Gene Flow Events Research Articles

The Role of Recent Admixture in Forming the Contemporary West Eurasian Genomic Landscape

SummaryOver the past few years, studies of DNA isolated from human fossils and archaeological remains have generated considerable novel insight into the history of our species. Several landmark papers have described the genomes of ancient humans across West Eurasia, demonstrating the presence of large-scale, dynamic population movements over the last 10,000 years, such that ancestry across present-day populations is likely to be a mixture of several ancient groups [1, 2, 3, 4, 5, 6, 7]. While these efforts are bringing the details of West Eurasian prehistory into increasing focus, studies aimed at understanding the processes behind the generation of the current West Eurasian genetic landscape have been limited by the number of populations sampled or have been either too regional or global in their outlook [8, 9, 10, 11]. Here, using recently described haplotype-based techniques [11], we present the results of a systematic survey of recent admixture history across Western Eurasia and show that admixture is a universal property across almost all groups. Admixture in all regions except North Western Europe involved the influx of genetic material from outside of West Eurasia, which we date to specific time periods. Within Northern, Western, and Central Europe, admixture tended to occur between local groups during the period 300 to 1200 CE. Comparisons of the genetic profiles of West Eurasians before and after admixture show that population movements within the last 1,500 years are likely to have maintained differentiation among groups. Our analysis provides a timeline of the gene flow events that have generated the contemporary genetic landscape of West Eurasia.

A genetic contribution from the Far East into Ashkenazi Jews via the ancient Silk Road.

Contemporary Jews retain a genetic imprint from their Near Eastern ancestry, but obtained substantial genetic components from their neighboring populations during their history. Whether they received any genetic contribution from the Far East remains unknown, but frequent communication with the Chinese has been observed since the Silk Road period. To address this issue, mitochondrial DNA (mtDNA) variation from 55,595 Eurasians are analyzed. The existence of some eastern Eurasian haplotypes in eastern Ashkenazi Jews supports an East Asian genetic contribution, likely from Chinese. Further evidence indicates that this connection can be attributed to a gene flow event that occurred less than 1.4 kilo-years ago (kya), which falls within the time frame of the Silk Road scenario and fits well with historical records and archaeological discoveries. This observed genetic contribution from Chinese to Ashkenazi Jews demonstrates that the historical exchange between Ashkenazim and the Far East was not confined to the cultural sphere but also extended to an exchange of genes.

Outbreeding effects in an inbreeding insect, Cimex lectularius

In some species, populations with few founding individuals can be resilient to extreme inbreeding. Inbreeding seems to be the norm in the common bed bug, Cimex lectularius, a flightless insect that, nevertheless, can reach large deme sizes and persist successfully. However, bed bugs can also be dispersed passively by humans, exposing inbred populations to gene flow from genetically distant populations. The introduction of genetic variation through this outbreeding could lead to increased fitness (heterosis) or be costly by causing a loss of local adaptation or exposing genetic incompatibility between populations (outbreeding depression). Here, we addressed how inbreeding within demes and outbreeding between distant populations impact fitness over two generations in this re-emerging public health pest. We compared fitness traits of families that were inbred (mimicking reproduction following a founder event) or outbred (mimicking reproduction following a gene flow event). We found that outbreeding led to increased starvation resistance compared to inbred families, but this benefit was lost after two generations of outbreeding. No other fitness benefits of outbreeding were observed in either generation, including no differences in fecundity between the two treatments. Resilience to inbreeding is likely to result from the history of small founder events in the bed bug. Outbreeding benefits may only be detectable under stress and when heterozygosity is maximized without disruption of coadaptation. We discuss the consequences of these results both in terms of inbreeding and outbreeding in populations with genetic and spatial structuring, as well as for the recent resurgence of bed bug populations.

