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New Vistas on the Distant Past

The genetic debate

In the days before we had much ancient DNA, it was easy to assume that the distribution of mitochondrial (mtDNA) haplogroups we see today is largely due to the Mesolithic recolonisation of Europe. Bryan Sykes argued this case in popular and scholarly works at the start of the present millennium. Initially the only mtDNA haplogroup that he linked to the later spread of Neolithic farmers into Europe from the Near East was J. He calculated that 80% of native Europeans could trace their ancestry to European hunter-gatherers. ^{1B. Sykes, The Seven Daughters of Eve (2001); M. Richards, B. Sykes et al, Tracing European founder lineages in the Near Eastern mtDNA pool, American Journal of Human Genetics, vol. 67, no. 5 (2000), pp. 1251-76.} At around the same time a similar conclusion was drawn from Y-DNA.^{2O. Semino et al, The genetic legacy of paleolithic Homo sapiens sapiens in extant Europeans: a Y chromosome perspective, Science, vol. 290 (2000), pp. 1155-59; and see J.T. Lell and D.C. Wallace, The peopling of Europe from the maternal and paternal perspectives, American Journal of Human Genetics, vol. 67, no. 6 (2000), pp.1376–1381.}

Could this be true? It seemed a triumphant vindication of those who had long held that agriculture was spread culturally, rather than by mass migration. Television programmes took up the tale. The Channel 4 series The Face of Britain (2007) and RTE's The Blood of the Irish (2009) presented the Celts of Britain and Ireland as descended from Mesolithic colonisers from the Continent. But by the time they were shown, population genetics had moved on.

Clines and waves

Geneticists realised that where they find the greatest genetic diversity of a haplogroup is most likely to be its point of origin, since the longer a lineage has been in a place, the longer it has had to accumulate mutations. That changed the picture. The Mesolithic re-colonisers moved from south to north, but the dominant Y-DNA genetic cline in Europe is from east to west. That suggests that later migrations bringing farming and/or metallurgy were more important in creating the present paternal lineages of Europe.^{3B. Arredi, E.S. Poloni, C. Tyler-Smith, The peopling of Europe, in M. Crawford (ed.), Anthropological Genetics: Theory, method and applications (2007).}

A study by Patricia Balaresque and colleagues relied heavily upon upon one type of calculation of genetic diversity - that based on STRs within the Y-Chromosome. They concentrated upon one particular subclade of R1b, concluding that it could be linked to the spread of farming into Europe.^{4P. Balaresque et al., A predominantly neolithic origin for European paternal lineages, PLoS Biology, vol. 8, no. 1 (2010).} Their approach was dismantled the following year by a reassessment which found no particular differences in diversity.^{5G.B.J. Busby et al., The peopling of Europe and the cautionary tale of Y chromosome lineage R-M269, Proceedings of the Royal Society B: Biological Sciences, published online before print, August 24, 2011.} Yet Kristian Herrera and colleagues show the variance of the whole R1b haplogroup to be clearly highest in Western Asia.^{6K. J. Herrera et al., Neolithic patrilineal signals indicate that the Armenian plateau was repopulated by agriculturalists, European Journal of Human Genetics, advance online 16 November 2011.} Only by ignoring the Asian data can one see little variance.

