Population Genetic Architecture Research Articles

Forensic Efficiency Estimation of a Homemade Six-Color Fluorescence Multiplex Panel and In-Depth Anatomy of the Population Genetic Architecture in Two Tibetan Groups.

The genetic information of the Chinese Tibetan group has been a long-standing research hotspot among population geneticists and archaeologists. Herein, 309 unrelated individuals from two Tibetan groups living in Qinghai Province, China (CTQ), and Tibet Autonomous Region, China (CTT), were successfully genotyped using a new homemade six-color fluorescence multiplex panel, which contained 59 autosomal deletion/insertion polymorphisms (au-DIPs), two mini short tandem repeats (miniSTRs), two Y-chromosomal DIPs, and one Amelogenin. The cumulative probability of matching and combined power of exclusion values for this new panel in CTQ and CTT groups were 1.9253E-27 and 0.99999729, as well as 1.5061E-26 and 0.99999895, respectively. Subsequently, comprehensive population genetic analyses of Tibetan groups and reference populations were carried out based on the 59 au-DIPs. The multitudinous statistical analysis results supported that Tibetan groups have close genetic affinities with East Asian populations. These findings showed that this homemade system would be a powerful tool for forensic individual identification and paternity testing in Chinese Tibetan groups and give us an important insight for further perfecting the genetic landscape of Tibetan groups.

Range-Wide Population Structure of 3 Deepwater Eteline Snappers Across the Indo-Pacific Basin.

Deep-sea habitats may drive unique dispersal and demographic patterns for fishes, but population genetic analyses to address these questions have rarely been conducted for fishes in these environments. This study investigates the population structure of 3 tropical deepwater snappers of the genus Etelis that reside at 100-400 m depth, with broad and overlapping distributions in the Indo-Pacific. Previous studies showed little population structure within the Hawaiian Archipelago for 2 of these species: Etelis coruscans and E. carbunculus. Here we extend sampling to the entire geographic range of each species to resolve the population genetic architecture for these 2 species, as well as a recently exposed cryptic species (Etelis sp.). One goal was to determine whether deepwater snappers are more dispersive than shallow-water fishes. A second goal was to determine whether submesophotic fishes have older, more stable populations than shallow reef denizens that are subject to glacial sea-level fluctuations. Both goals are pertinent to the management of these valuable food fishes. A total of 1153 specimens of E. coruscans from 15 geographic regions were analyzed, along with 1064 specimens of E. carbunculus from 11 regions, and 590 specimens of E. sp. from 16 regions. The first 2 species were analyzed with mtDNA and 9-11 microsatellite loci, while E. sp. was analyzed with mtDNA only. Etelis coruscans had a non-significant microsatellite global FST, but significant global mtDNA Ф ST = 0.010 (P = 0.0007), with the isolation of Seychelles in the western Indian Ocean, and intermittent signals of isolation for the Hawaiian Archipelago. Etelis carbunculus had a non-significant microsatellite global FST, and significant global mtDNA Ф ST = 0.021 (P = 0.0001), with low but significant levels of isolation for Hawai'i, and divergence between Tonga and Fiji. Etelis sp. had mtDNA Ф ST = 0.018 (P = 0.0005), with a strong pattern of isolation for both Seychelles and Tonga. Overall, we observed low population structure, shallow mtDNA coalescence (similar to near-shore species), and isolation at the fringes of the Indo-Pacific basin in Hawai'i and the western Indian Ocean. While most shallow-water species have population structure on the scale of biogeographic provinces, deepwater snapper populations are structured on the wider scale of ocean basins, more similar to pelagic fishes than to shallow-water species. This population structure indicates the capacity for widespread dispersal throughout the Indo-Pacific region.

Spatial genetics of brown hares (Lepus europaeus Pallas, 1778) from Turkey: Different gene pool architecture on either side of the Bosphorus?

