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Facsimile Del Frontespizio Della Tesi Di Dottorato Alma Mater Studiorum – Università di Bologna DOTTORATO DI RICERCA IN Biodiversità del Evoluzione Ciclo XXVI Settore Concorsuale di afferenza: 05/B1 - Zoologia e Antropologia Settore Scientifico disciplinare: BIO/08 - Antropologia THE GENETIC HISTORY OF ITALIANS: NEW INSIGHTS FROM UNIPARENTALLY-INHERITED MARKERS Presentata da Stefania Sarno Coordinatore Dottorato Relatore Prof.ssa Barbara Mantovani Prof. Davide Pettener Esame Finale – Anno 2014 Table of contents Table of contents GENERAL INTRODUCTION AND THESIS RATIONAL 1 1. Reconstructing human evolutionary history through genetic tools 2 2. A multi-level analysis approach in the study of the Italian population history and 3 genetic structure: from macro- to micro-geographic perspectives 3. Work outline 5 PART 1 - The genetic history and population structure of Italy: 11 a macro-geographic overview from the uniparental markers 1.1 Introduction 13 1.1.1 Pre-historical and historical population dynamics 14 1.1.1.1 Palaeolithic occupation and post-glacial re-expansions 14 1.1.1.2 Main migration patterns associated to the Neolithic transition 20 1.1.1.3 Population dynamics in historical times 29 1.1.2 A genetic overview on the Italian variability 34 1.1.2.1 Classical genetic markers 34 1.1.2.2 Uniparental molecular markers 38 1.1.2.3 Genome-wide based studies 42 1.2 Specific aims of the studies 45 1.3 Results and discussion 49 Article 1: 51 Boattini A, Martinez-Cruz B, Sarno S, Harmant C, Useli A, Sanz P, Yang-Yao D, Manry J, Ciani G, Luiselli D, Quintana-Murci L, Comas D, Pettener D, Genographic Consortium (2013) Uniparental markers in Italy reveal a sex-biased genetic structure and different historical strata. PLoS One. 8:e65441. doi:10.1371/journal.pone.0065441. Article 2: 65 Sarno S, Boattini A, Carta M, Ferri G, Alù M, Yang Yao D, Ciani G, Pettener D, Luiselli D (2014) An ancient Mediterranean melting pot: investigating the uniparental genetic structure and population history of Sicily and Southern Italy. PLoS One (submitted). 1.4 Comments 101 1.4.1 Clines or discontinuous structures in the Italian genetic landscape 102 1.4.2 Origin and structuring of the Italian Y-chromosomal gene pool 103 1.4.3 Contrasting maternal and paternal histories 109 i Table of contents PART 2 - Insights into the Italian micro-geographic genetic variability: 111 two case studies from ethno-linguistic and socio-economic enclaves of Italy 2.1 Introduction 113 2.1.1 Interaction between historical, geographic and cultural factors: how culture, space 115 and time shape the current genetic legacy 2.1.2 Marginal population as a simplified observatory in our understanding of human 116 genetic diversity and population history 2.1.3 Italian micro-geographic genetic variability: the role of socio-cultural factors 118 2.1.3.1 Ethno-linguistic factors: the case of the Albanian-speaking Arbereshe 120 (Sicily and Southern Italy) 2.1.3.2 Socio-economic factors: the case of the Partecipanza of San Giovanni in 123 Persiceto (Northern Italy) 2.2 Specific aims of the studies 125 2.3 Results and discussion 127 Article 3: 129 Sarno S, Carta M, Boattini A, Tofanelli S, Ferri G, Alù M, Motta V, Anagnostou P, Sineo L, Tagarelli G, Luiselli D, Pettener D. Same language, different genetic histories: high resolution analysis of Y-chromosome variability in the Arbereshe populations of Calabria and Sicily (in preparation). Article 4: 163 Boattini A, Sarno S, Pedrini P, Medoro C, Carta M, Tucci S, Ferri G, Alù M, Luiselli D, Pettener D. Traces of Medieval migrations in a socially-stratified population from Northern Italy. Evidence from uniparental markers and deep-rooted pedigrees (in preparation). 2.4 Comments 189 2.4.1 Isolation, culture and genetic history 190 CONCLUDING REMARKS AND FUTURE DIRECTIONS 193 1. Integrating macro- and micro-geographic perspectives of investigation 194 REFERENCES 199 Appendix I 206 Capocasa M, Anagnostou P, Bachis V, Battaggia C, Bertoncini S, Biondi G, Boattini B, Boschi I, Brisighelli F, Calò CM, Carta M, Coia V, Corrias L, Crivellaro F, Ferri G, Francalacci P, Franceschi ZA, Luiselli D, Morelli L, Rickards O, Robledo R, Sanna D, Sanna E, Sarno S, Tofanelli S, Vona G, Pettener D and Destro Bisol G (2014) Linguistic, geographic and genetic isolation: a collaborative study on Italian populations. J Anthropol. Sci. 92:1-32. doi 10.4436/JASS.92001 ii Abbreviations ABBREVIATIONS ABO ABO blood group system A.D. Anno Domini aDNA ancient DNA AMH Anatomically Modern Human ASD Average Square Distance B.C. Before Christ DNA Dideoxyribonucleic Acid HG Haplogroup HLA Histocompatibility Leucocyte Antigen HVS Hyper Variable Segment IBD Identical-By-Descent IBS Identity-By-State IW Impressed Ware culture KYBP Kilo Years Before Present LBK Linear BandKeramik culture LGM Last