scholarly journals The genetic architecture of temperature adaptation is shaped by population ancestry and not by selection regime

2021 ◽  
Vol 22 (1) ◽  
Author(s):  
Kathrin A. Otte ◽  
Viola Nolte ◽  
François Mallard ◽  
Christian Schlötterer
Keyword(s):  
Genetic Architecture ◽  
Natural Populations ◽  
Temperature Adaptation ◽  
Recent Analysis ◽  
Founder Population ◽  
Selection Regime ◽  
Hot Environment ◽  
Adaptive Architecture ◽  
Founder Populations ◽  
Large Heterogeneity

Abstract Background Understanding the genetic architecture of temperature adaptation is key for characterizing and predicting the effect of climate change on natural populations. One particularly promising approach is Evolve and Resequence, which combines advantages of experimental evolution such as time series, replicate populations, and controlled environmental conditions, with whole genome sequencing. Recent analysis of replicate populations from two different Drosophila simulans founder populations, which were adapting to the same novel hot environment, uncovered very different architectures—either many selection targets with large heterogeneity among replicates or fewer selection targets with a consistent response among replicates. Results Here, we expose the founder population from Portugal to a cold temperature regime. Although almost no selection targets are shared between the hot and cold selection regime, the adaptive architecture was similar. We identify a moderate number of targets under strong selection (19 selection targets, mean selection coefficient = 0.072) and parallel responses in the cold evolved replicates. This similarity across different environments indicates that the adaptive architecture depends more on the ancestry of the founder population than the specific selection regime. Conclusions These observations will have broad implications for the correct interpretation of the genomic responses to a changing climate in natural populations.

scholarly journals The adaptive architecture is shaped by population ancestry and not by selection regime

2020 ◽  
Author(s):  
Kathrin A. Otte ◽  
Viola Nolte ◽  
François Mallard ◽  
Christian Schlötterer
Keyword(s):  
Evolutionary Biology ◽  
Natural Populations ◽  
Recent Analysis ◽  
Founder Population ◽  
Selection Regime ◽  
Hot Environment ◽  
Adaptive Architecture ◽  
Founder Populations ◽  
Large Heterogeneity ◽  
Consistent Response

AbstractUnderstanding the genetic architecture of adaptive phenotypes is a key question in evolutionary biology. One particularly promising approach is Evolve and Resequence (E&R), which combines advantages of experimental evolution such as time series, replicate populations and controlled environmental conditions, with whole genome sequencing. The recent analysis of replicate populations from two different Drosophila simulans founder populations, which were adapting to the same novel hot environment, uncovered very different architectures - either many selection targets with large heterogeneity among replicates or fewer selection targets with a consistent response among replicates. Here, we exposed the founder population from Portugal to a cold temperature regime. Although almost no selection targets were shared between the hot and cold selection regime, the adaptive architecture was similar: we identified a moderate number of loci under strong selection (19 selected alleles, mean selection coefficient = 0.072) and very parallel responses in the cold evolved replicates. This similarity across different environments indicates that the adaptive architecture depends more on the ancestry of the founder population than the specific selection regime. These observations have a pronounced impact on our understanding of adaptation in natural populations.

scholarly journals Heritability of DNA methylation in threespine stickleback (Gasterosteus aculeatus)

Genetics ◽  
2021 ◽  
Vol 217 (1) ◽  
Author(s):  
Juntao Hu ◽  
Sara J S Wuitchik ◽  
Tegan N Barry ◽  
Heather A Jamniczky ◽  
Sean M Rogers ◽  
...  
Keyword(s):  
Dna Methylation ◽  
Genetic Architecture ◽  
Gasterosteus Aculeatus ◽  
Additive Genetic Variance ◽  
Natural Populations ◽  
Threespine Stickleback ◽  
Phenotypic Change ◽  
Cpg Sites ◽  
Cis And Trans ◽  
Methylation Variation

