Adaptive Genetic Variation Research Articles

Evolutionary rescue in a host-pathogen system results in coexistence not clearance.

The evolutionary rescue of host populations may prevent extinction from novel pathogens. However, the conditions that facilitate rapid evolution of hosts, in particular the population variation in host susceptibility, and the effects of host evolution in response to pathogens on population outcomes remain largely unknown. We constructed an individual‐based model to determine the relationships between genetic variation in host susceptibility and population persistence in an amphibian‐fungal pathogen (Batrachochytrium dendrobatidis) system. We found that host populations can rapidly evolve reduced susceptibility to a novel pathogen and that this rapid evolution led to a 71‐fold increase in the likelihood of host–pathogen coexistence. However, the increased rates of coexistence came at a cost to host populations; fewer populations cleared infection, population sizes were depressed, and neutral genetic diversity was lost. Larger adult host population sizes and greater adaptive genetic variation prior to the onset of pathogen introduction led to substantially reduced rates of extinction, suggesting that populations with these characteristics should be prioritized for conservation when species are threatened by novel infectious diseases.

Environmental and geographic variables are effective surrogates for genetic variation in conservation planning

Protected areas buffer species from anthropogenic threats and provide places for the processes that generate and maintain biodiversity to continue. However, genetic variation, the raw material for evolution, is difficult to capture in conservation planning, not least because genetic data require considerable resources to obtain and analyze. Here we show that freely available environmental and geographic distance variables can be highly effective surrogates in conservation planning for representing adaptive and neutral intraspecific genetic variation. We obtained occurrence and genetic data from the IntraBioDiv project for 27 plant species collected over the European Alps using a gridded sampling scheme. For each species, we identified loci that were potentially under selection using outlier loci methods, and mapped their main gradients of adaptive and neutral genetic variation across the grid cells. We then used the cells as planning units to prioritize protected area acquisitions. First, we verified that the spatial patterns of environmental and geographic variation were correlated, respectively, with adaptive and neutral genetic variation. Second, we showed that these surrogates can predict the proportion of genetic variation secured in randomly generated solutions. Finally, we discovered that solutions based only on surrogate information secured substantial amounts of adaptive and neutral genetic variation. Our work paves the way for widespread integration of surrogates for genetic variation into conservation planning.

Landscape genomics analysis of Achyranthes bidentata reveal adaptive genetic variations are driven by environmental variations relating to ecological habit

Knowledge on adaptive genetic variation in response to environmental variation is the key to understanding the adaptive evolution potential of species. China’s warm-temperate zone is an important climatic zone, but only a few landscape genomics studies have been conducted to understand the adaptive evolution of regional vegetation. In this study, natural populations of Achyranthes bidentata Blume were sampled in China’s warm-temperate zone to infer its adaptive evolution using landscape genomics methods. Four SCoT primers were used to investigate the adaptive evolution of A. bidentata in response to environmental variation across the warm-temperate zone of China. A total of 126 individuals from fifteen natural populations were successfully scored, and 202 unambiguous fragments were obtained. Twenty-three outlier loci were identified, eighteen outlier loci were significantly associated with environmental variables. Redundancy analytical results suggested that four environmental variables related to temperature and precipitation remarkably influenced the distribution of loci. The results provide empirical evidence that molecular markers with bias toward candidate functional genes might be suitable for landscape genomics studies. Temperature and precipitation jointly drive the adaptive evolution of A. bidentata. The key driving environmental factors identified in this study are mostly related to the ecological habit of A. bidentata. The species personality, i.e., ecological habit, seems to play an important role in the adaptive differentiation on A. bidentata.

Phylogeographic pattern suggests a general northeastward dispersal in the distribution of Machilus pauhoi in South China.

