Adaptive Variation Research Articles

Repeatability of adaptation in sunflowers reveals that genomic regions harbouring inversions also drive adaptation in species lacking an inversion

Local adaptation commonly involves alleles of large effect, which experience fitness advantages when in positive linkage disequilibrium (LD). Because segregating inversions suppress recombination and facilitate the maintenance of LD between locally adapted loci, they are also commonly found to be associated with adaptive divergence. However, it is unclear what fraction of an adaptive response can be attributed to inversions and alleles of large effect, and whether the loci within an inversion could still drive adaptation in the absence of its recombination-suppressing effect. Here, we use genome-wide association studies to explore patterns of local adaptation in three species of sunflower: Helianthus annuus, Helianthus argophyllus, and Helianthus petiolaris, which each harbour a large number of species-specific inversions. We find evidence of significant genome-wide repeatability in signatures of association to phenotypes and environments, which are particularly enriched within regions of the genome harbouring an inversion in one species. This shows that while inversions may facilitate local adaptation, at least some of the loci can still harbour mutations that make substantial contributions without the benefit of recombination suppression in species lacking a segregating inversion. While a large number of genomic regions show evidence of repeated adaptation, most of the strongest signatures of association still tend to be species-specific, indicating substantial genotypic redundancy for local adaptation in these species.

Repeatability of adaptation in sunflowers reveals that genomic regions harbouring inversions also drive adaptation in species lacking an inversion

Local adaptation commonly involves alleles of large effect, which experience fitness advantages when in positive linkage disequilibrium (LD). Because segregating inversions suppress recombination and facilitate the maintenance of LD between locally adapted loci, they are also commonly found to be associated with adaptive divergence. However, it is unclear what fraction of an adaptive response can be attributed to inversions and alleles of large effect, and whether the loci within an inversion could still drive adaptation in the absence of its recombination-suppressing effect. Here, we use genome-wide association studies to explore patterns of local adaptation in three species of sunflower: Helianthus annuus, Helianthus argophyllus, and Helianthus petiolaris, which each harbour a large number of species-specific inversions. We find evidence of significant genome-wide repeatability in signatures of association to phenotypes and environments, which are particularly enriched within regions of the genome harbouring an inversion in one species. This shows that while inversions may facilitate local adaptation, at least some of the loci can still harbour mutations that make substantial contributions without the benefit of recombination suppression in species lacking a segregating inversion. While a large number of genomic regions show evidence of repeated adaptation, most of the strongest signatures of association still tend to be species-specific, indicating substantial genotypic redundancy for local adaptation in these species.

Adaptive Variable-Damping Impedance Control for Unknown Interaction Environment

Aiming at the force-tracking error phenomenon of impedance control in an unknown surface environment, an adaptive variable-damping impedance control algorithm is proposed, and the stability and convergence of the algorithm are deduced. An adaptive-law selection rule is proposed to aim at the phenomenon that the adaptive parameters are too large to cause the system oscillation and overshoot and too small to cause the adaptive line variation in the curved surface environment. Finally, experiments conclude that the impedance control based on the adaptive variable-damping algorithm has a better force-tracking effect than the ordinary impedance control in the curved surface environment where the contact surface between the end-effector of the manipulator and the atmosphere is unknown.

Neighbouring Scots pine populations from contrasting climatic regions show substantial variability but consistent response to warming

Natural tree populations consist of individuals that exhibit intraspecific adaptive variation at a range of geographic scales, as a result of the balance between gene flow and selection. The spatial distribution and magnitude of such variation will influence the capacity of populations to adapt to forthcoming changing environmental conditions. The native Scots pine populations in Scotland represent what remains of the iconic Caledonian forest. Despite being distributed within a relatively narrow geographic area these populations occur across a steep East-West environmental gradient of increasing rainfall and temperature. We hypothesised that western populations compared to those from the east may be better adapted to warmer conditions and as a consequence, may respond differently to the increased temperature predicted during climate change. We conducted an experiment lasting 22 weeks in controlled environment chambers using a nested hierarchical design based on material from different regions (west or east), populations and families (half sibs). We examined the effects of two temperature scenarios, current temperature and warmer predicted temperature on percentage germination as well as growth and morphology of above and below-ground traits. Most of the variation occurred at the family level. Nevertheless, significant regional and population differences were detected, where eastern populations invested more in roots, exhibited fewer stomatal rows per needle and produced thinner roots. In addition, warmer temperatures had strong effects on early growth that were consistent in material from both regions and resulted in earlier germination, greater growth and biomass, but these effects were not accompanied by shifts in biomass partitioning. Although the strong effect of warming suggested temperature limitation for early growth in the study areas under current conditions our results did not support the idea that low seedling recruitment resulting from poor emergence and early growth would lead to a decline in Scottish populations of Scots pine under a warmer climate. Our results are informative regarding the adaptive potential in the populations and will contribute to the development of appropriate forest conservation strategies.

