Adaptation In Natural Populations Research Articles

Genetic architecture and correlations between the gut microbiome and gut gene transcription in Chinook salmon (Oncorhynchus tshawytscha).

Population divergence through selection can drive local adaptation in natural populations which has implications for the effective restoration of declining and extirpated populations. However, adaptation to local environmental conditions is complicated when both the host and its associated microbiomes must respond via co-evolutionary change. Nevertheless, for adaptation to occur through selection, variation in both host and microbiome traits should include additive genetic effects. Here we focus on host immune function and quantify factors affecting variation in gut immune gene transcription and gut bacterial community composition in early life-stage Chinook salmon (Oncorhynchus tshawytscha). Specifically, we utilized a replicated factorial breeding design to determine the genetic architecture (sire, dam and sire-by-dam interaction) of gut immune gene transcription and microbiome composition. Furthermore, we explored correlations between host gut gene transcription and microbiota composition. Gene transcription was quantified using nanofluidic qPCR arrays (22 target genes) and microbiota composition using 16 S rRNA gene (V5-V6) amplicon sequencing. We discovered limited but significant genetic architecture in gut microbiota composition and transcriptional profiles. We also identified significant correlations between gut gene transcription and microbiota composition, highlighting potential mechanisms for functional interactions between the two. Overall, this study provides support for the co-evolution of host immune function and their gut microbiota in Chinook salmon, a species recognized as locally adapted. Thus, the inclusion of immune gene transcription profile and gut microbiome composition as factors in the development of conservation and commercial rearing practices may provide new and more effective approaches to captive rearing.

Local Adaptation in Natural Populations of Toona ciliata var. pubescens Is Driven by Precipitation and Temperature: Evidence from Microsatellite Markers

Environmental factors are strong drivers of local adaptation in forest tree species. Toona ciliata var. pubescens, an endangered tree species endemic to China, is widely distributed across Eastern and Southwestern China. In this study, we used 8 genomic microsatellite markers and 17 EST-SSR markers across nine populations from the Yunnan–Kweichow Plateau and Eastern China, to explore the adaptive variation and genetic structure of T. ciliata var. pubescens. Patterns of population structure were apparent using a Bayesian clustering program, STRUCTURE, which identified four distinct clusters. We identified four outlier loci that were potentially under selection using the Dirichlet-multinomial and hierarchic simulation models. Through the Mantel test, it was found that geographic and climatic factors have jointly affected the genetic structure of T. ciliata var. pubescens in the study area. Based on redundancy analysis (RDA), it was shown that the correlation between climatic variables associated with variation is stronger than that of geographic variables. It is worth mentioning that the eight alleles from outlier loci have potentially adaptive and are associated with either precipitation or temperature variables. All analyses revealed high genetic diversity and significant genetic differentiation in the populations of T. ciliata var. pubescens. This indicated that the climatic variables including precipitation and temperature are drivers of local adaptation in the populations of T. ciliata var. pubescens.

Uncovering the genetic architecture of parallel evolution.

Identifying the genetic architecture underlying adaptive traits is exceptionally challenging in natural populations. This is because associations between traits not only mask the targets of selection but also create correlated patterns of genomic divergence that hinder our ability to isolate causal genetic effects. Here, we examine the repeated evolution of components of the auxin pathway that have contributed to the replicated loss of gravitropism (i.e. the ability of a plant to bend in response to gravity) in multiple populations of the Senecio lautus species complex in Australia. We use a powerful approach which combines parallel population genomics with association mapping in a Multiparent Advanced Generation Inter-Cross (MAGIC) population to break down genetic and trait correlations to reveal how adaptive traits evolve during replicated evolution. We sequenced auxin and shoot gravitropism-related gene regions in 80 individuals from six natural populations (three parallel divergence events) and 133 individuals from a MAGIC population derived from two of the recently diverged natural populations. We show that artificial tail selection on gravitropism in the MAGIC population recreates patterns of parallel divergence in the auxin pathway in the natural populations. We reveal a set of 55 auxin gene regions that have evolved repeatedly during the evolution of the species, of which 50 are directly associated with gravitropism divergence in the MAGIC population. Our work creates a strong link between patterns of genomic divergence and trait variation contributing to replicated evolution by natural selection, paving the way to understand the origin and maintenance of adaptations in natural populations.

