The Evolution of Larger Size in High Altitude Drosophila melanogaster has a Variable Genetic Architecture

Abstract Important uncertainties persist regarding the genetic architecture of adaptive trait evolution in natural populations, including the number of genetic variants involved, whether they are drawn from standing genetic variation, and whether directional selection drives them to complete fixation. Here, we take advantage of a unique natural population of Drosophila melanogaster from the Ethiopian highlands, which has evolved larger body size than any other known population of this species. We apply a bulk segregant quantitative trait locus (QTL) mapping approach to four unique crosses between highland Ethiopian and lowland Zambian populations for both thorax length and wing length. Results indicated a persistently variable genetic basis for these evolved traits (with largely distinct sets of QTLs for each cross), and at least a moderately polygenic architecture with relatively strong effects present. We complemented these mapping experiments with population genetic analyses of QTL regions and gene ontology enrichment analysis, generating strong hypotheses for specific genes and functional processes that may have contributed to these adaptive trait changes. Finally, we find that the genetic architectures our QTL mapping results for size traits mirror those from similar experiments on other recently-evolved traits in this species. Collectively, these studies suggest a recurring pattern of polygenic adaptation in this species, in which causative variants do not approach fixation and moderately strong effect loci are present.

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The Evolution of Larger Size in High Altitude Drosophila melanogaster has a Polymorphic Genetic Architecture

10.1101/2021.10.05.463286 ◽

2021 ◽

Author(s):

Quentin D Sprengelmeyer ◽

Justin B Lack ◽

Dylan T Braun ◽

Matthew J Monette ◽

John E. Pool

Keyword(s):

Drosophila Melanogaster ◽

Qtl Mapping ◽

Genetic Architecture ◽

Natural Populations ◽

Enrichment Analysis ◽

Thorax Length ◽

Adaptive Trait ◽

Polygenic Adaptation ◽

Trait Locus ◽

Population Genetic Analyses

Important uncertainties persist regarding the genetic architecture of adaptive trait evolution in natural populations, including the number of genetic variants involved, whether they are drawn from standing genetic variation, and whether directional selection drives them to complete fixation. Here, we take advantage of a unique natural population of Drosophila melanogaster from the Ethiopian highlands, which has evolved larger body size than any other known population of this species. We apply a bulk segregant quantitative trait locus (QTL) mapping approach to four unique crosses between highland Ethiopian and lowland Zambian populations for both thorax length and wing length. Results indicated a persistently variable genetic basis for these evolved traits (with largely distinct sets of QTLs for each cross), and at least a moderately polygenic architecture with relatively strong effects present. We complemented these mapping experiments with population genetic analyses of QTL regions and gene ontology enrichment analysis, generating strong hypotheses for specific genes and functional processes that may have contributed to these adaptive trait changes. Finally, we find that the genetic architectures our QTL mapping results for size traits mirror those from similar experiments on other recently-evolved traits in this species. Collectively, these studies suggest a recurring pattern of polygenic adaptation in this species, in which causative variants do not approach fixation and moderately strong effect loci are present.

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Consequences of Recombination Rate Variation on Quantitative Trait Locus Mapping Studies: Simulations Based on the Drosophila melanogaster Genome

Genetics ◽

10.1093/genetics/159.2.581 ◽

2001 ◽

Vol 159 (2) ◽

pp. 581-588

Author(s):

Mohamed A F Noor ◽

Aimee L Cunningham ◽

John C Larkin

Keyword(s):

Quantitative Trait Locus ◽

Drosophila Melanogaster ◽

Qtl Mapping ◽

Quantitative Trait ◽

Recombination Rate ◽

Genome Project ◽

Gene Density ◽

Rate Variation ◽

Trait Locus ◽

Recombination Rate Variation

Abstract We examine the effect of variation in gene density per centimorgan on quantitative trait locus (QTL) mapping studies using data from the Drosophila melanogaster genome project and documented regional rates of recombination. There is tremendous variation in gene density per centimorgan across this genome, and we observe that this variation can cause systematic biases in QTL mapping studies. Specifically, in our simulated mapping experiments of 50 equal-effect QTL distributed randomly across the physical genome, very strong QTL are consistently detected near the centromeres of the two major autosomes, and few or no QTL are often detected on the X chromosome. This pattern persisted with varying heritability, marker density, QTL effect sizes, and transgressive segregation. Our results are consistent with empirical data collected from QTL mapping studies of this species and its close relatives, and they explain the “small X-effect” that has been documented in genetic studies of sexual isolation in the D. melanogaster group. Because of the biases resulting from recombination rate variation, results of QTL mapping studies should be taken as hypotheses to be tested by additional genetic methods, particularly in species for which detailed genetic and physical genome maps are not available.