Abstract Epigenetic mechanisms underlying phenotypic change are hypothesized to contribute to population persistence and adaptation in the face of environmental change. To date, few studies have explored the heritability of intergenerationally stable methylation levels in natural populations, and little is known about the relative contribution of cis- and trans-regulatory changes to methylation variation. Here, we explore the heritability of DNA methylation, and conduct methylation quantitative trait loci (meQTLs) analysis to investigate the genetic architecture underlying methylation variation between marine and freshwater ecotypes of threespine stickleback (Gasterosteus aculeatus). We quantitatively measured genome-wide DNA methylation in fin tissue using reduced representation bisulfite sequencing of F1 and F2 crosses, and their marine and freshwater source populations. We identified cytosines (CpG sites) that exhibited stable methylation levels across generations. We found that additive genetic variance explained an average of 24–35% of the methylation variance, with a number of CpG sites possibly autonomous from genetic control. We also detected both cis- and trans-meQTLs, with only trans-meQTLs overlapping with previously identified genomic regions of high differentiation between marine and freshwater ecotypes. Finally, we identified the genetic architecture underlying two key CpG sites that were differentially methylated between ecotypes. These findings demonstrate a potential role for DNA methylation in facilitating adaptation to divergent environments and improve our understanding of the heritable basis of population epigenomic variation.

Genetic architecture and adaptive landscape of interior lodgepole pine (Pinuscontorta ssp. latifolia) in Canada

1995 ◽  
Vol 25 (12) ◽  
pp. 2010-2021 ◽  
Author(s):  
Chang-Yi Xie ◽  
Cheng C. Ying
Keyword(s):  
Genetic Variation ◽  
Central Region ◽  
Population Differentiation ◽  
Genetic Architecture ◽  
Lodgepole Pine ◽  
Natural Populations ◽  
High Elevation ◽  
Population Variation ◽  
Adaptive Landscape ◽  
Growth And Survival

The genetic architecture and adaptive landscape of interior lodgepole pine (Pinuscontorta ssp. latifolia Engelm. ex S. Wats.) in Canada were investigated in a provenance–family plantation located in central British Columbia. Fifty-three natural populations were sampled from three geographic regions covering the entire Canadian range, and their performance in growth and survival was recorded periodically over 20 years. Test results indicate that genetic variation among regions and among populations within regions was highly significant in all the traits investigated and accounted for, respectively, 53% and 41% of the total genetic variation in growth and 41% and 54% in survival. Within-population variation was also significant in growth but not in survival. Interior lodgepole pine in the central region demonstrated less genetic variation than in the northern and southern regions at both the population and family levels. In addition, the proportion of genetic variation associated with population was lower in the central region than in the other regions. Population differentiation in both growth and survival showed discernible elevational and geographic patterns. Regression models describing these adaptive patterns accounted for more than 80% of the among-population variation, and their veracity was verified with independent data. Populations of northern, coastal–interior transition, and high-elevation origin tended to have smaller trees with higher mortality. However, the patterns were not linear but differed in slope and (or) direction among regions. The adaptedness of populations tended to decrease as they were farther away from their origin, with a few exceptions displaying broad adaptation across more than 3° of latitude. As the test proceeded, population differentiation became more evident and adaptive clines became steeper. Some practical implications of these findings have been discussed.

scholarly journals The genetic architecture of helminth-specific immune responses in a wild population of Soay sheep (Ovis aries)

2019 ◽  
Author(s):  
A. M. Sparks ◽  
K. Watt ◽  
R. Sinclair ◽  
J. G. Pilkington ◽  
J. M. Pemberton ◽  
...  
Keyword(s):  
Immune Responses ◽  
Genetic Architecture ◽  
Wild Population ◽  
Natural Populations ◽  
Natural Conditions ◽  
Soay Sheep ◽  
Histocompatibility Complex ◽  
Immune Traits ◽  
Antibody Levels ◽  
Host Parasite

