ABSTRACT
Most tree species underwent cycles of contraction and expansion during the Quaternary. These cycles led to an ancient and complex genetic structure that has since been affected by extensive gene flow and by strong local adaptation. The extent to which hybridization played a role in this multi-layered genetic structure is important to be investigated. To study the effect of hybridization on the joint population genetic structure of two dominant species of the Eurasian boreal forest, Picea abies and P. obovata, we used targeted resequencing and obtained around 480 K nuclear SNPs and 87 chloroplast SNPs in 542 individuals sampled across most of their distribution ranges. Despite extensive gene flow and a clear pattern of Isolation-by-Distance, distinct genetic clusters emerged, indicating the presence of barriers and corridors to migration. Two cryptic refugia located in the large hybrid zone between the two species played a critical role in shaping their current distributions. The two species repeatedly hybridized during the Pleistocene and the direction of introgression depended on latitude. Our study suggests that hybridization helped both species to overcome main shifts in their distribution ranges during glacial cycles and highlights the importance of considering whole species complex instead of separate entities to retrieve complex demographic histories.
Subject(s)
Gene Flow , Genetics, Population , Hybridization, Genetic , Picea , Polymorphism, Single Nucleotide , Picea/genetics , Polymorphism, Single Nucleotide/genetics , Norway , DNA, Chloroplast/genetics , Biological Evolution , Sequence Analysis, DNAABSTRACT
Closely related species often use the same genes to adapt to similar environments. However, we know little about why such genes possess increased adaptive potential and whether this is conserved across deeper evolutionary lineages. Adaptation to climate presents a natural laboratory to test these ideas, as even distantly related species must contend with similar stresses. Here, we re-analyse genomic data from thousands of individuals from 25 plant species as diverged as lodgepole pine and Arabidopsis (~300 Myr). We test for genetic repeatability based on within-species associations between allele frequencies in genes and variation in 21 climate variables. Our results demonstrate significant statistical evidence for genetic repeatability across deep time that is not expected under randomness, identifying a suite of 108 gene families (orthogroups) and gene functions that repeatedly drive local adaptation to climate. This set includes many orthogroups with well-known functions in abiotic stress response. Using gene co-expression networks to quantify pleiotropy, we find that orthogroups with stronger evidence for repeatability exhibit greater network centrality and broader expression across tissues (higher pleiotropy), contrary to the 'cost of complexity' theory. These gene families may be important in helping wild and crop species cope with future climate change, representing important candidates for future study.
ABSTRACT
Introgression allows polyploid species to acquire new genomic content from diploid progenitors or from other unrelated diploid or polyploid lineages, contributing to genetic diversity and facilitating adaptive allele discovery. In some cases, high levels of introgression elicit the replacement of large numbers of alleles inherited from the polyploid's ancestral species, profoundly reshaping the polyploid's genomic composition. In such complex polyploids, it is often difficult to determine which taxa were the progenitor species and which taxa provided additional introgressive blocks through subsequent hybridization. Here, we use population-level genomic data to reconstruct the phylogenetic history of Betula pubescens (downy birch), a tetraploid species often assumed to be of allopolyploid origin and which is known to hybridize with at least four other birch species. This was achieved by modeling polyploidization and introgression events under the multispecies coalescent and then using an approximate Bayesian computation rejection algorithm to evaluate and compare competing polyploidization models. We provide evidence that B. pubescens is the outcome of an autoploid genome doubling event in the common ancestor of B. pendula and its extant sister species, B. platyphylla, that took place approximately 178,000-188,000 generations ago. Extensive hybridization with B. pendula, B. nana, and B. humilis followed in the aftermath of autopolyploidization, with the relative contribution of each of these species to the B. pubescens genome varying markedly across the species' range. Functional analysis of B. pubescens loci containing alleles introgressed from B. nana identified multiple genes involved in climate adaptation, while loci containing alleles derived from B. humilis revealed several genes involved in the regulation of meiotic stability and pollen viability in plant species.
