Patterns Of Introgression Research Articles

Asymmetry matters: A genomic assessment of directional biases in gene flow between hybridizing spruces.

Assessing directional bias in interspecific gene flow might be important in determining the evolutionary trajectory of closely related species pairs. Using a set of 300 single nucleotide polymorphisms (SNPs) having variable propensity to cross species boundary, we evaluated the genomic extent and direction of interspecific gene flow in a progenitor‐derivative spruce species pair (black spruce and red spruce). A higher rate of gene flow was found from black spruce toward red spruce purebreds than vice versa. This asymmetry could reflect the historical gene flow between the two taxa at the time of species inception and during postglacial colonization. A clear asymmetry in introgression was depicted by a greater gene flow between red spruce and hybrids than between black spruce and hybrids. While backcrossing toward red spruce was invariably high across the genome, the actual species boundary is between hybrids and black spruce where gene flow is impeded at those genomic regions impermeable to introgression. Associations between hybrid index and climatic variables (total annual precipitation and mean annual temperature) were tested, as these might indicate a role for exogenous selection in maintaining the species boundary. While an apparent association was found between the hybrid index and precipitation, it collapsed when considered in light of the directional bias in interspecific gene flow. Hence, considering asymmetrical patterns of introgression allowed us to falsify an apparent role for exogenous selection. Although this was not formerly tested here, we suggest that this pattern could result from asymmetrical endogenous selection, a contention that deserves further investigations.

Genotyping-by-sequencing of pear (Pyrus spp.) accessions unravels novel patterns of genetic diversity and selection footprints

Understanding of genetic diversity and marker-trait relationships in pears (Pyrus spp.) forms an important part of gene conservation and cultivar breeding. Accessions of Asian and European pear species, and interspecific hybrids were planted in a common garden experiment. Genotyping-by-sequencing (GBS) was used to genotype 214 accessions, which were also phenotyped for fruit quality traits. A combination of selection scans and association analyses were used to identify signatures of selection. Patterns of genetic diversity, population structure and introgression were also investigated. About 15 000 high-quality SNP markers were identified from the GBS data, of which 25% and 11% harboured private alleles for European and Asian species, respectively. Bayesian clustering analysis suggested negligible gene flow, resulting in highly significant population differentiation (Fst=0.45) between Asian and European pears. Interspecific hybrids displayed an average of 55% and 45% introgression from their Asian and European ancestors, respectively. Phenotypic (firmness, acidity, shape and so on) variation between accessions was significantly associated with genetic differentiation. Allele frequencies at large-effect SNP loci were significantly different between genetic groups, suggesting footprints of directional selection. Selection scan analyses identified over 20 outlier SNP loci with substantial statistical support, likely to be subject to directional selection or closely linked to loci under selection.

Pattern of natural introgression in a Nothofagus hybrid zone from South American temperate forests

Interspecific gene flow is a common phenomenon in Nothofagaceae species; however, the dynamics of introgression in hybrid zones remains largely unknown. We focused on two ecologically and morphologically different Nothofagus species from Patagonia, Nothofagus nervosa and Nothofagus obliqua. In a natural hybrid zone, we established two plots 280 m apart in altitude (ca. 1.9 °C difference in mean temperature), and two subplots which captured microsite variation (abundance and spatial distribution of species and predominance of wind direction). We used intensive sampling of individuals (2055, including adults and regeneration) and molecular genotyping of 6 highly species-specific nuclear microsatellites for the identification and classification of hybrids, based on estimates of ancestry and interclass heterozygosity. We evaluated the relative contribution of our sampling effects to variation in hybrid incidence and direction of introgression using generalized linear mixed effects models. We determined that introgressive hybridization occurs at a global rate of 7.8% and that variation was mostly explained by plots (frequency at low altitude was approximately twice that found at high altitude), while it was less influenced by subplots. The high altitude plot was dominated by late-generation backcrosses to N. obliqua (asymmetric bimodality), whereas the low altitude plot consisted of intermediate hybrids (unimodality) and showed asymmetry for introgression between subplots. Differences were not detected between adults and regeneration, suggesting early-acting reproductive isolating barriers. F1 hybrids occur at a global frequency of 3.8%, and are fertile, as the detection of first- and late-generation hybrids indicates.