Not that diversity is always a reliable guide. A present-day population could have acquired Y-DNA diversity from diverse waves of immigrants, or by a mass movement from place A to place B, taking with it the full diversity that it had at place A. So diversity is most convincing when supported by other evidence. In this case the chain of SNP mutations within R1b runs from east to west, with those which occurred earliest being most prevalent towards the east. On the global level, it is the chain of mutations within mtDNA and Y-DNA that enabled geneticists to work back to a genetic Adam and Eve in Africa at the root of the human family tree. The people closest to this Adam and Eve exhibit the highest genetic diversity in the world across the genome.^{7M. Melé et al., Recombination gives a new insight in the effective population size and the history of the Old World human populations, Molecular Biology and Evolution (online 1 September 2011 ahead of print); J. Xing et al., Toward a more uniform sampling of humangenetic diversity: a survey of worldwide populations by high-density genotyping, Genomics, vol. 96, no. 4 (October 2010), pp. 199-210; G. Laval et al., Formulating a historical and demographic model of recent human evolution based on resequencing data from noncoding regions, PLoS ONE,vol.5, no. 4 (2010): e10284; J. Chiaroni, P. Underhill and L.L. Cavalli-Sforza,Y chromosome diversity, human expansion, drift and cultural evolution, Proceedings of the National Academy of Sciences of the United States of America, vol.106, no. 48 (December 2009), pp. 20174-79; R.N. Gutenkunstet al., Inferring the joint demographic history of multiple populations from multidimensional SNP frequency data, PLoS Genetics, vol. 5, no. 10 (1 October 2009), pp. 1-11; M. DeGiorgio, M. Jakobssonet and N.A. Rosenberg,Explaining worldwide patterns of human genetic variation using a coalescent-based serial founder model of migration outward from Africa, Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 38 (Sep 2009), pp. 16057-16062; O. Deshpande, S.Batzoglou, M.W. Feldman and L.L. Cavalli-Sforza, A serial founder effect model for human settlement out of Africa, Proceeding of the Royal Society B: Biological Sciences, vol. 276 (2009), pp. 291-300; I. Ionita-Laza, C.Lange and N.M. Laird, Estimating the number of unseen variants in the human genome, Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 13 (March 2009), pp. 5008-5013; J. Z.Li et al, Worldwide human relationships inferred from genome-wide patterns of variation, Science, vol. 319, (2008), pp. 1100-04; G. Hellenthal, A. Auton, D. Falush, Inferring human colonization history using a copying model, PLoS Genetics, vol. 4, no. 5 (May 2008); Jakobsson, M. etal, Genotype, haplotype and copy-number variation in worldwide human populations, Nature, no. 451 (21 February 2008), pp. 998-1003; R.Klein, Out of Africa and the evolution of human behavior, Evolutionary Anthropology: Issues, News, and Reviews, vol. 17, no. 6 (2008), pp. 267- 281; Q. Ayub et al., Reconstruction of human evolutionary tree using polymorphic autosomal microsatellites, American Journal of Physical Anthropology, vol. 122 (2003), pp. 259-268.}

Jacques Chiaroni and his colleagues described the way that different kinds of genetic spread leave characteristic patterns. They have christened one the Surfing Effect. A mutation that occurs in the wave front of an expanding population will have an advantage. It will have a better chance of becoming predominant within the breeding group, because that is where the migrating population is smallest. A successful mutation will surf the wave and end up at saturation level where the expanding population meets a geographical barrier. A good example is the commonest Y-DNA haplogroup of western Europe - R1b1b2 (M269). It flooded over Europe from the east, spawning subclades as it went, until it was stopped by the Atlantic Ocean. On the Atlantic seaboard it reaches saturation level.^{8J. Chiaroni, P. Underhill and L.L. Cavalli-Sforza, Y chromosome diversity, human expansion, drift and cultural evolution, Proceedings of the National Academy of Sciences of the United States of America, vol.106, no. 48 (December 2009), pp. 20174-79; N.M Myres et al., A major Y-chromosome haplogroup R1b Holocene era founder effect in Central and Western Europe, European Journal of Human Genetics, vol. 19, no. 1 (January 2011), pp. 95–101.} How this might work in practice is demonstrated by a study of a population expansion in historic times. Genealogical analysis showed that majority of the present population of Saguenay Lac Saint-Jean in Quebec can be traced back to ancestors having lived directly on or close to the wave front of 17th-century expansion.^{9C. Moreau et al., Deep human genealogies reveal a selective advantage to be on an expanding wave front, Science, published online November 3 2011.}

