Positive diversifying selection is a pervasive adaptive force throughout the Drosophila radiation.

The growing genomic information on non-model organisms eases exploring the evolutionary history of biodiversity. This is particularly true for Drosophila flies, in which the number of sequenced species doubled recently. Because of its outstanding diversity of species, Drosophila has become one of the most important systems to study adaptive radiation. In this study, we performed a genome-wide analysis of positive diversifying selection on more than 2000 single-copy orthologous groups in 25 species using a recent method of increased accuracy for detecting positive diversifying selection. Adopting this novel approach enabled us to find a consistent selection signal throughout the genus Drosophila, and a total of 1342 single-copy orthologous groups were identified with a putative signal of positive diversifying selection, corresponding to 1.9% of all loci. Specifically, in lineages leading to D. grimshawi, a strong putative signal of positive diversifying selection was found related to cell, morphological, neuronal, and sensorial development and function. A recurrent signal of positive diversifying selection was found on genes related to aging and lifespan, suggesting that selection had shaped lifespan diversity in Drosophila, including extreme longevity. Our study, one of the largest and most comprehensive ones on genome-wide positive diversifying selection to date, shows that positive diversifying selection has promoted species-specific differentiation among evolutionary lineages throughout the Drosophila radiation. Acting on the same biological processes via different routes, positive diversifying selection has promoted diversity of functions and adaptive divergence.

• Publication year

  2017

• Venue

  Molecular Phylogenetics and Evolution

• Publication date

  2017-07-01

• Fields of study

  Biology, Medicine, Environmental Science

• Identifiers
  DOI 10.1016/j.ympev.2017.04.023PMID 28458014
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

• Chemosensory adaptations of the mountain fly Drosophila nigrosparsa (Insecta: Diptera) through genomics’ and structural biology’s lenses

  2017cited by this paper
• Innate-like functions of natural killer T cell subsets result from highly divergent gene programs

  2016cited by this paper
• Standardized benchmarking in the quest for orthologs

  2016cited by this paper
• Genomic Signatures of Speciation in Sympatric and Allopatric Hawaiian Picture-Winged Drosophila

  2016cited by this paper
• Drosophila melanogaster Hsp22: a mitochondrial small heat shock protein influencing the aging process

  2015cited by this paper
• Expression Divergence of Chemosensory Genes between Drosophila sechellia and Its Sibling Species and Its Implications for Host Shift

  2015cited by this paper
• mTORC2 is a tyrosine kinase

  2015cited by this paper
• Rapid adaptive radiation and host plant conservation in the Hawaiian picture wing Drosophila (Diptera: Drosophilidae).

  2015cited by this paper
• Malignant Drosophila tumors interrupt insulin signaling to induce cachexia-like wasting.

  2015cited by this paper
• Kiwi genome provides insights into evolution of a nocturnal lifestyle

  2015cited by this paper
• Basic mechanisms of longevity: A case study of Drosophila pro-longevity genes.

  2015cited by this paper
• Out of southern East Asia: the natural history of domestic dogs across the world

  2015cited by this paper
• Neuronal stathmins: a family of phosphoproteins cooperating for neuronal development, plasticity and regeneration.

  2015cited by this paper
• Engineering ePTEN, an enhanced PTEN with increased tumor suppressor activities

  2014cited by this paper
• InParanoid 8: orthology analysis between 273 proteomes, mostly eukaryotic

  2014cited by this paper
• Crystallographic structure of a small molecule SIRT1 activator-enzyme complex

  2014cited by this paper
• Comparative validation of the D. melanogaster modENCODE transcriptome annotation

  2014cited by this paper
• GenBank

  2014cited by this paper
• BEAST 2: A Software Platform for Bayesian Evolutionary Analysis

  2014influential reference
• Engrailed Alters the Specificity of Synaptic Connections of Drosophila Auditory Neurons with the Giant Fiber

  2014cited by this paper
• Protein structure modeling with MODELLER.

  2014cited by this paper
• Selecting optimal partitioning schemes for phylogenomic datasets

  2014cited by this paper
• Orthology Detection Combining Clustering and Synteny for Very Large Datasets

  2014cited by this paper
• Sequential axon-derived signals couple target survival and layer specificity in the Drosophila visual system.

  2014cited by this paper
• A Phylogeny-Based Benchmarking Test for Orthology Inference Reveals the Limitations of Function-Based Validation

  2014cited by this paper
• Receptor tyrosine kinases in Drosophila development.

  2013cited by this paper
• Hieranoid: hierarchical orthology inference.

  2013cited by this paper
• Serine Proteolytic Pathway Activation Reveals an Expanded Ensemble of Wound Response Genes in Drosophila

  2013cited by this paper
• Sexual Selection, Epistasis and Species Boundaries in Sympatric Hawaiian Picture-winged Drosophila

  2013cited by this paper
• Critiquing blind dating: the dangers of over-confident date estimates in comparative genomics.

  2013cited by this paper
• Phylogenomic insights into the cambrian explosion, the colonization of land and the evolution of flight in arthropoda.