The Population Divergence and Genetic Basis of Local Adaptation of Wild Soybean (Glycine soja) in China.

Glycine soja is the wild relative species of cultivated soybean. In this study, we investigated the population divergence and genetic basis of the local adaptation of wild soybean in China using genome-wide single-nucleotide polymorphisms (SNPs) of a population of 72 G. soja accessions. Using phylogenetic analysis, we observed that G. soja accessions clustered into three distinct groups, each corresponding to a specific geographic region, the northeastern region (NER), central region (CR), and southern region (SR), consistent with previous studies. Notably, we found a significant positive correlation between genetic and geographic distances. Further population structure analysis revealed each group was associated with an ancestral population and a specific geographic area. By utilizing the genome sequencing data of accessions from 16 different locations, we inferred the population history of these wild soybean groups. Our results indicate that the three groups diverged ~25,000 years ago, coinciding with the time of the last glacial maximum. The effective population size of the SR group expanded first, and subsequently, the NER and CR groups expanded approximately 5000 and 2500 years ago, respectively. Moreover, 83, 104, and 101 significant associated loci (SALs) were identified using genome-wide association analysis for annual mean temperature, annual precipitation, and latitude, respectively. Functional analysis of genes located in SALs highlighted candidate genes related to local adaptation. This study highlights the significant role of geographic isolation and environmental factors in shaping the genetic structure and adaptability of wild soybean populations. Furthermore, it emphasizes the value of wild soybean as a crucial genetic resource for enhancing the adaptability of cultivated soybeans, which have experienced a loss of genetic diversity due to domestication and intensive breeding practices. The insights gained from our research provide valuable information for the protection, conservation, and utilization of this important genetic resource.

Projection of current and future distribution of adaptive genetic units in an alpine ungulate.

Climate projections predict major changes in alpine environments by the end of the 21st century. To avoid climate-induced maladaptation and extinction, many animal populations will either need to move to more suitable habitats or adapt in situ to novel conditions. Since populations of a species exhibit genetic variation related to local adaptation, it is important to incorporate this variation into predictive models to help assess the ability of the species to survive climate change. Here, we evaluate how the adaptive genetic variation of a mountain ungulate-the Northern chamois (Rupicapra rupicapra)-could be impacted by future global warming. Based on genotype-environment association analyses of 429 chamois using a ddRAD sequencing approach, we identified genetic variation associated with climatic gradients across the European Alps. We then delineated adaptive genetic units and projected the optimal distribution of these adaptive groups in the future. Our results suggest the presence of local adaptation to climate in Northern chamois with similar genetic adaptive responses in geographically distant but climatically similar populations. Furthermore, our results predict that future climatic changes will modify the Northern chamois adaptive landscape considerably, with various degrees of maladaptation risk.

Gene expression and alternative splicing contribute to adaptive divergence of ecotypes.

Regulation of gene expression is a critical link between genotype and phenotype explaining substantial heritable variation within species. However, we are only beginning to understand the ways that specific gene regulatory mechanisms contribute to adaptive divergence of populations. In plants, the post-transcriptional regulatory mechanism of alternative splicing (AS) plays an important role in both development and abiotic stress response, making it a compelling potential target of natural selection. AS allows organisms to generate multiple different transcripts/proteins from a single gene and thus may provide a source of evolutionary novelty. Here, we examine whether variation in alternative splicing and gene expression levels might contribute to adaptation and incipient speciation of dune-adapted prairie sunflowers in Great Sand Dunes National Park, Colorado, USA. We conducted a common garden experiment to assess transcriptomic variation among ecotypes and analyzed differential expression, differential splicing, and gene coexpression. We show that individual genes are strongly differentiated for both transcript level and alternative isoform proportions, even when grown in a common environment, and that gene coexpression networks are disrupted between ecotypes. Furthermore, we examined how genome-wide patterns of sequence divergence correspond to divergence in transcript levels and isoform proportions and find evidence for both cis and trans-regulation. Together, our results emphasize that alternative splicing has been an underappreciated mechanism providing source material for natural selection at short evolutionary time scales.

