A genomic island linked to ecotype divergence in Atlantic cod

High gene flow and outcrossing within populations of two cryptic fungal pathogens on a native and non-native host in Cameroon

Levels of gene flow, Nm, were calculated for 34 predominantly self‐pollinated plants, using information on differentiation among populations, Gst. Gene flow levels varied from 0.01 to 6.55, and departed significantly from a uniform distribution. High, medium and low levels of gene flow were found among 15, 38, and 47 percent of the species, respectively. The average heterozygosity (H) and the Nm values showed a positively significant association. These results were compared to gene flow levels obtained with a limited number of predominantly outcrossed plants. Gene flow levels in several self‐pollinated species were comparable to those characteristic of some outcrossed species. Pollen flow, combined with long distance dispersal of propagules through various vectors may be responsible for the high levels of gene flow observed in self‐pollinated species. High gene flow may provide the genetic flexibility required for successful colonization, which is an essential feature of self‐pollinated plants.

Patterns of heterogeneous genomic differentiation have been well documented between closely related species, with some highly differentiated genomic regions ("genomic differentiation islands") spread throughout the genome. Differential levels of gene flow are proposed to account for this pattern, as genomic differentiation islands are suggested to be resistant to gene flow. Recent studies have also suggested that genomic differentiation islands could be explained by linked selection acting on genomic regions with low recombination rates. Here, we investigate genomic differentiation and gene-flow patterns for autosomes using RAD-seq data between two closely related species of long-tailed tits (Aegithalos bonvaloti and A.fuliginosus) in both allopatric and contact zone populations. The results confirm recent or ongoing gene flow between these two species. However, there is little evidence that the genomic regions that were found to be highly differentiated between the contact zone populations are resistant to gene flow, suggesting that differential levels of gene flow is not the cause of the heterogeneous genomic differentiation. Linked selection may be the cause of genomic differentiation islands between the allopatric populations with no or very limited gene flow, but this could not account for the heterogeneous genomic differentiation between the contact zone populations, which show evidence of recent or ongoing gene flow.

BackgroundLevels 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.MethodsIndividual 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.ResultsUnder 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.ConclusionsEven 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.

Patterns of divergence and polymorphism across hybrid zones can provide important clues as to their origin and maintenance. Unimodal hybrid zones or hybrid swarms are composed predominantly of recombinant individuals whose genomes are patchworks of alleles derived from each parental lineage. In contrast, bimodal hybrid zones contain few identifiable hybrids; most individuals fall within distinct genetic clusters. Distinguishing between hybrid swarms and bimodal hybrid zones can be important for taxonomic and conservation decisions regarding the status and value of hybrid populations. In addition, the causes of bimodality are important in understanding the generation and maintenance of biological diversity. For example, are distinct clusters mostly reproductively isolated and co-adapted gene complexes, or can distinctiveness be maintained by a few 'genomic islands' despite rampant gene flow across much of the genome? Here we focus on three patterns of distinctiveness in the face of gene flow between gartersnake taxa in the Great Lakes region of North America. Bimodality, the persistence of distinct clusters of genotypes, requires strong barriers to gene flow and supports recognition of distinct specialist (Thamnophis butleri) and generalist (Thamnophis radix) taxa. Concordance of DNA-based clusters with morphometrics supports the hypothesis that trophic morphology is a key component of divergence. Finally, disparity in the level of differentiation across molecular markers (amplified fragment length polymorphisms) indicates that distinctiveness is maintained by strong selection on a few traits despite high gene flow currently or in the recent past.

Cryptolepis sanguinolenta is an important medicinal plant used in the treatment of malaria in Ghana. Overharvesting, destruction of entire plant populations and poor seed viability have resulted in a substantial decrease in wild populations thereby threatening its long-term potential and survivability. In this study, fifteen polymorphic microsatellite loci were used to evaluate the genetic diversity and population structure of 179 C. sanguinolenta individuals among eight subpopulations in Ghana. The subpopulations were separated by a distance of 8.3 – 233.3 km. Our results indicated relatively high levels of genetic diversity (Ho= 0.41; He=0.61) and high gene flow (Nm=7.06), an indication of greater stability and adaptability within the ecosystem, limited genetic differentiation (mean FST=0.05; highest FST=0.1), which suggested insignificant differentiation among the subpopulations. The high levels of gene flow resulting from the wind-dispersed seeds might have contributed to the limited genetic differentiation among the subpopulations. The Bayesian cluster analysis revealed the presence of a population structure (K=2). A lack of isolation by distance (r=0.012; P=0.34) indicated an increase in the genetic similarity among the subpopulations as the geographic distance between them decreased. This study described the genetic diversity and population structure in the current C. sanguinolenta accessions and laid a foundation for future breeding efforts.

