A Simple Test Identifies Selection on Complex Traits

Beissinger, Tim; Kruppa, Jochen; Cavero, D.; Ha, Ngoc-Thuy; Erbe, Malena; Simianer, Henner

doi:10.1534/genetics.118.300857

Cited by 22 publications

(69 citation statements)

References 55 publications

(63 reference statements)

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“…We used LASSO SNPs as well as genome-wide quantile thresholds to conduct this analysis. We calculated a polygenic score [79, 80] by multiplying the clinal or seasonal effect size (including sign) by the GWAS effect size and sign and summing this product across all SNPs, all LASSO SNPs, the top 0.01% of the GWAS, or the top 0.1% of the GWAS (see S6 Table and Materials and Methods for details). In this test, we predict that concordant signal in the GWAS and the clinal/seasonal datasets should result in positive numbers that exceed permutations.…”

Section: Resultsmentioning

confidence: 99%

Unique genetic signatures of local adaptation over space and time for diapause, an ecologically relevant complex trait, inDrosophila melanogaster

Erickson

Weller

Song

et al. 2020

Preprint

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Organisms living in seasonally variable environments utilize cues such as light and temperature to induce plastic responses, enabling them to exploit favorable seasons and avoid unfavorable ones. Local adapation can result in variation in seasonal responses, but the genetic basis and evolutionary history of this variation remains elusive. Many insects, including Drosophila melanogaster, are able to undergo an arrest of reproductive development (diapause) in response to unfavorable conditions. In D. melanogaster, the ability to diapause is more common in high latitude populations, where flies endure harsher winters, and in the spring, reflecting differential survivorship of overwintering populations. Using a novel hybrid swarm-based genome wide association study, we examined the genetic basis and evolutionary history of ovarian diapause. We exposed outbred females to different temperatures and day lengths, characterized ovarian development for over 2800 flies, and reconstructed their complete, phased genomes. We found that diapause, scored at two different developmental cutoffs, has modest heritability, and we identified hundreds of SNPs associated with each of the two phenotypes. Alleles associated with one of the diapause phenotypes tend to be more common at higher latitudes, but these alleles do not show predictable seasonal variation. The collective signal of many small-effect, clinally varying SNPs can plausibly explain latitudinal variation in diapause seen in North America. Alleles associated with diapause are segregating at relatively high frequencies in Zambia, suggesting that variation in diapause relies on ancestral polymorphisms, and both pro- and anti-diapause alleles have experienced selection in North America. Finally, we utilized outdoor mesocosms to track diapause under natural conditions. We found that hybrid swarms reared outdoors evolved increased propensity for diapause in late fall, whereas indoor control populations experienced no such change. Our results indicate that diapause is a complex, quantitative trait with different evolutionary patterns across time and space.Author SummaryAnimals exhibit diverse strategies to cope with unfavorable conditions in temperate, seasonally varying environments. The model fly, Drosophila melanogaster, can enter a physiological state known as diapause under winter-like conditions. Diapause is characterized by an absence of egg maturation in females and is thought to conserve energy for survival during stressful times. The ability to diapause is more common in flies from higher latitudes and in offspring from flies that have recently overwintered. Therefore, diapause has been thought to be a recent adaptation to temperate climates. We identified hundreds of genetic variants that affect diapause and found that some vary predictably across latitudes in North America. We found little signal of repeated seasonality in diapause-associated genetic variants, but our populations evolved an increased ability to diapause in the winter when they were exposed to natural conditions. Combined, our results suggest that diapause-associated variants evolve differently across space and time. We find little evidence that diapause evolved recently in temperate environments; rather, SNPs associated with diapause tend to be quite common in Zambia, suggesting that diapause may promote survival under stresses other than cold. Our results provide future targets for research into the genetic underpinnings of this complex, ecologically relevant trait.

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Section: Resultsmentioning

confidence: 99%

Unique genetic signatures of local adaptation over space and time for diapause, an ecologically relevant complex trait, inDrosophila melanogaster

Erickson

Weller

Song

et al. 2020

Preprint

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“…In addition, this extension could allow the detection of adaptive changes in trait correlations. Second, these methods could be extended to take advantage of more sophisticated methods of genomic prediction than the additive model presented here (as in Beissinger et al 2018;Liu et al 2018). Pursuing this goal will require carefully addressing issues related to LD between marker loci.…”

Section: Discussionmentioning

confidence: 99%

Detecting Adaptive Differentiation in Structured Populations with Genomic Data and Common Gardens

et al. 2019

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Adaptation in quantitative traits often occurs through subtle shifts in allele frequencies at many loci—a process called polygenic adaptation. While a number of methods have been developed to detect polygenic adaptation in human populations, we lack clear strategies for doing so in many other systems. In particular, there is an opportunity to develop new methods that leverage datasets with genomic data and common garden trait measurements to systematically detect the quantitative traits important for adaptation. Here, we develop methods that do just this, using principal components of the relatedness matrix to detect excess divergence consistent with polygenic adaptation, and using a conditional test to control for confounding effects due to population structure. We apply these methods to inbred maize lines from the United States Department of Agriculture germplasm pool and maize landraces from Europe. Ultimately, these methods can be applied to additional domesticated and wild species to give us a broader picture of the specific traits that contribute to adaptation and the overall importance of polygenic adaptation in shaping quantitative trait variation.

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“…The phenotypes of each individual were not included in most of the signatures of selection detection analysis, hence the functional explanation of significant signals was usually less conclusive. Although a new methodology for the detection of signature of selection for specific complex traits was recently proposed by Beissinger et al [46], the phenotypic values were not always available in such research. The reported QTLs could serve as a reference or potential clue to understand the identified signatures of selection.…”

Section: Discussionmentioning

confidence: 99%

Genome-Wide Signatures of Selection Detection in Three South China Indigenous Pigs

Diao

Huang

Chen

et al. 2019

Genes

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South China indigenous pigs are famous for their superior meat quality and crude feed tolerance. Saba and Baoshan pigs without saddleback were located in the high-altitude area of Yunnan Province, while Tunchang and Ding’an pigs with saddleback were located in the low-altitude area of Hainan Province. Although these pigs are different in appearance, the underlying genetic differences have not been investigated. In this study, based on the single-nucleotide polymorphism (SNP) genotypes of 124 samples, both the cross-population extended haplotype homozygosity (XP-EHH) and the fixation index (FST) statistic were used to identify potential signatures of selection in these pig breeds. We found nine potential signatures of selection detected simultaneously by two methods, annotated 22 genes in Hainan pigs, when Baoshan pigs were used as the reference group. In addition, eleven potential signatures of selection detected simultaneously by two methods, annotated 24 genes in Hainan pigs compared with Saba pigs. These candidate genes were most enriched in GO: 0048015~phosphatidylinositol-mediated signaling and ssc00604: Glycosphingolipid biosynthesis—ganglio series. These selection signatures were likely to overlap with quantitative trait loci associated with meat quality traits. Furthermore, one potential selection signature, which was associated with different coat color, was detected in Hainan pigs. These results contribute to a better understanding of the underlying genetic architecture of South China indigenous pigs.

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A Simple Test Identifies Selection on Complex Traits

Cited by 22 publications

References 55 publications

Unique genetic signatures of local adaptation over space and time for diapause, an ecologically relevant complex trait, inDrosophila melanogaster

Unique genetic signatures of local adaptation over space and time for diapause, an ecologically relevant complex trait, inDrosophila melanogaster

Detecting Adaptive Differentiation in Structured Populations with Genomic Data and Common Gardens

Genome-Wide Signatures of Selection Detection in Three South China Indigenous Pigs

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