Refining by subclade

Early studies painted with a broad brush. Only a few mtDNA haplogroups had been discovered at that time; each was given a letter to identify it. Then researchers attempted to make sense of their distribution. The gradual process of breaking these parent groups down into subclades has created a more subtle picture. For example mtDNA T had been seen as Palaeolithic, yet sub-haplogroup Tl is one of the clearest examples of a lineage cluster with a much earlier expansion in Western Asia than in Europe.^{10K. Tambets et al, Complex Signals for Population Expansions in Europe and Beyond, in P. Bellwood and C. Renfrew (eds.), Examining the Farming/Language Dispersal Hypothesis (2002), pp. 454-5.} Both T and K have been found in the DNA of early farmers in the Levant and Europe.^{11E. Fernández, et al., Mitochondrial DNA genetic relationships at the ancient Neolithic site of Tell Halula, Forensic Science International: Genetics Supplement Series, vol.1, no. 1 (2008), pp. 271–273; W. Haak et al, Ancient DNA from the First European Farmers in 7500-Year-Old Neolithic Sites, Science, vol. 310, no. 5750 (2005), pp. 1016-1018.} Similarly, a closer look at mtDNA H reveals its complexity. H itself was born in the Near East and spread into Europe. H3 is largely limited to Europe and North Africa. Both H1 and H3 have their densest distribution in Iberia. From this it was argued that these two subclades spread from the Franco-Cantabrian glacial refuge as the climate warmed in the Mesolithic period.^{12A. Achilli et al, The molecular dissection of mtDNA Haplogroup H confirms that the Franco-Cantabrian glacial refuge was a major source for the European gene pool, American Journal of Human Genetics, vol. 75 (2004), pp.910–918; L Pereira et al, High-resolution mtDNA evidence for the late-glacial resettlement of Europe from an Iberian refugium, Genome Research, vol. 15 (2005), pp. 19-24.} This would be highly significant for the peopling of Europe. Not only is H itself the predominant haplogroup in Europe, carried by almost half of the population, but its commonest subclade is H1. It represents about 30% of H and 13% of the total European mtDNA pool. Yet breaking down H1 itself into subclades revealed that some are barely present in Iberia. H1a and H1b are densest in Eastern Europe (see Slavic genetic markers). Even more significantly, H1 and H3 have a low diversity in Cantabrian Spain and in particular among the Basques. Instead the highest diversity and allelic richness of H1 and H3 in Europe is found in north-eastern and north-central regions, while the Near East has the greatest overall diversity of H1, and North Africa that for H3. The once-popular idea of the Basques as the source population for most of modern-day Europe is not supported by this closer examination. ^{13O. García et al, Using mitochondrial DNA to test the hypothesis of a European post-glacial human recolonization from the Franco-Cantabrian refuge, Heredity, vol. 106 (2011), pp. 37–45; H. Ennafaa et al., Mitochondrial DNA haplogroup H structure in North Africa, BMC Genetics, vol.10 (2009), no. 8.}

Instead it suggests that H1 and possibly H3 arrived in Europe with the first farmers. Against this is one sample of H1b reported in Mesolithic DNA in Portugal.^{14H. Chandler, B. Sykes and J. Zilhão, Using ancient DNA to examine genetic continuity at the Mesolithic-Neolithic transition in Portugal, in P. Arias, R. Ontanon and C. Garcia-Monco (eds.), Actas del III Congreso del Neolitico en la Peninsula Iberica (2005), pp. 781-86.} However this comes from a study carried out some years ago, when ancient DNA studies were less reliable. The parent and grandparent of H (HV and R0) also have their origins in Western Asia. HVa, R0a, U7 and U3 have frequency peaks there, so their appearance in Europe may be another clue to the spread of farming.^{15A. Achilli et al, Mitochondrial DNA variation of modern Tuscans supports the Near Eastern origin of Etruscans, American Journal of Human Genetics, vol. 80, no. 4 (2007), pp. 759–768.}

H5* is most frequent and diverse in the western Caucasus, while H5a has a stronger European distribution. H5a is thought to be only 7000-8000 years old, so its wide, though low, spread over Europe suggests that significant migration took place even after the initial spread of farming.^{16U. Roostalu et al, Origin and expansion of haplogroup H, the dominant human mitochondrial DNA lineage in West Eurasia: the Near Eastern and Caucasian perspective, Molecular Biology and Evolution, vol. 24, no. 2 (2007), pp. 436-448.}

Dating

However debate has swung to and fro over the dating of haplogroups. Geneticists in recent years have often used Zhivotovsky's evolutionary effective dating method for Y-DNA, which adjusts the calculated pedigree (genealogical) mutation rate, since in some populations the latter produced unexpectedly late dates.^{17L.A. Zhivotovsky et al., The effective mutation rate at Y chromosome short tandem repeats, with application to human population-divergence time, American Journal of Human Genetics, vol. 74 (2004), pp. 50–61; L. A. Zhivotovsky, Difference between evolutionarily effective and germ line mutation rate due to stochastically varying haplogroup size, Molecular Biology and Evolution, vol. 23, no. 12 (2006), pp. 2268-2270.} Unfortunately this ad-hoc adjustment seems generally misapplied, producing dating estimates two or three times too old. For example Marcin Woźniak and colleagues point out that the pedigree mutation rate for R1a1a1g [M458] is more consistent with the archaeological record for the Slavs.^{18M. Woźniak et al., Similarities and distinctions in Y Chromosome gene pool of Western Slavs, American Journal of Physical Anthropology, vol. 142, no. 4 (2010), pp. 540-548.} A study of the Caucasus region found that genealogical estimates gave a good fit with the linguistic and archaeological dates, while the evolutionary effective rates fell far outside them.^{19O. Balanovsky et al., Parallel Evolution of Genes and Languages in the Caucasus Region, Molecular Biology and Evolution, published online ahead of print 13 May 2011.} Another approach is directly genealogical. Both surnames and Y-DNA haplogroups are passed down in the male line. A group of men with a surname of the same origin should have a common ancestor at the time of surname development. One study found that they mainly did, using a mutation rate similar to the genealogical rather than the evolutionary.^{20T.E. King and M.A. Jobling, Founders, drift, and infidelity: the relationship between Y chromosome diversity and patrilineal surnames, Molecular Biology and Evolution, vol. 26, no. 5 (May 2009), pp.1093-1102.}

