Mitochondrial Genome Sequences and Their Phylogeographic Interpretation

Vincent Macaulay, University of Glasgow, Glasgow, UK
Martin B Richards, University of Huddersfield, Huddersfield, UK

Published online: September 2013

DOI: 10.1002/9780470015902.20843.pub2

Abstract

The strong phylogenetic signal provided by mitochondrial deoxyribonucleic acid (mtDNA) sequences within species is being exploited to reconstruct the maternal genealogy and anchor it in space and time. This is the starting point for interpretations of the processes in population history that led to those patterns, as illustrated here for humans. Mitochondrial phylogeography began by revolutionising our view of modern human origins, with the demonstration that modern humans dispersed from Africa approximately 60 000 years ago. Now benefitting from the high genealogical and chronological resolution afforded by whole‐mtDNA sequences, and despite the advent of genome‐wide analyses, mtDNA continues to illuminate prehistoric settlement and dispersal history. It has often led to challenges to received wisdom, such as the stress on pre‐Neolithic dispersals at the end of the Ice Age in many parts of the world, and the database of contemporary variation is currently being augmented by rapidly increasing information from ancient DNA.

Key Concepts:

  • Mitochondrial DNA is now routinely analysed at the level of whole‐mtDNA genome sequences.

  • The human mtDNA gene tree is an estimate of the maternal genealogy and preserves a record of the dispersal history of our species, in the distribution of its branching points in space and time, or ‘phylogeography’.

  • A time scale is provided by an independently calibrated mutation rate, the ‘molecular clock’, which is now available for whole‐mtDNA sequences and allows for the effects of purifying selection.

  • Although phylogeographic inference can be criticised for lacking a formal hypothesis testing framework, proposed alternatives based on simulation are currently insufficient to tackle the nuances of real human dispersal histories.

  • Variation in mtDNA has led to a number of revolutionary models in human evolutionary history, beginning with the African origin of modern humans.

  • More recent suggestions have included a single southern‐coastal dispersal route out of Africa and the importance to the shaping of extant human diversity of hunter–gatherer dispersals and expansions at the end of the last Ice Age.

  • An increasing volume of data from ancient DNA holds great promise not only for testing interpretations of contemporary variation but also for identifying both ancient processes that left no trace in the modern gene pool and more recent dispersals that studying extant cannot resolve.

  • Genome‐wide analyses now allow both testing of hypotheses arising from mtDNA studies and access to many previously unanswerable questions, but mtDNA nevertheless retains a vital role due to its relative genealogical and chronological precision.

Keywords: phylogeography; phylogeny; mtDNA; archaeogenetics; genealogy; founder analysis

Figure 1.

The effect of a single migration event on the genealogy, motivating the idea of founder analysis. (a) All individuals in the settled region trace back to three individuals, who migrated from the source region. The source genealogy is deep (left); the settled gene genealogy (right) consists of a small number of clusters of closely related individuals that trace back to the three pioneers. (b) The reflection of this signal in the DNA sequences. Green circles are DNA sequences recovered from the settled region, red circles from the source region and the links in the network indicate the mutations that relate the sequences. (Small solid black circles are inferred sequences not actually observed.) The common ancestor is shown with a star. Founder analysis seeks to identify those sequences (marked by crosses) that migrated, and use the mutations that have accumulated on top of these ‘founder types’ to derive a lower bound on the time of the migration event. By identifying founder sequences explicitly, mutations that arose before the migration event (somewhere in the dashed part of the tree, upper right) will not be included at the time estimation.

close

References

Bandelt H‐J, Kong QP, Yao YG et al. (2006) Estimation of mutation rates and coalescence times: some caveats. In: Bandelt HJ, Macaulay V and Richards M (eds) Mitochondrial DNA and the Evolution of Homo sapiens, pp 47–90. Berlin: Springer–Verlag.