AbstractHost-parasite interactions are powerful drivers of evolutionary and ecological dynamics in natural populations. Variation in immune responses to infection is likely to shape the outcome of these interactions, with important consequences for the fitness of both host and parasite. However, little is known about how genetic variation contributes to variation in immune responses under natural conditions. Here, we examine the genetic architecture of variation in immune traits in the Soay sheep of St Kilda, an unmanaged population of sheep infected with strongyle gastrointestinal nematodes. We assayed IgA, IgE and IgG antibodies against the prevalent nematodeTeladorsagia circumcinctain the blood plasma of > 3,000 sheep collected over 26 years. Antibody levels were significantly heritable, ranging from 0.21 to 0.39 in lambs and from 0.23 to 0.57 in adults. IgA levels were strongly associated with a region on chromosome 24 explaining 21.1% and 24.5% of heritable variation in lambs and adults, respectively; this region was adjacent to two candidate loci, the Class II Major Histocompatibility Complex Transactivator (CIITA) and C-Type Lectin Domain Containing 16A (CLEC16A). Lamb IgA levels were also associated with the immunoglobulin heavy constant loci (IGH) complex on chromosome 18. Adult IgE levels and lamb IgG levels were associated with the major histocompatibility complex (MHC) on chromosome 20. This study provides evidence of high heritability of a complex immunological trait under natural conditions and provides the first evidence from a genome-wide study that large effect genes located outside the MHC region exist for immune traits in the wild.Author summaryHost-parasite interactions are powerful drivers of evolutionary and ecological dynamics in natural populations. Variation in immune responses to infection shapes the outcome of these interactions, with important consequences for the ability of the host and parasite to survive and reproduce. However, little is known about how much genes contribute to variation in immune responses under natural conditions. Our study investigates the genetic architecture of variation in three antibody types, IgA, IgE and IgG in a wild population of Soay sheep on the St Kilda archipelago in North-West Scotland. Using data collected over 26 years, we show that antibody levels have a heritable basis in lambs and adults and are stable over lifetime of individuals. We also identify several genomic regions with large effects on immune responses. Our study offers the first insights into the genetic control of immunity in a wild population, which is essential to understand how immune profiles vary in challenging natural conditions and how natural selection maintains genetic variation in complex immune traits.

scholarly journals The Genetic Architecture of Larval Aggregation Behavior in Drosophila

2020 ◽  
Author(s):  
Ross M McKinney ◽  
Yehuda Ben-Shahar
Keyword(s):  
Genetic Architecture ◽  
Single Gene ◽  
Natural Populations ◽  
Genetic Network ◽  
Aggregation Behavior ◽  
Physiological Mechanisms ◽  
Genetic Components ◽  
Level Of Aggregation ◽  
First Time ◽  
Coding Snp

AbstractMany insect species exhibit basal social behaviors such as aggregation, which play important roles in their feeding and mating ecologies. However, the evolutionary, genetic, and physiological mechanisms that regulate insect aggregation remain unknown for most species. Here, we used natural populations of Drosophila melanogaster to identify the genetic architecture that drives larval aggregation feeding behavior. By using quantitative and reverse genetic approaches, we have identified a complex neurogenetic network that plays a role in regulating the decision of larvae to feed in either solitude or as a group. Results from single gene, RNAi-knockdown experiments show that several of the identified genes represent key nodes in the genetic network that determines the level of aggregation while feeding. Furthermore, we show that a single non-coding SNP in the gene CG14205, a putative acyltransferase, is associated with both decreased mRNA expression and increased aggregate formation, which suggests that it has a specific role in inhibiting aggregation behavior. Our results identify, for the first time, the genetic components which interact to regulate naturally occurring levels of aggregation in D. melanogaster larvae.

scholarly journals Evolution of polygenic traits under global vs local adaptation

Genetics ◽  
2022 ◽  
Vol 220 (1) ◽  
Author(s):  
Sam Yeaman
Keyword(s):  
Local Adaptation ◽  
Complex Traits ◽  
Genetic Architecture ◽  
Population Genomics ◽  
Natural Populations ◽  
Evolutionary Process ◽  
Frequency Effect ◽  
Theoretical Predictions ◽  
Using Data ◽  
And Migration

Abstract Observations about the number, frequency, effect size, and genomic distribution of alleles associated with complex traits must be interpreted in light of evolutionary process. These characteristics, which constitute a trait’s genetic architecture, can dramatically affect evolutionary outcomes in applications from agriculture to medicine, and can provide a window into how evolution works. Here, I review theoretical predictions about the evolution of genetic architecture under spatially homogeneous, global adaptation as compared with spatially heterogeneous, local adaptation. Due to the tension between divergent selection and migration, local adaptation can favor “concentrated” genetic architectures that are enriched for alleles of larger effect, clustered in a smaller number of genomic regions, relative to expectations under global adaptation. However, the evolution of such architectures may be limited by many factors, including the genotypic redundancy of the trait, mutation rate, and temporal variability of environment. I review the circumstances in which predictions differ for global vs local adaptation and discuss where progress can be made in testing hypotheses using data from natural populations and lab experiments. As the field of comparative population genomics expands in scope, differences in architecture among traits and species will provide insights into how evolution works, and such differences must be interpreted in light of which kind of selection has been operating.

scholarly journals Host-pathogen coevolution increases genetic variation in susceptibility to infection