However problems with the pedigree rate remain. Dating estimates will vary according to which microsatellite loci are used, since some mutate faster than others. New approaches take this factor into account, but are only very recently reaching publication.^{21G. B. J. Busby and C. Capelli, Microsatellite choice and Y chromosome variation: attempting to select the best STRs to date human Y chromosome lineages, paper read at the European Human Genetics Conference at Amsterdam May 28 - 31 2011; G. B. J. Busby et. al., The peopling of Europe and the cautionary tale of Y chromosome lineage R-M269, Proceedings of the Royal Society B: Biological Sciences, published online before print, August 24, 2011; C. Burgarella and M. Navascués, Mutation rate estimates for 110 Y-chromosome STRs combining population and father–son pair data, European Journal of Human Genetics, vol. 19 (2011), pp. 70–75; W. Shi et al., A worldwide survey of human male demographic history based on Y-SNP and Y-STR data from the HGDP-CEPH populations, Molecular Biology and Evolution, vol. 27, no. 2 (2010), pp. 385-393.} Attempts to calibrate the human mtDNA clock are no less controversial.^{22B. M. Henn et al., Characterizing the time dependency of human mitochondrial DNA mutation rate estimates, Molecular Biology and Evolution, vol. 26 (2009), no. 1, pp. 217-230; Endicott et al., Evaluating the mitochondrial timescale of human evolution, Trends in Ecology and Evolution vol. 24, no. 9 (2009), pp. 515-521; S. Rosset et al., Maximum-likelihood estimation of site-specific mutation rates in human mitochondrial DNA from partial phylogenetic classification, Genetics, vol. 180 (November 2008), pp. 1511–1524; M.P. Cox, Accuracy of molecular dating with the rho statistic: deviations from coalescent expectations under a range of demographic models, Human Biology, vol. 80, no 4 (2008), pp.335-357; C.D. Millar et al., Mutation and evolutionary rates in Adélie Penguins from the Antarctic, PLoS Genetics vol. 4, no. 10 (October 2008).} To cap the confusion, a recent study found substantial variance in sex-specific mutation rates between families,^{23D.F. Conrad et al., Variation in genome-wide mutation rates within and between human families, Nature Genetics, Published online 12 June 2011 ahead of print.} throwing a cloud of doubt over all dating estimates.

Modern versus ancient DNA

Another problem arises from the common assumption that a modern population reflects an ancient local gene pool. That would be convenient. It is a lot easier to obtain blood or saliva samples from the living, than to retrieve DNA from skeletons. Yet several studies of ancient DNA (aDNA) have discovered no relationship between ancient people and those who now occupy the same area.^{24L. Melchior, Evidence of Authentic DNA from Danish Viking Age Skeletons Untouched by Humans for 1,000 Years, PLoS ONE 3(5): e2214; Töpf et al., Ancient human mtDNA genotypes from England reveal lost variation over the last millennium, Biology Letters, vol. 3, no. 5 (2007), pp. 550–553; Price et al., The impact of divergence time on the nature of population structure: an example from Iceland, PLoS Genetics vol 5, no. 6 (2009): e1000505; S. Guimaraes et al., Genealogical discontinuities among Etruscan, Medieval and contemporary Tuscans, Molecular Biology and Evolution, published online on July 1, 2009: doi:10.1093/molbev/msp126; S.E. Smith et al., Inferring population continuity versus replacement with aDNA: a cautionary tale from the Aleutian Islands, Human Biology, vol. 81, no. 4 (August 2009); B. Bramanti et al, Genetic Discontinuity Between Local Hunter-Gatherers and Central Europe’s First Farmers, Science, (published online September 3, 2009): DOI: 10.1126/science.1176869; H. Malmstrom et al, Ancient DNA Reveals Lack of Continuity between Neolithic Hunter-Gatherers and Contemporary Scandinavians, Current Biology, vol. 19 (Nov 2009), pp. 1–5.} For example the greatest modern density and diversity of H5* appears in the Western Caucasus, suggesting that it spread from there. Yet the Caucasus attracted Neolithic farmers from the Near East and numerous later waves of incomers, which might confuse the picture. H5 was present in Neolithic Syria, ^{25E. Fernández et al., Mitochondrial DNA genetic relationships at the ancient Neolithic site of Tell Halula, Forensic Science International: Genetics Supplement Series, vol.1, no. 1 (2008), pp. 271–273.} so the Near East is the more likely point of origin.