Lost in the hybridisation vortex: high-elevation Senecio hercynicus (Compositae, Senecioneae) is genetically swamped by its congener S. ovatus in the Bavarian Forest National Park (SE Germany)

Hybridisation is an important evolutionary process. The investigation of hybridisation along elevational gradients, with their steep abiotic and biotic clines, provides insight into the adaptation and maintenance of species in adjacent habitats. The rare Senecio hercynicus and its spreading congener S. ovatus are vertically vicariant species that show hybridisation in their range overlaps. In the present study, we used AFLP fingerprinting of 689 individuals from 38 populations to analyse population structure and introgression patterns along four elevational transects (650–1350 m) in the Bavarian Forest National Park, Gemany. Subsequently, we searched for loci putatively under divergent selection that may maintain ‘pure’ species despite hybrid formation by identifying taxon-specific alleles. A maximum-likelihood based hybrid index shows that the overall genetic differentiation among all populations was very low with a vanishingly small number of pure parental individuals. Almost 75% of the investigated individuals were classified as backcrosses towards S. ovatus. The highest S. hercynicus ancestry was found in the uppermost populations of two transects. Further, we found seven taxon-specific alleles being under divergent selection that correlated with climatic variables and deviating from neutral introgression. According to our results, hybridisation of S. ovatus and S. hercynicus has reached an advanced state of genetic swamping and there seems to be no driving force that is strong enough to keep both species as different lineages. Rather, S. ovatus appears to benefit through putatively adaptive introgression.

Harnessing the hidden genetic diversity for improving multiple abiotic stress tolerance in rice (Oryza sativa L.).

To develop superior rice varieties with improved yield in most rainfed areas of Asia/Africa, we started an introgression-breeding program for simultaneously improving yield and tolerances of multiple abiotic stresses. Using eight BC1 populations derived from a widely adaptable recipient and eight donors plus three rounds of phenotypic selection, we developed 496 introgression lines (ILs) with significantly higher yield under drought, salt and/or non-stress conditions in 5 years. Six new varieties were released in the Philippines and Pakistan and many more are being evaluated in multi-location yield trials for releasing in several countries. Marker-facilitated genetic characterization revealed three interesting aspects of the breeding procedure: (1) the donor introgression pattern in specific BC populations was characteristic; (2) introgression frequency in different genomic regions varied considerably, resulting primarily from strong selection for the target traits; and (3) significantly lower heterozygosity was observed in BC progenies selected for drought and salinity tolerance. Applying strong phenotypic selection under abiotic stresses in early segregating generations has major advantages for not only improving multiple abiotic stress tolerance but also achieving quicker homozygosity in early generations. This breeding procedure can be easily adopted by small breeding programs in developing countries to develop high-yielding varieties tolerant of abiotic stresses. The large set of trait-specific ILs can be used for genetic mapping of genes/QTL that affect target and non-target traits and for efficient varietal development by designed QTL pyramiding and genomics-based recurrent selection in our Green Super Rice breeding technology.

Phylogenomic Insights into Mouse Evolution Using a Pseudoreference Approach.

