years. Such evidence suggests the possi￾bility of continuous in situ evolution of Homo since its Received August 6, 1999; accepted for publication September 8, 1999; electronically published November 2, 1999. Address for correspondence and reprints: Dr. Li Jin, Human Genet￾ics Center, University of Texas-Houston, 6901 Bertner, Houston, TX 77030. E-mail: ljin@utsph.sph.uth.tmc.edu q 1999 by The American Society of Human Genetics. All rights reserved. 0002-9297/1999/6506-0028$02.00 arrival there (Brooks and Wood 1990; Li and Etler 1992; Wu and Poirier 1995; Etler 1996; Wolpoff 1996), which has been claimed to be a challenge to the well-known “out-of-Africa” hypothesis of modern human evolution (Cann et al. 1987; Vigilant et al. 1991). However, not all paleoanthropologists agree that the Asian fossil rec￾ord shows a clear continuity from Homo erectus to H. sapiens sapiens (Stringer and Andrew 1988; Wilson and Cann 1992), thereby casting doubt on the in situ Asian￾origin hypothesis. A recent study of Asian populations, which used mi￾crosatellite markers, questioned the validity of the in situ Asian-origin hypothesis and suggested that modern hu￾mans in eastern Asia originated from Africa (Chu et al. 1998). It also confirmed the previous observation of the substantial genetic and morphological differences be￾tween northern and southern Mongoloids (Zhao et al. 1986; Weng et al. 1989) and suggested that such dif￾ferences could be attributed to a northward migration in eastern Asia (Chu et al. 1998). However, the study fell short of providing unequivocal evidence in support of this hypothesis, because of the high mutation rates associated with the microsatellite markers used (Chu et al. 1998). Therefore, a systematic study based on stable and informative biallelic markers would shed more light on the prehistoric migrations in eastern Asia. Recently, researchers have recognized the power of Y￾chromosome markers in resolving the migratory patterns of modern humans (Jobling and Tyler-Smith 1995). The introduction of denaturing high-performance liquid chromatography, a powerful mutation-detection tech￾nique, has made it possible to efficiently identify biallelic markers on Y chromosomes (Oefner and Underhill 1995, 1998; Underhill et al. 1996, 1997b). The biallelic markers are single-base changes or small indels that usu￾ally have occurred only once during the evolution of human Y chromosomes and that are therefore more sta￾ble than microsatellite loci. The markers on the nonre-