Elsevier

Current Opinion in Insect Science

Volume 31, February 2019, Pages 99-105
Current Opinion in Insect Science

What can genetic association panels tell us about evolutionary processes in insects?

https://doi.org/10.1016/j.cois.2018.12.004Get rights and content

Highlights

  • •

    Genetic association panels provide a focus for research community efforts.

  • •

    Genetic association panels unite genetic variation and systems biology.

  • •

    The overlap between GWAS and selective sweeps provides insights into the selective forces shaping Drosophila populations.

  • •

    Optimal panel design depends upon species population history, robustness to inbreeding and research imperatives.

If we are to fully comprehend the evolution of insect diversity at a genomic level we need to understand how natural selection can alter genetically encoded characters within populations. Genetic association panels have the potential to be standard bearers in this endeavour. They enable the mapping of phenotypes to genotypes at unprecedented resolution while simultaneously providing population genomic samples that can be interrogated for the tell-tale signs of selection. Analyses of these panels promise to elucidate the entanglement of gene ontologies, pathways, developmental processes and evolutionary constraints, and inform how these are shaped by adaptation.

Introduction

To understand the way in which evolutionary processes have shaped insect genomes, selective signatures must be detected and interpreted, and putatively adaptive variants must be linked to phenotypes. The ability to sequence insect genomes at low-cost has not only fuelled population-genomic studies that can detect signatures of selection in the patterns of DNA polymorphism, but has also allowed phenotype-to-genotype mapping panels to be characterized at nucleotide resolution. In 2012, the Drosophila melanogaster community was introduced to two mapping panels, the Drosophila Genetic Reference Panel (DGRP; [1••]) and the Drosophila Synthetic Population Resource (DSPR; [2••,3]; Box 1).

Both the DGRP and the DSPR comprise genotyped inbred lines which are available to the research community for phenotyping. Association mapping approaches can then be used to implicate the involvement of quantitative trait loci (QTL) in any phenotype for which the panel exhibits variation. Aside from a reduced genotyping cost and hence workload for trait-mappers, the panel design offers additional benefits; repeated use of the resource incentivizes investment in its further characterization, for example in the refinement of genome sequences [4,5••] and addition of transcriptome data [6•]. Furthermore, phenotypes measured on a panel can be directly compared between one another and correlations can be assessed, implicating pleiotropy of genetic variants across traits.

Here we highlight key literature published over the last six years on the mapping panels of D. melanogaster, with a particular focus on adaptive traits. These panels are not informative to all aspects of insect biology, partly because of the limitations of the design of each panel but more importantly because D. melanogaster cannot be a model to all aspects of insect biology. So, a key aim of this article is to discuss criteria to be considered in the design of the ideal panel whether that be another Drosophila panel or a panel to be generated from another insect species.

Section snippets

Association mapping in Drosophila panels

To date, over 50 studies have phenotypically characterized the DGRP lines [reviewed in Refs. [7•,[21•]], and these span categories such as physiology [9], morphology [10, 11, 12], sensory perception [13], behaviour [14, 15, 16, 17], stress tolerance [18,19], life history traits [20], molecular processes [21•], susceptibility to CRISPR gene drives [22], and even the genetic basis of phenotypic variability [23] and plasticity [24,25]. By performing genome wide association studies (GWAS), it has

Systems genetics

A promising strategy for enhancing networks comes in the form of ‘systems genetics’ [41], where multiple ‘intermediate phenotypes’ (e.g. transcriptomic data) are mapped onto genetic variation and incorporated into association studies (Figure 1). Microarray transcriptomes have been published for adults of each sex from 185 DGRP lines, allowing the mapping of significant eQTL (expression quantitative trait loci; genetic variants statistically associated with levels of a particular transcript) for

Selective sweeps

A further dimension that can be added to association studies is the evidence for selection across panel genomes. Patterns of polymorphism in DNA sequences, such as patches of reduced nucleotide diversity, extended linkage disequilibrium or skews in the frequency spectrum, can provide compelling cases of positive selection acting upon genes [44]. Positive selection is not necessarily adaptive ([45] e.g. meiotic drive elements could generate such patterns) and not all adaptive variants will show