Genomic comparisons of closely related species have identified “islands” of locally elevated sequence divergence. Genomic islands may contain functional variants involved in local adaptation or reproductive isolation and may therefore play an important role in the speciation process. However, genomic islands can also arise through evolutionary processes unrelated to speciation, and examination of their properties can illuminate how new species evolve. Here, we performed scans for regions of high relative divergence (FST) in 12 species pairs of Darwin's finches at different genetic distances. In each pair, we identify genomic islands that are, on average, elevated in both relative divergence (FST) and absolute divergence (dXY). This signal indicates that haplotypes within these genomic regions became isolated from each other earlier than the rest of the genome. Interestingly, similar numbers of genomic islands of elevated dXY are observed in sympatric and allopatric species pairs, suggesting that recent gene flow is not a major factor in their formation. We find that two of the most pronounced genomic islands contain the ALX1 and HMGA2 loci, which are associated with variation in beak shape and size, respectively, suggesting that they are involved in ecological adaptation. A subset of genomic island regions, including these loci, appears to represent anciently diverged haplotypes that evolved early during the radiation of Darwin's finches. Comparative genomics data indicate that these loci, and genomic islands in general, have exceptionally low recombination rates, which may play a role in their establishment.

Population structure, genetic diversity, and geophylogeny of five populations of the Scarface rockskipper, Istiblennius pox Springer & Williams, 1994 were explored from two ecoregions using the D-loop marker of the mitochondrial control region. The results revealed no significant population genetic structure and no provable recent demographic expansion in the studied samples. The phylogeographic pattern retrieved in this study was a deep genealogical separation with major lineages broadly sympatric. The possible reasons for this phylogeographic pattern could be explained by the following: (i) high gene flow in a species with large evolutionary effective population size, in which some anciently separated lineages might by chance have been retained, whereas many intermediate genotypes were lost over time by gradual lineage sorting; and (ii) secondary contact and admixture between allopatrically evolved populations/lineages as a result of the Late Pleistocene glaciations, followed by recent and ongoing colonization events and high level of gene flow along the coasts of the Persian Gulf and Oman Sea, caused by larval dispersal. These findings were incongruent with previous morphological studies on this species from the same area, suggesting that phenotypic variability among the Scarface rockskipper populations may arise without major genetic differentiation.

Divergent natural selection, adaptive divergence and gene flow may interact in a number of ways. Recent studies have focused on the balance between selection and gene flow in natural populations, and empirical work has shown that gene flow can constrain adaptive divergence, and that divergent selection can constrain gene flow. A caveat is that phenotypic diversification may be under the direct influence of environmental factors (i.e. it may be due to phenotypic plasticity), in addition to partial genetic influence. In this case, phenotypic divergence may occur between populations despite high gene flow that imposes a constraint on genetic divergence. Plasticity may dampen the effects of natural selection by allowing individuals to rapidly adapt phenotypically to new conditions, thus slowing adaptive genetic divergence. On the other hand, plasticity may promote future adaptive divergence by allowing populations to persist in novel environments. Plasticity may promote gene flow between selective regimes by allowing dispersers to adapt to alternate conditions, or high gene flow may result in the selection for increased plasticity. Here I expand frameworks for understanding relationships among selection, adaptation and gene flow to include the effects of phenotypic plasticity in natural populations, and highlight its importance in evolutionary diversification.

Aim We assessed population differentiation and gene flow across the range of the blue-footed booby (Sula nebouxii) (1) to test the generality of the hypothesis that tropical seabirds exhibit higher levels of population genetic differentiation than their northern temperate counterparts, and (2) to determine if specialization to cold-water upwelling systems increases dispersal, and thus gene flow, in blue-footed boobies compared with other tropical sulids. Location Work was carried out on islands in the eastern tropical Pacific Ocean from Mexico to northern Peru. Methods We collected samples from 173 juvenile blue-footed boobies from nine colonies spanning their breeding distribution and used molecular markers (540 base pairs of the mitochondrial control region and seven microsatellite loci) to estimate population genetic differentiation and gene flow. Our analyses included classic population genetic estimation of pairwise population differentiation, population growth, isolation by distance, associations between haplotypes and geographic locations, and analysis of molecular variance, as well as Bayesian analyses of gene flow and population differentiation. We compared our results with those for other tropical seabirds that are not specialized to cold-water upwellings, including brown (Sula leucogaster), red-footed (S. sula) and masked (S. dactylatra) boobies. Results Blue-footed boobies exhibited weak global population differentiation at both mitochondrial and nuclear loci compared with all other tropical sulids. We found evidence of high levels of gene flow between colonies within Mexico and between colonies within the southern portion of the range, but reduced gene flow between these regions. We also found evidence for population growth, isolation by distance and weak phylogeographic structure. Main conclusions Tropical seabirds can exhibit weak genetic differentiation across large geographic distances, and blue-footed boobies exhibit the weakest population differentiation of any tropical sulid studied thus far. The weak population genetic structure that we detected in blue-footed boobies may be caused by increased dispersal, and subsequently increased gene flow, compared with other sulids. Increased dispersal by blue-footed boobies may be the result of the selective pressures associated with cold-water upwelling systems, to which blue-footed boobies appear specialized. Consideration of foraging environment may be particularly important in future studies of marine biogeography.