Subject(s)
Alleles , Betula , Genome, Plant , Phylogeny , Polyploidy , Betula/genetics , Betula/classification , Genetic Introgression , Hybridization, GeneticABSTRACT
Current global climate change is expected to affect biodiversity negatively at all scales leading to mass biodiversity loss. Many studies have shown that the distribution of allele frequencies across a species' range is often influenced by specific genetic loci associated with local environmental variables. This association reflects local adaptation and allele changes at those loci could thereby contribute to the evolutionary response to climate change. However, predicting how species will adapt to climate change from this type of data alone remains challenging. In the present study, we combined exome capture sequences and environmental niche reconstruction, to test multiple methods for assessing local adaptation and climate resilience in two widely distributed conifers, Norway spruce and Siberian spruce. Both species are keystone species of the boreal forest and share a vast hybrid zone. We show that local adaptation in conifers can be detected through allele frequency variation, population-level ecological preferences, and historical niche movement. Moreover, we integrated genetic and ecological information into genetic offset predictive models to show that hybridization plays a central role in expanding the niche breadth of the two conifer species and may help both species to cope better with future changing climates. This joint genetic and ecological analysis also identified spruce populations that are at risk under current climate change.
Subject(s)
Picea , Resilience, Psychological , Tracheophyta , Trees , Taiga , Climate Change , Hybridization, Genetic , Cycadopsida , Picea/geneticsABSTRACT
Anopheles gambiae s.l. has been the target of intense insecticide treatment since the mid-20th century to try and control malaria. A substitution in the ace-1 locus has been rapidly selected for, allowing resistance to organophosphate and carbamate insecticides. Since then, two types of duplication of the ace-1 locus have been found in An. gambiae s.l. populations: homogeneous duplications that are composed of several resistance copies, or heterogeneous duplications that contain both resistance and susceptible copies. The substitution induces a trade-off between resistance in the presence of insecticides and disadvantages in their absence: the heterogeneous duplications allow the fixation of the intermediate heterozygote phenotype. So far, a single heterogeneous duplication has been described in An. gambiae s.l. populations (in contrast with the multiple duplicated alleles found in Culex pipiens mosquitoes). We used a new approach, combining long and short-read sequencing with Sanger sequencing to precisely identify and describe at least nine different heterogeneous duplications, in two populations of An. gambiae s.l. We show that these alleles share the same structure as the previously identified heterogeneous and homogeneous duplications, namely 203-kb tandem amplifications with conserved breakpoints. Our study sheds new light on the origin and maintenance of these alleles in An. gambiae s.l. populations, and their role in mosquito adaptation.
Subject(s)
Anopheles , Culex , Insecticides , Animals , Anopheles/genetics , Insecticides/pharmacology , Insecticide Resistance/genetics , Alleles , Mosquito ControlABSTRACT
New mutations provide the raw material for evolution and adaptation. The distribution of fitness effects (DFE) describes the spectrum of effects of new mutations that can occur along a genome, and is, therefore, of vital interest in evolutionary biology. Recent work has uncovered striking similarities in the DFE between closely related species, prompting us to ask whether there is variation in the DFE among populations of the same species, or among species with different degrees of divergence, that is whether there is variation in the DFE at different levels of evolution. Using exome capture data from six tree species sampled across Europe we characterized the DFE for multiple species, and for each species, multiple populations, and investigated the factors potentially influencing the DFE, such as demography, population divergence, and genetic background. We find statistical support for the presence of variation in the DFE at the species level, even among relatively closely related species. However, we find very little difference at the population level, suggesting that differences in the DFE are primarily driven by deep features of species biology, and those evolutionarily recent events, such as demographic changes and local adaptation, have little impact.