Spatial Structure and Colonization Process of Varied Tit Populations in the Izu Islands

The Izu Islands of Japan are a geographically young volcanic archipelago nearer to the mainland than other islands used in speciation studies, such as the Galapagos Islands of Ecuador. On the Izu Islands, birds are likely to have undergone recent colonization and trait diversification. Three morphological groups of Varied Tits, Poecile varius, breed on the islands. The varius group, which has the smallest body size and is the same as that found on the mainland, breeds on the northernmost island (closest to the mainland). The namiyei group, which has an intermediate body size, breeds on two or three central islands, and the owstoni group, which has the largest body size, is found on several southern islands. To infer the gene flow ranges and colonization processes of Varied Tits with such obvious trait polymorphisms among the Izu Islands, we analyzed the genetic population structures of these three morphological groups. In genetic analysis of all samples, individuals were first divided into cluster A, which was composed of individuals from Kohzu Island (a central island) from the namiyei group, and cluster B, which was composed of individuals from mainland sites and other islands (excluding Kohzu and Niijima). The genetic characteristics of individuals from Niijima may indicate a recent gene flow event between clusters A and B. Individuals from the owstoni group were genetically similar to varius group individuals, despite the large distance between the breeding areas of these two groups. The second step of our analysis used samples from cluster B. These samples were grouped into three clusters, one of which was further classified into two clusters in our third-step analysis. In conclusion, we detected a hierarchical structure among Varied Tits breeding on the Izu Islands and inferred that ancestors of the owstoni group colonized from the mainland more recently than those of the namiyei group.

The lengths of admixture tracts.

The distribution of admixture tract lengths has received considerable attention, in part because it can be used to infer the timing of past gene flow events between populations. It is commonly assumed that these lengths can be modeled as independently and identically distributed (iid) exponential random variables. This assumption is fundamental for many popular methods that analyze admixture using hidden Markov models. We compare the expected distribution of admixture tract lengths under a number of population-genetic models to the distribution predicted by the Wright-Fisher model with recombination. We show that under the latter model, the assumption of iid exponential tract lengths does not hold for recent or for ancient admixture events and that relying on this assumption can lead to false positives when inferring the number of admixture events. To further investigate the tract-length distribution, we develop a dyadic interval-based stochastic process for generating admixture tracts. This representation is useful for analyzing admixture tract-length distributions for populations with recent admixture, a scenario in which existing models perform poorly.

New mitochondrial and nuclear evidences support recent demographic expansion and an atypical phylogeographic pattern in the spittlebug Philaenus spumarius (Hemiptera, Aphrophoridae).

Philaenus spumarius is a widespread insect species in the Holarctic region. Here, by focusing on the mtDNA gene COI but also using the COII and Cyt b genes and the nuclear gene EF-1α, we tried to explain how and when its current biogeographic pattern evolved by providing time estimates of the main demographic and evolutionary events and investigating its colonization patterns in and out of Eurasia. Evidence of recent divergence and expansion events at less than 0.5 Ma ago indicate that climate fluctuations in the Mid-Late Pleistocene were important in shaping the current phylogeographic pattern of the species. Data support a first split and differentiation of P. spumarius into two main mitochondrial lineages: the “western”, in the Mediterranean region and the “eastern”, in Anatolia/Caucasus. It also supports a following differentiation of the “western” lineage into two sub-lineages: the “western-Mediterranean”, in Iberia and the “eastern-Mediterranean” in the Balkans. The recent pattern seems to result from postglacial range expansion from Iberia and Caucasus/Anatolia, thus not following one of the four common paradigms. Unexpected patterns of recent gene-flow events between Mediterranean peninsulas, a close relationship between Iberia and North Africa, as well as high levels of genetic diversity being maintained in northern Europe were found. The mitochondrial pattern does not exactly match to the nuclear pattern suggesting that the current biogeographic pattern of P. spumarius may be the result of both secondary admixture and incomplete lineage sorting. The hypothesis of recent colonization of North America from both western and northern Europe is corroborated by our data and probably resulted from accidental human translocations. A probable British origin for the populations of the Azores and New Zealand was revealed, however, for the Azores the distribution of populations in high altitude native forests is somewhat puzzling and may imply a natural colonization of the archipelago.

