NatureCommonAncestors Article

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1 letters to nature The ages for MJG-I, MJG-II and MJG-III are considerably older Acknowledgements We thank R. J. Enkin for providing palaeomagnetic software. This work was 1 supported by the National Natural Science Foundation of China and Chinese Academy of than previous age estimates of Palaeolithic sites in northern China Sciences. R.P. was supported by the US National Science Foundation and the Smithsonian and indicate that humans might have reached northeast Asia earlier Human Origins Program. K.A.H. also received support from the US National Science than previously thought. Along with estimated ages for the sites of Foundation. 14 15 Gongwangling (1.15 Myr) and Xihoudu (1.27 Myr) in the 1 Competing interests statement The authors declare that they have no competing financial southern Loess Plateau and for Xiaochangliang (1.36 Myr) and interests. 16 Donggutuo (1.1 Myr) sites in the Nihewan basin, our new results imply an expansion and lengthy flourishing of human groups from and requests for materials should be addressed to R.X.Z. ([email protected] Correspondence and [email protected]) or R.P. ([email protected]). northern to north-central China during the early Pleistocene. The estimated age of 1.66 Myr for the MJG-III artefact layer pre- dates the previous oldest age of unambiguous human presence at 8 N in East Asia by about 0.3 Myr. Our findings, particularly for 40 the MJG-III layer, document the oldest coexistence of stone tools and man-made bone modifications in East Asia, indicating possible ... ... ... continuity with the oldest stone tools and artificial bone modifi- 17,18 Modelling the recent common cations reported in eastern Africa . Archaeological evidence at MJG indicates the oldest known use of animal tissues, especially ancestry of all living humans marrow processing, by early humans in Asia. The earliest archae- ological level in the Nihewan basin is slightly younger than the 3 2 1 Douglas L. T. Rohde & Joseph T. Chang , Steve Olson 1.75 Myr estimated age for early humans at the Dmanisi site at 40 8 N 2,3 latitude in western Eurasia . Our estimated ages also fall within the 1 Department of Brain and Cognitive Sciences, Massachusetts Institute of 1.66–1.51-Myr range for the earliest known human fossils in south- Technology, Cambridge, Massachusetts 02139, USA 19,20 2 east Asia . The combined evidence suggests that, near the start of 7609 Sebago Road, Bethesda, Maryland 20817, USA 3 Department of Statistics, Yale University, New Haven, Connecticut 06520, USA the Pleistocene, early human populations spread relatively rapidly ... ... across Asia, presumably from an African origin, and reached at least If a common ancestor of all living humans is defined as an N latitude. Our findings further establish that the earliest 40 8 individual who is a genealogical ancestor of all present-day populations to reach northeast Asia were able to survive for at people, the most recent common ancestor (MRCA) for a ran- least 500 kyr before the mid-Pleistocene onset of high-amplitude domly mating population would have lived in the very recent 21–23 climate oscillation A . 1–3 . However, the random mating model ignores essential past Received 19 February; accepted 8 July 2004; doi:10.1038/nature02829. aspects of population substructure, such as the tendency of individuals to choose mates from the same social group, and 1. Zhu, R. X. et al. Earliest presence of humans in northeast Asia. Nature 413–417 (2001). 413, the relative isolation of geographically separated groups. Here we 2. Gabunia, L. Earliest Pleistocene hominid cranial remains from Dmanisi, Republic of Georgia: et al. Science 288, 1019–1025 (2000). Taxonomy, geological setting, and age. show that recent common ancestors also emerge from two et al. A new skull of early Homo from Dmanisi, Georgia. Science 297, 85–89 (2002). 3. Vekua, A. models incorporating substantial population substructure. One 4. Wei, Q. Banshan Paleolithic site from the lower Pleistocene in the Nihewan Basin in northern China. model, designed for simplicity and theoretical insight, yields 13, Acta Anthropol. Sinica 223–238 (1994). explicit mathematical results through a probabilistic analysis. A 5. HPICR, Papers on Archaeology in Hebei Province 30–45 (East, Beijing, 1998). more elaborate second model, designed to capture historical 6. Potts, R. Early Hominid Activities at Olduvai (Aldine de Gruyter, New York, 1988). 