Subject(s)
Genetic Fitness , Models, Genetic , Mutation , Exome , Europe , Evolution, MolecularABSTRACT
Recent studies have highlighted the significant role of copy number variants (CNVs) in phenotypic diversity, environmental adaptation and species divergence across eukaryotes. The presence of CNVs also has the potential to introduce genotyping biases, which can pose challenges to accurate population and quantitative genetic analyses. However, detecting CNVs in genomes, particularly in non-model organisms, presents a formidable challenge. To address this issue, we have developed a statistical framework and an accompanying r software package that leverage allelic-read depth from single nucleotide polymorphism (SNP) data for accurate CNV detection. Our framework capitalises on two key principles. First, it exploits the distribution of allelic-read depth ratios in heterozygotes for individual SNPs by comparing it against an expected distribution based on binomial sampling. Second, it identifies SNPs exhibiting an apparent excess of heterozygotes under Hardy-Weinberg equilibrium. By employing multiple statistical tests, our method not only enhances sensitivity to sampling effects but also effectively addresses reference biases, resulting in optimised SNP classification. Our framework is compatible with various NGS technologies (e.g. RADseq, Exome-capture). This versatility enables CNV calling from genomes of diverse complexities. To streamline the analysis process, we have implemented our framework in the user-friendly r package 'rCNV', which automates the entire workflow seamlessly. We trained our models using simulated data and validated their performance on four datasets derived from different sequencing technologies, including RADseq (Chinook salmon-Oncorhynchus tshawytscha), Rapture (American lobster-Homarus americanus), Exome-capture (Norway spruce-Picea abies) and WGS (Malaria mosquito-Anopheles gambiae).
Subject(s)
DNA Copy Number Variations , Polymorphism, Single Nucleotide , Animals , Software , Exome , Norway , AlgorithmsABSTRACT
Phylogenetic analysis of polyploid hybrid species has long posed a formidable challenge as it requires the ability to distinguish between alleles of different ancestral origins in order to disentangle their individual evolutionary history. This problem has been previously addressed by conceiving phylogenies as reticulate networks, using a two-step phasing strategy that first identifies and segregates homoeologous loci and then, during a second phasing step, assigns each gene copy to one of the subgenomes of an allopolyploid species. Here, we propose an alternative approach, one that preserves the core idea behind phasing-to produce separate nucleotide sequences that capture the reticulate evolutionary history of a polyploid-while vastly simplifying its implementation by reducing a complex multistage procedure to a single phasing step. While most current methods used for phylogenetic reconstruction of polyploid species require sequencing reads to be pre-phased using experimental or computational methods-usually an expensive, complex, and/or time-consuming endeavor-phasing executed using our algorithm is performed directly on the multiple-sequence alignment (MSA), a key change that allows for the simultaneous segregation and sorting of gene copies. We introduce the concept of genomic polarization that, when applied to an allopolyploid species, produces nucleotide sequences that capture the fraction of a polyploid genome that deviates from that of a reference sequence, usually one of the other species present in the MSA. We show that if the reference sequence is one of the parental species, the polarized polyploid sequence has a close resemblance (high pairwise sequence identity) to the second parental species. This knowledge is harnessed to build a new heuristic algorithm where, by replacing the allopolyploid genomic sequence in the MSA by its polarized version, it is possible to identify the phylogenetic position of the polyploid's ancestral parents in an iterative process. The proposed methodology can be used with long-read and short-read high-throughput sequencing data and requires only one representative individual for each species to be included in the phylogenetic analysis. In its current form, it can be used in the analysis of phylogenies containing tetraploid and diploid species. We test the newly developed method extensively using simulated data in order to evaluate its accuracy. We show empirically that the use of polarized genomic sequences allows for the correct identification of both parental species of an allotetraploid with up to 97% certainty in phylogenies with moderate levels of incomplete lineage sorting (ILS) and 87% in phylogenies containing high levels of ILS. We then apply the polarization protocol to reconstruct the reticulate histories of Arabidopsis kamchatica and Arabidopsis suecica, two allopolyploids whose ancestry has been well documented. [Allopolyploidy; Arabidopsis; genomic polarization; homoeologs; incomplete lineage sorting; phasing; polyploid phylogenetics; reticulate evolution.].
Subject(s)
Arabidopsis , Humans , Phylogeny , Polyploidy , Tetraploidy , GenomicsABSTRACT
The current distribution and population structure of many species were, to a large extent, shaped by cycles of isolation in glacial refugia and subsequent population expansions. Isolation in and postglacial expansion through heterogeneous environments led to either neutral or adaptive divergence. Norway spruce is no exception, and its current distribution is the consequence of a constant interplay between evolutionary and demographic processes. We investigated population differentiation and adaptation of Norway spruce for juvenile growth, diameter of the stem, wood density, and tracheid traits at breast height. Data from 4461 phenotyped and genotyped Norway spruce from 396 half-sib families in two progeny tests were used to test for divergent selection in the framework of Q ST vs. F ST. We show that the macroscopic resultant trait (stem diameter), unlike its microscopic components (tracheid dimensions) and juvenile growth, was under divergent selection that predated the Last Glacial Maximum. Altogether, the current variation in these phenotypic traits in Norway spruce is better explained by local adaptation to ancestral environments than to current ones, where populations were partly preadapted, mainly through growth-related traits.