Advancing research on ectomycorrhizal fungal adaptation with landscape genomics.

Ectomycorrhizal (ECM) fungi serve key functions in forest ecosystems by supplying water and nutrients to tree hosts, yet mutualistic plant-fungi interactions are jeopardised by environmental alterations. Here, we discuss the great potential and current limitations of landscape genomics in investigating signatures of local adaptation in natural populations of ECM fungi.

The WZA: A window-based method for characterizing genotype-environment associations.

Genotype-environment association (GEA) studies have the potential to identify the genetic basis of local adaptation in natural populations. Specifically, GEA approaches look for a correlation between allele frequencies and putatively selective features of the environment. Genetic markers with extreme evidence of correlation with the environment are presumed to be tagging the location of alleles that contribute to local adaptation. In this study, we propose a new method for GEA studies called the Weighted-Z Analysis (WZA) that combines information from closely linked sites into analysis windows in a way that was inspired by methods for calculating FST . Performing GEA methods in analysis windows has the advantage that it takes advantage of the increased linkage disequilibrium expected surrounding sites subject to local adaptation. We analyse simulations modelling local adaptation to heterogeneous environments to compare the WZA with existing methods. In the majority of cases we tested, the WZA either outperformed single-SNP (single nucleotide polymorphism)-based approaches or performed similarly. In particular, the WZA outperformed individual SNP approaches when a small number of individuals or demes were sampled. Particularly troubling, we found that some GEA methods exhibit very high false positive rates. We applied the WZA to previously published data from lodgepole pine and identified candidate loci that were identified in the original study alongside numerous loci that were not found in the original study.

Rapid and transient evolution of local adaptation to seasonal host fruits in an invasive pest fly.

Both local adaptation and adaptive phenotypic plasticity can influence the match between phenotypic traits and local environmental conditions. Theory predicts that environments stable for multiple generations promote local adaptation, whereas highly heterogeneous environments favor adaptive phenotypic plasticity. However, when environments have periods of stability mixed with heterogeneity, the relative importance of local adaptation and adaptive phenotypic plasticity is unclear. Here, we used Drosophila suzukii as a model system to evaluate the relative influence of genetic and plastic effects on the match of populations to environments with periods of stability from three to four generations. This invasive pest insect can develop within different fruits, and persists throughout the year in a given location on a succession of distinct host fruits, each one being available for only a few generations. Using reciprocal common environment experiments of natural D.suzukii populations collected from cherry, strawberry, and blackberry, we found that both oviposition preference and offspring performance were higher on medium made with the fruit from which the population originated than on media made with alternative fruits. This pattern, which remained after two generations in the laboratory, was analyzed using a statistical method we developed to quantify the contributions of local adaptation and adaptive plasticity in determining fitness. Altogether, we found that genetic effects (local adaptation) dominate over plastic effects (adaptive phenotypic plasticity). Our study demonstrates that spatially and temporally variable selection does not prevent the rapid evolution of local adaptation in natural populations. The speed and strength of adaptation may be facilitated by several mechanisms including a large effective population size and strong selective pressures imposed by host plants.

Anatomical and physiological systematics of Capparis decidua (Forsskal.) Edgew from different habitats of Cholistan Desert, Pakistan

