Exceptional diversity, maintenance of polymorphism, and recent directional selection on the APL1 malaria resistance genes of Anopheles gambiae

PLoS Biology

Volumn 9, Issue 3, 2011, Pages

  Rottschaefer, Susan M ^a   Riehle, Michelle M ^b   Coulibaly, Boubacar ^c   Sacko, Madjou ^c   Niaré, Oumou ^c   Morlais, Isabelle ^d   Traoré, Sekou F ^c   Vernick, Kenneth D ^e   Lazzaro, Brian P ^a  

^a Department of Obstetrics Gynecology   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

^c UNIVERSITY OF BAMAKO   (Mali)

^d Institut de Recherche pour le Developpement Cameroon   (Cameroon)

^e INSTITUT PASTEUR   (France)

Author keywords

[No Author keywords available]

Indexed keywords

AFRICA; ALLELE; ANOPHELES GAMBIAE; APL1 GENE; ARTICLE; CHROMOSOME INVERSION; CONTROLLED STUDY; DNA POLYMORPHISM; GENE; GENE CLUSTER; GENE INTERACTION; GENE LOCUS; GENETIC VARIABILITY; INFECTION RESISTANCE; MALARIA; MOLECULAR EVOLUTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PLASMODIUM; SEASONAL VARIATION; TEP1 GENE; UNINDEXED SEQUENCE; ADAPTATION; ANIMAL; CHEMISTRY; DISEASE CARRIER; GENETIC POLYMORPHISM; GENETIC SELECTION; GENETICS; GEOGRAPHY; IMMUNOLOGY; INNATE IMMUNITY; PARASITOLOGY; PLASMODIUM FALCIPARUM; SEASON;

ANOPHELES GAMBIAE; PLASMODIUM FALCIPARUM;

INSECT PROTEIN;

ADAPTATION, BIOLOGICAL; ANIMALS; ANOPHELES GAMBIAE; EVOLUTION, MOLECULAR; GEOGRAPHY; IMMUNITY, INNATE; INSECT PROTEINS; INSECT VECTORS; PLASMODIUM FALCIPARUM; POLYMORPHISM, GENETIC; SEASONS; SELECTION, GENETIC;

EID: 79953725732     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1000600     Document Type: Article

References (55)