7. Potts, R., Behrensmeyer, A. K. & Ditchfield, P. Paleolandscape variation and Early Pleistocene hominid population dynamics in a more realistic way, is analysed compu- J. Hum. Evol. 37, 747–788 (1999). activities: Members 1 and 7, Olorgesailie Formation, Kenya. tationally through Monte Carlo simulations. These analyses 8. Tang, Y. J., Li, Y. & Chen, W. Y. Mammalian fossils and the age of Xiaochangliang paleolithic site of suggest that the genealogies of all living humans overlap in 74–83 (1995). 33, Vertebrata Palasiatica Yangyuan, Hebei. remarkable ways in the recent past. In particular, the MRCA of Geochronology, Timescales, and Stratigraphic Correlation 9. Berggren, W. A., et al. in (eds Berggren, W. A., all present-day humans lived just a few thousand years ago in Kent, D. V., Aubry, M. & Hardenbol, J.) 129–212 (SEPM Spec. Publ. 54, Tulsa, Oklahoma, 1995). et al. in Evidence for Evolution 10. Wei, Q., Essays in Honor of Prof. Chungchien Yong on the Hundredth — these models. Moreover, among all individuals living more than Anniversary of His Birth (ed. Tong, Y.) 193–207 (Ocean, Beijing, 1997). just a few thousand years earlier than the MRCA, each present- 11. Huang, W. P. & Fang, Q. R. Wushan Hominid Site 105–109 (Ocean, Beijing, 1991). day human has exactly the same set of genealogical ancestors. 20, 12. Qiu, Z. X. Nihewan fauna and Q/N boundary in China. Quat. Sci. 142–154 (2000). In investigations of the common ancestors of all living humans, et al. Dating transitionally magnetized lavas of the late Matuyama chron: Toward a new 13. Singer, B. S. 39 40 much attention has focused on descent through either exclusively Ar timescale of reversals and events. J. Geophys. Res. Ar/ 679–693 (1999). 104, Quat. Res. . Homo erectus 14. An, Z. S. & Ho, C. K. New magnetostratigraphic dates of Lantian 213–221 32, maternal or exclusively paternal lines, as occurs with mitochondrial 4,5 (1989). . But according to the more DNA and most of the Y chromosome 15. Zhu, R., An, Z., Potts, R. & Hoffman, K. A. Magnetostratigraphic dating of early humans in China. common genealogical usage of the term ‘ancestor’, ancestry encom- Earth Sci. Rev. 341–359 (2003). 61, passes all lines of descent through both males and females, so that Quaternary Geology and 16. Quaternary Research Association of China, Li, H. M. & Wang, J. D. the ancestors of an individual include all of that person’s parents, Environment of China 33–38 (Ocean, Beijing, 1982). 385, Nature 333–336 (1995). 17. Semaw, S. et al. 2.5-million-year-old stone tools from Gona, Ethiopia. grandparents, and so on. et al. Environment and behavior of 2.5-million-year-old Bouri hominids. Science 284, 18. de Heinzelin, J. For a population of size n , assuming random mating (and so 625–629 (1999). 2 has ignoring population substructure), probabilistic analysis et al. 1118–1121 19. Swisher, C. C. III Age of the earliest known hominids in Java, Indonesia. Science 263, , T proved that the number of generations back to the MRCA, n (1994). 40 39 .We n has a distribution that is sharply concentrated around log Early Pleistocene et al. 20. Larick, R. Ar/ 2 Ar ages for Bapang Formation hominins, Central Java, 98, 4866–4871 (2001). Proc. Natl Acad. Sci. USA Indonesia. log , n , meaning that the T express this using the notation n 2 (eds Barham, L. & Robson-Brown, Human Roots: Africa and Asia in the Middle Pleistocene 21. Potts, R. in converges in probability to 1 as /log .In n n !1 T quotient n 2 K.) 5–21 (Western Academic & Specialist Press, Bristol, 2001). contrast, the mean time to the MRCA along exclusively matrilineal 22. Clark, P. U., Alley, R. B. & Pollard, D. Northern Hemisphere ice-sheet influences on global climate 6 , and the distri- or patrilineal lines is approximately generations n Science 286, 1104–1111 (1999). change. 18 bution is not sharply concentrated. For example, in a panmictic 23. Tian, J., Wang, P., Cheng, X. & Li, Q. Astronomically tuned Plio-Pleistocene benthic d O record from South China Sea and Atlantic–Pacific comparison. Earth Planet. Sci. Lett. 203, 1015–1029 (2002). population of one million people, the genealogical MRCA would have lived about 20 generations ago, or around the year www.nature.com/nature Supplementary Information accompanies the paper on . 1400, assuming a generation time of 30 years. The MRCA along AD 562 NATURE | VOL 431 | 30 SEPTEMBER 2004 | www.nature.com/nature Nature 4 200 © Publishing Group