Capparis decidua a medicinal shrub belonging to the family Capparaceae, grows abundantly in wild regions of Asia, Africa, and Saudi Arabia. Due to its medicinal and nutritional value, a study on anatomical and physiological adaptations under various desert habitats was conducted. Results revealed that plants in saline areas showed significant anatomical and physiological modifications particularly in stem and roots show better survival under the harsh saline conditions of the desert. It was noted that the root epidermis thickness was not affected in a slightly saline environment as it showed no significant increasing or decreasing trend in the cross-section of the plant population from non-saline to slightly saline (p > 0.05) while it increased significantly in plants growing at highly saline (p < 0.05). Whereas endodermis cell area differs significantly between plants growing at all selected study sites it increased continuously with a rise in the salinity level of the soil (p < 0.05). Meanwhile, water storage capacity and reduction of water loss in the stem area, epidermis, and sclerenchyma were also recorded. In a highly saline environment, results intimate the deduction of photosynthetic pigments, an increase in total soluble proteins, total free amino acids, total soluble sugars, and proline, and a rise in stem and root tissue Na+, K+, Ca2+, and Cl− contents and meanwhile, accumulation of secondary metabolites (Phenolics and flavonoids). These anatomical and physiological adaptations in natural populations appear to be very important for their better survival in a harsh saline desert environment. It was concluded that C. decidua was found in all different edaphic habitats of the Cholistan Desert, due to its adaptive features, which were very obvious in this plant and highly saline site.

Natural variation in growth and leaf ion homeostasis in response to salinity stress in Panicum hallii.

Soil salinity can negatively impact plants growth, development and fitness. Natural plant populations restricted to coastal environments may evolve in response to saline habitats and therefore provide insights into the process of salinity adaptation. We investigated the growth and physiological responses of coastal and inland populations of Panicum hallii to experimental salinity treatments. Coastal genotypes demonstrated less growth reduction and superior ion homeostasis compared to the inland genotypes in response to saline conditions, supporting a hypothesis of local adaptation. We identified several QTL associated with the plasticity of belowground biomass, leaf sodium and potassium content, and their ratio which underscores the genetic variation present in this species for salinity responses. Genome-wide transcriptome analysis in leaf and root tissue revealed tissue specific overexpression of genes including several cation transporters in the coastal genotype. These transporters mediate sodium ion compartmentalization and potassium ion retention and thus suggests that maintenance of ionic homeostasis of the coastal genotypes might be due to the regulation of these ion transporters. These findings contribute to our understanding of the genetics and molecular mechanisms of salinity adaptation in natural populations, and widens the scope for genetic manipulation of these candidate genes to design plants more resilient to climate change.

Genomic footprints related with adaptation and fumonisins production in Fusarium proliferatum.

Fusarium proliferatum is the principal etiological agent of rice spikelet rot disease (RSRD) in China, causing yield losses and fumonisins contamination in rice. The intraspecific variability and evolution pattern of the pathogen is poorly understood. Here, we performed whole-genome resequencing of 67 F. proliferatum strains collected from major rice-growing regions in China. Population structure indicated that eastern population of F. proliferatum located in Yangtze River with the high genetic diversity and recombinant mode that was predicted as the putative center of origin. Southern population and northeast population were likely been introduced into local populations through gene flow, and genetic differentiation between them might be shaped by rice-driven domestication. A total of 121 distinct genomic loci implicated 85 candidate genes were suggestively associated with variation of fumonisin B1 (FB1) production by genome-wide association study (GWAS). We subsequently tested the function of five candidate genes (gabap, chsD, palA, hxk1, and isw2) mapped in our association study by FB1 quantification of deletion strains, and mutants showed the impact on FB1 production as compared to the wide-type strain. Together, this is the first study to provide insights into the evolution and adaptation in natural populations of F. proliferatum on rice, as well as the complex genetic architecture for fumonisins biosynthesis.

Thermal and latitudinal patterns in pace-of-life traits are partly mediated by the gut microbiome

The integration of life-history, physiological and behavioural traits into the pace-of-life generates a powerful framework to understand trait variation in nature both along environmental gradients and in response to environmental stressors. While the gut microbiome has been hypothesized as a candidate mechanism to underlie differentiation in the pace-of-life, this has been rarely studied. We investigated the role of the gut microbiome in contributing to the differentiation in pace-of-life and in thermal adaptation between populations of Ischnura elegans damselfly larvae inhabiting warmer low latitudes and colder high latitudes. We carried out a common-garden experiment, whereby we manipulated the exposure of the damselfly larvae to two key global warming factors: 4 °C warming and a 30 °C heat wave. Comparing the bacterial composition of the food source and the bacterioplankton indicated that damselfly larvae differentially take up bacteria from the surrounding environment and have a resident and functionally relevant microbiome. The gut microbiome differed between larvae of both latitudes, and this was associated with the host's latitudinal differentiation in activity, a key pace-of-life trait. Under heat wave exposure, the gut microbial community composition of high-latitude larvae converged towards that of the low-latitude larvae, with an increase in bacteria that likely are important in providing energy to cope with the heat wave. This suggests an adaptive latitude-specific shift in the gut microbiota matching the better ability of low-latitude hosts to deal with heat extremes. In general, our study provides evidence for the gut microbiome contributing to latitudinal differentiation in both the pace-of-life and in heat adaptation in natural populations.

