Evidence for Population-Specific Positive Selection on Immune Genes of Anopheles gambiae

Host-pathogen interactions can be powerful drivers of adaptive evolution, shaping the patterns of molecular variation at the genes involved. In this study, we sequenced alleles from 28 immune-related loci in wild samples of multiple genetic subpopulations of the African malaria mosquito Anopheles gambiae, obtaining unprecedented sample sizes and providing the first opportunity to contrast patterns of molecular evolution at immune-related loci in the recently discovered GOUNDRY population to those of the indoor-resting M and S molecular forms. In contrast to previous studies that focused on immune genes identified in laboratory studies, we centered our analysis on genes that fall within a quantitative trait locus associated with resistance to Plasmodium falciparum in natural populations of A. gambiae. Analyses of haplotypic and genetic diversity at these 28 loci revealed striking differences among populations in levels of genetic diversity and allele frequencies in coding sequence. Putative signals of positive selection were identified at 11 loci, but only one was shared by two subgroups of A. gambiae. Striking patterns of linkage disequilibrium were observed at several loci. We discuss these results with respect to ecological differences among these strata as well as potential implications for disease transmission.

• Publication year

  2012

• Venue

  G3: Genes, Genomes, Genetics

• Publication date

  2012-12-01

• Fields of study

  Biology, Medicine, Environmental Science

• Identifiers
  DOI 10.1534/g3.112.004473PMID 23275874PMCID 3516473
• 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.

• R: A language and environment for statistical computing.

  2014cited by this paper
• Anopheles gambiae pathogen susceptibility: the intersection of genetics, immunity and ecology.

  2012cited by this paper
• Differential Plasmodium falciparum infection of Anopheles gambiae s.s. molecular and chromosomal forms in Mali

  2012cited by this paper
• Behavioural responses of Anopheles gambiae sensu stricto M and S molecular form larvae to an aquatic predator in Burkina Faso

  2012cited by this paper
• A comprehensive gene expression atlas of sex- and tissue-specificity in the malaria vector, Anopheles gambiae

  2011cited by this paper
• A Cryptic Subgroup of Anopheles gambiae Is Highly Susceptible to Human Malaria Parasites

  2011cited by this paper
• MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods.

  2011cited by this paper
• Asymmetric introgression between the M and S forms of the malaria vector, Anopheles gambiae, maintains divergence despite extensive hybridization

  2011cited by this paper
• Exceptional Diversity, Maintenance of Polymorphism, and Recent Directional Selection on the APL1 Malaria Resistance Genes of Anopheles gambiae

  2011influential reference
• SNP Genotyping Defines Complex Gene-Flow Boundaries Among African Malaria Vector Mosquitoes

  2010cited by this paper
• Sequence-structure-function relations of the mosquito leucine-rich repeat immune proteins

  2010influential reference
• The genetics of human adaptation: hard sweeps, soft sweeps, and polygenic adaptation.

  2010cited by this paper
• Adaptive divergence between incipient species of Anopheles gambiae increases resistance to Plasmodium

  2010cited by this paper
• The demographic histories of the M and S molecular forms of Anopheles gambiae s.s.

  2010cited by this paper
• A behavioral mechanism underlying ecological divergence in the malaria mosquito Anopheles gambiae.

  2010cited by this paper
• seqphase: a web tool for interconverting phase input/output files and fasta sequence alignments

  2010cited by this paper
• Inferring selection in the Anopheles gambiae species complex: an example from immune-related serine protease inhibitors

  2009cited by this paper
• Fine Pathogen Discrimination within the APL1 Gene Family Protects Anopheles gambiae against Human and Rodent Malaria Species

  2009cited by this paper
• The Sequence Alignment/Map format and SAMtools

  2009cited by this paper
• The salivary transcriptome of Anopheles gambiae (Diptera: Culicidae) larvae: A microarray-based analysis.

  2009cited by this paper
• Living at the edge: biogeographic patterns of habitat segregation conform to speciation by niche expansion in Anopheles gambiae

  2009cited by this paper
• Implication of the Mosquito Midgut Microbiota in the Defense against Malaria Parasites

  2009cited by this paper
• Leucine-Rich Repeat Protein Complex Activates Mosquito Complement in Defense Against Plasmodium Parasites

  2009cited by this paper
• Identifying the most productive breeding sites for malaria mosquitoes in The Gambia

  2009cited by this paper
• Anopheles gambiae PGRPLC-Mediated Defense against Bacteria Modulates Infections with Malaria Parasites

  2009cited by this paper
• DnaSP v5: a software for comprehensive analysis of DNA polymorphism data

  2009influential reference
• Two mosquito LRR proteins function as complement control factors in the TEP1-mediated killing of Plasmodium.