ABSTRACT
Organophosphate and carbamate insecticides have largely been used worldwide to control mosquito populations. As a response, the same amino acid substitution in the ace-1 gene (G119S), conferring resistance to both insecticides, has been selected independently in many mosquito species. In Anopheles gambiae, it has recently been shown that the G119S mutation is actually part of homogeneous duplications that associate multiple resistance copies of the ace-1 gene. In this study, we showed that duplications of resistance copies of the ace-1 gene also exist in the Culex pipiens species complex. The number of copies is variable, and different numbers of copies are associated with different phenotypic trade-offs: we used a combination of bioassays and competition in population cages to show that having more resistance copies conferred higher resistance levels, but was also associated with higher selective disadvantage (or cost) in the absence of insecticide. These results further show the versatility of the genetic architecture of resistance to organophosphate and carbamate insecticides around the ace-1 locus and its role in fine-tuned adaptation to insecticide treatment variations.
Subject(s)
Anopheles , Culex , Insecticides , Animals , Culex/physiology , Insecticides/pharmacology , Insecticides/metabolism , DNA Copy Number Variations , Insecticide Resistance/genetics , Alleles , Anopheles/genetics , Carbamates , Organophosphates/pharmacologyABSTRACT
Vast population movements induced by recurrent climatic cycles have shaped the genetic structure of plant species. During glacial periods species were confined to low-latitude refugia from which they recolonized higher latitudes as the climate improved. This multipronged recolonization led to many lineages that later met and formed large contact zones. We utilize genomic data from 5000 Picea abies trees to test for the presence of natural selection during recolonization and establishment of a contact zone in Scandinavia. Scandinavian P. abies is today made up of a southern genetic cluster originating from the Baltics, and a northern one originating from Northern Russia. The contact zone delineating them closely matches the limit between two major climatic regions. We show that natural selection contributed to its establishment and maintenance. First, an isolation-with-migration model with genome-wide linked selection fits the data better than a purely neutral one. Second, many loci show signatures of selection or are associated with environmental variables. These loci, regrouped in clusters on chromosomes, are often related to phenology. Altogether, our results illustrate how climatic cycles, recolonization and selection can establish strong local adaptation along contact zones and affect the genetic architecture of adaptive traits.
Subject(s)
Abies , Selection, Genetic , Trees , Phenotype , Demography , Genetic VariationABSTRACT
The shift from outcrossing to selfing is one of the main evolutionary transitions in plants. It is accompanied by profound effects on reproductive traits, the so-called selfing syndrome. Because the transition to selfing also implies deep genomic and ecological changes, one also expects to observe a genomic selfing syndrome. We took advantage of the three independent transitions from outcrossing to selfing in the Capsella genus to characterize the overall impact of mating system change on RNA expression, in flowers but also in leaves and roots. We quantified the extent of both selfing and genomic syndromes, and tested whether changes in expression corresponded to adaptation to selfing or to relaxed selection on traits that were constrained in outcrossers. Mating system change affected gene expression in all three tissues but more so in flowers than in roots and leaves. Gene expression in selfing species tended to converge in flowers but diverged in the two other tissues. Hence, convergent adaptation to selfing dominates in flowers, whereas genetic drift plays a more important role in leaves and roots. The effect of mating system transition is not limited to reproductive tissues and corresponds to both adaptation to selfing and relaxed selection on previously constrained traits.