The Sensory Ecology of Speciation.

In this work, we explore the potential influence of sensory ecology on speciation, including but not limited to the concept of sensory drive, which concerns the coevolution of signals and sensory systems with the local environment. The sensory environment can influence individual fitness in a variety of ways, thereby affecting the evolution of both pre- and postmating reproductive isolation. Previous work focused on sensory drive has undoubtedly advanced the field, but we argue that it may have also narrowed our understanding of the broader influence of the sensory ecology on speciation. Moreover, the clearest examples of sensory drive are largely limited to aquatic organisms, which may skew the influence of contributing factors. We review the evidence for sensory drive across environmental conditions, and in this context discuss the importance of more generalized effects of sensory ecology on adaptive behavioral divergence. Finally, we consider the potential of rapid environmental change to influence reproductive barriers related to sensory ecologies. Our synthesis shows the importance of sensory conditions for local adaptation and divergence in a range of behavioral contexts and extends our understanding of the interplay between sensory ecology and speciation.

Genetic modification of a Hox locus drives mimetic color pattern variation in a highly polymorphic bumble bee.

Müllerian mimicry provides natural replicates ideal for exploring mechanisms underlying adaptive phenotypic divergence and convergence, yet the genetic mechanisms underlying mimetic variation remains largely unknown. The current study investigates the genetic basis of mimetic color pattern variation in a highly polymorphic bumble bee, Bombus breviceps (Hymenoptera, Apidae). In South Asia, this species and multiple comimetic species converge onto local Müllerian mimicry patterns by shifting the abdominal setal color from orange to black. Genetic crossing between the orange and black phenotypes suggested the color dimorphism being controlled by a single Mendelian locus, with the orange allele being dominant over black. Genome-wide association suggests that a locus at the intergenic region between two abdominal fate-determining Hox genes, abd-A and Abd-B is associated with the color change. This locus is therefore in the same intergenic region but not the same exact locus as found to drive red-black mid-abdominal variation in a distantly related bumble bee species, B. melanopygus. Gene expression analysis and RNA interferences suggest that differential expression of an intergenic long non-coding RNA between abd-A and Abd-B at the onset setal color differentiation may drive the orange black color variation by causing a homeotic shift late in development. Analysis of this same color locus in comimetic species reveals no sequence association with the same color shift, suggesting that mimetic convergence is achieved through distinct genetic routes. Our study establishes Hox regions as genomic hotspots for color pattern evolution in bumble bees, and demonstrates how pleiotropic developmental loci can drive adaptive radiations in nature.

Adaptive Variant of the Frank–Wolfe Algorithm for Convex Optimization Problems

Adaptive Variant of the Frank–Wolfe Algorithm for Convex Optimization Problems

Study of the Genetic Adaptation Mechanisms of Siberian Larch (Larix sibirica Ledeb.) Regarding Climatic Stresses Based on Dendrogenomic Analysis