1. World Malaria Report (2008) Geneva, Switzerland World Health Organization Press.
2. Fontenille D, Simard F, (2004) Unravelling complexities in human malaria transmission dynamics in Africa through a comprehensive knowledge of vector populations. Comp Immunol Microbiol Infect Dis 27: 357-375.
3. Niaré O, Markianos K, Volz J, Oduol F, Touré A, et al. (2002) Genetic loci affecting resistance to human malaria parasites in a West African mosquito vector population. Science 298: 213-216.
4. Riehle M. M, Markianos K, Niaré O, Xu J, Li J, et al. (2006) Natural malaria infection in Anopheles gambiae is regulated by a single genomic control region. Science 312: 577-579.
5. Menge D. M, Zhong D, Guda T, Gouagna L, Githure J, et al. (2006) Quantitative trait loci controlling refractoriness to Plasmodium falciparum in natural Anopheles gambiae mosquitoes from a malaria-endemic region in western Kenya. Genetics 173: 235-241.
6. Riehle M. M, Markianos K, Lambrechts L, Xia A, Sharakhov I, et al. (2007) A major genetic locus controlling natural Plasmodium falciparum infection is shared by East and West African Anopheles gambiae. Malar J 6: 87.
7. Riehle M. M, Xu J, Lazzaro B. P, Rottschaefer S. M, Coulibaly B, et al. (2008) Anopheles gambiae APL1 is a family of variable LRR proteins required for Rel1-mediated protection from the malaria parasite, Plasmodium berghei. PLoS ONE 3: e3672 doi:10.1371/journal.pone.0003672.
8. Mitri C, Jacques J. C, Thiery I, Riehle M. M, Xu J, et al. (2009) Fine pathogen discrimination within the APL1 gene family protects Anopheles gambiae against human and rodent malaria species. PLoS Pathog 5: e1000576 doi:10.1371/journal.ppat.1000576.
9. Habtewold T, Povelones M, Blagborough A. M, Christophides G. K, (2008) Transmission blocking immunity in the malaria non-vector mosquito Anopheles quadriannulatus species A. PLoS Pathog 4: e1000070 doi:10.1371/journal.ppat.1000070.
10. Osta M. A, Christophides G. K, Kafatos F. C, (2004) Effects of mosquito genes on Plasmodium development. Science 303: 2030-2032.
11. Fraiture M, Baxter R. H, Steinert S, Chelliah Y, Frolet C, et al. (2009) Two mosquito LRR proteins function as complement control factors in the TEP1-mediated killing of Plasmodium. Cell Host Microbe 5: 273-284.
12. Povelones M, Waterhouse R. M, Kafatos F. C, Christophides G. K, (2009) Leucine-rich repeat protein complex activates mosquito complement in defense against Plasmodium parasites. Science 324: 258-261.
13. Little T. J, Cobbe N, (2005) The evolution of immune-related genes from disease carrying mosquitoes: diversity in a peptidoglycan- and a thioester-recognizing protein. Insect Mol Biol 14: 599-605.
14. Obbard D. J, Linton Y. M, Jiggins F. M, Yan G, Little T. J, (2007) Population genetics of Plasmodium resistance genes in Anopheles gambiae: no evidence for strong selection. Mol Ecol 16: 3497-3510.
15. Simard F, Licht M, Besansky N. J, Lehmann T, (2007) Polymorphism at the defensin gene in the Anopheles gambiae complex: testing different selection hypotheses. Infect Genet Evol 7: 285-292.
16. Slotman M. A, Parmakelis A, Marshall J. C, Awono-Ambene P. H, Antonio-Nkondjo C, et al. (2007) Patterns of selection in anti-malarial immune genes in malaria vectors: evidence for adaptive evolution in LRIM1 in Anopheles arabiensis. PLoS One 2: e793 doi:10.1371/journal.pone.0000793.
17. Cohuet A, Krishnakumar S, Simard F, Morlais I, Koutsos A, et al. (2008) SNP discovery and molecular evolution in Anopheles gambiae, with special emphasis on innate immune system. BMC Genomics 9: 227.
18. Obbard D. J, Callister D. M, Jiggins F. M, Soares D. C, Yan G, et al. (2008) The evolution of TEP1, an exceptionally polymorphic immunity gene in Anopheles gambiae. BMC Evol Biol 8: 274.
19. Parmakelis A, Slotman M. A, Marshall J. C, Awono-Ambene P. H, Antonio-Nkondjio C, et al. (2008) The molecular evolution of four anti-malarial immune genes in the Anopheles gambiae species complex. BMC Evol Biol 8: 79.
20. Lehmann T, Hume J. C, Licht M, Burns C. S, Wollenberg K, et al. (2009) Molecular evolution of immune genes in the malaria mosquito Anopheles gambiae. PLoS One 4: e4549 doi:10.1371/journal.pone.0004549.
21. Obbard D. J, Welch J. J, Little T. J, (2009) Inferring selection in the Anopheles gambiae species complex: an example from immune-related serine protease inhibitors. Malar J 8: 117.
22. Blandin S, Shiao S. H, Moita L. F, Janse C. J, Waters A. P, et al. (2004) Complement-like protein TEP1 is a determinant of vectorial capacity in the malaria vector Anopheles gambiae. Cell 116: 661-670.
23. Dong Y, Aguilar R, Xi Z, Warr E, Mongin E, et al. (2006) Anopheles gambiae immune responses to human and rodent Plasmodium parasite species. PLoS Pathog 2: e52 doi:10.1371/journal.ppat.0020052.
24. Blandin S. A, Wang-Sattler R, Lamacchia M, Gagneur J, Lycett G, et al. (2009) Dissecting the genetic basis of resistance to malaria parasites in Anopheles gambiae. Science 326: 147-150.
