The impact of recent events on human genetic diversity

The historical record tells us stories of migrations, population expansions and colonization events in the last few thousand years, but what was their demographic impact? Genetics can throw light on this issue, and has mostly done so through the maternally inherited mitochondrial DNA (mtDNA) and the male-specific Y chromosome. However, there are a number of problems, including marker ascertainment bias, possible influences of natural selection, and the obscuring layers of the palimpsest of historical and prehistorical events. Y-chromosomal lineages are particularly affected by genetic drift, which can be accentuated by recent social selection. A diversity of approaches to expansions in Europe is yielding insights into the histories of Phoenicians, Roma, Anglo-Saxons and Vikings, and new methods for producing and analysing genome-wide data hold much promise. The field would benefit from more consensus on appropriate methods, and better communication between geneticists and experts in other disciplines, such as history, archaeology and linguistics.     

Differential maternal and paternal contributions to the genetic pool of Ibiza Island, Balearic Archipelago

We report on a comparison of the genetic diversity between Ibiza and the population of the other Balearic islands and also between the archipelago with respect to circum-Mediterranean populations. For such a comparison, autosomal and Y-chromosome STRs, as well as mtDNA sequence data analyzed from the same individuals, were studied. Analysis of 14 autosomal STRs showed that Ibiza had significant differentiation with respect to other Balearic populations and also with respect to insular and continental populations from the Mediterranean area. Nevertheless, the results obtained from the analysis of eight Y-STRs showed a high level of genetic homogeneity for eight western Mediterranean populations. On the other hand, these populations did not show a compacted group when mtDNA diversity was analyzed, since they showed genetic differentiation among them. The analyses of haplotypes shared between populations indicated that mtDNA haplotypes have drifted to higher frequencies than the Y chromosome. This fact could be due to a shared recent history between Ibiza and other western Mediterranean populations, with numerous male displacements originated by wars and, especially, commercial relations. The results of mtDNA from the Ibiza population could be due to a maternal Carthaginian/Phoenician founder effect, together with genetic drift, in accordance with the historical and demographic data of the area.     

Mitochondrial DNA Reveals Genetic Structuring of Pinna nobilis across the Mediterranean Sea

Pinna nobilis is the largest endemic Mediterranean marine bivalve. During past centuries, various human activities have promoted the regression of its populations. As a consequence of stringent standards of protection, demographic expansions are currently reported in many sites. The aim of this study was to provide the first large broad-scale insight into the genetic variability of P. nobilis in the area that encompasses the western Mediterranean, Ionian Sea, and Adriatic Sea marine ecoregions. To accomplish this objective twenty-five populations from this area were surveyed using two mitochondrial DNA markers (COI and 16S). Our dataset was then merged with those obtained in other studies for the Aegean and Tunisian populations (eastern Mediterranean), and statistical analyses (Bayesian model-based clustering, median-joining network, AMOVA, mismatch distribution, Tajima’s and Fu’s neutrality tests and Bayesian skyline plots) were performed. The results revealed genetic divergence among three distinguishable areas: (1) western Mediterranean and Ionian Sea; (2) Adriatic Sea; and (3) Aegean Sea and Tunisian coastal areas. From a conservational point of view, populations from the three genetically divergent groups found may be considered as different management units.     

Origins and Evolution of the Etruscans’ mtDNA

The Etruscan culture is documented in Etruria, Central Italy, from the 8^th to the 1^st century BC. For more than 2,000 years there has been disagreement on the Etruscans’ biological origins, whether local or in Anatolia. Genetic affinities with both Tuscan and Anatolian populations have been reported, but so far all attempts have failed to fit the Etruscans’ and modern populations in the same genealogy. We extracted and typed the hypervariable region of mitochondrial DNA of 14 individuals buried in two Etruscan necropoleis, analyzing them along with other Etruscan and Medieval samples, and 4,910 contemporary individuals from the Mediterranean basin. Comparing ancient (30 Etruscans, 27 Medieval individuals) and modern DNA sequences (370 Tuscans), with the results of millions of computer simulations, we show that the Etruscans can be considered ancestral, with a high degree of confidence, to the current inhabitants of Casentino and Volterra, but not to the general contemporary population of the former Etruscan homeland. By further considering two Anatolian samples (35 and 123 individuals) we could estimate that the genetic links between Tuscany and Anatolia date back to at least 5,000 years ago, strongly suggesting that the Etruscan culture developed locally, and not as an immediate consequence of immigration from the Eastern Mediterranean shores.     