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QTL Analysis for Downy Mildew Resistance in Cucumber Inbred Line PI 197088

Plant Disease ◽

10.1094/pdis-04-17-0491-re ◽

2018 ◽

Vol 102 (7) ◽

pp. 1240-1245 ◽

Cited By ~ 5

Author(s):

Lixia Li ◽

Huiqiang He ◽

Zhirong Zou ◽

Yuhong Li

Keyword(s):

Qtl Mapping ◽

Downy Mildew ◽

Genetic Architecture ◽

Plant Introduction ◽

Minor Effect ◽

Phenotypic Variance ◽

Chromosome 4 ◽

Phenotypic Data ◽

Trait Locus ◽

Simple Sequence

Downy mildew (DM), caused by Pseudoperonospora cubensis, is one of the major foliar diseases prevailing in cucumber-growing areas. The mechanism of DM resistance in cucumber, particularly the plant introduction (PI) 197088 from India, is presently unclear. Quantitative trait locus (QTL) mapping is an efficient approach to studying DM resistance genes in cucumber. In this study, we performed QTL mapping for DM resistance in PI 197088 with 183 F2-derived F3 (F2:3) families from the cross between PI 197088 (DM resistant) and Changchunmici (DM susceptible). A linkage map was constructed using 141 simple sequence repeat markers. Phenotypic data were collected from seven independent experiments. In total, five QTL were detected on chromosomes 1, 3, 4, and 5 with DM resistance contributed by PI 197088. The QTL on chromosome 4, dm4.1, was reproducibly detected in all indoor experiments, which could explain 27% of the phenotypic variance detected. Additionally, dm1.1 and dm5.2 showed moderate effects, while dm3.1 and dm5.1 were minor-effect QTL. This study revealed the unique genetic architecture of DM resistance in PI 197088, which may provide important guidance for efficient use in cucumber breeding for DM resistance.

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Explaining the heritability of an ecologically significant trait in terms of individual quantitative trait loci

Biology Letters ◽

10.1098/rsbl.2011.0409 ◽

2011 ◽

Vol 7 (6) ◽

pp. 896-898 ◽

Cited By ~ 13

Author(s):

Alison G. Scoville ◽

Young Wha Lee ◽

John H. Willis ◽

John K. Kelly

Keyword(s):

Qtl Mapping ◽

Quantitative Trait ◽

Complex Traits ◽

Genetic Variance ◽

Balancing Selection ◽

Natural Populations ◽

Population Based ◽

Population Variation ◽

Trait Locus ◽

Genomic Regions

Most natural populations display substantial genetic variation in behaviour, morphology, physiology, life history and the susceptibility to disease. A major challenge is to determine the contributions of individual loci to variation in complex traits. Quantitative trait locus (QTL) mapping has identified genomic regions affecting ecologically significant traits of many species. In nearly all cases, however, the importance of these QTLs to population variation remains unclear. In this paper, we apply a novel experimental method to parse the genetic variance of floral traits of the annual plant Mimulus guttatus into contributions of individual QTLs. We first use QTL-mapping to identify nine loci and then conduct a population-based breeding experiment to estimate V Q , the genetic variance attributable to each QTL. We find that three QTLs with moderate effects explain up to one-third of the genetic variance in the natural population. Variation at these loci is probably maintained by some form of balancing selection. Notably, the largest effect QTLs were relatively minor in their contribution to heritability.

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Deciphering Genetic Architecture of Adventitious Root and Related Shoot Traits in Populus Using QTL Mapping and RNA-Seq Data

International Journal of Molecular Sciences ◽

10.3390/ijms20246114 ◽

2019 ◽

Vol 20 (24) ◽

pp. 6114 ◽

Cited By ~ 4

Author(s):

Pei Sun ◽

Huixia Jia ◽

Yahong Zhang ◽

Jianbo Li ◽

Mengzhu Lu ◽

...

Keyword(s):