Late Miocene lineage divergence and ecological differentiation of rare endemic Juniperus blancoi: clues for the diversification of North American conifers

Western North America and Mexico contain a large number of conifer species. This diversity could be the product of orographic and climate changes of the late Tertiary and Quaternary. In this study, we focus on the evolutionary history of Juniperus blancoi, in order to determine the impact of climate change and environmental heterogeneity on population differentiation. We estimated the population structure, phylogenetic relationships and historical demography of J.blancoi populations using nuclear genes. We correlated genetic structure with ecological differentiation, divergence times and changes in population size. Populations of J.blancoi are differentiated into three lineages that correspond to low-, mid- and high-altitude populations. The three groups diversified in the late Miocene, early Pliocene, with only a few events of gene flow since then. Two lineages in the north exhibited a pattern of population growth during the Pleistocene that could be linked to climate changes. Populations of J.blancoi experienced significant ecological differentiation and early divergence events, which correspond to periods of global cooling and mountain uplift during the Miocene. This suggests that mountain ranges in tropical and subtropical latitudes play an important role in the speciation and persistence of conifer taxa in diversity hotspots, by providing diverse environmental conditions.

Four makes a party

Recent excavations in the Denisova Cave in the Altai Mountains of southern Siberia have yielded a wealth of hominin fossils from a site that has been occupied for perhaps 250,000 years or more. Now a high-quality genome sequence has been determined from a circa 50,000-year-old toe bone a proximal toe phalanx excavated from the east gallery of Denisova Cave in 2010. The sequence is that of a Neanderthal woman whose parents were closely related perhaps half-siblings or uncle and niece. Such inbreeding was also common among her recent ancestors. Comparisons with other archaic and present-day human genomes reveal several gene-flow events among Neanderthals, the closely related Denisovans and early modern humans, possibly including gene flow into Denisovans from an unknown archaic group. The high-quality Neanderthal genome also helps to establish a definitive list of substitutions that became fixed in modern humans after their separation from the ancestors of Neanderthals and Denisovans.

The complete genome sequence of a Neanderthal from the Altai Mountains

We present a high-quality genome sequence of a Neandertal woman from Siberia. We show that her parents were related at the level of half siblings and that mating among close relatives was common among her recent ancestors. We also sequenced the genome of a Neandertal from the Caucasus to low coverage. An analysis of the relationships and population history of available archaic genomes and 25 present-day human genomes shows that several gene flow events occurred among Neandertals, Denisovans and early modern humans, possibly including gene flow into Denisovans from an unknown archaic group. Thus, interbreeding, albeit of low magnitude, occurred among many hominin groups in the Late Pleistocene. In addition, the high quality Neandertal genome allows us to establish a definitive list of substitutions that became fixed in modern humans after their separation from the ancestors of Neandertals and Denisovans.

Efficient mitigation of founder effects during the establishment of a leading-edge oak population

Numerous plant species are shifting their range polewards in response to ongoing climate change. Range shifts typically involve the repeated establishment and growth of leading-edge populations well ahead of the main species range. How these populations recover from founder events and associated diversity loss remains poorly understood. To help fill this gap, we exhaustively investigated a newly established population of holm oak (Quercus ilex) growing more than 30 km ahead of the nearest larger stands. Pedigree reconstructions showed that plants belong to two non-overlapping generations and that the whole population originates from only two founder trees. The four first-generation trees that have reached maturity showed disparate mating patterns despite being full-sibs. Long-distance pollen immigration was notable despite the strong isolation of the stand: 6 per cent gene flow events in acorns collected on the trees (n = 255), and as much as 27 per cent among their established offspring (n = 33). Our results show that isolated leading-edge populations of wind-pollinated forest trees can rapidly restore their genetic diversity through the interacting effects of efficient long-distance pollen flow and purging of inbred individuals during recruitment. They imply that range expansions of these species are primarily constrained by initial propagule arrival rather than by subsequent gene flow.

