Evolutionary forces shaping genomic islands of population differentiation in humans

Background Levels of differentiation among populations depend both on demographic and selective factors: genetic drift and local adaptation increase population differentiation, which is eroded by gene flow and balancing selection. We describe here the genomic distribution and the properties of genomic regions with unusually high and low levels of population differentiation in humans to assess the influence of selective and neutral processes on human genetic structure. Methods Individual SNPs of the Human Genome Diversity Panel (HGDP) showing significantly high or low levels of population differentiation were detected under a hierarchical-island model (HIM). A Hidden Markov Model allowed us to detect genomic regions or islands of high or low population differentiation. Results Under the HIM, only 1.5% of all SNPs are significant at the 1% level, but their genomic spatial distribution is significantly non-random. We find evidence that local adaptation shaped high-differentiation islands, as they are enriched for non-synonymous SNPs and overlap with previously identified candidate regions for positive selection. Moreover there is a negative relationship between the size of islands and recombination rate, which is stronger for islands overlapping with genes. Gene ontology analysis supports the role of diet as a major selective pressure in those highly differentiated islands. Low-differentiation islands are also enriched for non-synonymous SNPs, and contain an overly high proportion of genes belonging to the 'Oncogenesis' biological process. Conclusions Even though selection seems to be acting in shaping islands of high population differentiation, neutral demographic processes might have promoted the appearance of some genomic islands since i) as much as 20% of islands are in non-genic regions ii) these non-genic islands are on average two times shorter than genic islands, suggesting a more rapid erosion by recombination, and iii) most loci are strongly differentiated between Africans and non-Africans, a result consistent with known human demographic history.

Genomics of Divergence along a Continuum of Parapatric Population Differentiation

The patterns of genomic divergence during ecological speciation are shaped by a combination of evolutionary forces. Processes such as genetic drift, local reduction of gene flow around genes causing reproductive isolation, hitchhiking around selected variants, variation in recombination and mutation rates are all factors that can contribute to the heterogeneity of genomic divergence. On the basis of 60 fully sequenced three-spined stickleback genomes, we explore these different mechanisms explaining the heterogeneity of genomic divergence across five parapatric lake and river population pairs varying in their degree of genetic differentiation. We find that divergent regions of the genome are mostly specific for each population pair, while their size and abundance are not correlated with the extent of genome-wide population differentiation. In each pair-wise comparison, an analysis of allele frequency spectra reveals that 25–55% of the divergent regions are consistent with a local restriction of gene flow. Another large proportion of divergent regions (38–75%) appears to be mainly shaped by hitchhiking effects around positively selected variants. We provide empirical evidence that alternative mechanisms determining the evolution of genomic patterns of divergence are not mutually exclusive, but rather act in concert to shape the genome during population differentiation, a first necessary step towards ecological speciation.

Land use causes genetic differentiation of life-history traits in Bromus hordeaceus

There is increasing evidence that species can evolve rapidly in response to environmental change. However, although land use is one of the key drivers of current environmental change, studies of its evolutionary consequences are still fairly scarce, in particular studies that examine land-use effects across large numbers of populations, and discriminate between different aspects of land use. Here, we investigated genetic differentiation in relation to land use in the annual grass Bromus hordeaceus. A common garden study with offspring from 51 populations from three regions and a broad range of land-use types and intensities showed that there was indeed systematic population differentiation of ecologically important plant traits in relation to land use, in particular due to increasing mowing and grazing intensities. We also found strong land-use-related genetic differentiation in plant phenology, where the onset of flowering consistently shifted away from the typical time of management. In addition, increased grazing intensity significantly increased the genetic variability within populations. Our study suggests that land use can cause considerable genetic differentiation among plant populations, and that the timing of land use may select for phenological escape strategies, particularly in monocarpic plant species.