Other genetic association panels

D. melanogaster is not the only species where panels are available. Recently a Drosophila. simulans panel, consisting of 170 inbred lines in a design similar to the DGRP, was described, and it confirms the strong evidence of parallel selective sweeps at Ace and Cyp6g1 loci [56, 57, 58]. There is also a panel of 110 lines in the more distantly related Drosophila serrata that has already been used to investigate the genetic architecture of cuticular hydrocarbon phenotypes [59]. There are of

Conclusions

While the conflicts between optimal panel design conditions make the ideal panel elusive, recognizing a panel’s limitations remains important in interpreting the results of association studies utilizing these resources (Box 2). Perhaps a way to resolve the contrasting imperatives of genotype-to-phenotype mapping with selection-to-phenotype mapping is to adopt a design with multiple nested panels. A subset of diverged lines could be used to optimize genotype-to-phenotype mapping, while related

Conflict of interest statement

Nothing declared.

References and recommended reading

Papers of particular interest, published within the period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

References (66)

  • E.G. King et al.

    Using Drosophila melanogaster to identify chemotherapy toxicity genes

    Genetics

    (2014)
  • C.A. Highfill et al.

    Naturally-segregating variation at Ugt86Dd contributes to nicotine resistance in Drosophila melanogaster

    Genetics

    (2017)
  • T.F. Mackay et al.

    The Drosophila melanogaster genetic reference panel

    Nature

    (2012)
  • E.G. King et al.

    Genetic dissection of a model complex trait using the Drosophila synthetic population resource

    Genome Res

    (2012)
  • E.G. King et al.

    Properties and power of the Drosophila synthetic population resource for the routine dissection of complex traits

    Genetics

    (2012)
  • W. Huang et al.

    Natural variation in genome architecture among 205 Drosophila melanogaster Genetic reference panel lines

    Genome Res

    (2014)
  • M. Chakraborty et al.

    Hidden genetic variation shapes the structure of functional elements in Drosophila

    Nat Genet

    (2018)
  • W. Huang et al.

    Genetic basis of transcriptome diversity in Drosophila melanogaster

    Proc Natl Acad Sci

    (2015)
  • R.R. Anholt et al.

    The road less traveled: from genotype to phenotype in flies and humans

    Mamm Genome

    (2018)
  • T.F. Mackay et al.

    Charting the genotype–phenotype map: lessons from the Drosophila melanogaster genetic reference panel

    Wiley Interdisc Rev: Dev Biol

    (2018)
  • L.M. Dembeck et al.

    Genetic architecture of natural variation in cuticular hydrocarbon composition in Drosophila melanogaster

    Elife

    (2015)
  • F. Muñoz‐Muñoz et al.

    Drosophila wing modularity revisited through a quantitative genetic approach

    Evolution

    (2016)
  • B. Takahara et al.

    Genome-wide association study on male genital shape and size in Drosophila melanogaster

    PLoS One

    (2015)
  • L. Zwarts et al.

    The genetic basis of natural variation in mushroom body size in Drosophila melanogaster

    Nat Commun

    (2015)
  • S. Uchizono et al.

    Genetic variation in taste sensitivity to sugars in Drosophila melanogaster

    Chem Senses

    (2017)
  • A.M. Scott et al.

    Sociability in fruit flies: genetic variation, heritability and plasticity

    Behav Genet

    (2018)
  • J. Shorter et al.

    Genetic architecture of natural variation in Drosophila melanogaster aggressive behavior

    Proc Natl Acad Sci U S A

    (2015)
  • G.H. Arya et al.

    The genetic basis for variation in olfactory behavior in Drosophila melanogaster

    Chem Senses

    (2015)
  • B.E. Gaertner et al.

    Heritable variation in courtship patterns in Drosophila melanogaster

    G3: Genes Genomes Genet

    (2015)
  • A.L. Weber et al.