A microRNA-microRNA crosstalk network inferred from genome-wide single nucleotide polymorphism variants in natural populations of Arabidopsis thaliana.

To adapt to variable natural conditions, plants have evolved several strategies to respond to different environmental stresses. MicroRNA (miRNA)-mediated gene regulation is one of such strategies. Variants, e.g., single nucleotide polymorphisms (SNPs) within the mature miRNAs or their target sites may cause the alteration of regulatory networks and serious phenotype changes. In this study, we proposed a novel approach to construct a miRNA–miRNA crosstalk network in Arabidopsis thaliana based on the notion that two cooperative miRNAs toward common targets are under a strong pressure to be inherited together across ecotypes. By performing a genome-wide scan of the SNPs within the mature miRNAs and their target sites, we defined a “regulation fate profile” to describe a miRNA–target regulation being static (kept) or dynamic (gained or lost) across 1,135 ecotypes compared with the reference genome of Col-0. The cooperative miRNA pairs were identified by estimating the similarity of their regulation fate profiles toward the common targets. The reliability of the cooperative miRNA pairs was supported by solid expressional correlation, high PPImiRFS scores, and similar stress responses. Different combinations of static and dynamic miRNA–target regulations account for the cooperative miRNA pairs acting on various biological characteristics of miRNA conservation, expression, homology, and stress response. Interestingly, the targets that are co-regulated dynamically by both cooperative miRNAs are more likely to be responsive to stress. Hence, stress-related genes probably bear selective pressures in a certain group of ecotypes, in which miRNA regulations on the stress genes reprogram. Finally, three case studies showed that reprogramming miRNA–miRNA crosstalk toward the targets in specific ecotypes was associated with these ecotypes’ climatic variables and geographical locations. Our study highlights the potential of miRNA–miRNA crosstalk as a genetic basis underlying environmental adaptation in natural populations.

Whole genome resequencing reveals signatures of rapid selection in a virus-affected commercial fishery.

Infectious diseases are recognized as one of the greatest global threats to biodiversity and ecosystem functioning. Consequently, there is a growing urgency to understand the speed at which adaptive phenotypes can evolve and spread in natural populations to inform future management. Here we provide evidence of rapid genomic changes in wild Australian blacklip abalone (Haliotis rubra) following a major population crash associated with an infectious disease. Genome scans on H. rubra were performed using pooled whole genome resequencing data from commercial fishing stocks varying in historical exposure to haliotid herpesvirus‐1 (HaHV‐1). Approximately 25,000 single nucleotide polymorphism loci associated with virus exposure were identified, many of which mapped to genes known to contribute to HaHV‐1 immunity in the New Zealand pāua (Haliotis iris) and herpesvirus response pathways in haliotids and other animal systems. These findings indicate genetic changes across a single generation in H. rubra fishing stocks decimated by HaHV‐1, with stock recovery potentially determined by rapid evolutionary changes leading to virus resistance. This is a novel example of apparently rapid adaptation in natural populations of a nonmodel marine organism, highlighting the pace at which selection can potentially act to counter disease in wildlife communities.