To create firm links between haplogroups and long-gone cultures there is no substitute for aDNA. Yet we should be cautious. The problem of contamination with modern DNA bedevilled ancient DNA study in its early years. Little weight can be placed on the results from early studies unless they have been replicated. More recent studies usually report their methodology in reassuring detail. However samples tend to be too small for statistical significance. Conclusions about the entire population of Europe cannot be drawn from a handful of individuals from the same grave, very probably related. Far greater statistical weight can be placed on those studies which sample more widely and achieve a higher number of results, and on the collective results of multiple studies. A body of knowledge is gradually building up, which has started to suggest the dates that particular haplogroups first arrived in Europe.

However, even if we can prove by ancient DNA that a particular haplogroup had arrived in a particular place by a given date, that doesn't rule out its arrival again in later waves of incomers. Indeed it could be arriving again right now on the latest plane. People will move about! This takes us back to a previous point. We need to discriminate between various subclades of the parent haplogroups. Ancient DNA tested recently to a high degree of resolution is the most valuable.

It might seem a statement of the obvious that present populations descend from ancient ones. However at least one author has put the cart before the horse and attempted to guess the origin of ancient DNA from that of present people. This is singularly foolish. The present spread of haplogroups tells a story of the migrations of the descendants of those ancient people. It is equally interesting if we find that they had no descendants. Many lineages will have died out simply by chance. Yet we may find some cultures, classes or individuals more prolific in their offspring.

Genome-wide vs sex-specific

Mapping the first human genome was a huge project, which took over a decade and cost three billion US dollars. Today both the time and cost of sequencing have dropped so sharply that a subsequent project to sequence 1000 genomes is well under way, while the International HapMap Project has reached a similar stage with over 1000 genomes. Both make it possible to compare full genomes from different ethnic groups, and additional genomes are available from regional projects. So genome-wide population comparisons are increasingly popular. They give a broad picture of the genetic make-up of a population and its affinities.

However these can only tell us if present-day population X has a similarity with present-day population Y. They cannot tell us how this arose. Sex-specific markers remain the clearest guide to migration, since mtDNA and Y-DNA are passed down from parent to child without recombination. The accumulation of spontaneous mutations along these lineages provide clear evidence of direction of flow. They also make it possible to detect sex-biased migration, for example male-dominated bands of traders taking local wives.

Progress

It will take time to tease out the many strands of migration and mobility that have created the present genetic kaleidoscope in Europe. Over the last decade there has been rapid progress. Where once there were simple trees for mtDNA and Y-DNA with a few bare branches, now there are bushy structures with a multitude of twigs, kept up to date online at ISOGG YDNA tree and PhyloTree (mtDNA). The breakdown into smaller and smaller subclades is crucial in distinguishing between different origins. Improved techniques of extracting ancient DNA give hope of driving down its cost and making the results more reliable. The quest for ancient DNA is becoming ever more ambitious, with entire genomes extracted for a few individuals.

Notes

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• Peopling of Europe
• First Europeans
• Mesolithic hunters
• Genetic debate
• Who do you look like?
• The first farmers
• Copper Age
• Indo-European family
• Indo-European genetics
• Linguistic arguments
• Beaker Folk
• Iron Age
• Early Greeks
• Etruscans and Romans
• Great Wandering
• Germani
• Goths and Vandals
• Slavs
• Vikings
• Conclusion
• Supplements
• Basques
• Origin stories
• Y-DNA I
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