2 letters to nature ð : n D log Þ D þ R , Furthermore, if we let denote the diameter of T 2 n Box 1 , since the IA point the graph, then the number of generations, U Graph-theoretical definitions n Þ , ð : n D log þ 77 : 1 U satisfies n 2 The length of a path in a graph, , is the number of edges in the path. G Computer simulations accord with these theoretical predictions. ) is defined to be and i For each pair of nodes ( i d , the distance G in j j , and U for small populations Tables 1 and 2 give distributions of T n n is G the length of a shortest path joining i and j . The radius of of varying sizes in graphs with one node, three connected nodes, five fully connected nodes and for a ten-node graph loosely based on R ¼ ð min{ } Þ ; i k d max i [ G k [ G world geography as shown in Fig. 1. In these simulations, neigh- bouring subpopulations exchange one pair of migrants per genera- . Assume R ¼ ) k d ( i , if max G is called a centre of i and a node G [ k 2 tion. Each mean is calculated from 100 model runs. Although R $ has one node) was treated previously G 0( 1; the case R ¼ . For n guaranteed to be accurate only for sufficiently large , the theoreti- each centre node i , let S be a set of minimal size that consists of i cal predictions describe the simulations quite well even for models # } R 2 1 for ): and satisfies min { neighbours of node i S < } i { [ j d k , j ( i is with just a few thousand individuals. Whenever n is doubled, T all G . H [ k is the minimum is defined as the number of nodes in S , H i i n 1 of H i is : G over all centres The diameter of , and D ¼ 1 2 , and is expected to increase by U D þ R expected to increase by i n H max D ¼ ( i , k d ). D 1.77. These predicted increases, which are listed in the last þ G i k [ , columns of Tables 1 and 2, agree closely with the simulation results. To hazard a rough first guess about human recent common ancestors, we could extrapolate the results for the graph of Fig. 1 to a exclusively maternal lines would have lived something like 50,000 growing population with a final size of 250 million. When applying in the order of one million generations ago. times earlier this model to a growing population, the fixed population size that — As genealogical ancestry is traced back beyond the MRCA, a provides the best approximation is the size at the time that the growing percentage of people in earlier generations are revealed to MRCA lived. We take this effective population size to be 250 million, be common ancestors of the present-day population. Tracing 1. AD which is approximately the global population in the year generations U further back in time, there was a threshold, let us say Starting from ¼ 16,000, a population of 250 million is reached n n ago, before which ancestry of the present-day population was an all U and T by doubling 14 times. Approximating the increases in n n or nothing affair. That is, each individual living at least U beyond the values seen in Tables 1 and 2 by their theoretical n generations ago was either a common ancestor of all of today’s < 34 þ 14 £ 3 ¼ T , we arrive at n predictions for each doubling of n humans or an ancestor of no human alive today. Thus, among all 14 þ 74 < 77 ¼ : 6 £ 169 76 generations (about 2,300 years) and U n generations ago, each present-day U individuals living at least generations (about 5,000 years). These estimates would suggest, n human has exactly the same set of ancestors. We refer to this point in with the exchange of just one pair of migrants per generation time as the identical ancestors (IA) point. As with the MRCA point, between large panmictic populations of realistic size, that the the IA point is also quite recent in a randomly mating population: , and all modern individuals BC MRCA appears in about the year 300 2 generations ago n 1.77 log , . U BC . Such estimates are have identical ancestors by about 3,000 2 n The major problem in applying these results to human popu- extremely tentative, and the model contains several obvious sources lations is that mating is not random in the real world. Mating of error, as it was motivated more by considerations of theoretical patterns are structured by geography, proximity, culture, language insight and tractability than by realism. Its main message is that and social class. Nevertheless, even in populations with considerable substantial forms of population subdivision can still be compatible internal structure, the time to the MRCA can be remarkably brief. with very recent common ancestors. To demonstrate this in a tractable mathematical model, consider a The dynamics of human subpopulations are much more complex divided into randomly mating subpopulations population of size