Introduction to general discussion. Evolution of adaptation by natural selection.
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Ferns are the second most diverse vascular plant lineage after angiosperms and have been a key ecological component of Earth's biodiversity for more than 380 million years. Importantly, ferns are sister to seed plants, providing a critical outgroup for understanding the evolution of seed plant features. Ferns are remarkably resilient to abiotic and biotic stresses due to a long evolutionary history with adaptations to diverse habitats, stresses, and herbivores. As a result, ferns produce a multitude of secondary metabolites with unique bioactivities; these chemicals are potentially linked to the adaptation of ferns to herbivory, various abiotic and biotic stresses, and changing environments. Assembled reference genomes and the identification of key metabolic compounds of multiple ferns have already made significant contributions to human health and well-being. Here, we review the recent scientific advances in fern research, including evolution, stress resistance, metabolites and medicinal utilization, and comparative multi-omics applications. We propose that integrated investigations involving ecological, physiological, and molecular techniques will facilitate the future research translation of fern resources in diverse areas including soil remediation, biopesticides, and medicine. Advances in our understanding of fern molecular biology will provide new insights into the evolution of land plants and promote the utilization of ferns for heightened environmental restoration, crop protection and human health.
Lygodactylus geckos represent a well-documented radiation of miniaturized lizards with diverse life-history traits that are widely distributed in Africa, Madagascar, and South America. The group has diversified into numerous species with high levels of morphological similarity. The evolutionary processes underlying such diversification remain enigmatic, because species live in different ecological biomes, ecoregions and microhabitats, while suggesting strikingly high levels of homoplasy. To underscore this evolutionary pattern, here we explore the shape variation of skull elements (i.e., cranium, jaw and inner ear) using 3D geometric morphometrics and phylogenetic comparative methods on computed tomography scans (CT-scan) of a sample encompassing almost all recognized taxa within Lygodactylus. The results of this work show that skull and inner ear shape variation is low (i.e., there is high overlapping on the morphospace) across geographic regions, macrohabitats and lifestyles, implying extensive homoplasy. Furthermore, we also found a strong influence of allometry shaping cranial variation both at intra and interspecific levels, suggesting a major constraint underlying skull architecture, probably as a consequence of its miniaturization. The remaining variation that is not allometric is independent of phylogeny and ecological adaptation and can probably be interpreted as the result of intrinsic developmental plasticity. This, in turn, supports the interpretation that speciation in this group is largely concordant with a non-adaptive hypothesis, which results mainly from vicariant processes.
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Second-generation (2G) bioethanol from lignocellulosic feedstocks is a sustainable alternative to fossil fuels. However, its production is constrained by the poor performance of industrial microbes in hydrolysates that are generated during biomass pretreatment. Scheffersomyces stipitis is a native xylose fermenting yeast and a promising platform for 2G bioethanol production, and adaptive evolution under hydrolysate stress has yielded strains with enhanced performance. However, the chromosomal basis of this adaptation is unknown. Here, we demonstrate that chromosome scale structural variation, rather than point mutations, underlies the improved phenotype of the evolved strains. By integrating long- and short-read genome sequencing, we identify two major chromosomal rearrangements in the top performing isolate: a reciprocal translocation between chromosomes 1 and 2 that disrupts the NUDIX hydrolase gene YSA1, and the formation of a mitotically stable 175 kb minichromosome derived from chromosome 5. Functional analyses show that disruption of YSA1 enhances xylose utilisation and ethanol yield, while the minichromosome contributes to improved performance in hydrolysate conditions. These findings provide direct evidence that balanced rearrangements and minichromosome formation can be selected during prolonged stress and can generate adaptive phenotypes. Taken together, our study establishes genome reorganisation as a key driver of adaptation in S. stipitis.
Rapid adaptive evolution can increase the competitive ability of invasive species in their non-native ranges. However, whether this increase is a general response and what drives it remain uncertain because the evidence is largely based on studies with limited sampling, inadequate consideration of population co-ancestry, and oversimplified estimates of competitive ability. We conduct a large-scale glasshouse experiment testing the effects of competition and drought on 100 native and 165 non-native populations of Erigeron canadensis, all genotyped to account for co-ancestry. Plants from non-native populations are significantly more competitive against other species than the conspecifics from native populations under both mesic and dry conditions. Genetic clustering indicates that the rapid evolution of competitive ability occurs independently in two out of four clusters in the non-native range. This advantage is present only during interspecific interactions and is absent during intraspecific competition. Repeated evolution of increased competitive ability suggests that adaptation following introduction can reshape species interactions and promote invasion success, even under future drought conditions, highlighting the importance of rapid evolution in determining the ecological impacts of invasive plants.