Dendrogenomics is a new interdisciplinary approach that allows joint analysis of dendrological and genomic data and opens up new ways to study the temporal dynamics of forest treelines, delineate spatial and temporal population structures, decipher individual tree responses to abiotic and biotic stresses, and evaluate the adaptive genetic potential of forest tree populations. These data are needed for the prediction of climate change effects and mitigation of the negative effects. We present here an association analysis of the variation of 27 individual tree traits, including adaptive dendrophenotypes reflecting the individual responses of trees to drought stress, such as the resistance (Rt), recovery (Rc), resilience (Rs), and relative resilience (RRs) indexes measured in 136 Siberian larch trees in 5 populations in the foothills of the Batenevsky Ridge (Kuznetsk Alatau, Republic of Khakassia, Russia), with variation of 9742 SNPs genotyped using ddRADseq in the same trees. The population structure of five closely located Siberian larch populations was relatively weak (FST = 0.018). We found that the level of individual heterozygosity positively correlated with the Rc and RR indices for the five studied drought periods and partly with the Rs indices for three drought periods. It seems that higher individual heterozygosity improves the adaptive capabilities of the tree. We also discovered a significant negative relationship between individual heterozygosity and the Rt index in four out of five periods, which means that growth slows down during droughts more in trees with higher individual heterozygosity and is likely associated with energy and internal resource reallocation toward more efficient water and energy usage and optimization of larch growth during drought years. We found 371 SNPs with potentially adaptive variations significantly associated with the variation of adaptive dendrophenotypes based on all three different methods of association analysis. Among them, 26 SNPs were located in genomic regions carrying functional genes: 21 in intergenic regions and 5 in gene-coding regions. Based on the obtained results, it can be assumed that these populations of Siberian larch have relatively high standing adaptive genetic variation and adaptive potential underlying the adaptations of larch to various climatic conditions.

Local adaptation and future climate vulnerability in a wild rodent

As climate change continues, species pushed outside their physiological tolerance limits must adapt or face extinction. When change is rapid, adaptation will largely harness ancestral variation, making the availability and characteristics of that variation of critical importance. Here, we used whole-genome sequencing and genetic-environment association analyses to identify adaptive variation and its significance in the context of future climates in a small Palearctic mammal, the bank vole (Clethrionomys glareolus). We found that peripheral populations of bank vole in Britain are already at the extreme bounds of potential genetic adaptation and may require an influx of adaptive variation in order to respond. Analyses of adaptive loci suggest regional differences in climate variables select for variants that influence patterns of population adaptive resilience, including genes associated with antioxidant defense, and support a pattern of thermal/hypoxic cross-adaptation. Our findings indicate that understanding potential shifts in genomic composition in response to climate change may be key to predicting species’ fate under future climates.

Inferring multi-locus selection in admixed populations.

Admixture, the exchange of genetic information between distinct source populations, is thought to be a major source of adaptive genetic variation. Unlike mutation events, which periodically generate single alleles, admixture can introduce many selected alleles simultaneously. As such, the effects of linkage between selected alleles may be especially pronounced in admixed populations. However, existing tools for identifying selected mutations within admixed populations only account for selection at a single site, overlooking phenomena such as linkage among proximal selected alleles. Here, we develop and extensively validate a method for identifying and quantifying the individual effects of multiple linked selected sites on a chromosome in admixed populations. Our approach numerically calculates the expected local ancestry landscape in an admixed population for a given multi-locus selection model, and then maximizes the likelihood of the model. After applying this method to admixed populations of Drosophila melanogaster and Passer italiae, we found that the impacts between linked sites may be an important contributor to natural selection in admixed populations. Furthermore, for the situations we considered, the selection coefficients and number of selected sites are overestimated in analyses that do not consider the effects of linkage among selected sites. Our results imply that linkage among selected sites may be an important evolutionary force in admixed populations. This tool provides a powerful generalized method to investigate these crucial phenomena in diverse populations.

Global genetic diversity, introgression, and evolutionary adaptation of indicine cattle revealed by whole genome sequencing

Indicine cattle, also referred to as zebu (Bos taurus indicus), play a central role in pastoral communities across a wide range of agro-ecosystems, from extremely hot semiarid regions to hot humid tropical regions. However, their adaptive genetic changes following their dispersal into East Asia from the Indian subcontinent have remained poorly documented. Here, we characterize their global genetic diversity using high-quality whole-genome sequencing data from 354 indicine cattle of 57 breeds/populations, including major indicine phylogeographic groups worldwide. We reveal their probable migration into East Asia was along a coastal route rather than inland routes and we detected introgression from other bovine species. Genomic regions carrying morphology-, immune-, and heat-tolerance-related genes underwent divergent selection according to Asian agro-ecologies. We identify distinct sets of loci that contain promising candidate variants for adaptation to hot semi-arid and hot humid tropical ecosystems. Our results indicate that the rapid and successful adaptation of East Asian indicine cattle to hot humid environments was promoted by localized introgression from banteng and/or gaur. Our findings provide insights into the history and environmental adaptation of indicine cattle.