Natural or Naturalized? Phylogeography Suggests That the Abundant Sea Urchin Arbacia lixula Is a Recent Colonizer of the Mediterranean

We present the global phylogeography of the black sea urchin Arbacia lixula, an amphi-Atlantic echinoid with potential to strongly impact shallow rocky ecosystems. Sequences of the mitochondrial cytochrome c oxidase gene of 604 specimens from 24 localities were obtained, covering most of the distribution area of the species, including the Mediterranean and both shores of the Atlantic. Genetic diversity measures, phylogeographic patterns, demographic parameters and population differentiation were analysed. We found high haplotype diversity but relatively low nucleotide diversity, with 176 haplotypes grouped within three haplogroups: one is shared between Eastern Atlantic (including Mediterranean) and Brazilian populations, the second is found in Eastern Atlantic and the Mediterranean and the third is exclusively from Brazil. Significant genetic differentiation was found between Brazilian, Eastern Atlantic and Mediterranean regions, but no differentiation was found among Mediterranean sub-basins or among Eastern Atlantic sub-regions. The star-shaped topology of the haplotype network and the unimodal mismatch distributions of Mediterranean and Eastern Atlantic samples suggest that these populations have suffered very recent demographic expansions. These expansions could be dated 94–205 kya in the Mediterranean, and 31–67 kya in the Eastern Atlantic. In contrast, Brazilian populations did not show any signature of population expansion. Our results indicate that all populations of A. lixula constitute a single species. The Brazilian populations probably diverged from an Eastern Atlantic stock. The present-day genetic structure of the species in Eastern Atlantic and the Mediterranean is shaped by very recent demographic processes. Our results support the view (backed by the lack of fossil record) that A. lixula is a recent thermophilous colonizer which spread throughout the Mediterranean during a warm period of the Pleistocene, probably during the last interglacial. Implications for the possible future impact of A. lixula on shallow Mediterranean ecosystems in the context of global warming trends must be considered.     

Maternal History of Oceania from Complete mtDNA Genomes: Contrasting Ancient Diversity with Recent Homogenization Due to the Austronesian Expansion

Archaeology, linguistics, and existing genetic studies indicate that Oceania was settled by two major waves of migration. The first migration took place approximately 40 thousand years ago and these migrants, Papuans, colonized much of Near Oceania. Approximately 3.5 thousand years ago, a second expansion of Austronesian-speakers arrived in Near Oceania and the descendants of these people spread to the far corners of the Pacific, colonizing Remote Oceania. To assess the female contribution of these two human expansions to modern populations and to investigate the potential impact of other migrations, we obtained 1,331 whole mitochondrial genome sequences from 34 populations spanning both Near and Remote Oceania. Our results quantify the magnitude of the Austronesian expansion and demonstrate the homogenizing effect of this expansion on almost all studied populations. With regards to Papuan influence, autochthonous haplogroups support the hypothesis of a long history in Near Oceania, with some lineages suggesting a time depth of 60 thousand years, and offer insight into historical interpopulation dynamics. Santa Cruz, a population located in Remote Oceania, is an anomaly with extreme frequencies of autochthonous haplogroups of Near Oceanian origin; simulations to investigate whether this might reflect a pre-Austronesian versus Austronesian settlement of the island failed to provide unequivocal support for either scenario.     