We determined allelic variation at eleven microsatellite loci to study the effect of the Bosphorus, the Sea of Marmara, and the Dardanelles on the population genetic architecture of brown hares, Lepus europaeus, from Anatolia and Turkish Thrace in the southeastern most Balkans. The latter region was connected with Anatolia during periods of the late Pleistocene and the early Holocene (until ca. 8000 y BP) enabling natural gene flow. Following a recent mitochondrial (mt) DNA-based phylogeographic model that suggested unidirectional ancient gene flow from Anatolia to the SE Balkans, we expected lower genetic diversity in hares from Turkish Thrace than Anatolia. The Turkish Thrace population might have been established only relatively recently as natural northwestward expansion of a long existing Anatolian population. Alternatively, it might have received late Pleistocene or Holocene gene flow by hares from eastern Europe from north of the Black Sea, even after the formation of the marine barrier. This might have produced a notable genetic distinction between the hares from either side of the Bosphorus, the Sea of Marmara, and the Dardanelles. We found significantly lower allelic richness in hares from Turkish Thrace than Anatolia, very little genetic admixture in the Turkish Thrace population, and only one allele at low frequency in Turkish Thrace that was not observed in Anatolian hares. On the contrary, many alleles of Anatolian hares were not recovered in hares from Turkish Thrace. Nevertheless, genetic divergence (Fst, Cavalli-Sforza & Edwards distances, AMOVA) between the hares from either side of the current marine barrier was low (Fst values <10%). All findings accord to our initial hypothesis that the hares from Turkish Thrace represent merely a somewhat genetically depleted version of the Anatolian hares. Seemingly, no strong drift has occurred in the Turkish Thrace population since the break-up of the Holocene landbridge, and there is no indication of gene flow from other regions in (eastern) Europe into the Turkish Thrace population. Spatial genetic approaches and standard population genetics (BAPS, GENELAND, STRUCTURE, F-statistics, Cavalli-Sforza & Edwards distances) indicated significant spatial genetic differentiation of hares across Anatolia, but also on a very low level. Overall, our results are concordant with the latest mtDNA based model of ancient gene flow in hares only from Anatolia to the southeastern Balkans across the Pleistocene and early Holocene landbridge; this implies that most or all of the Balkans have been colonized by hares exclusively originating eventually from Anatolia.

Enhancing Ebony? Common Associations With a cis-Regulatory Haplotype for Drosophila melanogaster Thoracic Pigmentation in a Japanese Population and Australian Populations.

The molecular underpinnings of pigmentation diversity in Drosophila have recently emerged as a model for understanding how the evolution of different cis-regulatory variants results in common adaptive phenotypes within species. We compared sequence variation in a 5′ regulatory region harboring a modular enhancer containing a ∼0.7-kb core element contributing to abdominal melanisation in African, and a ∼0.5-kb core element contributing to thoracic pigmentation in D. melanogaster from Japan, to tropical and temperate populations from eastern Australia previously shown to be divergent in thoracic pigmentation and ebony expression. The Australian populations exhibited strong association with the core enhancer polymorphism cluster in complete association with Dark and Light phenotypes from Iriomote, Japan. Moreover, the Iriomote Light and Dark core enhancer haplotypes are common to the Australian populations in the direction predicted by pigmentation phenotype. We also confirmed the Japanese patterns of linkage disequilibrium and association of the tropical inversion In(3R)Payne with the Light enhancer haplotype in the Australian tropical light population. A worldwide survey of the ∼0.5-kb ebony control region SNPs and haplotypes in a subset of the Drosophila Genome Nexus (DGN) populations suggest origins in the sub-Saharan ancestral region surrounding Zambia and subsequent invasion following colonization out of Africa. A previous study demonstrated complex within and between population genetic architecture for abdominal pigmentation which is also correlated with thoracic pigmentation in melanized DGN sub-Saharan populations; however, the ∼0.5-kb ebony control region was not associated and both haplotypes are common even in the most intensely pigmented D. melanogaster from high altitude Ethiopia. In the Australian populations, the strong phenotypic association with the enhancer SNPs and haplotypes that at least partly regulates ebony expression in the Iriomote population, our previous work demonstrating opposing clines for thoracic pigmentation and ebony expression, where the expression cline parallels the In(3R)Payne cline, and the concerted evolution of pigmentation intensity and ebony expression under rapid experimental evolution, all point to a common adaptive evolutionary pathway in distinct populations.

A Model of Compound Heterozygous, Loss-of-Function Alleles Is Broadly Consistent with Observations from Complex-Disease GWAS Datasets.

The genetic component of complex disease risk in humans remains largely unexplained. A corollary is that the allelic spectrum of genetic variants contributing to complex disease risk is unknown. Theoretical models that relate population genetic processes to the maintenance of genetic variation for quantitative traits may suggest profitable avenues for future experimental design. Here we use forward simulation to model a genomic region evolving under a balance between recurrent deleterious mutation and Gaussian stabilizing selection. We consider multiple genetic and demographic models, and several different methods for identifying genomic regions harboring variants associated with complex disease risk. We demonstrate that the model of gene action, relating genotype to phenotype, has a qualitative effect on several relevant aspects of the population genetic architecture of a complex trait. In particular, the genetic model impacts genetic variance component partitioning across the allele frequency spectrum and the power of statistical tests. Models with partial recessivity closely match the minor allele frequency distribution of significant hits from empirical genome-wide association studies without requiring homozygous effect sizes to be small. We highlight a particular gene-based model of incomplete recessivity that is appealing from first principles. Under that model, deleterious mutations in a genomic region partially fail to complement one another. This model of gene-based recessivity predicts the empirically observed inconsistency between twin and SNP based estimated of dominance heritability. Furthermore, this model predicts considerable levels of unexplained variance associated with intralocus epistasis. Our results suggest a need for improved statistical tools for region based genetic association and heritability estimation.