Understanding adaptive evolution and survival risks in understory herbs is crucial for the effective conservation of biodiversity. How environmental gradients shape species local adaptation patterns is not well understood, nor is how populations of understory herbs respond to a changing climate. In this study, we conducted population genomic analyses of Adenocaulon himalaicum (Asteraceae) with a pan-East Asian distribution, representing a good model for dominant understory herbs to elucidate adaptation mechanisms in heterogeneous forest ecosystems. Based on 34,398 putatively neutral single nucleotide polymorphisms (SNPs) across 27 populations, we identified three genetic lineages accompanied by high levels of genetic differentiation between populations. Our isolation by environment results (IBE) indicated a significant effect of environmental gradients on genomic variation of A. himalaicum (r = 0.18, p = 0.03). To decompose the relative contributions of climate, geography and population structure in explaining genetic variance, our partial RDA found that the prominent contribution of environmental effects (climatic and soil variables) explained 29% and 36% of the neutral and adaptive genetic variation, respectively. Using two genotype-environment association (GEA) methods, we identified 13 SNPs as candidates for core climate-related adaptation loci, with two of these loci further validated by qRT-PCR experiments. Projections of spatiotemporal genomic vulnerability under different future climate scenarios revealed that populations in the southeastern edge of the Himalayas, near the Sichuan Basin, the southernmost region of Northeast China and the northern Korean Peninsula, as well as northern Japan, were identified as the most vulnerable and should be prioritised for conservation. Therefore, our current study provides the genomic foundations for conservation and management strategies to elucidate how these understory herbs cope with future climate changes.
The olfactory receptor (OR) gene represent a significant multigene family in vertebrates, forming the core molecular basis of olfactory perception and playing a crucial role in the environmental adaptation of species. High-altitude ecosystems represent extreme habitats characterized by specific abiotic stresses, including low oxygen levels, low temperatures, and intense ultraviolet radiation. These environments also exhibit low aquatic biodiversity and a limited variety of odor molecules, factors that have influenced the adaptive evolution of the sensory systems in endemic species. However, the genetic mechanisms underlying olfactory adaptation in high-altitude freshwater fish remained inadequately understood. In this study, we performed comparative genomics analyses to reveal the evolutionary processes underlying the adaptive and functional evolution of OR genes in S. younghusbandi, a cyprinid fish endemic to the Qinghai-Xizang Plateau. The results indicated that, compared to their low-altitude relatives, S. younghusbandi possessed a significantly smaller number of OR genes, with only 98 genes, which revealed the contraction of the gene family. Phylogenetic analysis revealed that the OR genes of cyprinid fish could be categorized into two major lineages: type I and type II. The η and δ families, which perceive water-soluble odors, in S. younghusbandi underwent significant and specific expansion, while the ε family was completely absent. This pattern reflected adaptive changes in olfactory recognition to accommodate the simplified odor spectrum of high-altitude water bodies. Chromosomal localization analysis demonstrated that OR genes were clustered, and collinearity analysis confirmed the presence of conserved genomic fragments among species. Selection pressure analysis revealed that the Ka/Ks values of all homologous gene pairs were less than 1, indicating that the OR genes of S. younghusbandi underwent strong purifying selection as a group to preserve core olfactory function. A few genes exhibited relaxed selection characteristics, which may have facilitated the fine-tuning of adaptability to high-altitude environments. In conclusion, this study elucidated the evolutionary dynamics and adaptive characteristics of the OR gene in S. younghusbandi, offering a new perspective on the molecular mechanisms underlying olfactory adaptation at high altitudes and enriching the research on sensory evolution in vertebrates.