Comparative genomic studies are now possible across a broad range of evolutionary timescales, but the generation and analysis of genomic data across many different species still present a number of challenges. The most sophisticated genotyping and down-stream analytical frameworks are still predominantly based on comparisons to high-quality reference genomes. However, established genomic resources are often limited within a given group of species, necessitating comparisons to divergent reference genomes that could restrict or bias comparisons across a phylogenetic sample. Here, we develop a scalable pseudoreference approach to iteratively incorporate sample-specific variation into a genome reference and reduce the effects of systematic mapping bias in downstream analyses. To characterize this framework, we used targeted capture to sequence whole exomes (∼54 Mbp) in 12 lineages (ten species) of mice spanning the Mus radiation. We generated whole exome pseudoreferences for all species and show that this iterative reference-based approach improved basic genomic analyses that depend on mapping accuracy while preserving the associated annotations of the mouse reference genome. We then use these pseudoreferences to resolve evolutionary relationships among these lineages while accounting for phylogenetic discordance across the genome, contributing an important resource for comparative studies in the mouse system. We also describe patterns of genomic introgression among lineages and compare our results to previous studies. Our general approach can be applied to whole or partitioned genomic data and is easily portable to any system with sufficient genomic resources, providing a useful framework for phylogenomic studies in mice and other taxa.

Genomic insights into divergence and dual domestication of cultivated allotetraploid cottons

BackgroundCotton has been cultivated and used to make fabrics for at least 7000 years. Two allotetraploid species of great commercial importance, Gossypium hirsutum and Gossypium barbadense, were domesticated after polyploidization and are cultivated worldwide. Although the overall genetic diversity between these two cultivated species has been studied with limited accessions, their population structure and genetic variations remain largely unknown.ResultsWe resequence the genomes of 147 cotton accessions, including diverse wild relatives, landraces, and modern cultivars, and construct a comprehensive variation map to provide genomic insights into the divergence and dual domestication of these two important cultivated tetraploid cotton species. Phylogenetic analysis shows two divergent groups for G. hirsutum and G. barbadense, suggesting a dual domestication processes in tetraploid cottons. In spite of the strong genetic divergence, a small number of interspecific reciprocal introgression events are found between these species and the introgression pattern is significantly biased towards the gene flow from G. hirsutum into G. barbadense. We identify selective sweeps, some of which are associated with relatively highly expressed genes for fiber development and seed germination.ConclusionsWe report a comprehensive analysis of the evolution and domestication history of allotetraploid cottons based on the whole genomic variation between G. hirsutum and G. barbadense and between wild accessions and modern cultivars. These results provide genomic bases for improving cotton production and for further evolution analysis of polyploid crops.

Geographical variation in bill colour in the Long-tailed Finch: evidence for a narrow zone of admixture between sub-species

ABSTRACTThe Long-tailed Finch (Poephila acuticauda) is endemic to Australia’s northern tropics and comprises two sub-species differentiated by bill colour: yellow in the western sub-species acuticauda and red in the eastern sub-species hecki. We present an extensive survey of bill colour variation across the range of the Long-tailed Finch (more than 700 individuals collected across nearly 1500 km of range). Geographic clinal analysis using bill reflectance spectrophotometry data suggests that the greatest extent of bill colour admixture is only ~150 km wide and is centred approximately 50 km west of Katherine, Northern Territory (14.5° S, 132.3° E). Variation in bill colour is generally low outside of this zone, and across widely distributed allopatric populations of both sub-species. However, the best-fit clinal model supports a pattern of asymmetrical introgression of bill colour from the east into the west. The narrow geographic width of bill colour admixture between Long-tailed Finch sub-species and the estimated timing of secondary contact (14–21 kya) suggests a role for selection acting against hybrids and/or parentals in maintaining sub-species as independently evolving populations.

Introgression Makes Waves in Inferred Histories of Effective Population Size.

Human populations have a complex history of introgression and of changing population size. Human genetic variation has been affected by both these processes, so inference of past population size depends upon the pattern of gene flow and introgression among past populations. One remarkable aspect of human population history as inferred from genetics is a consistent "wave" of larger effective population sizes, found in both African and non-African populations, that appears to reflect events prior to the last 100,000 years. I carried out a series of simulations to investigate how introgression and gene flow from genetically divergent ancestral populations affect the inference of ancestral effective population size. Both introgression and gene flow from an extinct, genetically divergent population consistently produce a wave in the history of inferred effective population size. The time and amplitude of the wave reflect the time of origin of the genetically divergent ancestral populations and the strength of introgression or gene flow. These results demonstrate that even small fractions of introgression or gene flow from ancient populations may have visible effects on the inference of effective population size.