Population genomic evidence for genetic divergence in the Northwest Pacific Ark shell (Scapharca broughtonii)

Combining population genetics with genomic data has transformed scientist’s ability and resolution of making ecological inferences, thus making it possible to detect previously unidentified structures and obtain more accurate estimates of demographic parameters in wild populations. Ark shell is an economically and ecologically important marine species for fisheries industry in China, but its habitats have been severely damaged due to overexploitation of natural resources. Recently, protection of the ark shell as a natural resource has attracted extensive attention. Here, we identified 10,108 single-nucleotide polymorphisms using Restriction-site Associated DNA Sequencing (2b-RAD) to explore the structure of seven populations of S. broughtonii from the Asian Pacific Northwest region (four sites in China, two in Korea, and one in North Korea). A high level of genetic diversity was detected in all seven S. broughtonii populations. Pairwise FST estimates and neighbor-joining (NJ) tree topologies showed a clear division between the populations from China and Korea, and Chinese populations exhibited low levels of divergence from one another. This significant genetic divergence of the Chinese population implies that translocation of individuals for aquaculture should be properly managed for the preservation of genetic diversity and eventual local adaptation in natural populations.

The potential role of spatial sorting in speciation and adaptive radiations

Given that Matsubayashi and Yamaguchi (2022) admirably cover the general understanding of species radiations and suggest approaches to isolate underlying mechanisms, we concentrate on a novel concept of “spatial sorting” that has emerged from the biology of invasive species and highlights a distinct role of dispersal in generating evolutionary change. The potential role for spatial sorting to facilitate or impede adaptation in natural populations at large spatial scales has been broadly overlooked. Herein, we consider how speciation and adaptive radiations may be promoted or impeded by this underexplored evolutionary mechanism.

The genomic basis of high-elevation adaptation in wild house mice (Mus musculus domesticus) from South America.

Understanding the genetic basis of environmental adaptation in natural populations is a central goal in evolutionary biology. The conditions at high elevation, particularly the low oxygen available in the ambient air, impose a significant and chronic environmental challenge to metabolically active animals with lowland ancestry. To understand the process of adaptation to these novel conditions and to assess the repeatability of evolution over short timescales, we examined the signature of selection from complete exome sequences of house mice (Mus musculus domesticus) sampled across two elevational transects in the Andes of South America. Using phylogenetic analysis, we show that house mice colonized high elevations independently in Ecuador and Bolivia. Overall, we found distinct responses to selection in each transect and largely nonoverlapping sets of candidate genes, consistent with the complex nature of traits that underlie adaptation to low oxygen availability (hypoxia) in other species. Nonetheless, we also identified a small subset of the genome that appears to be under parallel selection at the gene and SNP levels. In particular, three genes (Col22a1, Fgf14, and srGAP1) bore strong signatures of selection in both transects. Finally, we observed several patterns that were common to both transects, including an excess of derived alleles at high elevation, and a number of hypoxia-associated genes exhibiting a threshold effect, with a large allele frequency change only at the highest elevations. This threshold effect suggests that selection pressures may increase disproportionately at high elevations in mammals, consistent with observations of some high-elevation diseases in humans.

Facilitating population genomics of non-model organisms through optimized experimental design for reduced representation sequencing

BackgroundGenome-wide data are invaluable to characterize differentiation and adaptation of natural populations. Reduced representation sequencing (RRS) subsamples a genome repeatedly across many individuals. However, RRS requires careful optimization and fine-tuning to deliver high marker density while being cost-efficient. The number of genomic fragments created through restriction enzyme digestion and the sequencing library setup must match to achieve sufficient sequencing coverage per locus. Here, we present a workflow based on published information and computational and experimental procedures to investigate and streamline the applicability of RRS.ResultsIn an iterative process genome size estimates, restriction enzymes and size selection windows were tested and scaled in six classes of Antarctic animals (Ostracoda, Malacostraca, Bivalvia, Asteroidea, Actinopterygii, Aves). Achieving high marker density would be expensive in amphipods, the malacostracan target taxon, due to the large genome size. We propose alternative approaches such as mitogenome or target capture sequencing for this group. Pilot libraries were sequenced for all other target taxa. Ostracods, bivalves, sea stars, and fish showed overall good coverage and marker numbers for downstream population genomic analyses. In contrast, the bird test library produced low coverage and few polymorphic loci, likely due to degraded DNA.ConclusionsPrior testing and optimization are important to identify which groups are amenable for RRS and where alternative methods may currently offer better cost-benefit ratios. The steps outlined here are easy to follow for other non-model taxa with little genomic resources, thus stimulating efficient resource use for the many pressing research questions in molecular ecology.