Experimental evolution is widely used to infer microbial responses to environmental change, yet most laboratory studies impose constant, well-mixed conditions that differ fundamentally from fluctuating, spatially structured field environments. We compared genomic evolution in the leaf litter-associated bacterium Curtobacterium strain MMLR14_002 under control and warming treatments in laboratory culture and in a complementary field experiment. Laboratory-derived isolates accumulated more mutations per genome and exhibited stronger locus-level parallelism, with mutations recurring in a small number of coding loci. Field-derived isolates accumulated fewer mutations per genome, and these mutations rarely occurred in the same coding loci across replicate populations. Instead, field isolates exhibited a higher proportion of intergenic mutations, with mutations recurring in the same intergenic regions across independent field deployments. When coding mutations were detected in the field, they were distributed across functionally diffuse targets and more often involved metabolic pathways than the core cellular processes repeatedly targeted during laboratory evolution. Warming itself did not consistently influence mutation accumulation or the genomic distribution of mutations; instead, laboratory and field contexts primarily shaped the accumulation, targets, and repeatability of genomic change. These results suggest that laboratory thermal evolution identifies adaptive routes favored under sustained selection but may overestimate coding-level parallelism under heterogeneous field conditions. Bridging laboratory and field evolution will likely require experimental designs that incorporate temporal variability and spatial heterogeneity characteristic of natural systems.IMPORTANCEA central goal of experimental evolution is to infer how microbes evolve in nature from laboratory studies. Here, we evaluate this assumption by comparing genomic evolution of a leaf litter-associated Curtobacterium strain in laboratory and field warming experiments to identify broad patterns rather than isolate the contribution of any single environmental factor. We find that the strong parallelism at coding loci observed under laboratory conditions is reduced in the field, while mutations recurring in the same intergenic regions across field deployments suggest that parallel evolution in nature may more often involve regulatory noncoding regions rather than coding targets. These results show that environmental context reshapes adaptive landscapes and may limit the parallelism of coding-level genomic responses inferred from homogeneous laboratory conditions.
Bacteria pose a serious threat to hosts through adaptive mutations that confer stress resistance and promote persistent colonization. Here, we describe an adaptive evolution event involving eight highly similar ST11-KL64 carbapenem-resistant Klebsiella pneumoniae (CRKP) strains, isolated from a non-infected inpatient who acquired two distinct CRKP strains, CRKP-F1 and CRKP-S2 during the first hospitalization, recovered, and was discharged after receiving antimicrobial therapy but subsequently experienced two additional recurrent febrile episodes and re-admission. The strain CRKP-S2 showed significantly enhanced resistance to oxidative stress, survival within macrophages, and internalization ability, and carried an additional ~72 kb fragment containing oxidative stress response factors (including NAD(P)-dependent oxidoreductases), and a ~ 19kb plasmid fragment harboring catA2, sul2, umuC/D genes, compared to the initial strain CRKP-F1. All four strains, CRKP-B3, CRKP-U4, CRKP-F5 and CRKP-S6, from the second hospitalization exhibited higher genetic similarity to CRKP-S2 than each other, and each of these strains has its own unique mutations compared to CRKP-S2. The third-hospitalization strain CRKP-U7 displayed the highest average nucleotide identity (ANI) with CRKP-S2, and possessed unique mutations in cecR, rlmA1, and selB, distinct from second-hospitalization strains. However, the last strain, CRKP-B8, carries a new gene mutation based on CRKP-U7 and exhibits greater host adaptability than all other isolates. While these findings are suggestive, whether the ~72-kb and ~19-kb fragments and mutations in CRKP-S2 drove enhanced colonization, and whether subsequent mutations contributed to subclones linked to recurrent febrile, or merely coincided, remains unclear. The possibility of mixed colonization by co-circulating subclones cannot be excluded, and functional validation is needed.
Adaptive laboratory evolution is able to generate microbial strains, which exhibit extreme phenotypes, revealing fundamental biological adaptation mechanisms. Here, we use adaptive laboratory evolution to evolve Escherichia coli strains that grow at temperatures as high as 45.3 °C, a temperature lethal to wild-type cells. The strains adopted a hypermutator phenotype and employed multiple systems-level adaptations that made global analysis of the DNA mutations difficult. Given the challenge at the genomic level, we were motivated to uncover high-temperature tolerance adaptation mechanisms at the transcriptomic level. We employed independently modulated gene set (iModulon) analysis to reveal five transcriptional mechanisms underlying growth at high temperatures. These mechanisms were connected to acquired mutations, changes in transcriptome composition, sensory inputs, phenotypes, and protein structures. They are as follows: (i) downregulation of general stress responses while upregulating the specific heat stress responses, (ii) upregulation of flagellar basal bodies without upregulating motility and upregulation fimbriae, (iii) shift toward anaerobic metabolism, (iv) shift in regulation of iron uptake away from siderophore production, and (v) upregulation of yjfIJKL, a novel heat tolerance operon whose structures we predicted with AlphaFold. iModulons associated with these five mechanisms explain nearly half of all variance in the gene expression in the adapted strains. These thermotolerance strategies reveal that optimal coordination of known stress responses and metabolism can be achieved with a small number of regulatory mutations and may suggest a new role for large protein export systems. Adaptive laboratory evolution with transcriptomic characterization is a productive approach for elucidating and interpreting adaptation to otherwise lethal stresses.