Genetic diversity and differentiation follow secondary succession in a multi-species study on woody plants from subtropical China

Aims: Species diversity and genetic diversity may be affected in parallel by similar environmental drivers. However, genetic diversity may also be affected independently by habitat characteristics. We aim at disentangling relationships between genetic diversity, species diversity and habitat characteristics of woody species in subtropical forest. Methods: We studied 11 dominant tree and shrub species in 27 plots in Gutianshan, China, and assessed their genetic diversity (Ar) and population differentiation (F’ST) with microsatellite markers. We tested if Ar and population specific F’ST were correlated to local species diversity and plot characteristics. Multi-model inference and model averaging were used to determine the relative importance of each predictor. Additionally we tested for isolation-by-distance and isolation-by-elevation by regressing pairwise F’ST against pairwise spatial and elevational distances. Important findings: Genetic diversity was not related to species diversity for any of the study species. Thus, our results do not support joint effects of habitat characteristics on these two levels of biodiversity. Instead, genetic diversity in two understory shrubs, Rhododendron simsii and Vaccinium carlesii, was affected by plot age with decreasing genetic diversity in successionally older plots. Population differentiation increased with plot age in Rhododendron simsii and Lithocarpus glaber. This shows that succession can reduce genetic diversity within, and increase genetic diversity between populations. Furthermore, we found four cases of isolation-by-distance and two cases of isolation-by-elevation. The former indicates inefficient pollen and seed dispersal by animals whereas the latter might be due to phenological asynchronies. These patterns indicate that succession can affect genetic diversity without parallel effects on species diversity and that gene flow in a continuous subtropical forest can be restricted even at a local scale.

Hidden Biodiversity in an Ecologically Important Freshwater Amphipod: Differences in Genetic Structure between Two Cryptic Species

Cryptic species, i.e. species that are morphologically hard to distinguish, have been detected repeatedly in various taxa and ecosystems. In order to evaluate the importance of this finding, we have to know in how far cryptic species differ in various aspects of their biology. The amphipod Gammarus fossarum is a key invertebrate in freshwater streams and contains several cryptic species. We examined the population genetic structure, genetic diversity and demographic history of two of them (type A and type B) using microsatellite markers and asked whether they show significant differences. We present results of population genetic analyses based on a total of 37 populations from the headwaters of two major European drainages, Rhine and Rhone. We found that, in both species, genetic diversity was geographically structured among and within drainages. For type A in the Rhine and type B in the Rhone, we detected significant patterns of isolation by distance. The increase of genetic differentiation with geographical distance, however, was much higher in type A than in type B. This result indicates substantial interspecific differences in population history and/or the extent of current gene flow between populations. In the Rhine, type B does not show evidence of isolation by distance, and population differentiation is relatively low across hundreds of kilometres. The majority of these populations also show signatures of recent bottlenecks. These patterns are consistent with a recent expansion of type B into the Rhine drainage. In summary, our results suggest considerable and previously unrecognized interspecific differences in the genetic structure of these cryptic keystone species.

Hybridization and adaptive radiation

Whether interspecific hybridization is important as a mechanism that generates biological diversity is a matter of controversy. Whereas some authors focus on the potential of hybridization as a source of genetic variation, functional novelty and new species, others argue against any important role, because reduced fitness would typically render hybrids an evolutionary dead end. By drawing on recent developments in the genetics and ecology of hybridization and on principles of ecological speciation theory, I develop a concept that reconciles these views and adds a new twist to this debate. Because hybridization is common when populations invade new environments and potentially elevates rates of response to selection, it predisposes colonizing populations to rapid adaptive diversification under disruptive or divergent selection. I discuss predictions and suggest tests of this hybrid swarm theory of adaptive radiation and review published molecular phylogenies of adaptive radiations in light of the theory. Some of the confusion about the role of hybridization in evolutionary diversification stems from the contradiction between a perceived necessity for cessation of gene flow to enable adaptive population differentiation on the one hand [1], and the potential of hybridization for generating adaptive variation, functional novelty and new species 2, 3 and 4 on the other. Much progress in the genetics 5, 6, 7, 8 and 9 and ecology of hybridization 9, 10 and 11, and in our understanding of the role of ecology in speciation (see Glossary) 12, 13 and 14 make a re-evaluation timely. Whereas botanists traditionally stressed the diversity-generating potential of hybridization 2, 3 and 14, zoologists traditionally saw it as a process that limits diversification [1] and refer to it mainly in the contexts of hybrid zones (Box 1) and reinforcement of reproductive isolation [15]. Judging by the wide distribution of allopolyploidy among plants, many plant species might be of direct hybrid origin or descended from a hybrid species in the recent past [16]. The ability to reproduce asexually might explain why allopolyploid hybrid species are more common in plants than in animals. Allopolyploidy arises when meiotic mismatch of parental chromosomes or karyotypes causes hybrid sterility. Mitotic error, duplicating the karyotype, can restore an asexually maintained hybrid line to fertility. Although bisexual allopolyploid hybrid species are not uncommon in fish [17] and frogs [18], the difficulty with which allopolyploid animals reproduce, typically requiring gynogenesis[19], makes establishment and survival of allopolyploid animal species difficult.