n than those in the simple graph model discussed above. Although that are linked by occasional migrants. The population is rep- these complexities make theoretical analysis difficult, a computer G , with a node for each subpopulation. resented by a graph, model incorporating more complicated forms of population sub- Edges indicate pairs of nodes that exchange a small number (for structure and migration allows the demographic history of human denote example, one pair) of migrants per generation. Let R populations to be simulated. The Supplementary Information be a quantity ranging between 0 and 1 D G the radius of , and let contains more details on the model and computations; here we G that depends on the structure of (see Box 1). A probabilistic briefly outline some of the main points. analysis (see Supplementary Information) shows that as , !1 n This model is based on a simplified projection of the world’s Table 1 T Simulations of n ¼ ¼ 1,000 n ¼ 2,000 n ¼ Graph n n 8,000 n ¼ 16,000 R þ D 4,000 ... ... ... One node 10.8 (0.4) 11.8 (0.4) 12.8 (0.4) 13.9 (0.3) 14.8 (0.4) 1.00 Three fully connected nodes 14.0 (0.7) 17.1 (0.9) 18.9 (0.8) 20.3 (1.0) 1.50 15.6 (0.7) Five fully connected nodes 15.8 (0.5) 17.8 (0.5) 19.6 (0.5) 21.5 (0.6) 1.75 14.0 (0.5) Ten-node graph shown in Fig. 1 21.1 (1.3) 24.3 (1.5) 27.6 (1.5) 30.5 (1.5) 33.8 (1.7) 3.00 ... ... ... (the number of generations back to the MRCA) for graph-structured populations exchanging a single pair of migrants per edge per generation. The Means (standard deviations in parentheses) of T n last column shows R þ . , the expected asymptotic increase in per doubling of T D n n U Simulations of Table 2 n 8,000 1,000 n ¼ 2,000 n ¼ 4,000 Graph ¼ ¼ n ¼ 16,000 D þ 1.77 n n ... ... ... 20.8 (1.6) 22.6 (1.5) 24.6 (1.5) 1.77 One node 28.3 (1.4) 26.5 (1.6) 27.4 (1.5) Three fully connected nodes 33.4 (1.5) 36.2 (1.7) 38.9 (1.5) 2.77 30.3 (1.4) 25.9 (1.3) 32.1 (1.7) 35.3 (1.5) 37.9 (1.4) 2.77 Five fully connected nodes 28.9 (1.4) 46.3 (2.7) 53.0 (2.7) 59.8 (2.7) Ten-node graph shown in Fig. 1 73.6 (2.7) 6.77 66.8 (2.9) ... ... ... (the number of generations back to the IA point) for graph-structured populations exchanging a single pair of migrants per edge per generation. The Means (standard deviations in parentheses) of U n last column shows U 1.77, the expected asymptotic increase in þ D per doubling of . n n 563 NATURE | VOL 431 | 30 SEPTEMBER 2004 | www.nature.com/nature Nature 4 200 © Publishing Group

3 letters to nature Figure 1 World map viewed as a ten-node graph. This graph has radius 3 and diameter 5. actual inhabited land masses and has three levels of substructure: port come from the country in which the port is located, with the continents, ‘countries’ and ‘towns.’ Figure 2 depicts the model’s remainder drawn from other countries in the continent in pro- AD 1500, with the geography and migration routes used before portion to their inverse squared distance. The value next to a port in countries shown as squares and the number of towns per country Fig. 2 is its migration rate, in people per generation, and the date in differing from continent to continent. Towns and countries rep- parentheses indicates when the port opens, if it is more recent than . When a port opens, there is BC resent both the local geographical areas and the relevant social and the start of the simulation in 20,000 usually a single generation of migration at a higher rate than the ethnic groups from which most people find mates. AD 1500, steady-state rate shown in the figure. After the year The model uses a simplified migration system in which each additional large ports, which are not shown, begin to open to person has a single opportunity to migrate from his or her town of simulate colonization of the Americas, Australia and elsewhere. birth. The probabilities of leaving a town or a country are set at Immediately before this, the native population of the Americas is various levels to reflect different migration patterns. Migrants who markedly reduced to simulate the effects of European-introduced move between towns can travel to any other town within the 7 . diseases country. A migrant who leaves a country for another country within Generations overlap in this model and we explicitly simulated the the same continent chooses the destination with a probability that lifespan and the times at which mating and reproduction events diminishes as the inverse square of the geographical distance. 