Speciation in Caucasian lizards: climatic dissimilarity of the habitats is more important than isolation time

Given sufficient time and limited gene flow, evolutionary lineages tend to transform into separate species. Mechanisms preventing assimilation during repeated gene-flow events include divergent adaptations and the development of pre- or postzygotic isolation. We analysed the morphological and genetic boundaries of three species of the rock lizard clade Darevskia ‘rudis’ (Darevskia rudis, Darevskia valentini, and Darevskia portschinskii) in relation to the environment, and tried to reconstruct evolutionary pathways underlying the observed separation among the species. We studied the geographic distribution of the scalation traits, microsatellite genotypes, and mitochondrial haplotypes. Our analyses showed consistent morphological and genetic patterns at the centre of the ranges for each species, but asymmetric distribution of alleles and scalation characters within the current contact zones among the species. The genetic and morphological diversification of the clade has been shaped during glacial isolation in an area of Southern Caucasus, away from the Black Sea Coast. The ancestral lineage of D. portschinskii separated from the common D. rudis–D. valentini lineage in the middle Pleistocene, and the two latter lineages separated in relatively recent geological time. Neither of the lineages attained complete lineage sorting; moreover, isolation and migration modelling have helped to detect recombinant gene flow from D. rudis to D. portschinskii (but not to D. valentini). This is most likely linked with climatically more similar suitable habitats between D. rudis and D. portschinskii than between D. valentini and the other two species. In itself, the isolation period was insufficient for the development of intrinsic isolation mechanisms in the system studied. Thus, differential landscape-dependent selection within the contact zones is likely to have triggered the rapid development of isolation mechanisms.

Uniparental Genetic Heritage of Belarusians: Encounter of Rare Middle Eastern Matrilineages with a Central European Mitochondrial DNA Pool

Ethnic Belarusians make up more than 80% of the nine and half million people inhabiting the Republic of Belarus. Belarusians together with Ukrainians and Russians represent the East Slavic linguistic group, largest both in numbers and territory, inhabiting East Europe alongside Baltic-, Finno-Permic- and Turkic-speaking people. Till date, only a limited number of low resolution genetic studies have been performed on this population. Therefore, with the phylogeographic analysis of 565 Y-chromosomes and 267 mitochondrial DNAs from six well covered geographic sub-regions of Belarus we strove to complement the existing genetic profile of eastern Europeans. Our results reveal that around 80% of the paternal Belarusian gene pool is composed of R1a, I2a and N1c Y-chromosome haplogroups – a profile which is very similar to the two other eastern European populations – Ukrainians and Russians. The maternal Belarusian gene pool encompasses a full range of West Eurasian haplogroups and agrees well with the genetic structure of central-east European populations. Our data attest that latitudinal gradients characterize the variation of the uniparentally transmitted gene pools of modern Belarusians. In particular, the Y-chromosome reflects movements of people in central-east Europe, starting probably as early as the beginning of the Holocene. Furthermore, the matrilineal legacy of Belarusians retains two rare mitochondrial DNA haplogroups, N1a3 and N3, whose phylogeographies were explored in detail after de novo sequencing of 20 and 13 complete mitogenomes, respectively, from all over Eurasia. Our phylogeographic analyses reveal that two mitochondrial DNA lineages, N3 and N1a3, both of Middle Eastern origin, might mark distinct events of matrilineal gene flow to Europe: during the mid-Holocene period and around the Pleistocene-Holocene transition, respectively.

Increasing phylogenetic resolution still informative for Y chromosomal studies on West-European populations

Many Y-chromosomal lineages which are defined in the latest phylogenetic tree of the human Y chromosome by the Y Chromosome Consortium (YCC) in 2008 are distributed in (Western) Europe due to the fact that a large number of phylogeographic studies focus on this area. Therefore, the question arises whether newly discovered polymorphisms on the Y chromosome will still be interesting to study Western Europeans on a population genetic level. To address this question, the West-European region of Flanders (Belgium) was selected as study area since more than 1000 Y chromosomes from this area have previously been genotyped at the highest resolution of the 2008 YCC-tree and coupled to in-depth genealogical data. Based on these data the temporal changes of the population genetic pattern over the last centuries within Flanders were studied and the effects of several past gene flow events were identified. In the present study a set of recently reported novel Y-SNPs were genotyped to further characterize all those Flemish Y chromosomes that belong to haplogroups G, R-M269 and T. Based on this extended Y-SNP set the discrimination power increased drastically as previous large (sub-)haplogroups are now subdivided in several non-marginal groups. Next, the previously observed population structure within Flanders appeared to be the result of different gradients of independent sub-haplogroups. Moreover, for the first time within Flanders a significant East-West gradient was observed in the frequency of two R-M269 lineages, and this gradient is still present when considering the current residence of the DNA donors. Our results thus suggest that an update of the Y-chromosomal tree based on new polymorphisms is still useful to increase the discrimination power based on Y-SNPs and to study population genetic patterns in more detail, even in an already well-studied region such as Western Europe.