Subject(s)
Capsella , Capsella/genetics , Self-Fertilization , Pollination/genetics , Biological Evolution , Flowers/genetics , Reproduction/genetics , Gene ExpressionABSTRACT
The colonization success of a species depends on the interplay between its phenotypic plasticity, adaptive potential and demographic history. Assessing their relative contributions during the different phases of a species range expansion is challenging, and requires large-scale experiments. Here, we investigated the relative contributions of plasticity, performance and demographic history to the worldwide expansion of the shepherd's purse, Capsella bursa-pastoris. We installed two large common gardens of the shepherd's purse, a young, self-fertilizing, allopolyploid weed with a worldwide distribution. One common garden was located in Europe, the other in Asia. We used accessions from three distinct genetic clusters (Middle East, Europe and Asia) that reflect the demographic history of the species. Several life-history traits were measured. To explain the phenotypic variation between and within genetic clusters, we analysed the effects of (i) the genetic clusters, (ii) the phenotypic plasticity and its association to fitness and (iii) the distance in terms of bioclimatic variables between the sampling site of an accession and the common garden, i.e. the environmental distance. Our experiment showed that (i) the performance of C. bursa-pastoris is closely related to its high phenotypic plasticity; (ii) within a common garden, genetic cluster was a main determinant of phenotypic differences; and (iii) at the scale of the experiment, the effect of environmental distance to the common garden could not be distinguished from that of genetic clusters. Phenotypic plasticity and demographic history both play important role at different stages of range expansion. The success of the worldwide expansion of C. bursa-pastoris was undoubtedly influenced by its strong phenotypic plasticity.
ABSTRACT
Contrasting theories exist regarding how Norway spruce (Picea abies) recolonized Fennoscandia after the last glaciation and both early Holocene establishments from western microrefugia and late Holocene colonization from the east have been postulated. Here, we show that Norway spruce was present in southern Fennoscandia as early as 14.7 ± 0.1 cal. kyr BP and that the millennia-old clonal spruce trees present today in central Sweden likely arrived with an early Holocene migration from the east. Our findings are based on ancient sedimentary DNA from multiple European sites (N = 15) combined with nuclear and mitochondrial DNA analysis of ancient clonal (N = 135) and contemporary spruce forest trees (N = 129) from central Sweden. Our other findings imply that Norway spruce was present shortly after deglaciation at the margins of the Scandinavian Ice Sheet, and support previously disputed finds of pollen in southern Sweden claiming spruce establishment during the Lateglacial.
Subject(s)
Picea , Pinus , DNA, Mitochondrial/genetics , Forests , Norway , Picea/genetics , Trees/geneticsABSTRACT
Rapid human-induced environmental changes like climate warming represent a challenge for forest ecosystems. Due to their biological complexity and the long generation time of their keystone tree species, genetic adaptation in these ecosystems might not be fast enough to keep track with conditions changing at such a fast pace. The study of adaptation to environmental change and its genetic mechanisms is therefore key for ensuring a sustainable support and management of forests. The 4-day conference of the European Research Group EvolTree (https://www.evoltree.eu) on the topic of "Genomics and Adaptation in Forest Ecosystems" brought together over 130 scientists to present and discuss the latest developments and findings in forest evolutionary research. Genomic studies in forest trees have long been hampered by the lack of high-quality genomics resources and affordable genotyping methods. This has dramatically changed in the last few years; the conference impressively showed how such tools are now being applied to study past demography, adaptation and interactions with associated organisms. Moreover, genomic studies are now finally also entering the world of conservation and forest management, for example by measuring the value or cost of interspecific hybridization and introgression, assessing the vulnerability of species and populations to future change, or accurately delineating evolutionary significant units. The newly launched conference series of EvolTree will hopefully play a key role in the exchange and synthesis of such important investigations. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s11295-022-01542-1.
ABSTRACT
Dose-response relationships reflect the effects of a substance on organisms, and are widely used in broad research areas, from medicine and physiology, to vector control and pest management in agronomy. Furthermore, reporting on the response of organisms to stressors is an essential component of many public policies (e.g. public health, environment), and assessment of xenobiotic responses is an integral part of World Health Organization recommendations. Building upon an R script that we previously made available, and considering its popularity, we have now developed a software package in the R environment, BioRssay, to efficiently analyze dose-response relationships. It has more user-friendly functions and more flexibility, and proposes an easy interpretation of the results. The functions in the BioRssay package are built on robust statistical analyses to compare the dose/exposure-response of various bioassays and effectively visualize them in probit-graphs.