House mouse dispersal in Iron Age Spain: a geometric morphometrics appraisal

During the Iron Age, sea trade in the Mediterranean increased, particularly with the expansion of Phoenician and Greek colonies in the Western Mediterranean. A side effect of these human movements was the involuntary dispersion of commensal species, such as the house mouse (Mus musculus domesticus). One archaeological layer dated from the 4th Century BC, coming from an Iberian village located in the Mediterranean coast of Spain, contained a large and reliable accumulation of small mammals. The presence of the house mouse was highly suspected within this layer. To assess its abundance quantitatively, we used a geometric morphometrics approach of the first lower molar contour using elliptical Fourier analysis. We also increased the power of the discrimination between the Algerian mouse (Mus spretus) and the house mouse by combining a dimension reduction approach together with different validation procedures. The relative importance of age, sex, and geographical origin onto the shape and form of the lower molar contour was also investigated. The results obtained demonstrate the presence and the dominance of the house mouse in the landscape surrounding the Iberian village in the 1st Millennium BC, only a few centuries after its arrival in the Western Mediterranean Basin. A cross‐validated linear discriminant function considering different Mediterranean populations suggest Morocco and France as the most probable geographical origins for the Algerian mouse, and Tunisia for the origin of house mice in North‐Eastern Spain. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 102 , 483–497.     

The Etruscans: a population-genetic study

The origins of the Etruscans, a non-Indo-European population of preclassical Italy, are unclear. There is broad agreement that their culture developed locally, but the Etruscans' evolutionary and migrational relationships are largely unknown. In this study, we determined mitochondrial DNA sequences in multiple clones derived from bone samples of 80 Etruscans who lived between the 7th and the 3rd centuries b.c. In the first phase of the study, we eliminated all specimens for which any of nine tests for validation of ancient DNA data raised the suspicion that either degradation or contamination by modern DNA might have occurred. On the basis of data from the remaining 30 individuals, the Etruscans appeared as genetically variable as modern populations. No significant heterogeneity emerged among archaeological sites or time periods, suggesting that different Etruscan communities shared not only a culture but also a mitochondrial gene pool. Genetic distances and sequence comparisons show closer evolutionary relationships with the eastern Mediterranean shores for the Etruscans than for modern Italian populations. All mitochondrial lineages observed among the Etruscans appear typically European or West Asian, but only a few haplotypes were found to have an exact match in a modern mitochondrial database, raising new questions about the Etruscans' fate after their assimilation into the Roman state.     

From depth to regional spatial genetic differentiation of Eunicella cavolini in the NW Mediterranean

Connectivity studies in the marine realm are of great importance to understand the evolutionary potential of populations in a context of growing pressures on the marine environment. Here, we investigated the effect of the local, regional, and depth spatial scale on the population genetic structure of the yellow gorgonian Eunicella cavolini, one of the most common octocoral species of the Mediterranean hard-bottom communities. This species, along with other sessile metazoans typical of coralligenous ecosystems, plays an important role in supporting biodiversity, but is also impacted by direct and indirect consequences of human activities, such as physical destruction or mortality events due to thermal anomalies. Samples were taken from 15 sites located in the Ligurian Sea (NW Mediterranean) in two adjacent regions 100 kilometres apart, i.e. from the areas of Marseille (France) and Portofino (Genoa, Italy), and were analysed using six microsatellite loci. A pattern of isolation by distance was observed at the regional as well as the local scales. Although E. cavolini showed less genetic structure than other Mediterranean octocorallian species, we observed a significant genetic differentiation between populations a few kilometres apart. A low genetic differentiation was also observed between shallow and deep populations. The occurrence of genetically differentiated populations of E. cavolini at the scale of kilometres has important consequences for the management of this species and of the associated communities.     