Bandelt H‐J, Macaulay VA and Richards MB (2002) What molecules can't tell us about the spread of languages and the Neolithic. In: Renfrew C and Bellwood P (eds) Examining the Language‐farming Dispersal Hypothesis. Cambridge: McDonald Institute for Archaeological Research.

Behar DM, van Oven M, Rosset S et al. (2012) A “Copernican” reassessment of the human mitochondrial DNA tree from its root. American Journal of Human Genetics 90: 675–684.

Behar DM, Villems R, Soodyall H et al. (2008) The dawn of human matrilineal diversity. American Journal of Human Genetics 82: 1–11.

Bramanti B, Thomas MG, Haak W et al. (2009) Genetic discontinuity between local hunter‐gatherers and Central Europe's first farmers. Science 326: 137–140.

Briggs AW, Good JM, Green RE et al. (2009) Targeted retrieval and analysis of five Neandertal mtDNA genomes. Science 325: 318–321.

Brotherton P, Haak W, Templeton J et al. (2013) Neolithic mitochondrial haplogroup H genomes and the genetic origins of Europeans. Nature Communications 4: 1764.

Cann RL, Stoneking M and Wilson AC (1987) Mitochondrial DNA and human evolution. Nature 325: 31–36.

Deguilloux MF, Leahy R, Pemonge MH and Rottier S (2012) European neolithization and ancient DNA: an assessment. Evolutionary Anthropology 21: 24–37.

Endicott P, Ho SYW, Metspalu M et al. (2009) Evaluating the mitochondrial timescale of human evolution. Trends in Ecology and Evolution 24: 515–521.

Endicott P, Ho SYW and Stringer C (2010) Using genetic evidence to evaluate four palaeoanthropological hypotheses for the timing of Neanderthal and modern human origins. Journal of Human Evolution 59: 87–95.

Fernandes V, Alshamali F, Alves M et al. (2012) The Arabian cradle: mitochondrial relicts of the first steps along the southern route out of Africa. American Journal of Human Genetics 90: 347–355.

Haak W, Balanovsky O, Sanchez JJ et al. (2010) Ancient DNA from European early Neolithic farmers reveals their Near Eastern affinities. PLoS Biology 8: e1000536.

Haak W, Forster P, Bramanti B et al. (2005) Ancient DNA from the first European farmers in 7500‐year‐old Neolithic sites. Science 310: 1016–1018.

Hill C, Soares P, Mormina M et al. (2007) A mitochondrial stratigraphy for Island Southeast Asia. American Journal of Human Genetics 80: 29–43.

Hudjashov G, Kivisild T, Underhill PA et al. (2007) Revealing the prehistoric settlement of Australia by Y chromosome and mtDNA analysis. Proceedings of the National Academy of Sciences of the USA 104: 8726–8730.

Kivisild T, Metspalu M, Bandelt H‐J et al. (2006) The world mtDNA phylogeny. In: Bandelt HJ, Macaulay V and Richards M (eds) Mitochondrial DNA and the Evolution of Homo sapiens, pp 150–179. Berlin: Springer–Verlag.

Kivisild T, Reidla M, Metspalu E et al. (2004) Ethiopian mitochondrial DNA heritage: tracking gene flows across and around the Gate of Tears. American Journal of Human Genetics 75: 752–770.

Kivisild T, Shen P, Wall DP et al. (2006) The role of selection in the evolution of human mitochondrial genomes. Genetics 172: 373–387.

Kong Q‐P, Bandelt H‐J, Sun C et al. (2006) Updating the East Asian mtDNA phylogeny: a prerequisite for the identification of pathogenic mutations. Human Molecular Genetics 15: 2076–2086.

Krause J, Briggs AW, Kircher M et al. (2010) A complete mtDNA genome of an early modern human from Kostenki, Russia. Current Biology 20: 231–236.

Macaulay V, Hill C, Achilli A et al. (2005) Single, rapid coastal settlement of Asia revealed by analysis of complete mitochondrial genomes. Science 308: 1034–1036.