Genetic Evidence of a Population Bottleneck and Inbreeding in the Endangered New Zealand Sea Lion, Phocarctos hookeri.

The New Zealand sea lion (NZSL) is of high conservation concern due to its limited distribution and its declining population size. Historically, it occupied most of coastal New Zealand, but is now restricted to a few coastal sites in southern mainland New Zealand and the sub-Antarctic Islands. NZSLs have experienced a recent reduction in population size due to sealing in the 1900s, which is expected to have resulted in increased inbreeding and a loss of genetic variation, potentially reducing the evolutionary capacity of the species and negatively impacting on its long-term prospects for survival. We used 17 microsatellite loci, previously shown to have cross-species applications in pinnipeds, to determine locus- and population-specific statistics for 1205 NZSLs from 7 consecutive breeding seasons. We show that the NZSL population has a moderate level of genetic diversity in comparison to other pinnipeds. We provide genetic evidence for a population reduction, likely caused by historical sealing, and a measure of allele sharing/parental relatedness (internal relatedness) that is suggestive of increased inbreeding in pups that died during recent epizootic episodes. We hypothesize that population bottlenecks and nonrandom mating have impacted on the population genetic architecture of NZSLs, affecting its population recovery.

Novel distal eQTL analysis demonstrates effect of population genetic architecture on detecting and interpreting associations.

Mapping expression quantitative trait loci (eQTL) has identified genetic variants associated with transcription rates and has provided insight into genotype–phenotype associations obtained from genome-wide association studies (GWAS). Traditional eQTL mapping methods present significant challenges for the multiple-testing burden, resulting in a limited ability to detect eQTL that reside distal to the affected gene. To overcome this, we developed a novel eQTL testing approach, “network-based, large-scale identification of distal eQTL” (NetLIFT), which performs eQTL testing based on the pairwise conditional dependencies between genes’ expression levels. When applied to existing data from yeast segregants, NetLIFT replicated most previously identified distal eQTL and identified 46% more genes with distal effects compared to local effects. In liver data from mouse lines derived through the Collaborative Cross project, NetLIFT detected 5744 genes with local eQTL while 3322 genes had distal eQTL. This analysis revealed founder-of-origin effects for a subset of local eQTL that may contribute to previously described phenotypic differences in metabolic traits. In human lymphoblastoid cell lines, NetLIFT was able to detect 1274 transcripts with distal eQTL that had not been reported in previous studies, while 2483 transcripts with local eQTL were identified. In all species, we found no enrichment for transcription factors facilitating eQTL associations; instead, we found that most trans-acting factors were annotated for metabolic function, suggesting that genetic variation may indirectly regulate multigene pathways by targeting key components of feedback processes within regulatory networks. Furthermore, the unique genetic history of each population appears to influence the detection of genes with local and distal eQTL.

Novel Distal eQTL Analysis Demonstrates Effect of Population Genetic Architecture on Detecting and Interpreting Associations

Novel Distal eQTL Analysis Demonstrates Effect of Population Genetic Architecture on Detecting and Interpreting Associations

Environmental margin and island evolution in Middle Eastern populations of the Egyptian fruit bat

Here, we present a study of the population genetic architecture and microevolution of the Egyptian fruit bat (Rousettus aegyptiacus) at the environmental margins in the Middle East using mitochondrial sequences and nuclear microsatellites. In contrast to the rather homogenous population structure typical of cave-dwelling bats in climax tropical ecosystems, a relatively pronounced isolation by distance and population diversification was observed. The evolution of this pattern could be ascribed to the complicated demographic history at higher latitudes related to the range margin fragmentation and complex geomorphology of the studied area. Lineages from East Africa and Arabia show divergent positions. Within the northwestern unit, the most marked pattern of the microsatellite data set is connected with insularity, as demonstrated by the separate status of populations from Saharan oases and Cyprus. These demes also exhibit a reduction in genetic variability, which is presumably connected with founder effects, drift and other potential factors related to island evolution as site-specific selection. Genetic clustering indicates a semipermeability of the desert barriers in the Sahara and Arabian Peninsula and a corridor role of the Nile Valley. The results emphasize the role of the island environment in restricting the gene flow in megabats, which is also corroborated by biogeographic patterns within the family, and suggests the possibility of nascent island speciation on Cyprus. Demographic analyses suggest that the colonization of the region was connected to the spread of agricultural plants; therefore, the peripatric processes described above might be because of or strengthened by anthropogenic changes in the environment.