Qtl Mapping ◽

Adventitious Root ◽

Adventitious Roots ◽

Genetic Architecture ◽

Populus Deltoides ◽

Transmembrane Domain ◽

Root Traits ◽

Rna Seq ◽

Correlation Relationship ◽

Trait Locus

Understanding the genetic architecture of adventitious root and related shoot traits will facilitate the cultivation of superior genotypes. In this study, we measured 12 adventitious root and related shoot traits of 434 F1 genotypes originating from Populus deltoides ‘Danhong’ × Populus simonii ‘Tongliao1’ and conducted an integrative analysis of quantitative trait locus (QTL) mapping and RNA-Seq data to dissect their genetic architecture and regulatory genes. Extensive segregation, high repeatability, and significant correlation relationship were detected for the investigated traits. A total of 150 QTLs were associated with adventitious root traits, explaining 3.1–6.1% of phenotypic variation (PVE); while 83 QTLs were associated with shoot traits, explaining 3.1–19.8% of PVE. Twenty-five QTL clusters and 40 QTL hotspots were identified for the investigated traits. Ten QTL clusters were overlapped in both adventitious root traits and related shoot traits. Transcriptome analysis identified 10,172 differentially expressed genes (DEGs) among two parents, three fine rooting and three poor-rooting genotypes, 143 of which were physically located within the QTL intervals. K-means cluster and weighted gene co-expression network analysis showed that PtAAAP19 (Potri.004G111400) encoding amino acid transport protein was tightly associated with adventitious roots and highly expressed in fine-rooting genotypes. Compare with ‘Danhong’, 153 bp deletion in the coding sequence of PtAAAP19 in ‘Tongliao1’ gave rise to lack one transmembrane domain, which might cause the variation of adventitious roots. Taken together, this study deciphered the genetic basis of adventitious root and related shoot traits and provided potential function genes for genetic improvement of poplar breeding.

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Funmap2: an R package for QTL mapping using longitudinal phenotypes

PeerJ ◽

10.7717/peerj.7008 ◽

2019 ◽

Vol 7 ◽

pp. e7008

Author(s):

Nating Wang ◽

Tinyi Chu ◽

Jiangtao Luo ◽

Rongling Wu ◽

Zhong Wang

Keyword(s):

Qtl Mapping ◽

Covariance Matrix ◽

Complex Traits ◽

Genetic Architecture ◽

R Package ◽

Information Criteria ◽

Functional Mapping ◽

Biological Knowledge ◽

Phenotypic Traits ◽

Trait Locus

Quantitative trait locus (QTL) mapping has been used as a powerful tool for inferring the complexity of the genetic architecture that underlies phenotypic traits. This approach has shown its unique power to map the developmental genetic architecture of complex traits by implementing longitudinal data analysis. Here, we introduce the R package Funmap2 based on the functional mapping framework, which integrates prior biological knowledge into the statistical model. Specifically, the functional mapping framework is engineered to include longitudinal curves that describe the genetic effects and the covariance matrix of the trait of interest. Funmap2 chooses the type of longitudinal curve and covariance matrix automatically using information criteria. Funmap2 is available for download at https://github.com/wzhy2000/Funmap2.

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Microbiome composition shapes rapid genomic adaptation of Drosophila melanogaster

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1907787116 ◽

2019 ◽

Vol 116 (40) ◽

pp. 20025-20032 ◽

Cited By ~ 20

Author(s):

Seth M. Rudman ◽

Sharon Greenblum ◽

Rachel C. Hughes ◽

Subhash Rajpurohit ◽

Ozan Kiratli ◽

...

Keyword(s):

Drosophila Melanogaster ◽

Natural Populations ◽

Microbiome Composition ◽

Adaptive Process ◽

Population Genomic ◽

Polygenic Adaptation ◽

Microbial Group ◽

Genomic Adaptation ◽

Microbe Interactions ◽

Host Microbe Interactions

Population genomic data has revealed patterns of genetic variation associated with adaptation in many taxa. Yet understanding the adaptive process that drives such patterns is challenging; it requires disentangling the ecological agents of selection, determining the relevant timescales over which evolution occurs, and elucidating the genetic architecture of adaptation. Doing so for the adaptation of hosts to their microbiome is of particular interest with growing recognition of the importance and complexity of host–microbe interactions. Here, we track the pace and genomic architecture of adaptation to an experimental microbiome manipulation in replicate populations of Drosophila melanogaster in field mesocosms. Shifts in microbiome composition altered population dynamics and led to divergence between treatments in allele frequencies, with regions showing strong divergence found on all chromosomes. Moreover, at divergent loci previously associated with adaptation across natural populations, we found that the more common allele in fly populations experimentally enriched for a certain microbial group was also more common in natural populations with high relative abundance of that microbial group. These results suggest that microbiomes may be an agent of selection that shapes the pattern and process of adaptation and, more broadly, that variation in a single ecological factor within a complex environment can drive rapid, polygenic adaptation over short timescales.