Stylosanthes guianensis is a leguminous forage crop of significant economic importance, primarily distributed in tropical and subtropical regions. It exhibits strong adaptability to various stresses, yet the genetic basis underlying this trait remains unclear. In this study, we constructed the first chromosome-scale reference genome of S. guianensis using a combination of Nanopore and Hi-C sequencing technologies. The assembled genome size is 1254 Mb, with 10 pseudochromosomes. Using Nanopore full-length transcriptome data, we generated high-quality transcript-level gene annotations, identifying 36 585 gene models and 110 601 transcripts. The repetitive sequences in S. guianensis account for 79.16% of the genome, with the extensive expansion of Gypsy elements in long terminal repeats contributing to its genome size enlargement. Comparative genomic and transcriptomic analyses revealed that flavonoid metabolism plays a pivotal role in stress adaptation, providing new insights into the genetic basis of stress tolerance. Additionally, we generated whole-genome methylation profiles under cold treatment and control conditions, offering valuable data for future epigenomic research. These findings provide essential molecular resources for understanding stress resilience in S. guianensis and advancing its molecular breeding.
Organisms living in desert habitats face multiple simultaneous pressures, such as high temperatures and arid, and the population dynamics and community diversity of small rodents are strongly affected by climate extremes. However, the potential mechanisms by which desert rodents adapt to arid remain largely unexplored. Here, we assembled a 3.18 Gb genome, including 25,812 protein-encoding genes, for Orientallactaga sibirica, which is widely distributed across both arid and semihumid environments in Eurasia. Orientallactaga sibirica has longer ears and hind limbs to enhance heat dissipation, which may be related to the positively selected genes, such as Fgf10, Fgf11, Hoxc4, Hoxd1, and Bmp4. The renal transcriptome revealed increased fat and carbohydrate metabolism for metabolic water production in O. sibirica residing in arid habitats. Pathways such as material metabolism, oxidative stress response, osmoregulation, and water and salt reabsorption were enriched in candidate genes, such as Avp, Ang, and Ace, under positive selection in O. sibirica. Moreover, amino acid replacement was observed in the protein sequences of seven candidate genes, including Aldh7a1, Lnpep, Wnk4, C1qc, and Awat2, and these specific amino acid replacements of genes such as Umod and Scnn1a were related to unique osmoregulation, osmotic protection, and water retention compensation mechanisms. Water deprivation under laboratory conditions induced the upregulation of Umod and Aldh7a1 expression, further supporting the results observed in the wild population. These findings demonstrate that the positively selected genes related to limb development and specific amino acid replacements in the genes Umod and Scnn1a for unique osmoregulation in the renal vascular system may contribute to arid adaptation in the desert rodent species O. sibirica. This study provides novel insights into the adaptive evolution of desert small mammals and can serve as a reference for future research on renal damage-related diseases, such as human kidney stones and salt-sensitive hypertension.
Genetic heterogeneity exists within all microbial populations, with sympatric cells of the same species often exhibiting single-nucleotide variations that influence phenotypic traits, including metabolic efficiency. However, the evolutionary dynamics of these strain-level differences in response to environmental stress remain poorly understood. Here, we present a first-of-its-kind study tracking the adaptive evolution of an anaerobic, carbon-fixing microbiota under a controlled engineered ecosystem focused on carbon dioxide bioconversion into methane. Leveraging strain-resolved metagenomics with an ad hoc variant calling and phasing approach, we mapped mutation trajectories and observed that the two dominant Methanothermobacter species maintained distinct sweeping haplotypes over time, most likely due to niche-specific metabolic roles. By combining population genetic statistics and peptide reconstruction, mer and mcrB genes emerged as potential drivers of archaeal strain-level competition. These findings pave the way for targeted engineering of microbial communities to enhance bioconversion efficiency, with significant implications for sustainable energy and carbon management in anaerobic systems.
Active transposable elements (TEs) are capable of generating new insertions in genomes and have historically been viewed as genomic parasites due to their largely detrimental or neutral effects. However, emerging evidence suggests that these elements also play a crucial role in driving adaptive evolution in insects. This mini-review synthesizes recent findings on how active TEs contribute to insect adaptation through various mechanisms, including regulation of gene expression, structural variation, and epigenetic effects. Notable examples of adaptation driven by active TEs include their roles in insecticide resistance, morphological adaptations, tolerance to harsh climates, and antiviral immune responses. We argue that while host silencing mechanisms, such as the piRNA pathway, tightly regulate TE activity to minimize harmful effects, the context-dependent activation of active TEs can generate beneficial genetic variation that enhances insect adaptations to anthropogenic and climatic pressures. Future research that integrates long-read sequencing, single-cell omics, and gene editing techniques will provide a robust mechanistic foundation for understanding the adaptive significance of active TEs in insects, with important implications for pest management, pollinator protection, and evolutionary biology.