Extensive Copy-Number Variation of Young Genes across Stickleback Populations

Duplicate genes emerge as copy-number variations (CNVs) at the population level, and remain copy-number polymorphic until they are fixed or lost. The successful establishment of such structural polymorphisms in the genome plays an important role in evolution by promoting genetic diversity, complexity and innovation. To characterize the early evolutionary stages of duplicate genes and their potential adaptive benefits, we combine comparative genomics with population genomics analyses to evaluate the distribution and impact of CNVs across natural populations of an eco-genomic model, the three-spined stickleback. With whole genome sequences of 66 individuals from populations inhabiting three distinct habitats, we find that CNVs generally occur at low frequencies and are often only found in one of the 11 populations surveyed. A subset of CNVs, however, displays copy-number differentiation between populations, showing elevated within-population frequencies consistent with local adaptation. By comparing teleost genomes to identify lineage-specific genes and duplications in sticklebacks, we highlight rampant gene content differences among individuals in which over 30% of young duplicate genes are CNVs. These CNV genes are evolving rapidly at the molecular level and are enriched with functional categories associated with environmental interactions, depicting the dynamic early copy-number polymorphic stage of genes during population differentiation.

Genetic consequences of habitat fragmentation during a range expansion

We investigate the effect of habitat fragmentation on the genetic diversity of a species experiencing a range expansion. These two evolutionary processes have not been studied yet, at the same time, owing to the difficulties of deriving analytic results for non-equilibrium models. Here we provide a description of their interaction by using extensive spatial and temporal coalescent simulations and we suggest guidelines for a proper genetic sampling to detect fragmentation. To model habitat fragmentation, we simulated a two-dimensional lattice of demes partitioned into groups (patches) by adding barriers to dispersal. After letting a population expand on this grid, we sampled lineages from the lattice at several scales and studied their coalescent history. We find that in order to detect fragmentation, one needs to extensively sample at a local level rather than at a landscape level. This is because the gene genealogy of a scattered sample is less sensitive to the presence of genetic barriers. Considering the effect of temporal changes of fragmentation intensities, we find that at least 10, but often >100, generations are needed to affect local genetic diversity and population structure. This result explains why recent habitat fragmentation does not always lead to detectable signatures in the genetic structure of populations. Finally, as expected, long-distance dispersal increases local genetic diversity and decreases levels of population differentiation, efficiently counteracting the effects of fragmentation.

A Method for Detecting Population Genetic Structure in Diverse, High Gene-Flow Species

Detecting small amounts of genetic subdivision across geographic space remains a persistent challenge. Often a failure to detect genetic structure is mistaken for evidence of panmixia, when more powerful statistical tests may uncover evidence for subtle geographic differentiation. Such slight subdivision can be demographically and evolutionarily important as well as being critical for management decisions. We introduce here a method, called spatial analysis of shared alleles (SAShA), that detects geographically restricted alleles by comparing the spatial arrangement of allelic co-occurrences with the expectation under panmixia. The approach is allele-based and spatially explicit, eliminating the loss of statistical power that can occur with user-defined populations and statistical averaging within populations. Using simulated data sets generated under a stepping-stone model of gene flow, we show that this method outperforms spatial autocorrelation (SA) and UST under common real-world conditions: at relatively high migration rates when diversity is moderate or high, especially when sampling is poor. We then use this method to show clear differences in the genetic patterns of 2 nearshore Pacific mollusks, Tegula funebralis (5 Chlorostoma funebralis) and Katharina tunicata, whose overall patterns of within-species differentiation are similar according to traditional population genetics analyses. SAShA meaningfully complements UST/FST, SA, and other existing geographic genetic analyses and is especially appropriate for evaluating species with high gene flow and subtle genetic differentiation.