Profile of David Reich

Profile of David Reich

Phylogeography and seed dispersal in islands: the case of Rumex bucephalophorus subsp. canariensis (Polygonaceae)

Rumex bucephalophorus subsp. canariensis is an endemic taxon to Macaronesia with diaspore polymorphism. The origin and colonizing route of this taxon in Macaronesia was studied using molecular data and information on diaspore types. Amplified fragment length polymorphism (AFLP) was used in 260 plants from 22 populations of R. bucephalophorus subsp. canariensis, four from the Madeiran archipelago and 18 from the Canary archipelago. Diaspore production was analysed in 9-50 plants from each population used for AFLP analysis. One hundred and one plants from the Madeiran archipelago and 375 plants from the Canary Islands were studied. For each plant the type of diaspore produced was recorded. Overall populations had low genetic diversity but they showed a geographical pattern of genetic diversity that was higher in the older eastern islands than in the younger western ones. Two types of dispersible diaspores were found: in the eastern Canary islands (Lanzarote, Fuerteventura and Gran Canaria), plants produced exclusively long-dispersible diaspores, whereas in the western Canary islands (Tenerife, La Gomera, El Hierro) and the Madeiran archipelago plants produced exclusively short-dispersible diaspores. Genetically, the studied populations fell into four main island groups: Lanzarote-Fuerteventura, Gran Canaria, Tenerife-El Hierro and La Gomera-Madeira archipelago. A Moroccan origin of R. bucephalophorus subsp. canariensis is hypothesized with a colonization route from the eastern to the western islands. In addition, at least one gene flow event from La Gomera to the Madeiran archipelago has taken place. During the colonization process the type of dispersible diaspore changed so that dispersability decreased in populations of the westernmost islands.

HIV Type 1 Origin and Transmission Dynamics Among Different Risk Groups in Sardinia: Molecular Epidemiology Within the Close Boundaries of an Italian Island

In Italy, the HIV-1 epidemic is still mainly sustained by the subtype B genetic form, although other and novel subtypes and circulating recombinant forms (CRFs) have been reported. A total of 215 HIV-1 pol gene sequences were collected between 1992 and 2010. Multiple alignments spanning subtype-specific HIV-1 B pol sequences were analyzed by Bayesian phylogenetic methods. Subtype B represented 90.7% (n=195) of the sequences. Three main clusters were detected. The root of the tree dated to 1987. Most of the observed viral gene flow events occurred from heterosexual to intravenous drug users (IDUs). Phylogenetic and molecular clock analysis showed an early HIV-1 subtype B introduction in the mid-1980s and dissemination within local risk-specific clusters. This is the first study to describe in detail the HIV-1 molecular epidemiology in one of the largest islands in the European basin. The future potential of the Sardinian epidemic as a hub between Southern and Northern Europe has to been considered.

Contemporary gene flow and mating system of Arabis alpina in a Central European alpine landscape

Gene flow is important in counteracting the divergence of populations but also in spreading genes among populations. However, contemporary gene flow is not well understood across alpine landscapes. The aim of this study was to estimate contemporary gene flow through pollen and to examine the realized mating system in the alpine perennial plant, Arabis alpina (Brassicaceae). An entire sub-alpine to alpine landscape of 2 km(2) was exhaustively sampled in the Swiss Alps. Eighteen nuclear microsatellite loci were used to genotype 595 individuals and 499 offspring from 49 maternal plants. Contemporary gene flow by pollen was estimated from paternity analysis, matching the genotypes of maternal plants and offspring to the pool of likely father plants. Realized mating patterns and genetic structure were also estimated. Paternity analysis revealed several long-distance gene flow events (≤1 km). However, most outcrossing pollen was dispersed close to the mother plants, and 84 % of all offspring were selfed. Individuals that were spatially close were more related than by chance and were also more likely to be connected by pollen dispersal. In the alpine landscape studied, genetic structure occurred on small spatial scales as expected for alpine plants. However, gene flow also covered large distances. This makes it plausible for alpine plants to spread beneficial alleles at least via pollen across landscapes at a short time scale. Thus, gene flow potentially facilitates rapid adaptation in A. alpina likely to be required under ongoing climate change.

