Genetic Architecture Of Adaptive Traits Research Articles

Community-wide genome sequencing reveals 30 years of Darwin's finch evolution.

A fundamental goal in evolutionary biology is to understand the genetic architecture of adaptive traits. Using whole-genome data of 3955 of Darwin's finches on the Galápagos Island of Daphne Major, we identified six loci of large effect that explain 45% of the variation in the highly heritable beak size of Geospiza fortis, a key ecological trait. The major locus is a supergene comprising four genes. Abrupt changes in allele frequencies at the loci accompanied a strong change in beak size caused by natural selection during a drought. A gradual change in Geospiza scandens occurred across 30 years as a result of introgressive hybridization with G. fortis. This study shows how a few loci with large effect on a fitness-related trait contribute to the genetic potential for rapid adaptive radiation.

Teasing apart the joint effect of demography and natural selection in the birth of a contact zone.

Vast population movements induced by recurrent climatic cycles have shaped the genetic structure of plant species. During glacial periods species were confined to low-latitude refugia from which they recolonized higher latitudes as the climate improved. This multipronged recolonization led to many lineages that later met and formed large contact zones. We utilize genomic data from 5000 Picea abies trees to test for the presence of natural selection during recolonization and establishment of a contact zone in Scandinavia. Scandinavian P. abies is today made up of a southern genetic cluster originating from the Baltics, and a northern one originating from Northern Russia. The contact zone delineating them closely matches the limit between two major climatic regions. We show that natural selection contributed to its establishment and maintenance. First, an isolation-with-migration model with genome-wide linked selection fits the data better than a purely neutral one. Second, many loci show signatures of selection or are associated with environmental variables. These loci, regrouped in clusters on chromosomes, are often related to phenology. Altogether, our results illustrate how climatic cycles, recolonization and selection can establish strong local adaptation along contact zones and affect the genetic architecture of adaptive traits.

Divergent Allometric Trajectories in Gene Expression and Coexpression Produce Species Differences in Sympatrically Speciating Midas Cichlid Fish.

The mechanisms of speciation without geographic isolation (i.e., sympatric speciation) remain debated. This is due in part to the fact that the genomic landscape that could promote or hinder species divergence in the presence of gene flow is still largely unknown. However, intensive research is now centered on understanding the genetic architecture of adaptive traits associated with this process as well as how gene expression might affect these traits. Here, using RNA-Seq data, we investigated gene expression of sympatrically speciating benthic and limnetic Neotropical cichlid fishes at two developmental stages. First, we identified groups of coexpressed genes (modules) at each stage. Although there are a few large and well-preserved modules, most of the other modules are not preserved across life stages. Second, we show that later in development more and larger coexpression modules are associated with divergence between benthic and limnetic fish compared with the earlier life stage. This divergence between benthic and limnetic fish in coexpression mirrors divergence in overall expression between benthic and limnetic fish, which is more pronounced later in life. Our results reveal that already at 1-day posthatch benthic and limnetic fish diverge in (co)expression, and that this divergence becomes more substantial when fish are free-swimming but still unlikely to have divergent swimming and feeding habits. More importantly, our study describes how the coexpression of several genes through development, as opposed to individual genes, is associated with benthic–limnetic species differences, and how two morphogenetic trajectories diverge as fish grow older.

Genetic redundancy fuels polygenic adaptation in Drosophila.

The genetic architecture of adaptive traits is of key importance to predict evolutionary responses. Most adaptive traits are polygenic—i.e., result from selection on a large number of genetic loci—but most molecularly characterized traits have a simple genetic basis. This discrepancy is best explained by the difficulty in detecting small allele frequency changes (AFCs) across many contributing loci. To resolve this, we use laboratory natural selection to detect signatures for selective sweeps and polygenic adaptation. We exposed 10 replicates of a Drosophila simulans population to a new temperature regime and uncovered a polygenic architecture of an adaptive trait with high genetic redundancy among beneficial alleles. We observed convergent responses for several phenotypes—e.g., fitness, metabolic rate, and fat content—and a strong polygenic response (99 selected alleles; mean s = 0.059). However, each of these selected alleles increased in frequency only in a subset of the evolving replicates. We discerned different evolutionary paradigms based on the heterogeneous genomic patterns among replicates. Redundancy and quantitative trait (QT) paradigms fitted the experimental data better than simulations assuming independent selective sweeps. Our results show that natural D. simulans populations harbor a vast reservoir of adaptive variation facilitating rapid evolutionary responses using multiple alternative genetic pathways converging at a new phenotypic optimum. This key property of beneficial alleles requires the modification of testing strategies in natural populations beyond the search for convergence on the molecular level.