8,9 , as described in more detail in Sup- occur for each individual Each continent has a number of port countries from which plementary Information. The birth rate of each continent or island migrants can travel to another continent. A fixed, large percentage was individually adjusted so that the populations match historical (for example, 95% in some simulations) of the migrants through a Geography and migration routes of the simulated model. Arrows denote ports given, the date in parentheses indicates when the port opens. Upon opening, there is Figure 2 and the adjacent numbers are their steady migration rates, in individuals per generation. If usually a first-wave migration burst at a higher rate, lasting one generation. NATURE | VOL 431 | 30 SEPTEMBER 2004 | www.nature.com/nature 564 Nature 4 200 © Publishing Group

4 letters to nature estimates, and growth rates were higher in under-populated areas. from that predicted by the model. Examples of such factors include Full-sized populations were used until the world population the existence of more diverse intercontinental migration routes, the BC . Subsequently, birth rates were reached 50 million in 1,000 large-scale movement and mixing of populations documented in 18 17 reduced to achieve a worldwide level of 55 million, carried out in , marked individual differences in fertility , the historical record such a way that sparsely populated areas were less affected. This and the population increase of the past two millennia, which would limit was a computational necessity, but simulations show that result in more migrants. population growth has little effect, especially if it occurs after the Actual migration rates among populations are very poorly known MRCA has died. and undoubtedly have varied considerably in different times and With 5% of individuals migrating out of their home town, 0.05% places. Studies of hunter-gatherer groups and subsistence agricul- migrating out of their home country, and 95% of port users born in tural communities have found that anywhere from 1% (ref. 19) to as the country from which the port emanates, the simulations produce much as 30% (ref. 20) of mates are from outside the group. The BC and a mean IA date of 5,353 . BC a mean MRCA date of 1,415 tendency of most human groups to marry out with surrounding Interestingly, the MRCAs are nearly always found in eastern Asia. groups, at least to a limited extent, links networks of ancestry within This is due to the proximity of this region to both Eurasia and either specific regions (see http://www.compapp.dcu.ie/ humphrys/ , the remote Pacific islands or the Americas, allowing the MRCA’s FamTree/Royal/Famous.descents.html). descendants to reach a few major world regions in a relatively short Given the remaining uncertainties about migration rates and time. real-world mating patterns, the date of the MRCA for everyone Arguably, this simulation is far too conservative, especially given living today cannot be identified with great precision. Nevertheless, its prediction that, even in densely populated Eurasia, only 55.3 our results suggest that the most recent common ancestor for the 1500. If the AD people will leave each country per generation in world’s current population lived in the relatively recent past — migration rate among towns is increased to 20%, the local port users perhaps within the last few thousand years. And a few thousand are reduced to 80%, and the migration rates between countries and years before that, although we have received genetic material in continents are scaled up by factors of 5 and 10, respectively, the markedly different proportions from the people alive at the time, 55 and the mean IA date is 2,158 AD mean MRCA date is as recent as the ancestors of everyone on the Earth today were exactly the same. . The predictions of the simple ten-node graph model sketched BC Further work is needed to determine the effect of this common earlier fall somewhere between these dates and those of the more ancestry on patterns of genetic variation in structured popu- 21–24 conservative computational model. lations . But to the extent that ancestry is considered in genea- The model also can be used to calculate the percentage of ancestry logical rather than genetic terms, our findings suggest a remarkable that current individuals receive from different parts of the world. In proposition: no matter the languages we speak or the colour of our generations sufficiently far removed from the present, some ances- skin, we share ancestors who planted rice on the banks of the tors appear much more often than do others