Spatial and temporal variation in population genetic structure of wild Nile tilapia (Oreochromis niloticus) across Africa

Background: Reconstructing the evolutionary history of a species is challenging. It often depends not only on the past biogeographic and climatic events but also the contemporary and ecological factors, such as current connectivity and habitat heterogeneity. In fact, these factors might interact with each other and shape the current species distribution. However, to what extent the current population genetic structure reflects the past and the contemporary factors is largely unknown. Here we investigated spatio-temporal genetic structures of Nile tilapia (Oreochromis niloticus) populations, across their natural distribution in Africa. While its large biogeographic distribution can cause genetic differentiation at the paleo-biogeographic scales, its restricted dispersal capacity might induce a strong genetic structure at micro-geographic scales. Results: Using nine microsatellite loci and 350 samples from ten natural populations, we found the highest genetic differentiation among the three ichthyofaunal provinces and regions (Ethiopian, Nilotic and Sudano-Sahelian) (R(ST) = 0.38 - 0.69). This result suggests the predominant effect of paleo-geographic events at macro-geographic scale. In addition, intermediate divergences were found between rivers and lakes within the regions, presumably reflecting relatively recent interruptions of gene flow between hydrographic basins (R(ST) = 0.24 - 0.32). The lowest differentiations were observed among connected populations within a basin (R(ST) = 0.015 in the Volta basin). Comparison of temporal sample series revealed subtle changes in the gene pools in a few generations (F = 0 - 0.053). The estimated effective population sizes were 23 - 143 and the estimated migration rate was moderate (m similar to 0.094 - 0.097) in the Volta populations. Conclusions: This study revealed clear hierarchical patterns of the population genetic structuring of O. niloticus in Africa. The effects of paleo-geographic and climatic events were predominant at macro-geographic scale, and the significant effect of geographic connectivity was detected at micro-geographic scale. The estimated effective population size, the moderate level of dispersal and the rapid temporal change in genetic composition might reflect a potential effect of life history strategy on population dynamics. This hypothesis deserves further investigation. The dynamic pattern revealed at micro-geographic and temporal scales appears important from a genetic resource management as well as from a biodiversity conservation point of view.

Population genomic tests of models of adaptive radiation in Lake Victoria Region cichlid fish

Adaptive radiation is usually thought to be associated with speciation, but the evolution of intraspecific polymorphisms without speciation is also possible. The radiation of cichlid fish in Lake Victoria (LV) is perhaps the most impressive example of a recent rapid adaptive radiation, with 600+ very young species. Key questions about its origin remain poorly characterized, such as the importance of speciation versus polymorphism, whether species persist on evolutionary time scales, and if speciation happens more commonly in small isolated or in large connected populations. We used 320 individuals from 105 putative species from Lakes Victoria, Edward, Kivu, Albert, Nabugabo and Saka, in a radiation-wide amplified fragment length polymorphism (AFLP) genome scan to address some of these questions. We demonstrate pervasive signatures of speciation supporting the classical model of adaptive radiation associated with speciation. A positive relationship between the age of lakes and the average genomic differentiation of their species, and a significant fraction of molecular variance explained by above-species level taxonomy suggest the persistence of species on evolutionary time scales, with radiation through sequential speciation rather than a single starburst. Finally the large gene diversity retained from colonization to individual species in every radiation suggests large effective population sizes and makes speciation in small geographical isolates unlikely.

Bacillus anthracis: Molecular taxonomy, population genetics, phylogeny and patho-evolution