25. Lehmann T, Diabate A, (2008) The molecular forms of Anopheles gambiae: a phenotypic perspective. Infect Genet Evol 8: 737-746.
26. Hudson R. R, Kaplan N. L, (1988) The coalescent process in models with selection and recombination. Genetics 120: 831-840.
27. Castric V, Bechsgaard J, Schierup M. H, Vekemans X, (2008) Repeated adaptive introgression at a gene under multiallelic balancing selection. PLoS Genet 4: e1000168 doi:10.1371/journal.pgen.1000168.
28. McDonald J. H, Kreitman M, (1991) Adaptive protein evolution at the Adh locus in Drosophila. Nature 351: 652-654.
29. Wright S. I, Charlesworth B, (2004) The HKA test revisited: a maximum-likelihood-ratio test of the standard neutral model. Genetics 168: 1071-1076.
30. Besansky N. J, Krzywinski J, Lehmann T, Simard F, Kern M, et al. (2003) Semipermeable species boundaries between Anopheles gambiae and Anopheles arabiensis: evidence from multilocus DNA sequence variation. Proc Natl Acad Sci U S A 100: 10818-10823.
31. Parmakelis A, Moustaka M, Poulakakis N, Louis C, Slotman M. A, et al. (2010) Anopheles immune genes and amino acid sites evolving under the effect of positive selection. PLoS One 5: e8885 doi:10.1371/journal.pone.0008885.
32. Kern A. D, Jones C. D, Begun D. J, (2004) Molecular population genetics of male accessory gland proteins in the Drosophila simulans complex. Genetics 167: 725-735.
33. Lazzaro B. P, (2005) Elevated polymorphism and divergence in the class C scavenger receptors of Drosophila melanogaster and D. simulans. Genetics 169: 2023-2034.
34. Yamaguchi-Kabata Y, Shimada M. K, Hayakawa Y, Minoshima S, Chakraborty R, et al. (2008) Distribution and effects of nonsense polymorphisms in human genes. PLoS One 3: e3393 doi:10.1371/journal.pone.0003393.
35. Coluzzi M, Sabatini A, Petrarca V, Di Deco M. A, (1979) Chromosomal differentiation and adaptation to human environments in the Anopheles gambiae complex. Trans R Soc Trop Med Hyg 73: 483-497.
36. Powell J. R, Petrarca V, della Torre A, Caccone A, Coluzzi M, (1999) Population structure, speciation, and introgression in the Anopheles gambiae complex. Parassitologia 41: 101-113.
37. Touré Y. T, Petrarca V, Traoré S. F, Coulibaly A, Maiga H. M, et al. (1998) The distribution and inversion polymorphism of chromosomally recognized taxa of the Anopheles gambiae complex in Mali, West Africa. Parassitologia 40: 477-511.
38. Maynard Smith J, Haigh J, (1974) The hitch-hiking effect of a favourable gene. Genet Res 23: 23-35.
39. Braverman J. M, Hudson R. R, Kaplan N. L, Langley C. H, Stephan W, (1995) The hitchhiking effect on the site frequency spectrum of DNA polymorphisms. Genetics 140: 783-796.
40. Tajima F, (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123: 585-595.
41. Fu Y. X, Li W. H, (1993) Statistical tests of the neutrality of mutations. Genetics 133: 693-709.
42. Zeng K, Mano S, Shi S, Wu C. I, (2007) Comparisons of site- and haplotype-frequency methods for detecting positive selection. Mol Biol Evol 24: 1562-1574.
43. White B. J, Lawniczak M. K. L, Cheng C, Coulibaly M. B, Wilson M. D, et al. (2011) Adaptive divergence between incipient species of Anopheles gambiae increases resistance to Plasmodium. Proc Natl Acad Sci 108: 244-249.
44. Turner T. L, Hahn M. W, Nuzhdin S. V, (2005) Genomic islands of speciation in Anopheles gambiae. PLoS Biol 3: e285 doi:10.1371/journal.pbio.0030285.
45. Turner T. L, Hahn M. W, (2007) Locus- and population-specific selection and differentiation between incipient species of Anopheles gambiae. Mol Biol Evol 24: 2132-2138.
46. Levashina E. A, Moita L. F, Blandin S, Vriend G, Lagueux M, et al. (2001) Conserved role of a complement-like protein in phagocytosis revealed by dsRNA knockout in cultured cells of the mosquito, Anopheles gambiae. Cell 104: 709-718.
47. Ewens W. J, (1972) Sampling theory of selectively neutral alleles. Theor Pop Biol 3: 87-112.
48. Hudson R. R, Boos D. D, Kaplan N. L, (1992) A statistical test for detecting geographic subdivision. Mol Biol Evol 9: 138-151.
49. Holt R. A, Subramanian G. M, Halpern A, Sutton G. G, Charlab R, et al. (2002) The genome sequence of the malaria mosquito Anopheles gambiae. Science 298: 129-149.
50. Favia G, Lanfrancotti A, Spanos L, Sidén-Kiamos I, Louis C, (2001) Molecular characterization of ribosomal DNA polymorphisms discriminating among chromosomal forms of Anopheles gambiae s.s. Insect Mol Biol 10: 19-23.
51. White B. J, Santolamazza F, Kamau L, Pombi M, Grushko O, et al. (2007) Molecular karyotyping of the 2La inversion in Anopheles gambiae. Am J Trop Med Hyg 76: 334-339.
52. Librado P, Rozas J, (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25: 1451-1452.
53. Hudson R. R, (2002) Generating samples under a Wright-Fisher neutral model. Bioinformatics 18: 337-338.
54. Hudson R. R, Slatkin M, Maddison W. P, (1992) Estimation of levels of gene flow from DNA sequence data. Genetics 132: 583-589.
55. Kumar S, Tamura K, Nei M, (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Briefings in Bioinformatics 5: 150-163.