Macaulay V, Richards M, Hickey E et al. (1999) The emerging tree of West Eurasian mtDNAs: a synthesis of control‐region sequences and RFLPs. American Journal of Human Genetics 64: 232–249.

Malyarchuk B, Derenko M, Grzybowski T et al. (2010) The peopling of Europe from the mitochondrial haplogroup U5 perspective. PLoS One 21: e10285.

Malyarchuk B, Grzybowski T, Derenko M et al. (2008) Mitochondrial DNA phylogeny in Eastern and Western Slavs. Molecular Biology and Evolution 25: 1651–1658.

Mellars P, Gori KC, Carr M, Soares P and Richards MB (2013) Genetic and archaeological perspectives on the initial modern human colonization of southern Asia. Proceedings of the National Academy of Sciences of the United States of America 110: 10699–10704.

Metspalu M, Kivisild T, Bandelt H‐J, Richards M and Villems R (2006) The pioneer settlement of modern humans in Asia. In: Bandelt HJ, Macaulay V and Richards M (eds) Mitochondrial DNA and the Evolution of Homo sapiens, pp 181–199. Berlin: Springer–Verlag.

Nielsen R and Beaumont MA (2009) Statistical inferences in phylogeography. Molecular Ecology 18: 1034–1047.

Olivieri A, Achilli A, Pala M et al. (2006) The mtDNA legacy of the Levantine Early Upper Palaeolithic in Africa. Science 314: 1767–1770.

Pala M, Achilli A, Olivieri A et al. (2009) Mitochondrial haplogroup U5b3: a distant echo of the Epipaleolithic in Italy and the legacy of the early Sardinians. American Journal of Human Genetics 84: 814–821.

Pala M, Olivieri A, Achilli A et al. (2012) Mitochondrial DNA signals of Late Glacial re‐colonization of Europe from Near Eastern refugia. American Journal of Human Genetics 90: 915–924.

Perego UA, Achilli A, Angerhofer N et al. (2009) Distinctive Paleo‐Indian migration routes from Beringia marked by two rare mtDNA haplogroups. Current Biology 19: 1–8.

Perego UA, Angerhofer N, Pala M et al. (2010) The initial peopling of the Americas: a growing number of founding mitochondrial genomes from Beringia. Genome Research 20: 1174–1179.

Pereira L, Silva NM, Franco‐Suarte R et al. (2010) Population expansion in the North African Late Pleistocene signalled by mitochondrial DNA haplogroup U6. BMC Evolutionary Biology 10: 390.

Pinhasi R, Thomas MG, Hofreiter M et al. (2012) The genetic history of Europeans. Trends in Genetics 28: 496–505.

Plaza S, Salas A, Calafell F et al. (2004) Insights into the western Bantu dispersal: mtDNA lineage analysis in Angola. Human Genetics 115: 439–447.

Rasmussen M, Guo X, Wang Y et al. (2011) An Aboriginal Australian genome reveals separate human dispersals into Asia. Science 334: 94–98.

Reich D, Green RE, Kircher M et al. (2010) Genetic history of an archaic hominin group from Denisova Cave in Siberia. Nature 468: 1053–1060.

Richards M, Bandelt H‐J, Kivisild T and Oppenheimer S (2006) A model for the dispersal of modern humans out of Africa. In: Bandelt H‐J, Macaulay V and Richards M (eds) Mitochondrial DNA and the Evolution of Homo sapiens, pp 225–265. Berlin: Springer–Verlag.

Richards M, Macaulay V, Hickey E et al. (2000) Tracing European founder lineages in the Near Eastern mtDNA pool. American Journal of Human Genetics 67: 1251–1276.

Richards M, Rengo C, Cruciani F et al. (2003) Extensive female‐mediated gene flow from sub‐Saharan Africa into Near Eastern Arab populations. American Journal of Human Genetics 72: 1059–1064.