Understanding the evolutionary mechanisms generating parallel genomic divergence patterns among replicate ecotype pairs remains an important challenge in speciation research. We investigated the genomic divergence between the anadromous parasitic river lamprey (Lampetra fluviatilis) and the freshwater-resident nonparasitic brook lamprey (Lampetra planeri) in nine population pairs displaying variable levels of geographic connectivity. We genotyped 338 individuals with RAD sequencing and inferred the demographic divergence history of each population pair using a diffusion approximation method. Divergence patterns in geographically connected population pairs were better explained by introgression after secondary contact, whereas disconnected population pairs have retained a signal of ancient migration. In all ecotype pairs, models accounting for differential introgression among loci outperformed homogeneous migration models. Generating neutral predictions from the inferred divergence scenarios to detect highly differentiated markers identified greater proportions of outliers in disconnected population pairs than in connected pairs. However, increased similarity in the most divergent genomic regions was found among connected ecotype pairs, indicating that gene flow was instrumental in generating parallelism at the molecular level. These results suggest that heterogeneous genomic differentiation and parallelism among replicate ecotype pairs have partly emerged through restricted introgression in genomic islands.

Genetic variation and population genetic structure of the large yellow croaker (Larimichthys crocea) based on genome‐wide single nucleotide polymorphisms in farmed and wild populations

The genetic diversity of the Red Bororo and White Fulani cattle breeds of Cameroon and Nigeria was assessed with a panel of 32 markers. Estimates for the various indices of genetic diversity, total number of alleles (TNA), mean observed number of alleles (MNA), mean effective number of alleles (MNE), observed heterozygosity (Hob) and expected heterozygosity (Hex), were higher at microsatellite loci than at protein loci. Mean Hex values were above 71% at microsatellite loci in all the breeds and ranged from 37% to 41.6% at milk protein loci and from 40.9% to 45.6% at blood protein loci. The highest TNA and MNA of microsatellites were recorded for the Nigerian White Fulani. MNE of milk protein loci was highest in the Cameroonian Red Bororo, while TNA of blood protein loci was highest in the Cameroonian White Fulani. The high genetic diversity levels indicate the presence of the necessary ingredients for improvement breeding and conservation. Multi-locus estimates of within-population inbreeding (f), total inbreeding (F) and population differentiation (theta) of the breeds were significantly different from zero, except for theta of blood proteins. A high level of gene flow was found between the breeds (5.829). The phylogenetic relationship existing among the four breeds is greatly influenced by location. The high gene flow between the breeds may lead to a loss of genetic diversity through genetic uniformity and a reduction in opportunities for future breed development. We propose an improvement scheme with aims to prevent loss of genetic diversity, improve productivity and reduce uncontrolled genetic exchanges between breeds.

Fasciola hepatica, the liver fluke, is a trematode parasite of considerable economic importance to the livestock industry and is a re-emerging zoonosis that poses a risk to human health in F. hepatica-endemic areas worldwide. Drug resistance is a substantial threat to the current and future control of F. hepatica, yet little is known about how the biology of the parasite influences the development and spread of resistance. Given that F. hepatica can self-fertilise and therefore inbreed, there is the potential for greater population differentiation and an increased likelihood of recessive alleles, such as drug resistance genes, coming together. This could be compounded by clonal expansion within the snail intermediate host and aggregation of parasites of the same genotype on pasture. Alternatively, widespread movement of animals that typically occurs in the UK could promote high levels of gene flow and prevent population differentiation. We identified clonal parasites with identical multilocus genotypes in 61% of hosts. Despite this, 84% of 1579 adult parasites had unique multilocus genotypes, which supports high levels of genotypic diversity within F. hepatica populations. Our analyses indicate a selfing rate no greater than 2%, suggesting that this diversity is in part due to the propensity for F. hepatica to cross-fertilise. Finally, although we identified high genetic diversity within a given host, there was little evidence for differentiation between populations from different hosts, indicating a single panmictic population. This implies that, once those emerge, anthelmintic resistance genes have the potential to spread rapidly through liver fluke populations.

Landscape genomic studies analyze spatial patterns of genetic variation to test hypotheses about how demographic history, gene flow, and natural selection have shaped populations. For decades, angiosperm trees have served as outstanding model systems for landscape-scale genetic studies due to their extensive geographic ranges, large effective population sizes, abundant genetic diversity, and high gene flow. These characteristics were recognized early in the landscape genetics literature, and studies on angiosperm trees, particularly Populus and Quercus, tested hypotheses about how landscape features shaped neutral patterns of gene flow and population divergence. More recently, advances in sequencing and analysis methodologies have allowed for greater opportunities to directly test how natural selection acting locally across the landscape has shaped the genome-wide diversity of populations, often in the context of broad climatic gradients in growing season length. Despite, the methodological gains and successes of the last decade, landscape genomics studies face new challenges of study design, hypothesis testing, and validation. Here, we explore the development of landscape genetics and genomics in angiosperm trees and what we have learned from investigating the evolutionary consequences of life as a tree in heterogeneous landscapes. We outline the past, present, and potential future of landscape genomic studies in angiosperm trees, highlighting successes of the field, challenges to overcome, and ideas that scientists from all backgrounds engaged in landscape genomics should consider.