Machilus pauhoi Kanehira is an important timber species in China. A provenance trial was recently set up to evaluate the growth performance of trees from different localities, with the aim of designing seed transfer guidelines. Here, we tested twelve nuclear microsatellite markers derived from other species of the Lauraceae family and investigated population genetic structure in M. pauhoi. Both the number of observed alleles per locus (Na) and the polymorphic information content (PIC) significantly decreased against the latitude, but showed an insignificant decrease against the longitude. Heterozygosity (Ho) and gene diversity (h) exhibited a weak correlation with geographic location. Private alleles were present in multiple populations, and a moderate level of population genetic differentiation was detected (Gst = 0.1691). The joint pattern of genetic diversity (Na, PIC, Ho, and h) suggests that general northeastward dispersal led to the current distribution of M. pauhoi. Significant but weak effects of isolation-by-distance (IBD) occurred, implicating the mountain ranges as the major barrier to gene flow. Both STRUCTURE and hierarchical clustering analyses showed three distinct groups of populations related to the physical connectivity among mountain ranges. A priority in designing genetic conservation should be given to the populations at the southwest side of the species’ distribution. This conservation strategy can also be combined with the pattern of adaptive genetic variation from the provenance trial for comprehensive genetic resource management of native M. pauhoi.

When can refuges mediate the genetic effects of fire regimes? A simulation study of the effects of topography and weather on neutral and adaptive genetic diversity in fire-prone landscapes.

Understanding how landscape heterogeneity mediates the effects of fire on biodiversity is increasingly important under global changes in fire regimes. We used a simulation experiment to investigate how fire regimes interact with topography and weather to shape neutral and selection-driven genetic diversity under alternative dispersal scenarios, and to explore the conditions under which microrefuges can maintain genetic diversity of populations exposed to recurrent fire. Spatial heterogeneity in simulated fire frequency occurred in topographically complex landscapes, with fire refuges and fire-prone "hotspots" apparent. Interannual weather variability reduced the effect of topography on fire patterns, with refuges less apparent under high weather variability. Neutral genetic diversity was correlated with long-term fire frequency under spatially heterogeneous fire regimes, being higher in fire refuges than fire-prone areas, except under high dispersal or low fire severity (low mortality). This generated different spatial genetic structures in fire-prone and fire-refuge components of the landscape, despite similar dispersal. In contrast, genetic diversity was only associated with time since the most recent fire in flat landscapes without predictable refuges and hotspots. Genetic effects of selection driven by fire-related conditions depended on selection pressure, migration distance and spatial heterogeneity in fire regimes. Allele frequencies at a locus conferring higher fitness under successional environmental conditions followed a pattern of "temporal adaptation" to contemporary conditions under strong selection pressure and high migration. However, selected allele frequencies were correlated with spatial variation in long-term mean fire frequency (relating to environmental predictability) under weak dispersal, low selection pressure and strong spatial heterogeneity in fire regimes.

Drift, selection, or migration? Processes affecting genetic differentiation and variation along a latitudinal gradient in an amphibian

BackgroundPast events like fluctuations in population size and post-glacial colonization processes may influence the relative importance of genetic drift, migration and selection when determining the present day patterns of genetic variation. We disentangle how drift, selection and migration shape neutral and adaptive genetic variation in 12 moor frog populations along a 1700 km latitudinal gradient. We studied genetic differentiation and variation at a MHC exon II locus and a set of 18 microsatellites.ResultsUsing outlier analyses, we identified the MHC II exon 2 (corresponding to the β-2 domain) locus and one microsatellite locus (RCO8640) to be subject to diversifying selection, while five microsatellite loci showed signals of stabilizing selection among populations. STRUCTURE and DAPC analyses on the neutral microsatellites assigned populations to a northern and a southern cluster, reflecting two different post-glacial colonization routes found in previous studies. Genetic variation overall was lower in the northern cluster. The signature of selection on MHC exon II was weaker in the northern cluster, possibly as a consequence of smaller and more fragmented populations.ConclusionOur results show that historical demographic processes combined with selection and drift have led to a complex pattern of differentiation along the gradient where some loci are more divergent among populations than predicted from drift expectations due to diversifying selection, while other loci are more uniform among populations due to stabilizing selection. Importantly, both overall and MHC genetic variation are lower at northern latitudes. Due to lower evolutionary potential, the low genetic variation in northern populations may increase the risk of extinction when confronted with emerging pathogens and climate change.