Hybridization and genetic introgression patterns between two South American catfish along their sympatric distribution range

The presence of introgressive hybridization in the wild, especially that resulting from human interference, can have negative impacts on biodiversity. Genetic tools provide essential information for species and hybrid identification, facilitating the conservation of natural resources. Here, we tested a set of markers to precisely elucidate introgressive hybridization between Pseudoplatystoma corruscans and Pseudoplatystoma reticulatum, two South American catfishes. New microsatellites showed high interspecific genetic divergence, and simulated data demonstrated the high power of STRUCTURE and NEWHYBRIDS for hybrid identification and classification, especially when all 11 nuclear markers were used. The investigation of real populations suggested that natural hybridization is rare. Otherwise, different hybridization scenarios were observed in two wild populations: one involving advanced backcrosses and the other involving high admixture. Our data represent the first detailed evaluation of genetic introgression between these species in Parana and Paraguay Basins and suggest that genetic contamination is occurring through F1 hybrids from aquaculture facilities. The results also provide a useful set of markers for monitoring escapees to aid in the conservation of the wild population and sustainable aquaculture. Additionally, species genotypic data are freely available to be used in the future as “parental species reference” in Bayesian methods assignments.

Adaptive signal coloration maintained in the face of gene flow in a Hispaniolan Anolis Lizard

BackgroundStudies of geographic variation can provide insight into the evolutionary processes involved in the early stages of biological diversification. In particular, multiple, replicated cases of geographic trait divergence present a powerful approach to study how patterns of introgression and adaptive divergence can vary with geographic space and time. In this study, we conduct replicated, fine-scaled molecular genetic analyses of striking geographic dewlap color variation of a Hispaniolan Anolis lizard, Anolis distichus, to investigate whether adaptive trait divergence is consistently associated with speciation, whereby genetic divergence is observed with neutral markers, or whether locally adapted traits are maintained in the face of continued gene flow.ResultsWe find instances where shifts in adaptive dewlap coloration across short geographic distances are associated with reproductive isolation as well as maintained in the face of gene flow, suggesting the importance of both processes in maintaining geographic dewlap variation.ConclusionOur study suggests that adaptive dewlap color differences are maintained under strong divergent natural selection, but this divergence does not necessarily lead to anole speciation.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-016-0763-4) contains supplementary material, which is available to authorized users.

Asymmetrical introgression patterns between rusty-necklaced partridge (Alectoris magna) and chukar partridge (Alectoris chukar) in China.

The rusty-necklaced partridge (Alectoris magna) and the chukar partridge (Alectoris chukar) are the most common gamebirds in northern China. Previous comparisons of mitochondrial DNA (mtDNA) have revealed an introgression phenomenon between 2 species of partridge in the Liupan Mountain region of China. mtDNA is maternally inherited, making it difficult to determine the origin of parental genes. We assessed the genetic variation and gene flow between these 2 species of partridges using 8 microsatellite loci as neutral diagnostic markers in 171 samples from the hybrid zone. Our data revealed an extensive divergence of genetic structure between populations of rusty-necklaced partridges and chukar partridges. In this study, we found that 19 samples had been previously morphologically identified as rusty-necklaced partridge were genetically identified as hybrids through Bayesian analysis using STRUCTURE analysis. These hybrids exhibited a mosaic of alleles that were derived from both parental lineages. However, chukar partridges did not present the genotype of the rusty-necklaced partridge. Thus, our findings demonstrate that the hybridization between the 2 species was the result of asymmetrical introgression, with gene flow occurring only from the chukar partridge to the rusty-necklaced partridge. In addition, we also note the high linkage disequilibrium in populations of the rusty-necklaced partridge. These results indicate that although unidirectional introgression did not reduce genetic diversity of the Alectoris partridges, it affected the balance of gene flow between populations. The data from microsatellite DNA prompted our concern about the genetic integrity of the rusty-necklaced partridge.