BACKGROUND: Centromeres are crucial for precise chromosome segregation and maintaining genome stability during cell division. However, their evolutionary dynamics, particularly in polyploid organisms with complex genomic architectures, remain largely enigmatic. Allopolyploid wheat, with its well-defined hierarchical ploidy series and recent polyploidization history, serves as an excellent model to explore centromere evolution. RESULTS: In this study, we perform a systematic comparative analysis of centromeres in common wheat and its corresponding ancestral species, utilizing the latest comprehensive reference genome assembly available. Our findings reveal that wheat centromeres predominantly consist of five types of centromeric-specific retrotransposon elements (CRWs), with CRW1 and CRW2 being the most prevalent. We identify distinct evolutionary trajectories in the functional centromeres of each subgenome, characterized by variations in copy number, insertion age, and CRW composition. By utilizing CENH3-ChIP data across various ploidy levels, we uncover a series of CRW invasion events that have shaped the evolution of AA subgenome centromeres. Conversely, the evolutionary process of the DD subgenome centromeres involves their expansion from diploid to hexaploid wheat, facilitating adaptation to a larger genomic context. Integration of complete einkorn centromere assemblies and Aegilops tauschii pan-genomes further revealed subgenome-specific centromere evolutionary trajectories. By inclusion of synthetic hexaploid from S2-S3 generations, alongside 2x/6 × natural accessions, we demonstrate that DD subgenome centromere expansion represents a gradual evolutionary process rather than an immediate response to polyploidization. CONCLUSIONS: Our study provides a comprehensive landscape of centromere adaptation, evolution, and maturation, along with insights into how retrotransposon invasions drive centromere evolution in polyploid wheat.
Adaptive evolution in response to varying environments, leading to population divergence, is among the most intriguing processes of speciation. However, the extent to which these adaptive processes effectively drive population divergence amidst ongoing gene flow remains controversial. Our study addresses this by analyzing population genetic structure, gene flow, and genomic divergence between lineages of a tapeworm parasite (Ligula intestinalis) isolated from sympatric fish hosts. This parasite, which must overcome host immunological defenses for successful infection, significantly impacts host health. Utilizing genome-wide Single Nucleotide Polymorphisms (SNPs) and transcriptome data, we investigated whether host species impose distinct selection pressures on parasite populations. Genetic clustering analyses revealed clear divergence, with parasites from bream (Abramis brama) forming a distinct genetic cluster separate from those infecting roach (Rutilus rutilus), rudd (Scardinius erythrophthalmus), and bleak (Alburnus alburnus). Demographic modeling indicated isolation with continuous gene flow as the most plausible scenario for this divergence. Selection analyses identified 896 SNPs under selection, displaying low to moderate nucleotide diversity and genetic divergence compared with neutral loci. Transcriptome profiling supported these findings, revealing distinct gene expression profiles between parasite populations. Examination of selected SNPs and differentially expressed genes identified candidate genes linked to immune evasion mechanisms, potentially driving ecological speciation. This research highlights the interplay of host specificity, population demography, and disruptive selection in ecological speciation. By dissecting genomic factors, our study improves the understanding of mechanisms facilitating population divergence despite ongoing gene flow.
The olive family (Oleaceae) comprises numerous species of economic, horticultural, and medicinal importance. Despite its significance, the evolutionary history of this complex family remains enigmatic. Here, we generated a high-quality haplotype-resolved genome of Forsythia suspensa, a distylous species that occupies a key phylogenetic position in Oleaceae. The 2 haplotypes exhibit significant allelic divergence with potential allele-specific regulation. We reconstructed the polyploidization history of Oleaceae by confirming and precisely dating a shared whole-genome triplication and an independent whole-genome duplication event. We revealed a complex reticulate evolution that gave rise to the tribe Oleeae: an initial hybridization between Forsythieae (♂) and Jasmineae (♀), a subsequent backcrossing event, and a final whole-genome duplication. We identified a novel tandemly duplicated pectin methylesterase inhibitor gene cluster that regulates filament length and pollen size via restricting cell elongation in the long-styled morph. Dosage augmentation via stepwise cluster formation (0.99 to 3.83 Mya) may contribute to maintaining stamen traits of the long-styled morph. These FsPMEIs are co-expressed with many cell wall-related genes, suggesting a functional link in cell wall modification. Our study reveals the reticulate evolution in Oleaceae and a novel gene cluster controlling stamen development in F. suspensa and provides valuable haplotype-resolved genomic resources for heterostylous species, offering novel framework and molecular pathways to understand plant adaptive evolution.