UC Irvine UC Irvine Previously Published Works Title Mitochondrial variability in the Mediterranean area: a complex stage for human migrations. Permalink https://escholarship.org/uc/item/4p72d0rd Journal Annals of human biology, 45(1) ISSN 0301-4460 Authors De Angelis, Flavio Scorrano, Gabriele Martínez-Labarga, Cristina et al. Publication Date 2018-02-01 DOI 10.1080/03014460.2017.1416172 Peer reviewed eScholarship.org Powered by the California Digital Library University of California Annals of Human Biology ISSN: 0301-4460 (Print) 1464-5033 (Online) Journal homepage: http://www.tandfonline.com/loi/iahb20 Mitochondrial variability in the Mediterranean area: a complex stage for human migrations Flavio De Angelis, Gabriele Scorrano, Cristina Martínez-Labarga, Giuseppina Scano, Fabio Macciardi & Olga Rickards To cite this article: Flavio De Angelis, Gabriele Scorrano, Cristina Martínez-Labarga, Giuseppina Scano, Fabio Macciardi & Olga Rickards (2018) Mitochondrial variability in the Mediterranean area: a complex stage for human migrations, Annals of Human Biology, 45:1, 5-19, DOI: 10.1080/03014460.2017.1416172 To link to this article: https://doi.org/10.1080/03014460.2017.1416172 View supplementary material Published online: 30 Jan 2018. Submit your article to this journal View related articles View Crossmark data Citing articles: 1 View citing articles Full Terms & Conditions of access and use can be found at http://www.tandfonline.com/action/journalInformation?journalCode=iahb20 ANNALS OF HUMAN BIOLOGY, 2018 VOL. 45, NO. 1, 5–19 https://doi.org/10.1080/03014460.2017.1416172 REVIEW Mitochondrial variability in the Mediterranean area: a complex stage for human migrations aà aà a a b Flavio De Angelis , Gabriele Scorrano , Cristina Martınez-Labarga , Giuseppina Scano , Fabio Macciardi and Olga Rickardsa aCentre of Molecular Anthropology for Ancient DNA Studies, University of Rome “Tor Vergata”, Rome, Italy; bLaboratory of Molecular Psychiatry, Department of Psychiatry and Human Behavior, University of California, Irvine, CA, USA ABSTRACT ARTICLE HISTORY Context: The Mediterranean area has always played a significant role in human dispersal due to the Received 22 November 2017 large number of migratory events contributing to shape the cultural features and the genetic pool of Revised 30 November 2017 its populations. Accepted 5 December 2017 Objective: This paper aims to review and diachronically describe the mitogenome variability in the Mediterranean population and the main demic diffusions that occurred in this area over time. KEYWORDS Methods: Frequency distributions of the leading mitochondrial haplogroups have been geographically Mediterranean Basin; and chronologically evaluated. The variability of U5b and K lineages has been focussed to broaden the complete mitochondrial knowledge of their genetic histories. genomes; Mediterranean Results: The mitochondrial genetic makeup of Palaeolithic hunter-gatherers is poorly defined within mitochondrial lineages; the extant Mediterranean populations, since only a few traces of their genetic contribution are still mtDNA human populations detectable. The Neolithic lineages are more represented, suggesting that the Neolithic revolution had a marked effect on the peopling of the Mediterranean area. The largest effect, however, was provided by historical migrations. Conclusion: Although the mitogenome variability has been widely used to try and clarify the evolution of the Mediterranean genetic makeup throughout almost 50 000 years, it is necessary to collect whole genome data on both extinct and extant populations from this area to fully reconstruct and interpret the impact of multiple migratory waves and their cultural and genetic consequences on the structure of the Mediterranean populations. Introduction related biological consequences (Cerezo et al., 2012). Accordingly, the exploration of the genetic structure of The Mediterranean area has always played a significant role extant Mediterranean populations could be pivotal in infer- in the expansion of human populations, because it repre- ring their demographic history through research comparing sents a bridge for humans among three continents: Europe, ancient and extant genetic data to determine possible signa- Africa and Asia. Indeed, during human pre-history and his- tures of ancient routes (Fu et al., 2016; Gamba et al., 2014; tory, a profusion of demic movements and cultural interac- Gunther€ et al., 2015; Hofmanova et al., 2016). tions occurred in this area, contributing to shape the The selected genetic markers suitable for phylogenetic biological features and genetic pool of modern European and phylogeographic analyses have, for a long time, been populations. Since the Pleistocene, when the first out of the