The evolution of Hessian fly from the Old World to the New World: Evidence from molecular markers

Eighteen polymorphic microsatellite loci and 11 single‐nucleotide polymorphisms were genotyped in 1 095 individual Hessian fly specimens representing 23 populations from North America, southern Europe, and southwest Asia. The genotypes were used to assess genetic diversity and interrelationship of Hessian fly populations. While phylogenetic analysis indicates that the American populations most similar to Eurasian populations come from the east coast of the United States, genetic distance is least between (Alabama and California) and (Kazakhstan and Spain). Allelic diversity and frequency vary across North America, but they are not correlated with distance from the historically documented point of introduction in New York City or with temperature or precipitation. Instead, the greatest allelic diversity mostly occurs in areas with Mediterranean climates. The microsatellite data indicate a general deficiency for heterozygotes in Hessian fly. The North American population structure is consistent with multiple introductions, isolation by distance, and human‐abetted dispersal by bulk transport of puparia in infested straw or on harvesting equipment.     

A new perspective of human origin and dispersals derived from the microevolution of teeth

Recent genetic studies have heightened the expectation that the origin of modern humans will be defined, but one clear vision has yet to be developed. The study of teeth has historically been an informative means to help define human dispersals. Quantitative tooth data is presented encompassing worldwide human populations. A null hypothesis phylogeny developed from the multivariate analysis of the microevolution of the dental phenotype was interpreted to be broadly in accord with the dominant interpretation of genetic, archaeological, and other dental data by showing that the first division in the dispersion of extant humanity was within sub-Sahara Africans; i.e., San, and Western Africans and Bantu. This "out-of-Africa" interpretation of the graphical results suggests that the first modern human African emigrants not to go extinct were Southeast Asian Negritos. All Eurasians then emerged and expanded through a series of extinct antecedent populations branching from the short lineage extending from Negritos to Australian aborigines. Caucasoids were the first group to fission from this stock. Under this hypothesis, the next to have emerged were antecedent Southeast Asians, from which present Southeast Asians and then antecedent east Central Asians then diverged. Independently, people from the region of Mongolia and all Native Americans arose as daughter populations from antecedent east Central Asians. The broad outline of humanity studied here cannot disprove the equally explanatory protean multiregional hypotheses, but with the inclusion of hominids and further modern human populations either parts of the multiregional hypothesis or the outlined more linear evolutionary scenario likely can be refuted.     

Inferring the Joint Demographic History of Multiple Populations from Multidimensional SNP Frequency Data

Demographic models built from genetic data play important roles in illuminating prehistorical events and serving as null models in genome scans for selection. We introduce an inference method based on the joint frequency spectrum of genetic variants within and between populations. For candidate models we numerically compute the expected spectrum using a diffusion approximation to the one-locus, two-allele Wright-Fisher process, involving up to three simultaneous populations. Our approach is a composite likelihood scheme, since linkage between neutral loci alters the variance but not the expectation of the frequency spectrum. We thus use bootstraps incorporating linkage to estimate uncertainties for parameters and significance values for hypothesis tests. Our method can also incorporate selection on single sites, predicting the joint distribution of selected alleles among populations experiencing a bevy of evolutionary forces, including expansions, contractions, migrations, and admixture. We model human expansion out of Africa and the settlement of the New World, using 5 Mb of noncoding DNA resequenced in 68 individuals from 4 populations (YRI, CHB, CEU, and MXL) by the Environmental Genome Project. We infer divergence between West African and Eurasian populations 140 thousand years ago (95% confidence interval: 40–270 kya). This is earlier than other genetic studies, in part because we incorporate migration. We estimate the European (CEU) and East Asian (CHB) divergence time to be 23 kya (95% c.i.: 17–43 kya), long after archeological evidence places modern humans in Europe. Finally, we estimate divergence between East Asians (CHB) and Mexican-Americans (MXL) of 22 kya (95% c.i.: 16.3–26.9 kya), and our analysis yields no evidence for subsequent migration. Furthermore, combining our demographic model with a previously estimated distribution of selective effects among newly arising amino acid mutations accurately predicts the frequency spectrum of nonsynonymous variants across three continental populations (YRI, CHB, CEU).     