on any current Yangtze, who first domesticated horses on the steppes of the individual’s family tree, and can therefore be expected to contribute Ukraine, who hunted giant sloths in the forests of North and 1,10,11 .For proportionately more to his or her genetic inheritance South America, and who laboured to build the Great Pyramid of example, a present-day Norwegian generally owes the majority of Khufu. A his or her ancestry to people living in northern Europe at the IA Received 30 December 2003; accepted 14 July 2004; doi:10.1038/nature02842. point, and a very small portion to people living throughout the rest 1. Wachter, K. W. in Genealogical Demography (eds Dyke, B. & Morrill, W. T.) 85–93 (Academic, New of the world. Furthermore, because DNA is inherited in relatively York, 1980). large segments from ancestors, an individual will receive little or no Adv. Appl. Probab. 31, 2. Chang, J. T. Recent common ancestors of all present-day individuals. actual genetic inheritance from the vast majority of the ancestors 1002–1026, 1027–1038 (1999). 12 . living at the IA point 3. Derrida, B., Manrubia, S. C. & Zanette, D. H. On the genealogy of a population of biparental 303–315 (2000). 203, J. Theor. Biol. individuals. Several factors could cause the time to the true MRCA or IA point ̈ ̈ 4. Ingman, M., Kaessmann, H., Pa bo, S. & Gyllensten, U. Mitochondrial genome variation and the a to depart from the predictions of our model. If a group of humans origin of modern humans. Nature 408, 708–713 (2000). were completely isolated, then no mixing could occur between that 5. Thomson, R., Pritchard, J. K., Shen, P., Oefner, P. J. & Feldman, M. W. Recent common ancestry of 97, human Y chromosomes: Evidence from DNA sequence data. Proc. Natl Acad. Sci. USA 7360–7365 group and others, and the MRCA would have to have lived before (2000). the start of the isolation. A more recent MRCA would not arise until 6. Hudson, R. R. in (eds Harvey, P. H. & Partridge, L.) 1–44 Oxford Surveys of Evolutionary Biology the groups were once again well integrated. In the case of Tasmania, (Oxford Univ. Press, New York, 1990). which may have been completely isolated from mainland Australia 7. Stannard, D. E. (Oxford Univ. Press, American Holocaust: Columbus and the Conquest of the New World New York, 1992). between the flooding of the Bass Strait, 9,000–12,000 years ago, and Death Rates by Age, Race, and Sex, United States, 1900–1953, 8. US National Office of Vital Statistics, the European colonization of the island, starting in 1803 (ref. 13), Special Reports Vol. 43 (US Government Printing Office, Washington DC, 1956). Vital Statistics — the IA date for all living humans must fall before the start of 12, J. Evol. Biol. 9. Pletcher, S. D. Model fitting and hypothesis testing for age-specific mortality data. isolation. However, the MRCA date would be unaffected, because 430–439 (1999). 10. Ohno, S. The Malthusian parameter of ascents: What prevents the exponential increase of one’s today there are no remaining native Tasmanians without some ancestors? 93, 15276–15278 (1996). Proc. Natl Acad. Sci. USA European or mainland Australian ancestry. 11. Derrida, B., Manrubia, S. C. & Zanette, D. H. Distribution of repetitions of ancestors in genealogical No large group is known to have maintained complete repro- 281, trees. Physica A 1–16 (2000). ductive isolation for extended periods. The populations on either 12. Wiuf, C. & Hein, J. On the number of ancestors to a DNA sequence. 147, 1459–1468 (1997). Genetics 423–446 (1995). 13. Jones, R. Tasmanian archaeology: Establishing the sequences. Ann. Rev. Anthropol. 24, side of the Bering Strait appear to have exchanged mates throughout 14 14. Fitzhugh, W. W. & Chausonnet, V. (eds) Crossroads of Continents: Cultures of Siberia and Alaska . Religious the period documented in the archaeological record (Smithsonian Institution Press, Washington DC, 1988). isolates such as the Samaritans occasionally have absorbed migrants ́ -Tamir, B. et al. 15. Bonne Maternal and paternal lineages of the Samaritan isolate: Mutation rates and 15 . Even populations on isolated Pacific from outside the group Ann. Hum. Genet. 153–164 (2003). time to most recent common male ancestor. 67, 16 16. Morton, N. E., Harris, D. E., Yee, S. & Lew, R. Pingelap and Mokil atolls: Migration. Am. J. Hum. Genet. . islands have experienced occasional infusions of newcomers 23, 339–349 (1971). Even if rates of migration between some adjoining populations (Duke Univ. Press, Cultures in Contact: World Migrations in the Second Millennium 17. Hoerder, D. are very low, the time to the MRCA tends not to change substan- Durham, North Carolina, 2002). tially. For example, with a migration rate across the Bering Strait of 717–721 (2003). 