Assessing the Impact of Pollen-mediated Gene Flow from GM Herbicide Tolerant <i>Brassica Napus</i> into Common Wild Relatives in Ireland

Although now we have had many years of research completed on assessing the potential environmental impact of GM crops, concern remains over their potential impact on biodiversity in the rural landscape. In particular, issues have arisen in regards to the modification of crops with traits that could introgress into sexually compatible wild relatives. In contrast to wheat, barley, potato and maize, Brassica napus (oilseed rape) is the only commercial crop grown in Ireland at present with the potential to successfully transfer its DNA, via pollen-mediated gene flow, into inter-related weed species. This review details the species in question and by examining the relevant literature that relates to Irish agronomic conditions, demonstrates that gene flow is likely to occur, especially to an earlier used cultivar, Brassica rapa. However, the critical factor remains not that GM traits will flow from the commercial source but what might the consequences of said gene flow events be. This review indicates that the conferred trait in question (in this case, herbicide tolerance) can only impact on weed diversity in the presence of selecting herbicide action. In the absence of the herbicide, the GM traits will be lost from the wild species over time and will not confer any selective advantage that could facilitate population growth.

Diversity and population structure of black soybean landraces originating from Tanba and neighboring regions

Black soybean landraces that had been cultivated in Tanba region and the neighboring regions and conserved black soybean landraces, including those from other regions in Japan, were used in this study. The polymorphisms of 78 SSR markers in nuclear DNA and 6 SSRs in chloroplast DNA were analyzed in the black soybean landrace populations. The result of phylogenic analysis revealed that the black soybeans can be classified into six clades. The landraces originating from Tanba region were classed into first and second clades, and two chloroplast genotypes were found in the population of black soybeans from the Tanba region. Genotype A chloroplast was predominantly identified in major populations of the Tanba, while genotype B was widely distributed in the black soybean population. Population structure analysis in the Japanese black soybean accessions inferred there are six groups. The black soybean landrace from the Tanba region was classified into three groups, mainly corresponding to the distance-based phylogenic results. The two groups were probably derived from different ancestors with Type A and B chloroplast genomes, respectively, whereas the other group showed both types of chloroplast genome. The admixture situations suggested that the landraces in the main group have been widely cultivated in Tanba region, while the landraces that belong to other groups were cultivated in localized area. Several phenotypes were compared among genotype groups, dividing into two sub-groups: founder sub-group and admixed sub-group. Phenotypic differences were observed between founder landraces in group 1 and group 3. On the other hand, landraces in admixture landraces in group 1 and group 2 segregated for several traits, while founder landraces in group 1 were stabled for each trait. These observations suggest that gene flow events have occurred between different founder landraces.

ASSESSING THE IMPACT OF POLLEN-MEDIATED GENE FLOW FROM GM HERBICIDE TOLERANT BRASSICA NAPUS INTO COMMON WILD RELATIVES IN IRELAND

Although now we have had many years of research completed on assessing the potential environmental impact of GM crops, concern remains over their potential impact on biodiversity in the rural landscape. In particular, issues have arisen in regards to the modification of crops with traits that could introgress into sexually compatible wild relatives. In contrast to wheat, barley, potato and maize, Brassica napus (oilseed rape) is the only commercial crop grown in Ireland at present with the potential to successfully transfer its DNA, via pollen-mediated gene flow, into inter-related weed species. This review details the species in question and by examining the relevant literature that relates to Irish agronomic conditions, demonstrates that gene flow is likely to occur, especially to an earlier used cultivar, Brassica rapa. However, the critical factor remains not that GM traits will flow from the commercial source but what might the consequences of said gene flow events be. This review indicates that the conferred trait in question (in this case, herbicide tolerance) can only impact on weed diversity in the presence of selecting herbicide action. In the absence of the herbicide, the GM traits will be lost from the wild species over time and will not confer any selective advantage that could facilitate population growth.