Genomic structural variants constrain and facilitate adaptation in natural populations of Theobroma cacao, the chocolate tree

Genomic structural variants (SVs) can play important roles in adaptation and speciation. Yet the overall fitness effects of SVs are poorly understood, partly because accurate population-level identification of SVs requires multiple high-quality genome assemblies. Here, we use 31 chromosome-scale, haplotype-resolved genome assemblies of Theobroma cacao-an outcrossing, long-lived tree species that is the source of chocolate-to investigate the fitness consequences of SVs in natural populations. Among the 31 accessions, we find over 160,000 SVs, which together cover eight times more of the genome than single-nucleotide polymorphisms and short indels (125 versus 15 Mb). Our results indicate that a vast majority of these SVs are deleterious: they segregate at low frequencies and are depleted from functional regions of the genome. We show that SVs influence gene expression, which likely impairs gene function and contributes to the detrimental effects of SVs. We also provide empirical support for a theoretical prediction that SVs, particularly inversions, increase genetic load through the accumulation of deleterious nucleotide variants as a result of suppressed recombination. Despite the overall detrimental effects, we identify individual SVs bearing signatures of local adaptation, several of which are associated with genes differentially expressed between populations. Genes involved in pathogen resistance are strongly enriched among these candidates, highlighting the contribution of SVs to this important local adaptation trait. Beyond revealing empirical evidence for the evolutionary importance of SVs, these 31 de novo assemblies provide a valuable resource for genetic and breeding studies in Tcacao.

Adaptive and Plastic Responses to Environmental Variation: Introduction to a Virtual Symposium in The Biological Bulletin.

Adaptive and Plastic Responses to Environmental Variation: Introduction to a Virtual Symposium in The Biological Bulletin.

Monarch Butterfly Migration as an Integrative Model of Complex Trait Evolution.

AbstractUnderstanding the genetic architecture of complex trait adaptation in natural populations requires the continued development of tractable models that explicitly confront organismal and environmental complexity. A decade of high-throughput sequencing-based investigations into the genomic basis of migration points to an integrative framework that incorporates quantitative genetics, evolutionary developmental biology, phenotypic plasticity, and epigenetics to explain migration evolution. In this perspective, I argue that the transcontinental migration of the monarch butterfly (Danaus plexippus) can serve as a compelling system to study the mechanism of evolutionary lability of a complex trait. Monarchs show significant phenotypic and genotypic diversity across their global range, with phenotypic switching that allows for explicit study of evolutionary lability. A developmental approach for elucidating how migratory traits are generated and functionally integrated will be important for understanding the evolution of monarch migration traits. I propose a plasticity threshold model to describe migration lability, and I describe novel functional techniques that will help resolve open questions and model assumptions. I conclude by considering the relationships between adaptive genetic architecture, anthropogenic climate change, and conservation management practice and the timeliness of the monarch migration model to illuminate these connections given the rapid decline of the North American migration.

Robustness and predictability of evolution in bottlenecked populations

Deterministic and stochastic evolutionary processes drive adaptation in natural populations. The strength of each component process is determined by the population size: deterministic components prevail in very large populations, while stochastic components are the driving mechanisms in small ones. Many natural populations, however, experience intermittent periods of growth, moving through states in which either stochastic or deterministic processes prevail. This growth is often countered by population bottlenecks, which abound in both natural and laboratory populations. Here we investigate how population bottlenecks shape the process of adaptation. We demonstrate that adaptive trajectories in populations experiencing regular bottlenecks can be naturally scaled in time units of generations; with this scaling the time courses of adaptation, fitness variance, and genetic diversity all become relatively insensitive to the timing of population bottlenecks, provided the bottleneck size exceeds a few thousand individuals. We also include analyses at the genotype level to investigate the impact of population bottlenecks on the predictability and distribution of evolutionary pathways. Irrespective of the timing of population bottlenecks, we find that predictability increases with population size. We also find that predictability of the adaptive pathways increases in increasingly rugged fitness landscapes. Overall, our work reveals that both the adaptation rate and the predictability of evolutionary trajectories are relatively robust to population bottlenecks.