The population genetics of the Jewish people

Adherents to the Jewish faith have resided in numerous geographic locations over the course of three millennia. Progressively more detailed population genetic analysis carried out independently by multiple research groups over the past two decades has revealed a pattern for the population genetic architecture of contemporary Jews descendant from globally dispersed Diaspora communities. This pattern is consistent with a major, but variable component of shared Near East ancestry, together with variable degrees of admixture and introgression from the corresponding host Diaspora populations. By combining analysis of monoallelic markers with recent genome-wide variation analysis of simple tandem repeats, copy number variations, and single-nucleotide polymorphisms at high density, it has been possible to determine the relative contribution of sex-specific migration and introgression to map founder events and to suggest demographic histories corresponding to western and eastern Diaspora migrations, as well as subsequent microevolutionary events. These patterns have been congruous with the inferences of many, but not of all historians using more traditional tools such as archeology, archival records, linguistics, comparative analysis of religious narrative, liturgy and practices. Importantly, the population genetic architecture of Jews helps to explain the observed patterns of health and disease-relevant mutations and phenotypes which continue to be carefully studied and catalogued, and represent an important resource for human medical genetics research. The current review attempts to provide a succinct update of the more recent developments in a historical and human health context.Electronic supplementary materialThe online version of this article (doi:10.1007/s00439-012-1235-6) contains supplementary material, which is available to authorized users.

Climate effects on life cycle variation and population genetic architecture of the black bean aphid, Aphis fabae

Aphid species may exhibit different reproductive modes ranging from cyclical to obligate parthenogenesis. The distribution of life cycle variation in aphids is generally determined by ecological forces, mainly climate, because only sexually produced diapausing eggs can survive harsh winters or periods of absence of suitable host plants. Aphids are thus interesting models to investigate intrinsic and environmental factors shaping the competition among sexual and asexual lineages. We conducted a Europe-wide sampling of black bean aphids, Aphis fabae, and combined population genetic analyses based on microsatellite data with an experimental determination of life cycle strategies. Aphids were collected from broad beans (Vicia faba) as well as some Chenopodiaceae, but we detected no genetic differentiation between aphids from different host plants. Consistent with model predictions, life cycle variation was related to climate, with aphids from areas with cold winters investing more in sexual reproduction than aphids from areas with mild winters. Accordingly, only populations from mild areas exhibited a clear genetic signature of clonal reproduction. These differences arise despite substantial gene flow over large distances, which was evident from a very low geographic population structure and a lack of isolation-by-distance among 18 sites across distances of more than 1000 km. There was virtually no genetic differentiation between aphids with different reproductive modes, suggesting that new asexual lineages are formed continuously. Indeed, a surprising number of A. fabae genotypes even from colder climates produced some parthenogenetic offspring under simulated winter conditions. From this we predict that a shift to predominantly asexual reproduction could take place rapidly under climate warming.

Productivity differences between dandelion (Taraxacum officinale; Asteraceae) clones from pollution impacted versus non-impacted soils

Common dandelions (Taraxacum officinale Weber, sensu lato; Asteraceae) introduced to North America form an assemblage of asexual (agamospermous), clonal lineages derived from Eurasian mixed sexual and asexual populations. We investigated whether selection for more pollution tolerant clonal lineages occurs at polluted sites and selection for more pollution intolerant lineages occurs at unpolluted sites. We tested the above hypothesis by performing reciprocal greenhouse productivity experiments in which unique dandelion clones (12 clones, identified by DNA fingerprinting, from each site type) sampled from two unpolluted and two polluted (moderately enhanced Cu, Pb and Zn soil concentrations) sites were grown pairwise in both unpolluted (nutrient solution only) and polluted (nutrient solution + Cu, Pb and Zn) media (n = 48 paired tests for each media type). Dandelion clones from polluted sites produced fewer and smaller leaves, shorter roots and smaller root diameters, reduced shoot and root dry weights, and reduced total biomass compared to clones from unpolluted sites when clones were grown in unpolluted-media (P ≤ 0.05). In contrast, clones taken from unpolluted sites were shown to produce significantly fewer and shorter leaves, shorter roots and smaller root diameters, reduced shoot and root dry weights, reduced total biomass, a reduced shoot : root biomass ratio, and have much lower survival compared to clones from polluted sites when both were grown in polluted-media (P ≤ 0.05). These results reveal that there was increased selection against unpolluted-site clonal lineages in polluted-media and against polluted-site clonal lineages in unpolluted-media. Across all treatments, clones from unpolluted sites growing in unpolluted-media had the highest proximate measures of fitness. Overall, these findings provide insight into the relationships among anthropogenic environmental contamination and the consequent effects of selective forces acting on dandelion clones and their population genetic architecture.