Dynamics of mtDNA introgression during species range expansion: insights from an experimental longitudinal study.

Introgressive hybridization represents one of the long-lasting debated genetic consequences of species range expansion. Mitochondrial DNA has been shown to heavily introgress between interbreeding animal species that meet in new sympatric areas and, often, asymmetric introgression from local to the colonizing populations has been observed. Disentangling among the evolutionary and ecological processes that might shape this pattern remains difficult, because they continuously act across time and space. In this context, long-term studies can be of paramount importance. Here, we investigated the dynamics of mitochondrial introgression between two mosquito species (Aedes mariae and Ae. zammitii ) during a colonization event that started in 1986 after a translocation experiment. By analyzing 1,659 individuals across 25 years, we showed that introgression occurred earlier and at a higher frequency in the introduced than in the local species, showing a pattern of asymmetric introgression. Throughout time, introgression increased slowly in the local species, becoming reciprocal at most sites. The rare opportunity to investigate the pattern of introgression across time during a range expansion along with the characteristics of our study-system allowed us to support a role of demographic dynamics in determining the observed introgression pattern.

Beyond clines: lineages and haplotype blocks in hybrid zones.

Hybrid zones formed between recently diverged populations offer an opportunity to study the mechanisms underlying reproductive isolation and the process of speciation. Here, we use a combination of analytical theory and explicit forward simulations to describe how selection against hybrid genotypes impacts patterns of introgression across genomic and geographic space. By describing how lineages move across the hybrid zone, in a model without coalescence, we add to modern understanding of how clines form and how parental haplotypes are broken up during introgression. Working with lineages makes it easy to see that clines form in about 1/s generations, where s is the strength of selection against hybrids, and linked clines persist over a genomic scale of 1/T, where T is the age, in generations, of the hybrid zone. Locally disadvantageous alleles tend to exist as small families, whose lineages trace back to the side from which they originated at speed s dispersal distances per generation. The lengths of continuous tracts of ancestry provide an additional source of information: blocks of ancestry surrounding incompatibilities can be substantially longer than the genomewide average block length at the same spatial location, an observation that might be used to identify candidate targets of selection.

Past lake shore dynamics explain present pattern of unidirectional introgression across a habitat barrier

Introgression patterns between divergent lineages are often characterized by asymmetry in the direction and among-marker variation in the extent of gene flow, and therefore inform on the mechanisms involved in differentiation and speciation. In the present study, we test the hypothesis that unidirectional introgression between two phenotypically and genetically distinct lineages of the littoral, rock-dwelling cichlid fish Tropheus moorii across a wide sandy bay is linked to observed differences in mate preferences between the two lineages. This hypothesis predicts bi-directional nuclear gene flow and was rejected by congruent patterns of introgression in mtDNA, AFLP and microsatellite markers, with admixture confined to the populations west of the bay. This pattern can be explained on the basis of habitat changes in the course of lake level fluctuations, which first facilitated the development of a symmetric admixture zone including the area corresponding to the present sand bay and then shaped asymmetry by causing local extinctions and cessation of gene flow when this area became once more inhabitable. This conforms with previous assumptions that habitat dynamics are a primary determinant of population-level evolution in Tropheus. In this respect, Tropheus may be representative of species whose preferred habitat is subject to frequent re-structuring.