Subject(s)
Biological Assay/statistics & numerical data , Biostatistics , Software , Animals , Biostatistics/instrumentation , Biostatistics/methods , Dose-Response Relationship, Drug , Humans , Lethal Dose 50 , Public Health/statistics & numerical dataABSTRACT
Trees must cope with the attack of multiple pathogens, often simultaneously during their long lifespan. Ironically, the genetic and molecular mechanisms controlling this process are poorly understood. The objective of this study was to compare the genetic component of resistance in Norway spruce to Heterobasidion annosum s.s. and its sympatric congener Heterobasidion parviporum. Heterobasidion root- and stem-rot is a major disease of Norway spruce caused by members of the Heterobasidion annosum species complex. Resistance to both pathogens was measured using artificial inoculations in half-sib families of Norway spruce trees originating from central to northern Europe. The genetic component of resistance was analysed using 63,760 genome-wide exome-capture sequenced SNPs and multitrait genome-wide associations. No correlation was found for resistance to the two pathogens; however, associations were found between genomic variants and resistance traits with synergic or antagonist pleiotropic effects to both pathogens. Additionally, a latitudinal cline in resistance in the bark to H. annosum s.s. was found; trees from southern latitudes, with a later bud-set and thicker stem diameter, allowed longer lesions, but this was not the case for H. parviporum. In summary, this study detects genomic variants with pleiotropic effects which explain multiple disease resistance from a genic level and could be useful for selection of resistant trees to both pathogens. Furthermore, it highlights the need for additional research to understand the evolution of resistance traits to multiple pathogens in trees.
Subject(s)
Basidiomycota , Picea , Basidiomycota/genetics , Genomics , Norway , Picea/genetics , Plant Diseases/geneticsABSTRACT
BACKGROUND: Genome-wide association studies (GWAS) identify loci underlying the variation of complex traits. One of the main limitations of GWAS is the availability of reliable phenotypic data, particularly for long-lived tree species. Although an extensive amount of phenotypic data already exists in breeding programs, accounting for its high heterogeneity is a great challenge. We combine spatial and factor-analytics analyses to standardize the heterogeneous data from 120 field experiments of 483,424 progenies of Norway spruce to implement the largest reported GWAS for trees using 134 605 SNPs from exome sequencing of 5056 parental trees. RESULTS: We identify 55 novel quantitative trait loci (QTLs) that are associated with phenotypic variation. The largest number of QTLs is associated with the budburst stage, followed by diameter at breast height, wood quality, and frost damage. Two QTLs with the largest effect have a pleiotropic effect for budburst stage, frost damage, and diameter and are associated with MAP3K genes. Genotype data called from exome capture, recently developed SNP array and gene expression data indirectly support this discovery. CONCLUSION: Several important QTLs associated with growth and frost damage have been verified in several southern and northern progeny plantations, indicating that these loci can be used in QTL-assisted genomic selection. Our study also demonstrates that existing heterogeneous phenotypic data from breeding programs, collected over several decades, is an important source for GWAS and that such integration into GWAS should be a major area of inquiry in the future.
Subject(s)
Genome, Plant , Picea/genetics , Plant Proteins/genetics , Protein Serine-Threonine Kinases/genetics , Quantitative Trait Loci , Gene Expression Profiling , Gene Expression Regulation, Plant , Genetic Variation , Genome-Wide Association Study , Genotype , Multigene Family , Phenotype , Plant Breeding/methods , Plant Dispersal/physiology , Plant Proteins/classification , Plant Proteins/metabolism , Protein Serine-Threonine Kinases/classification , Protein Serine-Threonine Kinases/metabolism , Selection, GeneticABSTRACT
The outcome of species range expansion depends on the interplay of demographic, environmental and genetic factors. Self-fertilizing species usually show a higher invasive ability than outcrossers but selfing and bottlenecks during colonization also lead to an increased genetic load. The relationship between genomic and phenotypic characteristics of expanding populations has, hitherto, rarely been tested experimentally. We analysed how accessions of the shepherd's purse, Capsella bursa-pastoris, from the colonization front or from the core of the natural range performed under increasing density of competitors. First, accessions from the front showed a lower fitness than those from the core. Second, for all accessions, competitor density impacted negatively both vegetative growth and fruit production. However, despite their higher genetic load and lower absolute performances, accessions from the front were less affected by competition than accessions from the core. This seems to be due to phenotypic trade-offs and a shift in phenology that allow accessions from the front to avoid competition.