  2009cited by this paper
• Anopheles Fibrinogen-related Proteins Provide Expanded Pattern Recognition Capacity against Bacteria and Malaria Parasites*

  2009cited by this paper
• Ecological niche partitioning between Anopheles gambiae molecular forms in Cameroon: the ecological side of speciation

  2009cited by this paper
• Dynamics of transmission of Plasmodium falciparum by Anopheles arabiensis and the molecular forms M and S of Anopheles gambiae in Dielmo, Senegal

  2008cited by this paper
• Spawning salmon disrupt trophic coupling between wolves and ungulate prey in coastal British Columbia

  2008cited by this paper
• Genome Analysis Of Vectorial Capacity In Major Anopheles Vectors Of Malaria Parasites

  2008cited by this paper
• High Levels of Hybridization between Molecular Forms of Anopheles gambiae from Guinea Bissau

  2008cited by this paper
• SNP discovery and molecular evolution in Anopheles gambiae, with special emphasis on innate immune system

  2008cited by this paper
• Insertion polymorphisms of SINE200 retrotransposons within speciation islands of Anopheles gambiae molecular forms

  2008cited by this paper
• The molecular forms of Anopheles gambiae: a phenotypic perspective.

  2008cited by this paper
• Evidence for divergent selection between the molecular forms of Anopheles gambiae: role of predation

  2008cited by this paper
• Population genetics of Plasmodium resistance genes in Anopheles gambiae: no evidence for strong selection

  2007cited by this paper
• Mutations in smooth muscle α-actin (ACTA2) lead to thoracic aortic aneurysms and dissections

  2007cited by this paper
• Patterns of Selection in Anti-Malarial Immune Genes in Malaria Vectors: Evidence for Adaptive Evolution in LRIM1 in Anopheles arabiensis

  2007influential reference
• Compound tests for the detection of hitchhiking under positive selection.

  2007influential reference
• A major genetic locus controlling natural Plasmodium falciparum infection is shared by East and West African Anopheles gambiae

  2007cited by this paper
• Evaluating the Effect of Postmating Isolation Between Molecular Forms of Anopheles gambiae (Diptera: Culicidae)

  2007cited by this paper
• Comparisons of site- and haplotype-frequency methods for detecting positive selection.

  2007cited by this paper
• Molecular karyotyping of the 2La inversion in Anopheles gambiae.

  2007cited by this paper
• Evolutionary Dynamics of Immune-Related Genes and Pathways in Disease-Vector Mosquitoes

  2007cited by this paper
• Natural Malaria Infection in Anopheles gambiae Is Regulated by a Single Genomic Control Region

  2006cited by this paper
• Anopheles gambiae Immune Responses to Human and Rodent Plasmodium Parasite Species

  2006cited by this paper
• Molecular evolution of plant immune system genes.

  2006cited by this paper
• LDheatmap: An R Function for Graphical Display of Pairwise Linkage Disequilibria Between Single Nucleotide Polymorphisms

  2006cited by this paper
• Statistical Tests for Detecting Positive Selection by Utilizing High-Frequency Variants

  2006cited by this paper
• Disease and Evolution

  2006cited by this paper
• Quantitative Trait Loci Controlling Refractoriness to Plasmodium falciparum in Natural Anopheles gambiae Mosquitoes From a Malaria-Endemic Region in Western Kenya

  2006cited by this paper
• Immune signaling pathways regulating bacterial and malaria parasite infection of the mosquito Anopheles gambiae.

  2005cited by this paper
• Microarray analysis of genes showing variable expression following a blood meal in Anopheles gambiae

  2005cited by this paper
• THE SIGNATURE OF POSITIVE SELECTION ON STANDING GENETIC VARIATION

  2005influential reference
• Species and Populations of the Anopheles gambiae Complex in Cameroon with Special Emphasis on Chromosomal and Molecular Forms of Anopheles gambiae s.s.

  2005cited by this paper
• A Scan for Positively Selected Genes in the Genomes of Humans and Chimpanzees

  2005cited by this paper
• Biology of Toll receptors: lessons from insects and mammals

  2004cited by this paper
• Theoretical and practical advances in genome halving

  2004cited by this paper
• Natural selection drives Drosophila immune system evolution.

  2003cited by this paper
• Inferring Nonneutral Evolution from Human-Chimp-Mouse Orthologous Gene Trios

  2003influential reference
• Characterization of four Toll related genes during development and immune responses in Anopheles gambiae.

  2002cited by this paper
• The Toll and Imd pathways are the major regulators of the immune response in Drosophila

  2002influential reference
• Genetic Loci Affecting Resistance to Human Malaria Parasites in a West African Mosquito Vector Population

  2002cited by this paper
• Evolutionary genetics of invasive species

  2002influential reference
• Generating samples under a Wright-Fisher neutral model of genetic variation

  2002cited by this paper
• Speciation Within Anopheles gambiae-- the Glass Is Half Full

  2002cited by this paper
• Molecular characterization of ribosomal DNA polymorphisms discriminating among chromosomal forms of Anopheles gambiae s.s.

  2001cited by this paper
• Toll receptors in innate immunity.

  2001cited by this paper
• Molecular evidence of incipient speciation within Anopheles gambiae s.s. in West Africa

  2001influential reference
• A new statistical method for haplotype reconstruction from population data.

  2001cited by this paper
• A comparison of estimators of the population recombination rate.

  2000cited by this paper
• Inference of population structure using multilocus genotype data.