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Ethanol resistance in Drosophila melanogaster has increased in parallel cold-adapted populations and shows a variable genetic architecture within and between populations

10.22541/au.161064161.14860829/v1 ◽

2021 ◽

Author(s):

Quentin Sprengelmeyer ◽

John E Pool

Keyword(s):

Drosophila Melanogaster ◽

Genetic Architecture ◽

Genetic Basis ◽

Biological Diversity ◽

European Population ◽

Membrane Composition ◽

Trait Evolution ◽

Adaptive Trait ◽

Standing Variation ◽

Ethanol Resistance

Understanding the genetic properties of adaptive trait evolution is a fundamental crux of biological inquiry that links molecular processes to biological diversity. Important uncertainties persist regarding the genetic predictability of adaptive trait change, the role of standing variation, and whether adaptation tends to result in the fixation of favored variants. Here, we use the recurrent evolution of enhanced ethanol resistance in Drosophila melanogaster during this species’ worldwide expansion as a promising system to add to our understanding of the genetics of adaptation. We find that elevated ethanol resistance has evolved at least three times in different cooler regions of the species’ modern range - not only at high latitude but also in two African high altitude regions - and that ethanol and cold resistance may have a partially shared genetic basis. Applying a bulk segregant mapping framework, we find that the genetic architecture of ethanol resistance evolution differs substantially not only between our three resistant populations, but also between two crosses involving the same European population. We then apply population genetic scans for local adaptation within our quantitative trait locus regions, and we find potential contributions of genes with annotated roles in spindle localization, membrane composition, sterol and alcohol metabolism, and other processes. We also apply simulation-based analyses that confirm the variable genetic basis of ethanol resistance and hint at a moderately polygenic architecture. However, these simulations indicate that larger-scale studies will be needed to more clearly quantify the genetic architecture of adaptive evolution, and to firmly connect trait evolution to specific causative loci.

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The Genetic Architecture of Cold Tolerance in Natural-Populations of Drosophila-Melanogaster and Drosophila-Simulans

Australian Journal of Zoology ◽

10.1071/zo9900163 ◽

1990 ◽

Vol 38 (2) ◽

pp. 163 ◽

Cited By ~ 4

Author(s):

JK Davidson

Keyword(s):

Drosophila Melanogaster ◽

Cold Tolerance ◽

Genetic Architecture ◽

Population Sample ◽

Natural Populations ◽

Diallel Analysis ◽

Humid Tropics ◽

Additive Genetic Effects ◽

Isofemale Strains ◽

Made In

Genetic analysis of cold tolerance was applied to samples of recently collected isofemale strains of Drosophila melanogaster and D. simulans from natural populations from diverse climates. The temperate zone locality of Melbourne was sampled twice for both species, once in 1986 and again in 1987. In 1987, D. melanogaster collections were also made in the humid tropics at Townsville and the wet/dry tropical locality of Darwin. D. simulans was also collected in Townsville in 1987 but it was not found in Darwin. Diallel analysis was performed for each population sample, so there were seven diallels, each with from 9 to 12 strains which were randomly chosen. Diallel analyses showed that cold tolerance was mainly controlled by additive genetic effects. This pattern was consistent across time, across populations and across species. It is proposed that natural populations of both members of the sibling species have the genetic architecture necessary for adaptive phenotypic response to selection by intermittent periods of low temperature.

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The genetic basis of Drosophila melanogaster defense against Beauveria bassiana explored through evolve and resequence and quantitative trait locus mapping

10.1101/2021.03.31.437898 ◽

2021 ◽

Author(s):

Parvin Shahrestani ◽

Elizabeth King ◽

Reza Ramezan ◽

Mark Phillips ◽

Melissa Riddle ◽

...

Keyword(s):

Quantitative Trait Locus ◽

Drosophila Melanogaster ◽

Qtl Mapping ◽

Beauveria Bassiana ◽

Quantitative Trait ◽

Genetic Basis ◽

Immune Defense ◽

Cross Resistance ◽

Antifungal Immunity ◽

Trait Locus

Many of the molecular mechanisms for antifungal immunity in Drosophila melanogaster have been defined, but relatively little is known about the genetic basis for variation in antifungal immunity in natural populations. Using two population genetic approaches, Quantitative Trait Locus (QTL) Mapping and Evolve and Resequence (E&R), we explored the genetics underlying D. melanogaster immune defense against infection with the fungus Beauveria bassiana. Immune defense was highly variable both in the recombinant inbred lines from the Drosophila Synthetic Population Resource used for our QTL Mapping and in the synthetic outbred populations used in our E&R study. Survivorship of infection improved dramatically over just 10 generations in the E&R study, and continued to increase for an additional 9 generations, revealing a trade-off with uninfected longevity. Populations selected for increased defense against B. bassiana evolved cross resistance to a second, distinct B. bassiana strain but not to bacterial pathogens. The QTL mapping study revealed that sexual dimorphism in defense depends on host genotype, and the E&R study indicated that dimorphism also depends on the specific pathogen to which the host is exposed. Both the QTL Mapping and E&R experiments generated lists of potentially causal candidate genes, although these lists were non-overlapping.

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