Genetic variation in compensatory feeding for dietary dilution in a generalist caterpillar

Increasing the rate of food consumption is a common adaptive strategy that allows herbivores to compensate for declines in nutrient concentrations in plant tissues. Herbivores that are better able to compensate for dietary dilution may have selective advantages under nutritionally poor conditions. In order for compensatory feeding to respond to selection, there must be standing heritable variation for this trait. However, empirical data substantiating the adaptive significance and genetic variability of compensatory feeding are rare. By employing a full-sib, split-brood design, this study presents quantitative genetic analyses on the nutrient consumption rates of the generalist caterpillar, Spodoptera exigua, raised on semi-synthetic diets differing in nutrient concentrations. When encountering a diluted diet, caterpillars exhibited a compensatory increase in food consumption rate, but the extent of this increase was not sufficient to fully compensate for dietary dilution. A significant gene-environment interaction for consumption rate indicated that the capacity of caterpillars to compensate for dietary dilution varied across genotypes. The broad-sense heritability of compensatory feeding was 0.51. Caterpillar genotypes with a higher compensatory capacity suffered lower performance losses on the diluted diet than did those with a lower capacity. This study has implications for understanding how herbivores can evolutionarily respond to nutritional challenges.

An integrated framework to identify wildlife populations under threat from climate change.

Climate change is a major threat to global biodiversity that will produce a range of new selection pressures. Understanding species responses to climate change requires an interdisciplinary perspective, combining ecological, molecular and environmental approaches. We propose an applied integrated framework to identify populations under threat from climate change based on their extent of exposure, inherent sensitivity due to adaptive and neutral genetic variation and range shift potential. We consider intraspecific vulnerability and population‐level responses, an important but often neglected conservation research priority. We demonstrate how this framework can be applied to vertebrates with limited dispersal abilities using empirical data for the bat Plecotus austriacus. We use ecological niche modelling and environmental dissimilarity analysis to locate areas at high risk of exposure to future changes. Combining outlier tests with genotype–environment association analysis, we identify potential climate‐adaptive SNPs in our genomic data set and differences in the frequency of adaptive and neutral variation between populations. We assess landscape connectivity and show that changing environmental suitability may limit the future movement of individuals, thus affecting both the ability of populations to shift their distribution to climatically suitable areas and the probability of evolutionary rescue through the spread of adaptive genetic variation among populations. Therefore, a better understanding of movement ecology and landscape connectivity is needed for predicting population persistence under climate change. Our study highlights the importance of incorporating genomic data to determine sensitivity, adaptive potential and range shift potential, instead of relying solely on exposure to guide species vulnerability assessments and conservation planning.

Evolutionary dynamics of an expressed MHC class IIβ locus in the Ranidae (Anura) uncovered by genome walking and high-throughput amplicon sequencing

The Major Histocompatibility Complex (MHC) is a genomic region encoding immune loci that are important and frequently used markers in studies of adaptive genetic variation and disease resistance. Given the primary role of infectious diseases in contributing to global amphibian declines, we characterized the hypervariable exon 2 and flanking introns of the MHC Class IIβ chain for 17 species of frogs in the Ranidae, a speciose and cosmopolitan family facing widespread pathogen infections and declines. We find high levels of genetic variation concentrated in the Peptide Binding Region (PBR) of the exon. Ten codons are under positive selection, nine of which are located in the mammal-defined PBR. We hypothesize that the tenth codon (residue 21) is an amphibian-specific PBR site that may be important in disease resistance. Trans-species and trans-generic polymorphisms are evident from exon-based genealogies, and co-phylogenetic analyses between intron, exon and mitochondrial based reconstructions reveal incongruent topologies, likely due to different locus histories. We developed two sets of barcoded adapters that reliably amplify a single and likely functional locus in all screened species using both 454 and Illumina based sequencing methods. These primers provide a resource for multiplexing and directly sequencing hundreds of samples in a single sequencing run, avoiding the labour and chimeric sequences associated with cloning, and enabling MHC population genetic analyses. Although the primers are currently limited to the 17 species we tested, these sequences and protocols provide a useful genetic resource and can serve as a starting point for future disease, adaptation and conservation studies across a range of anuran taxa.

Genetic variation of major histocompatibility complex genes in the endangered red-crowned crane.