Single-Locus versus Multilocus Patterns of Local Adaptation to Climate in Eastern White Pine (Pinus strobus, Pinaceae).

Natural plant populations are often adapted to their local climate and environmental conditions, and populations of forest trees offer some of the best examples of this pattern. However, little empirical work has focused on the relative contribution of single-locus versus multilocus effects to the genetic architecture of local adaptation in plants/forest trees. Here, we employ eastern white pine (Pinus strobus) to test the hypothesis that it is the inter-genic effects that primarily drive climate-induced local adaptation. The genetic structure of 29 range-wide natural populations of eastern white pine was determined in relation to local climatic factors using both a reference set of SSR markers, and SNPs located in candidate genes putatively involved in adaptive response to climate. Comparisons were made between marker sets using standard single-locus outlier analysis, single-locus and multilocus environment association analyses and a novel implementation of Population Graphs. Magnitudes of population structure were similar between the two marker sets. Outlier loci consistent with diversifying selection were rare for both SNPs and SSRs. However, genetic distances based on the multilocus among population covariances (cGD) were significantly more correlated to climate, even after correcting for spatial effects, for SNPs as compared to SSRs. Coalescent simulations confirmed that the differences in mutation rates between SSRs and SNPs did not affect the topologies of the Population Graphs, and hence values of cGD and their correlations with associated climate variables. We conclude that the multilocus covariances among populations primarily reflect adaptation to local climate and environment in eastern white pine. This result highlights the complexity of the genetic architecture of adaptive traits, as well as the need to consider multilocus effects in studies of local adaptation.

Utility of closely related taxa for genetic studies of adaptive variation and speciation: Current state and perspectives in plants with focus on forest tree species

AbstractStudies of adaptation and speciation have greatly benefited from rapid progress of DNA sequencing and genotyping technologies. Comparative genomics of closely related taxa has great potential to advance evolutionary research on genetic architecture of adaptive traits and reproductive isolation. Such studies that utilized closely related plant species and ecotypes have already provided some important insights into genomic regions and/or genes that are potentially involved in local adaptation and speciation. The choice of an appropriate species model for such research is crucial. The paper discusses current approaches used to reveal the patterns of intra‐ and interspecific divergence due to natural selection. Its outcomes in herbaceous plants and forest trees are briefly summarized and compared to reveal general regularities concerning evolutionary processes. We then highlight the importance of multispecies studies and discuss the utility of several related pine taxa as fine candidates for evolutionary inferences. Genetically similar but ecologically and phenotypically diverged taxa seem a promising study system to search for genomic patterns of speciation and adaptive variation.

Fifteen years of genomewide scans for selection: trends, lessons and unaddressed genetic sources of complication.

Genomewide scans for natural selection (GWSS) have become increasingly common over the last 15 years due to increased availability of genome-scale genetic data. Here, we report a representative survey of GWSS from 1999 to present and find that (i) between 1999 and 2009, 35 of 49 (71%) GWSS focused on human, while from 2010 to present, only 38 of 83 (46%) of GWSS focused on human, indicating increased focus on nonmodel organisms; (ii) the large majority of GWSS incorporate interpopulation or interspecific comparisons using, for example F(ST), cross-population extended haplotype homozygosity or the ratio of nonsynonymous to synonymous substitutions; (iii) most GWSS focus on detection of directional selection rather than other modes such as balancing selection; and (iv) in human GWSS, there is a clear shift after 2004 from microsatellite markers to dense SNP data. A survey of GWSS meant to identify loci positively selected in response to severe hypoxic conditions support an approach to GWSS in which a list of a priori candidate genes based on potential selective pressures are used to filter the list of significant hits a posteriori. We also discuss four frequently ignored determinants of genomic heterogeneity that complicate GWSS: mutation, recombination, selection and the genetic architecture of adaptive traits. We recommend that GWSS methodology should better incorporate aspects of genomewide heterogeneity using empirical estimates of relevant parameters and/or realistic, whole-chromosome simulations to improve interpretation of GWSS results. Finally, we argue that knowledge of potential selective agents improves interpretation of GWSS results and that new methods focused on correlations between environmental variables and genetic variation can help automate this approach.

Conservatism and novelty in the genetic architecture of adaptation in Heliconius butterflies.