Bacillus anthracis, the etiological agent of anthrax, manifests a particular bimodal lifestyle. This bacterial species alternates between short replication phases of 20-40 generations that strictly require infection of the host, normally causing death, interrupted by relatively long, mostly dormant phases as spores in the environment. Hence, the B. anthracis genome is highly homogeneous. This feature and the fact that strains from nearly all parts of the world have been analysed for canonical single nucleotide polymorphisms (canSNPs) and variable number tandem repeats (VNTRs) has allowed the development of molecular epidemiological and molecular clock models to estimate the age of major diversifications in the evolution of B. anthracis and to trace the global spread of this pathogen, which was mostly promoted by movement of domestic cattle with settlers and by international trade of contaminated animal products. From a taxonomic and phylogenetic point of view, B. anthracis is a member of the Bacillus cereus group. The differentiation of B. anthracis from B. cereus sensu strict, solely based on chromosomal markers, is difficult. However, differences in pathogenicity clearly differentiate B. anthracis from B. cereus and are marked by the strict presence of virulence genes located on the two virulence plasmids pXO1 and pXO2, which both are required by the bacterium to cause anthrax. Conversely, anthrax-like symptoms can also be caused by organisms with chromosomal features that are more closely related to B. cereus, but which carry these virulence genes on two plasmids that largely resemble the B. anthracis virulence plasmids. (C) 2011 Elsevier B.V. All rights reserved.

Genetic Variation and Population Structure in Native Americans

We examined genetic diversity and population structure in the American landmass using 678 autosomal microsatellite markers genotyped in 422 individuals representing 24 Native American populations sampled from North, Central, and South America. These data were analyzed jointly with similar data available in 54 other indigenous populations worldwide, including an additional five Native American groups. The Native American populations have lower genetic diversity and greater differentiation than populations from other continental regions. We observe gradients both of decreasing genetic diversity as a function of geographic distance from the Bering Strait and of decreasing genetic similarity to Siberians-signals of the southward dispersal of human populations from the northwestern tip of the Americas. We also observe evidence of: (1) a higher level of diversity and lower level of population structure in western South America compared to eastern South America, (2) a relative lack of differentiation between Mesoamerican and Andean populations, (3) a scenario in which coastal routes were easier for migrating peoples to traverse in comparison with inland routes, and (4) a partial agreement on a local scale between genetic similarity and the linguistic classification of populations. These findings offer new insights into the process of population dispersal and differentiation during the peopling of the Americas.

Spatial isolation and genetic differentiation in naturally fragmented plant populations of the Swiss Alps

Aims The effect Of anthropogenic landscape fragmentation on the genetic diversity and adaptive potential of plant populations is a major issue in conservation biology. However, little is known about the partitioning of genetic diversity in alpine species, which occur in naturally fragmented habitats. Here, we, investigate molecular patterns of three alpine plants (Epilobium fleischeri, Geum reptans and Campanula thyrsoides) across Switzerland and ask whether Spatial isolation has led to high levels of populations differentiation, increasing over distance, and a decrease of within-population variability. We further hypothesize that file contrasting potential for long-distance dispersal (LDD) of Seed in these Species will considerably influence and explain diversity partitioning. Methods For each study species, we Sampled 20-23 individuals from each of 20-32 populations across entire Switzerland. We applied Random Amplified Polymorphic Dimorphism markers to assess genetic diversity within (Nei's expected heterozygosity, H-e; percentage of polymorphic hands, P-P) and among (analysis of molecular variance, Phi(st)) populations and correlated population size and altitude with within-populalion diversity. Spatial patterns of genetic relatedness were investigated using Mantel tests and standardized major axis regression as well as unweighted pair group method with arithmetic mean cluster analyses and Monmonier's algorithm. To avoid known biases, We standardized the numbers of populations, individuals and markers using multiple random reductions. We modelled LDD with a high alpine wind data set using the terminal velocity and height of seed release as key parameters. Additionally, we assessed a number of important life-history traits and factors that potentially influence genetic diversity partitioning (e.g. breeding system, longevity and population size). Important findings For all three species, We found a significant isolation-by-distance relationship but only a moderately high differentiation among populations (Phi(st): 22.7, 48 and 16.8%, for E. fleischeri, G. reptans and C. thyrsoides, respectively). Within-population diversity (H-c: 0.19-0.21, P-p: 62-75%) was not reduced in comparison to known results from lowland species and even small populations with < 50 reproductive individuals contained high levels of genetic diversity. We further found no indication that a high long-distance seed dispersal potential enhances genetic connectivity among populations. Gene flow seems to have a strong stochastic component causing large dissimilarity between population pairs irrespective of the spatial distance. Our results suggest that other life-history traits, especially the breeding System, may play an important role in genetic diversity partitioning. We conclude that spatial isolation in the alpine environment has a strong influence on population relatedness but that a number of factors can considerably influence the strength of this relationship.