Populations that have drastically decreased in the past often have low genetic variation, which may increase the risk of extinction. The genes of major histocompatibility complex (MHC) play an important role in the adaptive immune response of jawed vertebrates. Maintenance of adaptive genetic diversity such as that of MHC genes is important for wildlife conservation. Here, we determined genotypes of exon 3 of MHC class IA genes (MHCIA) and exon 2 of MHC class IIB genes (MHCIIB) to evaluate genetic variation of the endangered red-crowned crane population on Hokkaido Island, Japan, which experienced severe population decline in the past. We identified 16 and 6 alleles of MHCIA and MHCIIB, respectively, from 152 individuals. We found evidence of a positive selection at the antigen-binding sites in MHCIA exon 3 and MHCIIB exon 2. The phylogenetic analyses indicated evidence of trans-species polymorphism among the crane MHC genes. The genetic variability in both classes of MHC genes at the population level was low. No geographic structure was found based on the genetic diversity of microsatellite and MHC genes. Our study provides useful data for the optimal management of the red-crowned crane population in Hokkaido and can contribute to future studies on MHC genes of the continental populations of the red-crowned crane and other crane species.

Neutral Genetic Processes Influence MHC Evolution in Threatened Gopher Tortoises (Gopherus polyphemus).

Levels of adaptive genetic variation influence how species deal with environmental and ecological change, but these levels are frequently inferred using neutral genetic markers. Major histocompatibility complex (MHC) genes play a key role in the adaptive branch of the immune system and have been used extensively to estimate levels of adaptive genetic variation. Parts of the peptide binding region, sites where MHC molecules directly interact with pathogen and self-proteins, were sequenced from a MHC class I (95/441 tortoises) and class II (245/441 tortoises) gene in threatened and nonthreatened populations of gopher tortoises (Gopherus polyphemus), and adaptive genetic variation at MHC genes was compared to neutral genetic variation derived from 10 microsatellite loci (441 tortoises). Genetic diversity at the MHC class II locus and microsatellites was greater in populations in the nonthreatened portion of the gopher tortoise's range (MHC class II difference in mean A = 8.11, AR = 0.79, HO = 0.51, and HE = 0.16; microsatellite difference in mean A = 1.05 and AR = 0.47). Only MHC class II sequences showed evidence of positive selection (dN/dS > 1, Z = 1.81, P = 0.04). Historical gene flow as estimated with Migrate-N was greater than recent migration estimated with BayesAss, suggesting that populations were better connected in the past when habitat was less fragmented. MHC genetic differentiation was correlated with microsatellite differentiation (Mantel r = 0.431, P = 0.001) suggesting neutral genetic processes are influencing MHC evolution, and advantageous MHC alleles could be lost due to genetic drift.

Simulating the spread of selection-driven genotypes using landscape resistance models for desert bighorn sheep.

Landscape genetic studies based on neutral genetic markers have contributed to our understanding of the influence of landscape composition and configuration on gene flow and genetic variation. However, the potential for species to adapt to changing landscapes will depend on how natural selection influences adaptive genetic variation. We demonstrate how landscape resistance models can be combined with genetic simulations incorporating natural selection to explore how the spread of adaptive variation is affected by landscape characteristics, using desert bighorn sheep (Ovis canadensis nelsoni) in three differing regions of the southwestern United States as an example. We conducted genetic sampling and least-cost path modeling to optimize landscape resistance models independently for each region, and then simulated the spread of an adaptive allele favored by selection across each region. Optimized landscape resistance models differed between regions with respect to landscape variables included and their relationships to resistance, but the slope of terrain and the presence of water barriers and major roads had the greatest impacts on gene flow. Genetic simulations showed that differences among landscapes strongly influenced spread of adaptive genetic variation, with faster spread (1) in landscapes with more continuously distributed habitat and (2) when a pre-existing allele (i.e., standing genetic variation) rather than a novel allele (i.e., mutation) served as the source of adaptive genetic variation. The combination of landscape resistance models and genetic simulations has broad conservation applications and can facilitate comparisons of adaptive potential within and between landscapes.

Genes and Group Membership Predict Gidgee Skink (Egernia stokesii) Reproductive Pairs.