Understanding the genetic architecture of adaptive traits has been at the centre of modern evolutionary biology since Fisher; however, evaluating how the genetic architecture of ecologically important traits influences their diversification has been hampered by the scarcity of empirical data. Now, high-throughput genomics facilitates the detailed exploration of variation in the genome-to-phenotype map among closely related taxa. Here, we investigate the evolution of wing pattern diversity in Heliconius, a clade of neotropical butterflies that have undergone an adaptive radiation for wing-pattern mimicry and are influenced by distinct selection regimes. Using crosses between natural wing-pattern variants, we used genome-wide restriction site-associated DNA (RAD) genotyping, traditional linkage mapping and multivariate image analysis to study the evolution of the architecture of adaptive variation in two closely related species: Heliconius hecale and H. ismenius. We implemented a new morphometric procedure for the analysis of whole-wing pattern variation, which allows visualising spatial heatmaps of genotype-to-phenotype association for each quantitative trait locus separately. We used the H. melpomene reference genome to fine-map variation for each major wing-patterning region uncovered, evaluated the role of candidate genes and compared genetic architectures across the genus. Our results show that, although the loci responding to mimicry selection are highly conserved between species, their effect size and phenotypic action vary throughout the clade. Multilocus architecture is ancestral and maintained across species under directional selection, whereas the single-locus (supergene) inheritance controlling polymorphism in H. numata appears to have evolved only once. Nevertheless, the conservatism in the wing-patterning toolkit found throughout the genus does not appear to constrain phenotypic evolution towards local adaptive optima.

Genome-wide association mapping of phenotypic traits subject to a range of intensities of natural selection in Timema cristinae.

The genetic architecture of adaptive traits can reflect the evolutionary history of populations and also shape divergence among populations. Despite this central role in evolution, relatively little is known regarding the genetic architecture of adaptive traits in nature, particularly for traits subject to known selection intensities. Here we quantitatively describe the genetic architecture of traits that are subject to known intensities of differential selection between host plant species in Timema cristinae stick insects. Specifically, we used phenotypic measurements of 10 traits and 211,004 single-nucleotide polymorphisms (SNPs) to conduct multilocus genome-wide association mapping. We identified a modest number of SNPs that were associated with traits and sometimes explained a large proportion of trait variation. These SNPs varied in their strength of association with traits, and both major and minor effect loci were discovered. However, we found no relationship between variation in levels of divergence among traits in nature and variation in parameters describing the genetic architecture of those same traits. Our results provide a first step toward identifying loci underlying adaptation in T. cristinae. Future studies will examine the genomic location, population differentiation, and response to selection of the trait-associated SNPs described here.

Ecological genomics of local adaptation

It is increasingly important to improve our understanding of the genetic basis of local adaptation because of its relevance to climate change, crop and animal production, and conservation of genetic resources. Phenotypic patterns that are generated by spatially varying selection have long been observed, and both genetic mapping and field experiments provided initial insights into the genetic architecture of adaptive traits. Genomic tools are now allowing genome-wide studies, and recent theoretical advances can help to design research strategies that combine genomics and field experiments to examine the genetics of local adaptation. These advances are also allowing research in non-model species, the adaptation patterns of which may differ from those of traditional model species.

MATING SYSTEM, HALDANE'S SIEVE, AND THE DOMESTICATION PROCESS

Mating systems are expected to have a strong influence on both the dynamic of adaptation and the genetic architecture of adaptive traits. In particular, the bias toward the fixation of dominant or partially dominant beneficial mutations predicted under outcrossing (Haldane's sieve) is expected to be reduced under self-fertilization. To test this prediction in plants, we considered domestication as an example of adaptation. We compiled data from studies reporting the degree of dominance of quantitative trait loci (QTL) involved in the domestication syndrome. We found that adaptation to cultivation mostly proceeded through the selection of recessive and partially recessive genes in predominantly selfing species whereas a much larger fraction of domestication-related QTL were dominant or partially dominant in outcrossers, as expected under Haldane's sieve. Our study also showed that levels of dominance in mixed mating crop species resemble those observed in selfers, suggesting that recessive alleles can contribute to adaptation even under moderate selfing rates. Although these results rely on a particular example of adaptation, they constitute one of the first attempts to test theoretical expectations on the level of dominance of genes involved in plant adaptation.