  2013cited by this paper
• GeneMANIA Prediction Server 2013 Update

  2013cited by this paper
• Selectome update: quality control and computational improvements to a database of positive selection

  2013cited by this paper
• Genetics and epigenetics of aging and longevity

  2013cited by this paper
• Patterns of Positive Selection in Seven Ant Genomes

  2013influential reference
• Genome-wide signatures of convergent evolution in echolocating mammals

  2013cited by this paper
• MITOS: improved de novo metazoan mitochondrial genome annotation.

  2013influential reference
• STRAW: Species TRee Analysis Web server

  2013cited by this paper
• Forkhead Transcription Factor Fd3F Cooperates with Rfx to Regulate a Gene Expression Program for Mechanosensory Cilia Specialization

  2012cited by this paper
• SPAdes: A New Genome Assembly Algorithm and Its Applications to Single-Cell Sequencing

  2012cited by this paper
• Divergence of desiccation-related traits in two Drosophila species of the takahashii subgroup from the western Himalayas

  2012cited by this paper
• The effects of alignment error and alignment filtering on the sitewise detection of positive selection.

  2012cited by this paper
• The functions and regulation of the PTEN tumour suppressor

  2012influential reference
• Detecting Individual Sites Subject to Episodic Diversifying Selection

  2012cited by this paper
• The frizzled/stan pathway and planar cell polarity in the Drosophila wing.

  2012cited by this paper
• IDBA-UD: a de novo assembler for single-cell and metagenomic sequencing data with highly uneven depth

  2012cited by this paper
• Wnt/β-catenin signaling and disease.

  2012cited by this paper
• Mechanisms and functions of Hedgehog signalling across the metazoa

  2011cited by this paper
• Orthology prediction methods: A quality assessment using curated protein families

  2011cited by this paper
• New Dystrophin/Dystroglycan interactors control neuron behavior in Drosophila eye

  2011cited by this paper
• Statistical properties of the branch-site test of positive selection.

  2011cited by this paper
• A random effects branch-site model for detecting episodic diversifying selection.

  2011cited by this paper
• High sensitivity to aligner and high rate of false positives in the estimates of positive selection in the 12 Drosophila genomes.

  2011cited by this paper
• MACSE: Multiple Alignment of Coding SEquences Accounting for Frameshifts and Stop Codons

  2011cited by this paper
• RNA-Seq unleashed

  2011cited by this paper
• dSir2 and longevity in Drosophila.

  2011cited by this paper
• HHblits: lightning-fast iterative protein sequence searching by HMM-HMM alignment

  2011cited by this paper
• optix Drives the Repeated Convergent Evolution of Butterfly Wing Pattern Mimicry

  2011cited by this paper
• Asymmetric and non-uniform evolution of recently duplicated human genes

  2010cited by this paper
• FastTree 2 – Approximately Maximum-Likelihood Trees for Large Alignments

  2010cited by this paper
• Identification of a candidate adaptive polymorphism for Drosophila life history by parallel independent clines on two continents

  2010cited by this paper
• The Sequence Read Archive

  2010cited by this paper
• Holm's Sequential Bonferroni Procedure

  2010cited by this paper
• The effect of insertions, deletions, and alignment errors on the branch-site test of positive selection.

  2010cited by this paper
• A maximum pseudo-likelihood approach for estimating species trees under the coalescent model

  2010cited by this paper
• Phylogenetic and Functional Assessment of Orthologs Inference Projects and Methods

  2009cited by this paper
• Phylogenetic taxonomy in Drosophila.

  2009cited by this paper
• Phylogenetic taxonomy in Drosophila: Problems and prospects

  2009cited by this paper
• How confident can we be that orthologs are similar, but paralogs differ?

  2009cited by this paper
• Reliabilities of identifying positive selection by the branch-site and the site-prediction methods

  2009cited by this paper
• Bayesian Inference of Species Trees from Multilocus Data

  2009cited by this paper
• Evolution of protein-coding genes in Drosophila.

  2008cited by this paper
• Detecting genetic responses to environmental change

  2008cited by this paper
• Drosophila chemoreceptor gene evolution: selection, specialization and genome size

  2008cited by this paper
• Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources

  2008influential reference
• A Database of Wing Diversity in the Hawaiian Drosophila

  2007influential reference
• Clustal W and Clustal X version 2.0

  2007cited by this paper
• Evolution of genes and genomes on the Drosophila phylogeny

  2007influential reference
• Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments.

  2007cited by this paper
• A screen for immunity genes evolving under positive selection in Drosophila

  2007cited by this paper
• Assessing Performance of Orthology Detection Strategies Applied to Eukaryotic Genomes

  2007cited by this paper
• Frizzled/PCP signalling: a conserved mechanism regulating cell polarity and directed motility

  2007cited by this paper
• Evolutionary rate analyses of orthologs and paralogs from 12 Drosophila genomes.

  2007cited by this paper
• The MPI Bioinformatics Toolkit for protein sequence analysis

  2006cited by this paper
• Benchmarking ortholog identification methods using functional genomics data

  2006cited by this paper
• AMiGA: the arthropodan mitochondrial genomes accessible database

  2006cited by this paper
• The Drosophilidae (Diptera) of Fennoscandia and Denmark

  2005cited by this paper
• Evaluation of an improved branch-site likelihood method for detecting positive selection at the molecular level.