Extensive outcrossing and androdioecy in a vertebrate species that otherwise reproduces as a self-fertilizing hermaphrodite

The mangrove killifish (Kryptolebias marmoratus) is the only vertebrate known to be capable of self-fertilization. Its gonad is typically an ovotestis that simultaneously produces eggs and sperm, and fertilization is internal. Although most populations of this species consist primarily or exclusively of hermaphroditic individuals, gonochoristic males occur at approximately 20% frequency in a natural population at Twin Cays, Belize. Here we use a battery of 36 microsatellite loci to document a striking genetic pattern (high intraspecimen heterozygosities and low within-population linkage disequilibria) that differs qualitatively from the highly homozygous (or "clonal") genetic architecture characteristic of killifish populations previously studied in Florida, where males are much rarer. These findings document that outcrossing (probably between gonochoristic males and hermaphrodites) is common at the Belize site, and, more importantly, they demonstrate the dramatic impact that functional androdioecy can have on the population genetic architecture of this reproductively unique vertebrate species.

Potential biases of incomplete linear models in heritability estimation and breeding value prediction

Potential biases associated with incomplete linear models in the estimation of heritability and the prediction of breeding values have been investigated. Results indicate that estimates of additive genetic variance and heritability as well as predicted parental breeding values from incomplete models will inevitably be biased as long as the true variance components of ignored effects are not zero. While models ignoring the interaction effect of males and females (SCA) × environment (E) interaction downwardly biased the estimates of additive genetic variance and heritability, models ignoring SCA and (or) the additive genetic effect (GCA) × E interaction yielded upward biases. The magnitudes of biases are functions of population genetic architecture, mating design, and field experimental design and can be precisely assessed with formulae derived for balanced data. Numerical simulations using unbalanced data of different mating and field experimental designs suggest that the formulae from balanced data can be used to approximate the minimum biases associated with unbalanced data. Because of the magnitudes of biases for some typical forest genetic scenarios, it is suggested that models ignoring SCA and (or) GCA × E should be avoided when the numbers of test sites and crosses per parent are small. However, incomplete model ignoring SCA × E interaction may be used to reduce computational demand with only negligible consequences.

When oceans meet: a teleost shows secondary intergradation at an Indian–Pacific interface

The Indo-West Pacific is characterized by extraordinary marine species diversity. The evolutionary mechanisms responsible for generating this diversity remain puzzling, but are often linked to Pleistocene sea level fluctuations. The impact of these sea level changes on the population genetic architecture of the estuarine fish Lates calcarifer are investigated via a natural experiment in a region of the Indo-West Pacific known to have undergone considerable change during the Pleistocene. L. calcarifer, a coastline-restricted catadromous teleost, provides an excellent model for studying the effects of sea level change as its habitat requirements potentially make it sensitive to the region's physical history. Evidence was found for a large phylogenetic break (4% mtDNA control region; 0.47% ATPase 6 and 8) either side of the Torres Strait, which separates the Western Pacifc and Indian Oceans, although some mixing of the clades was evident. This suggests clinal secondary introgression of the clades via contemporary gene flow. Further, populations on Australia's east coast appear to have passed through a bottleneck. This was linked to the historical drying of the Great Barrier Reef coastal lagoon, which resulted in a significant loss of habitat and forced retreat into isolated refugia. These results suggest that historical eustatic changes have left a significant imprint on the molecular diversity within marine species as well as among those in the Indo-West Pacifc.

Genetic structure in a population of a tropical tree Ocotea tenera (Lauraceae): influence of avian seed dispersal.

We studied the influence of avian seed dispersal on the structuring of genetic diversity in a population of a tropical tree, Ocotea tenera (Lauraceae). The seeds of O. tenera are principally dispersed by four, relatively specialized, fruit-eating bird species (emerald toucanets, keel-billed toucans, resplendent quetzals, and three-wattled bellbirds). We found high genetic diversity within the overall population and significant, nonrandom structuring of that diversity among subpopulations. Subpopulations contained members of several sibling groups, and most saplings within subpopulations were shown not to be the progeny of adult trees within the same subpopulation. Our data indicate that O. tenera subpopulations are founded with several seeds from few maternal families, and that this mode of establishment is an important determinant of population genetic architecture.