mitochondrial DNA (mtDNA) and the non-recombining Africa dispersal of Homo sapiens took place (Hublin et al., region of the Y-chromosome. The mtDNA genome and the 2017), the Mediterranean territories represented a significant Y-chromosome are uniparental genetic systems which pro- stage for human expansion (Sazzini et al., 2014). Even today, vide a female and a male perspective, respectively, and since the Mediterranean Sea is often used as a migratory route they do not recombine, they change over generations only from Africa and the Near East to Europe: globalisation, there- by an accumulation of mutations, ultimately creating patrilin- fore, continues to increase the genetic variability of eal and matrilineal lines called haplogroups. Different hap- Mediterranean populations. logroups can be geographically and chronologically observed In this frame, the particular spatial distribution patterns of among different human populations. Their ultimate distribu- genetic lineages in contemporary human populations could tion and frequency are also constrained by the effect of provide meaningful insights into migrations and multiple other factors they interact with, like cultural traits and geo- gene flows contributing to demographic changes and their graphical obstacles. CONTACT Flavio De Angelis [email protected]; Olga Rickards [email protected] Centre of Molecular Anthropology for Ancient DNA Studies, University of Rome Tor Vergata, Piano 0, Sett. G, Via della Ricerca Scientifica 1, 00173 Rome, Italy à These authors contributed equally to the paper. Supplemental data for this article can be accessed here. ß 2017 Informa UK Limited, trading as Taylor & Francis Group 6 F. DE ANGELIS ET AL. Despite this surely useful approach, today such an evolu- (van Oven & Kayser, 2009) to produce unambiguous trees tionary analysis based only on the mt- or the Y-DNA markers able to support inferences on where the direct (or indirect) has been unable to adequately dissect the overall genetic descendants of the ancient sequences have appeared. makeup of worldwide human populations: the recent devel- opments of Next Generation Sequencing (NGS) techniques Pre-history of the Mediterranean fully accomplish this task, providing several whole genomes from extant and ancient samples. Homo sapiens originated in Africa 200 thousand years ago Indeed, a great deal of data on whole genomes has been (kya) (Hublin et al., 2017; Mellars, 2006) and began to colon- generated by international consortia for both modern popu- ise the remaining continents 60–80 kya. The first modern ‘ ’ lations, such as the 1000 Genome Project (The 1000 humans moved to Europe 43 kya, carrying M and N mito- Genomes Project Consortium, 2015), and ancient people chondrial haplogroups (Benazzi et al., 2011; Higham et al., (Allentoft et al., 2015; Fu et al., 2016; Haak et al., 2015; 2014; Ingman et al., 2000; Stoneking, 2008)(Figure 1) and Hofmanova et al., 2016). These advances make possible a succeeded in the replacement of the existing species, Homo merged data analysis that could contribute to a holistic neanderthalensis (Hublin, 2011), whose mitochondrial sequen- understanding of genetic variability in present and ancient ces fall outside the mtDNA variability of Homo sapiens (Green human groups (Rasmussen et al., 2010; Reich et al., 2010). et al., 2008;Prufer€ et al., 2017), even though at the nuclear Nonetheless, certain important questions about human DNA level a certain degree of interbreeding has been movements in the Mediterranean area are still far from being detected (Sankararaman et al., 2012). A drastic climatic event, fully addressed, mainly because available data about whole the Last Glacial Maximum (LGM), occurred 27–19 kya during genomes related to past Mediterranean populations are scarce. As the ancient DNA data from the Mediterranean peo- the Upper Palaeolithic period and markedly influenced the ple have been to date almost exclusively derived from the demographic dispersal and genetic variability of early analysis of well, but heterogeneously covered mitochondrial European hunter gatherers (Tallavaara et al., 2015). If the pre- genomes, the purpose of this review is to broadly depict the LGM European populations were characterised by human variability of mtDNA in the Mediterranean region and to bet- mitochondrial variability, mainly constituted by R, U and M ter describe the genetic landscape of the leading human lineages (Posth et al., 2016; Seguin-Orlando et al., 2014), the migration routes. The analytical strategy to accomplish this LGM represented a bottleneck for genetic diversity: U sub- goal is the evaluation of the frequency distributions of the haplogroups were the sole lineages identified in early post- leading mitochondrial haplogroups,