Genomics-informed conservation units reveal spatial variation in climate vulnerability in a migratory bird.

Identifying genetic conservation units (CUs) in threatened species is critical for the preservation of adaptive capacity and evolutionary potential in the face of climate change. However, delineating CUs in highly mobile species remains a challenge due to high rates of gene flow and genetic signatures of isolation by distance. Even when CUs are delineated in highly mobile species, the CUs often lack key biological information about what populations have the most conservation need to guide management decisions. Here we implement a framework for CU identification in the Canada Warbler (Cardellina canadensis), a migratory bird species of conservation concern, and then integrate demographic modelling and genomic offset to guide conservation decisions. We find that patterns of whole genome genetic variation in this highly mobile species are primarily driven by putative adaptive variation. Identification of CUs across the breeding range revealed that Canada Warblers fall into two evolutionarily significant units (ESU), and three putative adaptive units (AUs) in the South, East, and Northwest. Quantification of genomic offset, a metric of genetic changes necessary to maintain current gene-environment relationships, revealed significant spatial variation in climate vulnerability, with the Northwestern AU being identified as the most vulnerable to future climate change. Alternatively, quantification of past population trends within each AU revealed the steepest population declines have occurred within the Eastern AU. Overall, we illustrate that genomics-informed CUs provide a strong foundation for identifying current and future regional threats that can be used to inform management strategies for a highly mobile species in a rapidly changing world.

Genomic Basis of Freshwater Adaptation in the Palaemonid Prawn GenusMacrobrachium: Convergent Evolution Following Multiple Independent Colonization Events.

Adaptation to different salinity environments can enhance morphological and genomic divergence between related aquatic taxa. Species of prawns in the genus Macrobrachium naturally inhabit different osmotic niches and possess distinctive lifecycle traits associated with salinity tolerance. This study was conducted to investigate the patterns of adaptive genomic divergence during freshwater colonization in 34 Macrobrachium species collected from four continents; Australia, Asia, North and South America. Genotyping-by-sequencing (GBS) technique identified 5018 loci containing 82,636 single nucleotide polymorphisms (SNPs) that were used to reconstruct a phylogenomic tree. An additional phylogeny was reconstructed based on 43 candidate genes, previously identified as being potentially associated with freshwater adaptation. Comparison of the two phylogenetic trees revealed contrasting topologies. The GBS tree indicated multiple independent continent-specific invasions into freshwater by Macrobrachium lineages following common marine ancestry, as species with abbreviated larval development (ALD), i.e., species having a full freshwater life history, appeared reciprocally monophyletic within each continent. In contrast, the candidate gene tree showed convergent evolution for all ALD species worldwide, forming a single, well-supported clade. This latter pattern is likely the result of common evolutionary pressures selecting key mutations favored in continental freshwater habitats Results suggest that following multiple independent invasions into continental freshwaters at different evolutionary timescales, Macrobrachium taxa experienced adaptive genomic divergence, and in particular, convergence in the same genomic regions with parallel shifts in specific conserved phenotypic traits, such as evolution of larger eggs with abbreviated larval developmental.

Divergent selection in a Mediterranean pine on local spatial scales

Abstract The effects of selection on an organism's genome are hard to detect on small spatial scales, as gene flow can swamp signatures of local adaptation. Therefore, most genome scans to detect signatures of environmental selection are performed on large spatial scales; however, divergent selection on the local scale (e.g. between contrasting soil conditions) has also been demonstrated, in particular for herbaceous plants. Here, we hypothesised that in topographically complex landscapes, microenvironment variability is strong enough to leave a selective footprint in the genomes of long‐lived organisms. To test this, we investigated paired south‐ versus north‐facing Pinus pinaster stands on the local scale, with trees growing in close vicinity (≤820 m distance between paired south‐ and north‐facing stands), in a Mediterranean mountain area. While trees on north‐facing slopes experience less radiation, trees on south‐facing slopes suffer from especially harsh conditions, particularly during the dry summer season. Two outlier analyses consistently revealed five putatively adaptive loci (out of 4034), in candidate genes two of which encoded non‐synonymous substitutions. Additionally, one locus showed consistent allele frequency differences in all three stand pairs indicating divergent selection despite high gene flow on the local scale. Permutation tests demonstrated that our findings were robust. Functional annotation of these candidate genes revealed biological functions related to abiotic stress response, such as water availability, in other plant species. Synthesis. Our study highlights how divergent selection in heterogeneous microenvironments shapes and maintains the functional genetic variation within populations of long‐lived forest tree species, being the first to focus on adaptive genetic divergence between south‐ and north‐facing slopes within continuous forest stands. This is especially relevant in the current context of climate change, as this variation is at the base of plant population responses to future climate.