    Genome-wide association analysis of oxidative stress resistance in Drosophila melanogaster

    PloS One

    (2012)
  • M.S. Bou Sleiman et al.

    Genetic, molecular and physiological basis of variation in Drosophila gut immunocompetence

    Nat Commun

    (2015)
  • M.F. Durham et al.

    Genome-wide analysis in Drosophila reveals age-specific effects of SNPs on fitness traits

    Nat Commun

    (2014)
  • C.M. Hunter et al.

    The genetic architecture of natural variation in recombination rate in Drosophila melanogaster

    PLoS Genet

    (2016)
  • J. Champer et al.

    Multiple loci of small effect confer wide variability in efficiency and resistance rate of CRISPR gene drive

    bioRxiv

    (2018)
  • J.F. Ayroles et al.

    Behavioral idiosyncrasy reveals genetic control of phenotypic variability

    Proc Natl Acad Sci U S A

    (2015)
  • F. Morgante et al.

    Genetic architecture of micro-environmental plasticity in Drosophila melanogaster

    Sci Rep

    (2015)
  • E. Lafuente et al.

    Genetic basis of thermal plasticity variation in Drosophila melanogaster body size

    PLoS Genet

    (2018)
  • P.M. Visscher et al.

    10 years of GWAS discovery: biology, function, and translation

    Am J Hum Genet

    (2017)
  • T. Fournier et al.

    Genetic backgrounds and hidden trait complexity in natural populations

    Curr Opin Genet Dev

    (2017)
  • M. Ørsted et al.

    Strong impact of thermal environment on the quantitative genetic basis of a key stress tolerance trait

    Heredity

    (2018)
  • M.A. Najarro et al.

    Identifying loci contributing to natural variation in xenobiotic resistance in Drosophila

    PLoS Genet

    (2015)
  • M.A. Najarro et al.

    Loci contributing to boric acid toxicity in two reference populations of Drosophila melanogaster

    G3: Genes Genomes Genet

    (2017)
  • T.N. Marriage et al.

    Fine-mapping nicotine resistance loci in Drosophila using a multiparent advanced generation inter-cross population

    Genetics

    (2014)

    • Cited by (5)

    • Genomic and transcriptomic analyses in Drosophila suggest that the ecdysteroid kinase-like (EcKL) gene family encodes the ‘detoxification-by-phosphorylation’ enzymes of insects

      2020, Insect Biochemistry and Molecular Biology
      Citation Excerpt :

      However, detoxification genes tend to have other characteristic properties, including transcriptional induction by xenobiotics (Willoughby et al., 2006; Giraudo et al., 2010) and enriched expression in tissues with known detoxification roles, like the midgut, Malpighian tubules and fat body (Yang et al., 2007). Phenotypes discovered during genetic experiments can also indicate detoxification functions, including susceptibility via gene disruption (Wang et al., 2018) or tolerance via overexpression (Daborn et al., 2007); genome- and transcriptome-wide association studies can also identify candidate genes for detoxification-related phenotypes using naturally occurring variation (Robin et al., 2019). Additionally, genes encoding detoxification enzymes are thought to undergo gene duplication and loss at a faster rate than those encoding enzymes with important housekeeping functions (Kawashima and Satta, 2014; Thomas, 2007).

    • Optimizing sampling design and sequencing strategy for the genomic analysis of quantitative traits in natural populations

      2022, Molecular Ecology Resources

    • Global patterns in genomic diversity underpinning the evolution of insecticide resistance in the aphid crop pest Myzus persicae

      2021, Communications Biology

    • Sublethal larval exposure to imidacloprid impacts adult behaviour in Drosophila melanogaster

      2020, Journal of Evolutionary Biology

    • Cis- And trans-acting variants contribute to survivorship in a naïve Drosophila melanogaster population exposed to ryanoid insecticides

      2019, Proceedings of the National Academy of Sciences of the United States of America
    View full text
    © 2018 Elsevier Inc. All rights reserved.