Glacial Maximum mtDNA mitochondrial DNA NRY Non-recombining Region of the Y-chromosome PC Principal Component SNP Single Nucleotide Polymorphism STR Short Tandem Repeat TMRCA Time of the Most Recent Common Ancestors YBP Year Before Present iii GENERAL INTRODUCTION AND THESIS RATIONALE 1 General introduction 1. Reconstructing human evolutionary history through genetic tools Detecting and interpreting the existing patterns of genetic variation within and between human populations has long been one of the major aims of population genetic studies. In the last decades, the increasing availability of genetic data from worldwide sets of human populations has offered new powerful tools for population geneticists to ask new questions about our past (Wilkins, 2006). Studying the human populations genetic structure and the spatial distribution of genetic variation has helped increasing our knowledge on human population prehistory and proto-history (Ramachandran et al., 2010). It also allowed shedding new lights into the main demographic processes which led to the present-day patterns of genetic variability within and among human groups. The existence of various classes of molecular markers, differing from one another for both their patterns of inheritance and evolving mutation rates (Garrigan and Hammer, 2006), has made it possible not only to trace the genetic history of human populations separated either in ancient or more recent times, but also to investigate the evolutionary forces that have subsequently addressed their differentiation over time (Sazzini et al., 2014). Two portions of our genome, commonly referred to as uniparental markers (namely Y- chromosome and mitochondrial DNA), have long been used in population genetic studies to reconstruct and compare the male and female genetic histories and demographic patterns at different geographical and cultural scales (Wilkins et al. 2006). Since they are uniparentally transmitted - hence free from the reshuffling effect of recombination - the subsequent occurrence of neutral mutations in these genetic systems defines maternal and paternal lineages whose origin (phylogenetic relationships) and diffusion pattern (phylogeographic distribution) are traceable back in time and space, actually reflecting the population past history and mobility (Jobling et al., 2004, Underhill and Kivisild 2007, Jobling et al., 2013). In addition, by largely escaping selective pressures, these markers offer the chance to specifically investigate the effect of genetic drift, admixture, geographic isolation and/or cultural practices on the present-day frequency and geographic distribution patterns of genetic variation (Sazzini et al., 2014). More recently, genome-wide autosomal SNP data and X-chromosome genetic markers have offered new important tools to reveal population genetic sub-structures and to test detailed hypotheses about human demographic histories, despite being individually less reliable in reconstructing traceable genealogies (Wilkins et al., 2006; Henn et al., 2010). Since the first pioneer studies by Cavalli-Sforza and colleagues (1994) on the “History and Geography of Human Genes”, the European country has attracted particular interest of population genetic studies. Classical, uniparental and autosomal markers (Cavalli-Sforza et al., 1994; Barbujani 2 Thesis rationale et al., 1994; Rosser et al. 2000; Semino et al, 2000; Chikhi et al. 2002; Lao et al., 2008; Novembre et al., 2008; Balaresque et al., 2010) agreed in revealing a principal South-East to North-West (SE- NW) distribution pattern of genetic variation within Europe, which has been mainly associated to the major prehistoric demographic events that affected the peopling history of the continent over time: namely the first colonisation by Anatomically Modern Humans (AMH), the post-glacial re- expansion from Southern-European refuges, and the Neolithic diffusion of agriculture from the Near East. Within this European genetic continuum, some internal population genetic sub-structures have been however invoked at more fine-grained regional scales (for instance within Finland and Italy, Lao et al., 2008; Nelis et al., 2009), and different geographic, cultural or linguistic isolates (such as Basques, Finns, Sardinians and Jewish; Bertranpetit et al., 1995; Thomas et al., 2002; Fraumene et al., 2006; Calò et al, 2008; Palo et al., 2009; Novembre and Ramachandran, 2011; Ostrer and Skorecki, 2013) confirmed to be genetic isolates as well. Therefore, if the genetic landscape of present-day European and Mediterranean populations has been widely explored under a continental point of view, on the other hand the extent to which continent-wide trends are re- shaped or modified at micro-geographical levels, and the measure of geographic, cultural or demographic
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