Nuclear introgression without mitochondrial introgression in two turtle species exhibiting sex‐specific trophic differentiation

Despite the presence of reproductive barriers between species, interspecific gene introgression has been documented in a range of natural systems. Comparing patterns of genetic introgression in biparental versus matrilineal markers can potentially reveal sex‐specific barriers to interspecific gene flow. Hybridization has been documented in the freshwater turtles Graptemys geographica and G. pseudogeographica, whose ranges are largely sympatric. Morphological differentiation between the species is restricted to females, with female G. geographica possessing large heads and jaws compared to the narrow heads of G. pseudogeographica females. If hybrid females are morphologically intermediate, they may be less successful at exploiting parental feeding niches, thereby limiting the introgression of maternally inherited, but not biparental, molecular markers. We paired sequence data with stable isotope analysis and examined sex‐specific genetic introgression and trophic differentiation in sympatric populations of G. geographica and G. pseudogeographica. We observed introgression from G. pseudogeographica into G. geographica at three nuclear loci, but not at the mitochondrial locus. Analysis of ∂15N and ∂13C was consistent with species differences in trophic positioning in females, but not males. These results suggest that ecological divergence in females may reduce the opportunity for gene flow in this system.

Hybrid origin of European Vipers (Vipera magnifica and Vipera orlovi) from the Caucasus determined using genomic scale DNA markers.

BackgroundStudying patterns of introgression can illuminate the role of hybridization in speciation, and help guide decisions relevant to the conservation of rare taxa. Vipera magnifica and Vipera orlovi are small vipers that have high conservation status due to their rarity and restricted distributions in an area of the Caucasus region where two other related species are present – V. kaznakovi and V. renardi. Despite numerous observations of hybridization between different species of small vipers, and the potential of a hybrid origin for V. magnifica and V. orlovi based on their distribution with respect to V. kaznakovi and V. renardi, hypotheses of a hybrid origin have not been formally tested. Here we generate genomic-scale data by performing next generation sequencing of double digest restriction-site associated DNA libraries, and use these multilocus data to test whether these two species are of hybrid origin.ResultsWe generated over nine hundred loci for 38 specimens of six taxa, and analysed the dataset using Bayesian clustering and multivariate methods, as well as Patterson D-statistics, which can distinguish between incomplete lineage sorting and introgression as explanations for shared polymorphism. The results demonstrate a pattern of historical admixture in the two purported hybrids that is consistent with past gene flow from V. renardi into V. kaznakovi. The average admixture proportion in individuals was low (6.39 %) in the case of V. magnifica, but was higher in V. orlovi (19.02 %). We also show that the specific individual samples used in D-statistic tests can have a significant impact on inferences regarding the magnitude of introgression, suggesting the importance of including multiple individuals in these analyses.ConclusionsOur results support the conclusion that both V. orlovi and V. magnifica had formed through a hybridization event between V. kaznakovi and V. renardi. Given a low proportion of admixture and absence of clear ecological and morphological differences V. magnifica should be treated as a marginal population of V. kaznakovi. Further studies that include analyses of ecological segregation of V. orlovi from parental taxa and search for evolutionary consequences of hybridisation would clarify if V. orlovi is a distinct hybrid species. Until this we recommend preserving the current taxonomy and protection status of V. orlovi.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-016-0647-7) contains supplementary material, which is available to authorized users.

Differential introgression and the maintenance of species boundaries in an advanced generation avian hybrid zone.