2018 ◽  
Author(s):  
Elizabeth ML Duxbury ◽  
Jonathan P Day ◽  
Davide Maria Vespasiani ◽  
Yannik Thüringer ◽  
Ignacio Tolosana ◽  
...  
Keyword(s):  
Genetic Variation ◽  
Genetic Variants ◽  
Genetic Architecture ◽  
Natural Populations ◽  
Major Effect ◽  
Cross Infection ◽  
Host Susceptibility ◽  
Susceptibility To Infection ◽  
Host Parasite Interactions ◽  
Host Parasite

AbstractIt is common to find considerable genetic variation in susceptibility to infection in natural populations. We have investigated whether natural selection increases this variation by testing whether host populations show more genetic variation in susceptibility to pathogens that they naturally encounter than novel pathogens. In a large cross-infection experiment involving four species of Drosophila and four host-specific viruses, we always found greater genetic variation in susceptibility to viruses that had coevolved with their host. We went on to examine the genetic architecture of resistance in one host species, finding that there are more major-effect genetic variants in coevolved host-parasite interactions. We conclude that selection by pathogens increases genetic variation in host susceptibility, and much of this effect is caused by the occurrence of major-effect resistance polymorphisms within populations.

scholarly journals Pre- and post-mating reproductive isolation evolve independently during rapid adaptation to high temperature

2021 ◽  
Author(s):  
Sheng-Kai Hsu ◽  
Wei-Yun Lai ◽  
Johannes Novak ◽  
Felix Lehner ◽  
Ana Marija Jakšić ◽  
...  
Keyword(s):  
Reproductive Isolation ◽  
Natural Populations ◽  
Cuticular Hydrocarbon ◽  
Ecological Speciation ◽  
Temperature Adaptation ◽  
Rapid Adaptation ◽  
Epistatic Interactions ◽  
Males And Females ◽  
Altered Lipid Metabolism ◽  
Altered Lipid

Ambient temperature is one major ecological factor driving adaptation in natural populations, but its impact on the emergence of new species is not yet clear. Here, we explored the evolution of reproductive isolation during temperature adaptation by exposing 10 replicate Drosophila simulans populations to a hot temperature regime. Within less than 200 generations, both pre- and post-mating reproductive isolation evolved. The altered lipid metabolism of evolved flies also affected the cuticular hydrocarbon (CHCs) profiles. Different CHC profiles could explain the emerged assortative mating between ancestral and evolved populations. Hence, we identified the hallmark of ecological speciation driven by temperature adaptation. While this pre-mating isolation occurred only between ancestral and evolved replicate populations, post-mating reproductive isolation was observed among evolved replicate populations. We propose that epistatic interactions of reproduction-related genes between males and females resulted in adaptive co-evolution. Incompatibilities between different gene combinations favored in each replicate could explain the observed post-mating reproductive isolation. We anticipate that this mutation-order-like speciation from standing genetic variation, a new speciation process, is widespread in nature when highly polygenic traits are involved in adaptation.

scholarly journals Gene buddies: linked balanced polymorphisms reinforce each other even in the absence of epistasis

PeerJ ◽  
2018 ◽  
Vol 6 ◽  
pp. e5110 ◽  
Author(s):  
Jacob A. Tennessen
Keyword(s):  
Genetic Architecture ◽  
Evolutionary Dynamics ◽  
Balancing Selection ◽  
Natural Populations ◽  
Adaptive Variation ◽  
Recombination Rates ◽  
Future Studies ◽  
Close Physical Proximity ◽  
Selection For ◽  
Independent Effects

The fates of genetic polymorphisms maintained by balancing selection depend on evolutionary dynamics at linked sites. While coevolution across linked, epigenetically-interacting loci has been extensively explored, such supergenes may be relatively rare. However, genes harboring adaptive variation can occur in close physical proximity while generating independent effects on fitness. Here, I present a model in which two linked loci without epistasis are both under balancing selection for unrelated reasons. Using forward-time simulations, I show that recombination rate strongly influences the retention of adaptive polymorphism, especially for intermediate selection coefficients. A locus is more likely to retain adaptive variation if it is closely linked to another locus under balancing selection, even if the two loci have no interaction. Thus, two linked polymorphisms can both be retained indefinitely even when they would both be lost to drift if unlinked. While these results may be intuitive, they have important implications for genetic architecture: clusters of mutually reinforcing genes may underlie phenotypic variation in natural populations, and such genes cannot be assumed to be functionally associated. Future studies that measure selection coefficients and recombination rates among closely linked genes will be fruitful for characterizing the extent of this phenomenon.

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