72, Am. J. Hum. Genet. The genetic legacy of the Mongols. et al. 18. Zerjal, T. 19. Weiss, K. M. & Maruyama, T. Archeology, population genetics and studies of human racial ancestry. just one person in each direction every ten generations, rather than Am. J. Phys. Anthropol. 44, 31–50 (1976). the ten per generation in the more conservative simulation 20. Ward, R. H. & Neel, J. V. Gene frequencies and microdifferentiation among the Makiritare indians. IV. only increases from 3,415 years to 3,668 years. T described earlier, n A comparison of a genetic network with ethnohistory and migration matrices; a new index of genetic isolation. 538–561 (1970). 22, Am. J. Hum. Genet. Conversely, other factors could reduce the time to the MRCA NATURE | VOL 431 | 30 SEPTEMBER 2004 | www.nature.com/nature 565 Nature 4 200 © Publishing Group

5 letters to nature 9–12 21. Jorde, L. B. in Current Developments in Anthropological Genetics (eds Mielke, J. H. & Crawford, M. H.) , but have been limited to fewer than ten generations. responses 135–208 (Plenum, New York, 1980). The long-term response to selection and the properties of popu- 22. Notohara, M. The coalescent and the genealogical process in geographically structured populations. remain unknown, and constitute an lations adapted to elevated CO 2 59–75 (1990). J. Math. Biol. 29, 23. Wilkinson-Herbots, H. M. Genealogy and subpopulation differentiation under various models of important limit on our ability to predict future plant productivity. J. Math. Biol. 37, 535–585 (1998). population structure. We used a microbial model system in which large population size new hope for a difficult and divided 24. Hey, J. & Machado, C. A. The study of structured populations — and short generation time make it possible to evaluate evolutionary 535–543 (2003). 4, Nature Rev. Genet. science. change caused by the spread of novel mutations over hundreds of Chlamydomonas reinhardtii is a unicellular green alga generations. Supplementary Information . www.nature.com/nature accompanies the paper on that has been extensively used to study the physiology and genetics 13 Acknowledgements The research of D.L.T.R. was supported by the National Institutes of Health. . It possesses a carbon-concentrating mechanism of photosynthesis near the active (CCM), which increases the concentration of CO 2 Competing interests statement The authors declare that they have no competing financial site of ribulose 1,5-bisphosphate carboxylase–oxygenase (Rubisco), interests. in common with most other eukaryotic microalgae that have been 14 . We set up ten isogenic selection lines from each of two studied Correspondence and requests for materials should be addressed to D.L.T.R. ([email protected]). (ambient ancestral genotypes, half being grown at ambient CO 2 lines) and half at a concentration that increased from ambient to 1,050 p.p.m. over about 600 generations and was then maintained at 5 cells this level for a further 400 generations (high lines). At least 10 per line were transferred for 125 transfers in a buffered, nutrient- ... ... ... rich medium. The history of these lines thus emulates the con- ditions that photosynthetic organisms are likely to experience Phenotypic consequences of 1,000 levels alone. during the next century or so, with respect to CO 2 concentration is The physiological effect of elevated CO generations of selection at 2 expected to be an increase in photosynthesis, causing an increase elevated CO in a green alga in growth. Net photosynthesis in the ambient lines increased by 2 (Fig. 1a). The about 30% when they were grown at high CO 2 ́ ambient lines diverged through time so that by the end of the Sine ad Collins & Graham Bell experiment they varied significantly in the rate of photosynthesis Biology Department, McGill University, Montreal, Quebec H3A 1B1, Canada ¼ 9.0, P , 0.001) F (one-way analysis of variance (ANOVA): 9,18 ... ... concentrations. The high lines had when grown at ambient CO 2 Estimates of the effect of increasing atmospheric CO concen- 2 , which increased by normal rates of photosynthesis at ambient CO 2 trations on future global plant production rely on the physio- . However, more than 50% as an average over all lines at high CO 2 logical response of individual plants or plant communities when this effect was very inconsistent: one group of high lines had low exposed to high CO (refs 1–6). Plant populations may adapt to 2 rates whereas a second group had very high rates of photosynthesis the changing atmosphere, however, such that the evolved plant concentration (Fig. 1a). This distinction was not related at high CO 2 communities of the next century are likely to be genetically to the identity of the ancestor, and represented significantly more 7–12 different from contemporary communities . The properties divergence in photosynthetic rates than was seen in the ambient of these future communities are unknown, introducing a bias 0.005). ¼ ¼ P 10.5, F lines ( 1,16 of unknown sign and magnitude into projections of global was correlated The growth rate of cultures grown at elevated CO 2 carbon pool dynamics. Here we report a long-term selection with their photosynthetic rate among the ambient lines, but not experiment to investigate the phenotypic consequences of selec- on among the high lines (Fig. 1b). The physiological effect of CO 2 tion for growth at elevated CO concentrations. After about 1,000 2 photosynthesis was reflected by growth in pure culture, where the generations, selection lines of the unicellular green alga Chlamy- maximal rate of increase (Fig. 1c) and the limiting density (Fig. 1d) failed to evolve specific adaptation to a CO domonas concen- 2 of both the ambient and the high lines are enhanced substantially by tration of 1,050 parts per million. Some lines, however, evolved a . However, there was no indication of a parallel evolution- high CO 2 syndrome involving high rates of photosynthesis and respiration, ary response: by the end of the selection experiment, the high lines combined with higher chlorophyll content and reduced cell size. ; their had not become specifically adapted to growth at high CO 2 These lines also grew poorly at ambient concentrations of CO . 2 being no greater than, and perhaps even less growth at high CO 2 We tentatively attribute this outcome to the accumulation of than, the growth of the ambient lines. There was nevertheless an conditionally neutral mutations in genes affecting the carbon indirect response: the growth of some high lines was markedly concentration mechanism. concentrations where two of the lines impaired at ambient CO 2 1,2 Plant growth depends on CO , which is expected concentration could scarcely be propagated. This result was supported by the 2 to rise from current levels of about 400 parts per million (p.p.m.) to outcome of competition assays in which the selection lines were 3 between 700 and 1,000 p.p.m. during the next century . In response, mixed with standard genetically marked strains and the change in 4 6 5 global plant productivity in forests , grasslands , agroecosystems frequency during growth in culture recorded (Table 1). The high and other ecosystems is expected to increase. Projections of future , lines had considerably lower competitive ability at ambient CO 2 net primary productivity are complicated by synchronous changes where three of them (including the two with strongly reduced growth in temperature and other factors, but most models predict increases in pure culture) were such weak competitors that they were consist- in the land–atmosphere and ocean–atmosphere fluxes from current ently eliminated by the tester strains within 10–15 generations. They 5 Pg C per 2 petagrams (Pg) C per year to about 2 .2 values of were, however, no more successful than the ambient lines at high 3 year . This process is likely to be complicated by shifts in the species . In short, 1,000 generations of selection at high CO concen- CO 2 2 7 composition of plant communities , and more fundamentally by ,whereas trations had caused no increase in growth at high CO 2 evolutionary changes within plant populations. In the very long term, was often considerably reduced. growth at ambient CO 2 this may involve the extinction of some groups and the radiation of Photosynthesis is linearly related to respiration in the dark 8 others , but within a few hundred generations most plant popu- ; this relationship is the same for among lines at ambient CO 2 lations may adapt to the increased supply of inorganic carbon. Chlamydo- ambient and high lines (Fig. 2a). It has been shown in Selection experiments with plants have demonstrated a variety of consumption provide a monas that post-illumination rates of O 2 566 NATURE | VOL 431 | 30 SEPTEMBER 2004 | www.nature.com/nature Nature 4 200 © Publishing Group

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