  2005cited by this paper
• Chance caught on the wing: cis-regulatory evolution and the origin of pigment patterns in Drosophila

  2005cited by this paper
• Molecular signatures of natural selection.

  2005influential reference
• Diverse roles of eph receptors and ephrins in the regulation of cell migration and tissue assembly.

  2004cited by this paper
• False-positive selection identified by ML-based methods: examples from the Sig1 gene of the diatom Thalassiosira weissflogii and the tax gene of a human T-cell lymphotropic virus.

  2004cited by this paper
• Accuracy and Power of Statistical Methods for Detecting Adaptive Evolution in Protein Coding Sequences and for Identifying Positively Selected Sites

  2004cited by this paper
• A search for doxycycline-dependent mutations that increase Drosophila melanogaster life span identifies the VhaSFD, Sugar baby, filamin, fwd and Cctl genes

  2003cited by this paper
• gcm2 promotes glial cell differentiation and is required with glial cells missing for macrophage development in Drosophila.

  2002cited by this paper
• Testing the neutral theory of molecular evolution with genomic data from Drosophila

  2002cited by this paper
• germ cell-less acts to repress transcription during the establishment of the Drosophila germ cell lineage.

  2002cited by this paper
• Distinct in vivo requirements for establishment versus maintenance of transcriptional repression

  2002cited by this paper
• Glide2, a second glial promoting factor in Drosophila melanogaster

  2001cited by this paper
• Molecular Phylogenetics and Evolution

  2001cited by this paper

• Progressive coevolution of the yeast centromere and kinetochore.

  2025cites this paper
• Comparative selective pressure analysis on mitochondrial protein-coding genes in flying squirrels (Pteromyini) and tree squirrels (Sciurini)

  2024influential citation
• Novel Sex-Specific Genes and Diverse Interspecific Expression in the Antennal Transcriptomes of Ithomiine Butterflies

  2024cites this paper
• Gene expression, evolution, and the genetics of electrosensing in the smalltooth sawfish, Pristis pectinata

  2024cites this paper
• Evolutionary dynamics of genome size and content during the adaptive radiation of Heliconiini butterflies

  2023cites this paper
• The evolution of intramitochondriality in Midichloria bacteria.

  2023cites this paper
• Evolutionary Divergence and Radula Diversification in Two Ecomorphs from an Adaptive Radiation of Freshwater Snails

  2022cites this paper
• The origin and evolution of mitochondrial tropism in Midichloria bacteria

  2022cites this paper
• Molecular Evolution of Ecological Specialisation: Genomic Insights from the Diversification of Murine Rodents

  2021cites this paper
• Gene diversity explains variation in biological features of insect killing fungus, Beauveria bassiana

  2021cites this paper
• Differential gene expression in Drosophilamelanogaster and D.nigrosparsa infected with the same Wolbachia strain

  2020cites this paper
• Integrated structural and evolutionary analysis reveals common mechanisms underlying adaptive evolution in mammals

  2020cites this paper
• Genomic Signature of Shifts in Selection in a Subalpine Ant and Its Physiological Adaptations

  2020cites this paper
• Radula diversification promotes ecomorph divergence in an adaptive radiation of freshwater snails

  2020cites this paper
• Characterization of two MHC II genes (DOB, DRB) in white-tailed deer (Odocoileus virginianus)

  2020cites this paper
• Elevated rates of positive selection drive the evolution of pestiferousness in the Colorado potato beetle (Leptinotarsa decemlineata, Say)

  2019cites this paper
• Integrated evolutionary and structural analysis reveals xenobiotics and pathogens as the major drivers of mammalian adaptation

  2019cites this paper
• Major range loss predicted from lack of heat adaptability in an alpine Drosophila species.

  2019cites this paper
• Genomic signature of shifts in selection in a sub-alpine ant and its physiological adaptations

  2019cites this paper
• Patterns of positive selection on the transcriptome of western Iberian Squalius fish: a new approach accounting for alternative splicing

  2019influential citation
• Is temperature preference in the laboratory ecologically relevant for the field? The case of Drosophila nigrosparsa

  2019cites this paper
• Large-Scale Comparative Analysis of Codon Models Accounting for Protein and Nucleotide Selection

  2019cites this paper
• Hawaiian Drosophila as an Evolutionary Model Clade: Days of Future Past

  2018cites this paper
• Life‐history traits and physiological limits of the alpine fly Drosophila nigrosparsa (Diptera: Drosophilidae): A comparative study

  2018cites this paper
• Computational prediction of the phenotypic effects of genetic variants: basic concepts and some application examples in Drosophila nervous system genes

  2017cites this paper
• Modeling Codon Rate Variation: Robust Inference of Protein and Nucleotide Selection

  2017cites this paper
• Identifying the minimum number of microsatellite loci needed to assess population genetic structure: A case study in fly culturing

  2017cites this paper
• Title : 1 Rapid expansion and visual specialization of learning and memory centers 2 in

  year unknowncites this paper