Salas A, Richards M, De la Fe T et al. (2002) The making of the African mtDNA landscape. American Journal of Human Genetics 71: 1082–1111.

Scally A and Durbin R (2012) Revising the human mutation rate: implications for understanding human evolution. Nature Reviews Genetics 13: 745–753.

Skoglund P, Malmström H, Raghavan M et al. (2012) Origins and genetic legacy of Neolithic farmers and hunter‐gatherers in Europe. Science 336: 466–469.

Soares P, Achilli A, Semino O et al. (2010) The archaeogenetics of Europe. Current Biology 20: R174–R183.

Soares P, Alshamali F, Pereira JB et al. (2012) The expansion of mtDNA haplogroup L3 within and out of Africa. Molecular Biology and Evolution 29: 915–927.

Soares P, Ermini L, Thomson N et al. (2009) Correcting for purifying selection: an improved human mitochondrial molecular clock. American Journal of Human Genetics 84: 740–759.

Soares P, Rito T, Trejaut J et al. (2011) Ancient voyaging and Polynesian origins. American Journal of Human Genetics 88: 239–247.

Sun C, Kong Q‐P, Mg Palanichamy et al. (2006) The dazzling array of basal branches in the mtDNA macrohaplogroup M from India as inferred from complete genomes. Molecular Biology and Evolution 23: 683–690.

Tambets K, Rootsi S, Kivisild T et al. (2004) The western and eastern roots of the Saami – the story of genetic “outliers” told by mitochondrial DNA and Y chromosomes. American Journal of Human Genetics 74: 661–682.

Tamm E, Kivisild T, Reidla M et al. (2007) Beringian standstill and spread of Native American founders. PLoS One 2: e829.

Vigilant L, Stoneking M, Harpending H et al. (1991) African populations and the evolution of human mitochondrial DNA. Science 253: 1503–1507.

Further Reading

Avise JC (2000) Phylogeography: The History and Formation of Species. Cambridge, MA: Harvard University Press.

Bandelt H‐J, Macaulay V and Richards M (eds) (2006) Human Mitochondrial DNA and the Evolution of Homo sapiens. Berlin: Springer.

Bellwood P and Renfrew C (eds) (2002) Examining the Farming/Language Dispersal Hypothesis. Cambridge: McDonald Institute for Archaeological Research.

Jobling M, Hollox E, Kivisild T, Tyler‐Smith C, Hurles M (2013) Human Evolutionary Genetics: Origins, Peoples and Disease. 2nd edn. Oxford: Garland Science.

Oppenheimer S (2003) Out of Eden: The Peopling of the World. London: Constable.

Renfrew C and Boyle K (eds) (2000) Archaeogenetics: DNA and the Population Prehistory of Europe. Cambridge: McDonald Institute for Archaeological Research.

Richards M (2003) The Neolithic invasion of Europe. Annual Review of Anthropology 32: 135–162.

Richards M and Macaulay V (2001) The mitochondrial gene tree comes of age. American Journal of Human Genetics 68: 1315–1320.

Templeton AR (2005) Haplotype trees and modern human origins. Yearbook of Physical Anthropology 48: 33–59.

Torroni A, Achilli A, Macaulay V, Richards M and Bandelt H‐J (2006) Harvesting the fruit of the human mtDNA tree. Trends in Genetics 22: 339–345.

Related Sub-Topics:

Population Structure and Genetics | Reconstruction of Phylogeny | Molecular Evolution | Human Evolution
Contact Editor close
Submit a note to the editor about this article by filling in the form below.

* Required Field

Article Title: Mitochondrial Genome Sequences and Their Phylogeographic Interpretation
 
How to Cite close
Macaulay, Vincent, and Richards, Martin B(Sep 2013) Mitochondrial Genome Sequences and Their Phylogeographic Interpretation. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.20843.pub2]