Due to their role in mate choice, disease resistance and kin recognition, genes of the major histocompatibility complex (MHC) are good candidates for investigating genetic-based mate choice. MHC-based mate choice is context dependent and influenced by many factors including social structure. Social structure diversity makes the Egernia group of lizards suitable for comparative studies of MHC-based mate choice. We investigated mate choice in the gidgee skink (Egernia stokesii), a lizard that exhibits high levels of social group and spatial stability. Group membership was incorporated into tests of the good genes as heterozygosity and compatible genes hypotheses for adaptive (MHC) and neutral (microsatellite) genetic diversity (n = 47 individuals genotyped). Females were more likely to pair with a male with higher MHC diversity and with whom they had a lower degree of microsatellite relatedness. Males were more likely to pair with a female with higher microsatellite heterozygosity and with whom they shared a lower proportion of MHC alleles. Lizards were more likely to mate with an individual from within, rather than outside, their social group, which confirmed earlier findings for this species and indicated mate choice had already largely occurred prior to either social group formation or acceptance of an individual into an existing group. Thus, a combination of genes and group membership, rather than group membership alone, predicted mate choice in this species. This work will contribute to an enhanced understanding of squamate group formation and a deeper understanding of the evolution of sociality within all vertebrates.

Landscape Population Genomics of Forsythia (Forsythia suspensa) Reveal That Ecological Habitats Determine the Adaptive Evolution of Species.

Understanding the genetic mechanisms of adaptation to environmental variables is a key concern in molecular ecology and evolutionary biology. Determining the adaptive evolutionary direction and evaluating the adaptation status of species can improve our understanding of these mechanisms. In this study, we sampled 20 populations of Forsythia suspensa to infer the relationship between environmental variables and adaptive genetic variations. Population structure analysis revealed that four genetic groups of F. suspensa exist resulting from divergent selection driven by seven environmental variables. A total of 26 outlier loci were identified by both BayeScan and FDIST2, 23 of which were environment-associated loci (EAL). Environmental association analysis revealed that the environmental variables related to the ecological habitats of F. suspensa are associated with high numbers of EAL. Results of EAL characterization in F. suspensa are consistent with the hypothesis that ecological habitats determine the adaptive evolution of this species. Moreover, a model of species adaptation to environmental variables was proposed in this study. The adaptation model was used to further evaluate the adaptation status of F. suspensa to environmental variables. This study will be useful to help us in understanding the adaptive evolution of species in regions lacking strong selection pressure.

Selection and genetic drift in captive versus wild populations: an assessment of neutral and adaptive (MHC-linked) genetic variation in wild and hatchery brown trout (Salmo trutta) populations

Captive bred individuals are often released into natural environments to supplement resident populations. Captive bred salmonid fishes often exhibit lower survival rates than their wild brethren and stocking measures may have a negative influence on the overall fitness of natural populations. Stocked fish often stem from a different evolutionary lineage than the resident population and thus may be maladapted for life in the wild, but this phenomenon has also been linked to genetic changes that occur in captivity. In addition to overall loss of genetic diversity via captive breeding, adaptation to captivity has become a major concern. Altered selection pressure in captivity may favour alleles at adaptive loci like the Major Histocompatibility Complex (MHC) that are maladaptive in natural environments. We investigated neutral and MHC-linked genetic variation in three autochthonous and three hatchery populations of Austrian brown trout (Salmo trutta). We confirm a positive selection pressure acting on the MHC II β locus, whereby the signal for positive selection was stronger in hatchery versus wild populations. Additionally, diversity at the MHC II β locus was higher, and more uniform among hatchery samples compared to wild populations, despite equal levels of diversity at neutral loci. We postulate that this stems from a combination of stronger genetic drift and a weakening of positive selection at this locus in wild populations that already have well adapted alleles for their specific environments.

Can MHC-assortative partner choice promote offspring diversity? A new combination of MHC-dependent behaviours among sexes in a highly successful invasive mammal.

Sexual selection involving genetically disassortative mate choice is one of several evolutionary processes that can maintain or enhance population genetic variability. Examples of reproductive systems in which choosers (generally females) select mates depending on their major histocompatibility complex (MHC) genes have been reported for several vertebrate species. Notably, the role of MHC-dependent choice not in mating contexts, but in other kinds of social interactions such as in the establishment of complex social systems, has not yet drawn significant scientific interest and is virtually absent from the literature. We have investigated male and female MHC-dependent choice in an invasive population of North American raccoons (Procyon lotor) in Germany. Both male and female raccoons rely on olfaction for individual recognition. Males have an unusually complex social system in which older individuals choose unrelated younger ones to form stable male coalitions that defend territories and a monopoly over females. We have confirmed that females perform MHC-disassortative mate choice and that this behaviour fosters genetic diversity of offspring. We have also observed that males build coalitions by choosing male partners depending on their MHC, but in an assortative manner. This is the first observation of antagonistic MHC-dependent behaviours among sexes. We show that this is the only combination of MHC-dependent partner choice that leads to outbreeding. In the case of introduced raccoons, such behaviours can act together to promote the invasive potential of the species by increasing its adaptive genetic divergence.