  2000cited by this paper
• Three novel mammalian toll-like receptors: gene structure, expression, and evolution.

  2000cited by this paper
• Hitchhiking under positive Darwinian selection.

  2000cited by this paper
• The biology of Toll-like receptors.

  2000cited by this paper
• Population structure, speciation, and introgression in the Anopheles gambiae complex.

  1999cited by this paper
• Horseshoe crab acetyl group-recognizing lectins involved in innate immunity are structurally related to fibrinogen.

  1999cited by this paper
• Molecular characterization of ticks and tick-borne pathogens.

  1999cited by this paper
• NF-kappa B and Rel proteins: evolutionarily conserved mediators of immune responses.

  1998cited by this paper
• DNA variation at the Sod locus of Drosophila melanogaster: an unfolding story of natural selection.

  1997cited by this paper
• Immune factor Gambif1, a new rel family member from the human malaria vector, Anopheles gambiae.

  1996influential reference
• Controlling the false discovery rate: a practical and powerful approach to multiple testing

  1995cited by this paper
• Functional analysis and regulation of nuclear import of dorsal during the immune response in Drosophila.

  1995cited by this paper
• Disease and evolution

  1991cited by this paper
• Statistical method for testing the neutral mutation hypothesis by DNA polymorphism.

  1989cited by this paper
• A test of neutral molecular evolution based on nucleotide data.

  1987cited by this paper
• ESTIMATING F‐STATISTICS FOR THE ANALYSIS OF POPULATION STRUCTURE

  1984cited by this paper
• Chromosomal differentiation and adaptation to human environments in the Anopheles gambiae complex.

  1979cited by this paper
• The homozygosity test of neutrality.

  1978influential reference
• On the number of segregating sites in genetical models without recombination.

  1975cited by this paper
• The hitch-hiking effect of a favourable gene.

  1974cited by this paper
• The hitch-hiking effect of a favourable gene.

  1974cited by this paper
• Bmc Evolutionary Biology the Evolution of Tep1, an Exceptionally Polymorphic Immunity Gene in Anopheles Gambiae

  year unknowncited by this paper

• Chromatin landscape, transcriptomic and ChIP-seq profiling of Anopheles stephensi MSQ43 cell line

  2025cites this paper
• Insight into the structural hierarchy of the protease cascade that regulates the mosquito melanization response

  2023cites this paper
• A Population Genomic Investigation of Immune Cell Diversity and Phagocytic Capacity in a Butterfly

  2021cites this paper
• Evidence for Divergent Selection on Immune Genes between the African Malaria Vectors, Anopheles coluzzii and A. gambiae

  2020cites this paper
• Geographic variation in hemocyte diversity and phagocytic propensity shows a diffuse genomic signature in the green veined white butterfly

  2019cites this paper
• Microevolutionary selection dynamics acting on immune genes of the green‐veined white butterfly, Pieris napi

  2018cites this paper
• Toxicological Efficacy of Flower Extracts From Chrysanthemum cinerariifolium and Leaf Extracts From Eucalyptus camaldulensis and Nicotiana tabaccum on Anopheles gambiae s.s. Giles Mosquito Larvae.

  2018cites this paper
• Sources of variance in immunological traits: evidence of congruent latitudinal trends across species

  2017cites this paper
• Insect Antimicrobial Defences: A Brief History, Recent Findings, Biases, and a Way Forward in Evolutionary Studies

  2017cites this paper
• Molecular evolution and population genetics of a Gram-negative binding protein gene in the malaria vector Anopheles gambiae (sensu lato)

  2016cites this paper
• Plasmodium Oocysts: Overlooked Targets of Mosquito Immunity.

  2016cites this paper
• Disease vectors in the era of next generation sequencing

  2016cites this paper
• Genetic Structure of a Local Population of the Anopheles gambiae Complex in Burkina Faso

  2016cites this paper
• Correction: An Evolution-Based Screen for Genetic Differentiation between Anopheles Sister Taxa Enriches for Detection of Functional Immune Factors

  2016cites this paper
• The kdr-bearing haplotype and susceptibility to Plasmodium falciparum in Anopheles gambiae: genetic correlation and functional testing

  2015cites this paper
• Association mapping by pooled sequencing identifies TOLL 11 as a protective factor against Plasmodium falciparum in Anopheles gambiae

  2015cites this paper
• An Evolution-Based Screen for Genetic Differentiation between Anopheles Sister Taxa Enriches for Detection of Functional Immune Factors

  2015cites this paper
• Stress dependent infection cost of the human malaria agent Plasmodium falciparum on its natural vector Anopheles coluzzii.

  2014cites this paper
• Speciation in Anopheles gambiae — The Distribution of Genetic Polymorphism and Patterns of Reproductive Isolation Among Natural Populations

  2013cites this paper
• Equivalent susceptibility of Anopheles gambiae M and S molecular forms and Anopheles arabiensis to Plasmodium falciparum infection in Burkina Faso

  2013cites this paper
• Diverged Alleles of the Anopheles gambiae Leucine-Rich Repeat Gene APL1A Display Distinct Protective Profiles against Plasmodium falciparum

  2012cites this paper