High levels of population subdivision in a morphologically conserved Mediterranean toad (Alytes cisternasii) result from recent,multiple refugia: evidence from mtDNA,microsatellites and nuclear genealogies

Pleistocene glaciations often resulted in differentiation of taxa in southern European peninsulas, producing the high levels of endemism characteristic of these regions (e.g. the Iberian Peninsula). Despite their small ranges, endemic species often exhibit high levels of intraspecific differentiation as a result of a complex evolutionary history dominated by successive cycles of fragmentation, expansion and subsequent admixture of populations. Most evidence so far has come from the study of species with an Atlantic distribution in northwestern Iberia, and taxa restricted to Mediterranean‐type habitats remain poorly studied. The Iberian Midwife toad (Alytes cisternasii) is a morphologically conserved species endemic to southwestern and central Iberia and a typical inhabitant of Mediterranean habitats. Applying highly variable genetic markers from both mitochondrial and nuclear genomes to samples collected across the species’ range, we found evidence of high population subdivision within A. cisternasii. Mitochondrial haplotypes and microsatellites show geographically concordant patterns of genetic diversity, suggesting population fragmentation into several refugia during Pleistocene glaciations followed by subsequent events of geographical and demographic expansions with secondary contact. In addition, the absence of variation at the nuclear β‐fibint7 and Ppp3caint4 gene fragments suggests that populations of A. cisternasii have been recurrently affected by episodes of extinction and recolonization, and that documented patterns of population subdivision are the outcome of recent and multiple refugia. We discuss the evolutionary history of the species with particular interest in the increasing relevance of Mediterranean refugia for the survival of genetically differentiated populations during the Pleistocene glaciations as revealed by studies in co‐distributed taxa.     

High genetic divergence of hormogastrid earthworms (Annelida, Oligochaeta) in the central Iberian Peninsula: evolutionary and demographic implications

Hormogastridae earthworms are highly important for the functioning of the Mediterranean soil system. However, little is known about the species distribution and genetic diversity of these soil invertebrates. In the present study, the genetic differentiation and gene flow were studied among populations of hormogastrids from the central Iberian Peninsula. A 648-bp portion of the mitochondrial cytochrome c oxidase I gene was sequenced for 82 individuals from 7 localities, resulting in the identification of 38 haplotypes exclusive to localities. All of the individuals were morphologically identified as Hormogaster elisae , but the high genetic divergence found among populations (up to 20.20%) suggests the occurrence of more than one cryptic species within this region. Further analysis of the phylogenetic relationships revealed six different evolutionary lineages coincident with geographical location, including the two nearest populations Molar and Redueña as one evolutionary unit. From these results, at least three new species could be inferred, in addition to the morphospecies H. elisae s.s . Partitioning of genetic variance among populations indicated that isolation by distance was the primary agent for differentiation of the investigated hormogastrid populations. Our data suggest that the evolutionary lineages for H. elisae s.l. originated between the late Miocene and the early Pleistocene, but that mtDNA genealogies coalesce on a more recent scale of a few thousand years.     

Spatial and temporal synchrony in reptile population dynamics in variable environments

Resources are seldom distributed equally across space, but many species exhibit spatially synchronous population dynamics. Such synchrony suggests the operation of large-scale external drivers, such as rainfall or wildfire, or the influence of oasis sites that provide water, shelter, or other resources. However, testing the generality of these factors is not easy, especially in variable environments. Using a long-term dataset (13–22 years) from a large (8000 km²) study region in arid Central Australia, we tested firstly for regional synchrony in annual rainfall and the dynamics of six reptile species across nine widely separated sites. For species that showed synchronous spatial dynamics, we then used multivariate follow a multivariate auto-regressive state–space (MARSS) models to predict that regional rainfall would be positively associated with their populations. For asynchronous species, we used MARSS models to explore four other possible population structures: (1) populations were asynchronous, (2) differed between oasis and non-oasis sites, (3) differed between burnt and unburnt sites, or (4) differed between three sub-regions with different rainfall gradients. Only one species showed evidence of spatial population synchrony and our results provide little evidence that rainfall synchronizes reptile populations. The oasis or the wildfire hypotheses were the best-fitting models for the other five species. Thus, our six study species appear generally to be structured in space into one or two populations across the study region. Our findings suggest that for arid-dwelling reptile populations, spatial and temporal dynamics are structured by abiotic events, but individual responses to covariates at smaller spatial scales are complex and poorly understood.     