BackgroundEvolutionary processes, including selection and differential fitness, shape the introgression of genetic material across a hybrid zone, resulting in the exchange of some genes but not others. Differential introgression of molecular or phenotypic markers can thus provide insight into factors contributing to reproductive isolation. We characterized patterns of genetic variation across a hybrid zone between two tidal marsh birds, Saltmarsh (Ammodramus caudacutus) and Nelson’s (A. nelsoni) sparrows (n = 286), and compared patterns of introgression among multiple genetic markers and phenotypic traits.ResultsGeographic and genomic cline analyses revealed variable patterns of introgression among marker types. Most markers exhibited gradual clines and indicated that introgression exceeds the spatial extent of the previously documented hybrid zone. We found steeper clines, indicating strong selection for loci associated with traits related to tidal marsh adaptations, including for a marker linked to a gene region associated with metabolic functions, including an osmotic regulatory pathway, as well as for a marker related to melanin-based pigmentation, supporting an adaptive role of darker plumage (salt marsh melanism) in tidal marshes. Narrow clines at mitochondrial and sex-linked markers also offer support for Haldane’s rule. We detected patterns of asymmetrical introgression toward A. caudacutus, which may be driven by differences in mating strategy or differences in population density between the two species.ConclusionsOur findings offer insight into the dynamics of a hybrid zone traversing a unique environmental gradient and provide evidence for a role of ecological divergence in the maintenance of pure species boundaries despite ongoing gene flow.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-016-0635-y) contains supplementary material, which is available to authorized users.

Heterogeneous genome divergence, differential introgression, and the origin and structure of hybrid zones.

Hybrid zones have been promoted as windows on the evolutionary process and as laboratories for studying divergence and speciation. Patterns of divergence between hybridizing species can now be characterized on a genomewide scale, and recent genome scans have focused on the presence of 'islands' of divergence. Patterns of heterogeneous genomic divergence may reflect differential introgression following secondary contact and provide insights into which genome regions contribute to local adaptation, hybrid unfitness and positive assortative mating. However, heterogeneous genome divergence can also arise in the absence of any gene flow, as a result of variation in selection and recombination across the genome. We suggest that to understand hybrid zone origins and dynamics, it is essential to distinguish between genome regions that are divergent between pure parental populations and regions that show restricted introgression where these populations interact in hybrid zones. The latter, more so than the former, reveal the likely genetic architecture of reproductive isolation. Mosaic hybrid zones, because of their complex structure and multiple contacts, are particularly good subjects for distinguishing primary intergradation from secondary contact. Comparisons among independent hybrid zones or transects that involve the 'same' species pair can also help to distinguish between divergence with gene flow and secondary contact. However, data from replicate hybrid zones or replicate transects do not reveal consistent patterns; in a few cases, patterns of introgression are similar across independent transects, but for many taxa, there is distinct lack of concordance, presumably due to variation in environmental context and/or variation in the genetics of the interacting populations.

Genomic and functional approaches reveal a case of adaptive introgression from Populus balsamifera (balsam poplar) in P.trichocarpa (black cottonwood).

Natural hybrid zones in forest trees provide systems to study the transfer of adaptive genetic variation by introgression. Previous landscape genomic studies in Populus trichocarpa, a keystone tree species, indicated genomic footprints of admixture with its sister species Populus balsamifera and identified candidate genes for local adaptation. Here, we explored the patterns of introgression and signals of local adaptation in P.trichocarpa and P.balsamifera, employing genome resequencing data from three chromosomes in pure species and admixed individuals from wild populations. Local ancestry analysis in admixed P.trichocarpa revealed a telomeric region in chromosome 15 with P.balsamifera ancestry, containing several candidate genes for local adaptation. Genomic analyses revealed signals of selection in certain genes in this region (e.g. PRR5, COMT1), and functional analyses based on gene expression variation and correlations with adaptive phenotypes suggest distinct functions of the introgressed alleles. In contrast, a block of genes in chromosome 12 paralogous to the introgressed region showed no signs of introgression or signatures of selection. We hypothesize that the introgressed region in chromosome 15 has introduced modular or cassette-like variation into P.trichocarpa. These linked adaptive mutations are associated with a block of genes in chromosome 15 that appear to have undergone neo- or subfunctionalization relative to paralogs in a duplicated region on chromosome 12 that show no signatures of adaptive variation. The association between P.balsamifera introgressed alleles with the expression of adaptive traits in P.trichocarpa supports the hypothesis that this is a case of adaptive introgression in an ecologically important foundation species.