From adaptation to molecular evolution

There have been an increasing number of calls in recent years for a ‘post-modern' synthesis of evolutionary biology, extending the modern synthesis of the 40–50's by including molecular aspects of development (evo–devo), phenotypic plasticity driving genetic evolution, or epigenetic inheritance (for example, Pigliucci, 2007). This illustrates an infusion of evolutionary thinking into all aspects of modern biology, creating a need for integrative approaches and increased exchange between complementary fields. These calls often go along with a healthy questioning of orthodoxy in the light of current empirical evidence. However, alternatives should be scrutinized with as much skepticism as the mainstream theory they aim to replace or improve. We need to ask whether each theory—Neo-Darwinism or the proposed alternative—is sufficient to explain observed patterns, not whether it is necessary. That some observed patterns could be due to another process does not argue against Neo-Darwinism, if this other process is not a sufficient explanation in other situations. As an analogy, relativity theory is not always necessary to explain the motion of particles, but it is sufficient to account for all known mechanics, whereas Newton's theory is not. Interpreting the enormous amount of emerging molecular data requires such an integrative approach. To use these data to infer population processes behind patterns of adaptation, we need models that describe how natural selection operates on traits, how this translates into changes in nucleotide sequences, and whether unique molecular signatures can be detected under alternative, plausible scenarios. In a recent paper in this journal, Hughes (2011) argues that, because current statistical approaches fail to reliably detect strong evidence of positive selection at the molecular level (while they reveal substantial evidence of purifying selection), we need to explain the origin of adaptation at the phenotypic level by a process other than the Neo-Darwinian one, that is, cumulative substitutions of beneficial mutations. Specifically, he proposes that adaptation may arise when ancestral phenotypic plasticity in a variable environment is lost in a more homogeneous environment by the accumulation of deleterious mutations under relaxed selection (the plasticity–relaxation–mutation hypothesis, or PRM). He suggests that most evolutionists have overlooked this alternative explanation, because it does not fit their Neo-Darwinian understanding of adaptation. We hold that the PRM hypothesis is neither a more parsimonious hypothesis, nor one more consistent with data, than the Neo-Darwinian mode of adaptation. Patterns of molecular evolution can agree well with predictions from the Neo-Darwinian view of adaptation, provided we use more explicit models for phenotypic selection in a new environment and for the genetic architecture of adaptive traits.

Ecological genetics of freshwater fish: a short review of the genotype–phenotype connection

Molecular ecology or ecological genetics is an expanding application of population genetics which has flourished in the last two decades but it is dominated by systematic and phylogeographic studies, with relatively little emphasis on the study of the genetic basis of the process of adaptation to different ecological conditions. The relationship between genotype and adaptive phenotypes is weak because populations are often difficult to quantify and experiments are logistically challenging or unfeasible. Interestingly, in freshwater fish, studies to characterize the genetic architecture of adaptive traits are not as rare as in other vertebrate groups. In this review, we summarize the few cases where the relationship between the ecology and genetics of freshwater fish is more developed, namely the relationship between genetic markers and ecological phenotypes.

Darwinism renewed: contemporary studies of plant adaptation

Darwinism renewed: contemporary studies of plant adaptation

A microarray's view of life in the desert: adding a powerful evolutionary genomics tool to the packrat's midden

Identifying the genetic architecture of adaptive traits is fundamental to understanding how organisms respond to their environment, over both ecological and evolutionary timeframes. Microarray technology that allows us to capture the simultaneous expression of thousands of genes provides unparalleled insight into how organisms cope with their environment at the transcriptional level. Recent studies in Molecular Ecology demonstrate how microarrays can rapidly identify which genes and pathways allow organisms to face some of the most fundamental physiological challenges posed by the environment, including compensation for the hypoxic and thermal stress of high-altitudes (Cheviron et al. 2008) and, in this issue, the biotransformation of toxic plant secondary compounds by mammals (Magnanou et al. 2009). Microarrays (Ekins et al. 1989; Fodor et al. 1991) are glass slides affixed with hundreds to thousands of oligonucleotide or cDNA sequences (probes). Messenger RNA transcripts (typically reverse transcribed to cDNA) are isolated from a tissue/sample of interest and hybridized to the array. Binding to specific probes indicates that a particular gene was transcriptionally active at or near the time of sampling and thus provides a potentially comprehensive measure of gene expression. Although a tremendously powerful tool, commercially produced oligonucleotide arrays are only available for a handful of model organisms. Nonetheless, evolutionary ecologists have exploited this resource by using a cross-species hybridization approach (e.g. Saetre et al. 2004), that is, hybridizing a model organism array with a nonmodel sample (Bar-Or et al. 2007). Magnanou et al. (2009) present a novel example of using a model muroid microarray (Agilent Technologies, Rattus) to study physiological response in a wild, nonmodel muroid, Neotoma.