Climate drives adaptive genetic responses associated with survival in big sagebrush (Artemisia tridentata).

A genecological approach was used to explore genetic variation for survival in Artemisia tridentata (big sagebrush). Artemisia tridentata is a widespread and foundational shrub species in western North America. This species has become extremely fragmented, to the detriment of dependent wildlife, and efforts to restore it are now a land management priority. Common‐garden experiments were established at three sites with seedlings from 55 source‐populations. Populations included each of the three predominant subspecies, and cytotype variations. Survival was monitored for 5 years to assess differences in survival between gardens and populations. We found evidence of adaptive genetic variation for survival. Survival within gardens differed by source‐population and a substantial proportion of this variation was explained by seed climate of origin. Plants from areas with the coldest winters had the highest levels of survival, while populations from warmer and drier sites had the lowest levels of survival. Survival was lowest, 36%, in the garden that was prone to the lowest minimum temperatures. These results suggest the importance of climatic driven genetic differences and their effect on survival. Understanding how genetic variation is arrayed across the landscape, and its association with climate can greatly enhance the success of restoration and conservation.

Nucleotide polymorphisms associated with climate, phenology and physiological traits in European beech (Fagus sylvatica L.)

Although European beech (Fagus sylvatica L.) is one of the most widespread and ecologically and commercially most important deciduous trees in Europe, little is known about its adaptive genetic variation. We explored single-nucleotide polymorphism (SNP) variation in candidate genes for budburst and drought resistance in beech populations sampled across most of the distribution range, represented in an international provenance trial. SNP variation was monitored for six candidate genes, in 114 individuals from 19 natural populations. Population structure was deduced from the analysis of 20 nuclear microsatellite markers. Different methods to detect imprints of natural selection were used (F ST-outlier, SNP-climate regression, association tests). The F ST-outlier approach identified the COV gene with unambiguous signal of selection, which is an orthologue of Arabidopsis gene for a membrane protein previously reported as phenology-related. Based on environmental association analysis at the population level, the dehydrin gene was found associated with drought-related climatic variables. At the individual level, dehydrin gene also showed a significant association with chlorophyll fluorescence parameters, which are considered stress markers. The importance of the knowledge of physiological variation and geographical patterns of adaptive genetic variation for guiding reproductive materials transfer under climate change is stressed.

Primer development for amplification of toll-like genes for the assessment of adaptive genetic diversity in vulnerable grassland bird species

Assessing genetic diversity in species of conservation concern is a critical parameter to implement management plans that may increase their viability. Traditionally, genetic diversity has been assessed using neutral genes; nevertheless, recent perspectives have proposed that genetic variation under natural selection (adaptive genes) is more representative of the adaptive potential of a population or species. Toll-like receptors (TLR) are an innate immune gene family that binds to Pathogen Associated Molecular Patterns. These receptors evolved under positive selection and by coevolution; therefore, they represent adaptive genetic diversity. We designed and tested six pairs of primers that amplify TLR genes in seven grassland species, one of the most vulnerable North American bird groups. Analysis of the sequences showed that all were polymorphic and evolved under positive selection, with the exception of TLR3, which evolved neutrally. These primers may constitute a useful tool for conservation studies for grassland sparrow species.

Temporal and spatial instability in neutral and adaptive (MHC) genetic variation in marginal salmon populations

The role of marginal populations for the long-term maintenance of species’ genetic diversity and evolutionary potential is particularly timely in view of the range shifts caused by climate change. The Centre-Periphery hypothesis predicts that marginal populations should bear reduced genetic diversity and have low evolutionary potential. We analysed temporal stability at neutral microsatellite and adaptive MHC genetic variation over five decades in four marginal Atlantic salmon populations located at the southern limit of the species’ distribution with a complicated demographic history, which includes stocking with foreign and native salmon for at least 2 decades. We found a temporal increase in neutral genetic variation, as well as temporal instability in population structuring, highlighting the importance of temporal analyses in studies that examine the genetic diversity of peripheral populations at the margins of the species’ range, particularly in face of climate change.