Y Chromosomes of 40% Chinese Descend from Three Neolithic Super-Grandfathers

Demographic change of human populations is one of the central questions for delving into the past of human beings. To identify major population expansions related to male lineages, we sequenced 78 East Asian Y chromosomes at 3.9 Mbp of the non-recombining region, discovered >4,000 new SNPs, and identified many new clades. The relative divergence dates can be estimated much more precisely using a molecular clock. We found that all the Paleolithic divergences were binary; however, three strong star-like Neolithic expansions at ∼6 kya (thousand years ago) (assuming a constant substitution rate of 1×10⁻⁹/bp/year) indicates that ∼40% of modern Chinese are patrilineal descendants of only three super-grandfathers at that time. This observation suggests that the main patrilineal expansion in China occurred in the Neolithic Era and might be related to the development of agriculture.     

Around the Mediterranean: an extreme example of loop migration in a long‐distance migratory passerine

An important issue in migration research is how small‐bodied passerines pass over vast geographical barriers; in European–African avian migration, these are represented by the Mediterranean Sea and the Sahara Desert. Eastern (passing eastern Mediterranean), central (passing Apennine Peninsula) and western (via western Mediterranean) major migration flyways are distinguished for European migratory birds. The autumn and spring migration routes may differ (loop migration) and there could be a certain level of individual flexibility in how individuals navigate themselves during a single migration cycle. We used light‐level loggers to map migration routes of barn swallows Hirundo rustica breeding in the centre of a wide putative contact zone between the northeastern and southernwestern European populations that differ in migration flyways utilised and wintering grounds. Our data documented high variation in migration patterns and wintering sites of tracked birds (n = 19 individuals) from a single breeding colony, with evidence for loop migration in all but one of the tracked swallows. In general, two migratory strategies were distinguished. In the first, birds wintering in a belt stretching from southcentral to southern Africa that used an eastern route for both the spring and autumn migration, then shifted their spring migration eastwards (anti‐clockwise loops, n = 12). In the second, birds used an eastern or central route to their wintering grounds in central Africa, shifting the spring migration route westward (clockwise loops, n = 7). In addition, we observed an extremely wide clockwise loop migration encompassing the entire Mediterranean, with one individual utilising both the eastern (autumn) and western (spring) migratory flyway during a single annual migration cycle. Further investigation is needed to ascertain whether clockwise migratory loops encircling the entire Mediterranean also occur other small long‐distance passerine species.     

Spatial expansions and travelling waves of rabies in vampire bats

A major obstacle to anticipating the cross-species transmission of zoonotic diseases and developing novel strategies for their control is the scarcity of data informing how these pathogens circulate within natural reservoir populations. Vampire bats are the primary reservoir of rabies in Latin America, where the disease remains among the most important viral zoonoses affecting humans and livestock. Unpredictable spatiotemporal dynamics of rabies within bat populations have precluded anticipation of outbreaks and undermined widespread bat culling programs. By analysing 1146 vampire bat-transmitted rabies (VBR) outbreaks in livestock across 12 years in Peru, we demonstrate that viral expansions into historically uninfected zones have doubled the recent burden of VBR. Viral expansions are geographically widespread, but severely constrained by high elevation peaks in the Andes mountains. Within Andean valleys, invasions form wavefronts that are advancing towards large, unvaccinated livestock populations that are heavily bitten by bats, which together will fuel high transmission and mortality. Using spatial models, we forecast the pathways of ongoing VBR epizootics across heterogeneous landscapes. These results directly inform vaccination strategies to mitigate impending viral emergence, reveal VBR as an emerging rather than an enzootic disease and create opportunities to test novel interventions to manage viruses in bat reservoirs.