Within- and between-population comparisons suggest independently acting selection maintaining parallel clines in Scots pine (Pinus sylvestris).

Parallel clines in traits related to adaptation in a species can be due to independent selection on a pair of traits, or due to selection in one trait resulting in a parallel cline in a correlated trait. To distinguish between the mechanisms giving rise to parallel adaptive population divergence of multiple traits along an environmental gradient we need to study variation, correlations, and selective forces within individual populations along the gradient. In many tree species, budset timing (BST) forms a latitudinal cline, and parallel clinal variation is also found in other seedling traits, such as first-year height (FYH) and fall frost injury (FFI). In this study, we set up a common garden experiment with open pollinated progeny from natural populations of Scots pine (Pinus sylvestris), with one large sample from single population (500 families) and smaller samples from across a latitudinal gradient. BST, FYH and induced FFI were first measured in a greenhouse. The seedlings were then planted in the field, where survival and height were measured at the age of 9 years as fitness proxies. We compared between- and within-population variation and genetic correlations of these three seedling traits, and estimated selection gradients at the family level in our main population, taking into account the potential effects of seed weight. Between-population genetic correlations between seedling traits were high (0.76-0.95). Within-population genetic correlations in the main population were lower (0.14-0.35), as in other populations (0.10-0.39). Within population, extensive adaptive variation persists in the seedling traits, in line with rather weak selection gradients, yet maintaining the clines. Although our sampling does not cover the whole cline equally, the results suggest that the individual clines in these traits are maintained by largely independently acting selection, which results in fewer constraints in adaptation under changing climate.

Habitat fragmentation affects climate adaptation in a forest herb

Abstract Climate change and the resulting increased drought frequencies pose considerable threats to forest herb populations, particularly where additional environmental challenges jeopardize responses to selection. Specifically, habitat fragmentation may hamper climate adaptation by altering the distribution of adaptive genetic variation and may also induce evolutionary changes in mating systems. To assess how habitat fragmentation disrupts climate adaptation, we conducted a common garden experiment with Primula elatior offspring originating from 24 populations sampled along a latitudinal gradient with varying climate and landscape characteristics. We then quantified a range of vegetative, regulatory and reproductive traits under distinct soil moisture regimes to evaluate imprints of local adaptation and phenotypic plasticity. Additionally, we conducted a more extensive field campaign in 60 populations along the same latitudinal gradient to evaluate the potential evolutionary breakdown of reciprocal herkogamy. For large, connected populations, our results demonstrated an evolutionary shift from a strategy in southern populations that seems aligned with drought avoidance—where plants minimize their exposure to dry conditions and optimize photosynthesis—to a drought tolerance strategy in northern populations, where plants are adapted to function despite water scarcity. However, habitat fragmentation disrupted climate clines and the adaptive responses to drought stress in key traits related to growth, biomass allocation and water regulation. Additionally, our findings indicate the onset of evolutionary breakdown in reciprocal herkogamy and divergence in other key flower traits. The disruption of climate clines, drought responses and adaptations in mating systems contributed to a substantially diminished flowering investment across the distribution range, with the most pronounced effects observed in southern fragmented populations. Synthesis. We present novel empirical evidence of how habitat fragmentation disrupts climate adaptation and drought tolerance in a wide range of traits along the range of the forest herb Primula elatior. These findings emphasize the need to account for habitat fragmentation while designing effective conservation strategies in order to preserve and restore resilient meta‐populations of forest herbs amidst ongoing global changes.

Genomes of an endangered rattlesnake show that neutral genetic variation predicts adaptive genetic variation and genetic load.

Genomes of an endangered rattlesnake show that neutral genetic variation predicts adaptive genetic variation and genetic load.